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1
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Chen YA, Ng PY, Garcia-Ruiz D, Elliot A, Palmer B, Assunção Carvalho RMCD, Tseng LF, Lee CS, Tsai KH, Greenhouse B, Chang HH. Genetic surveillance reveals low but sustained malaria transmission with clonal replacement in Sao Tome and Principe. COMMUNICATIONS MEDICINE 2025; 5:199. [PMID: 40425726 PMCID: PMC12116912 DOI: 10.1038/s43856-025-00905-8] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/18/2024] [Accepted: 05/09/2025] [Indexed: 05/29/2025] Open
Abstract
BACKGROUND Despite efforts to eliminate malaria in Sao Tome and Principe (STP), cases have recently increased. Understanding residual transmission structure is crucial for developing effective elimination strategies. METHODS This study collected surveillance data and generated amplicon sequencing data from 980 samples between 2010 and 2016 to examine the genetic structure of the parasite population. RESULTS Here we show that the mean multiplicity of infection (MOI) is 1.3, with 11% polyclonal infections, indicating low transmission intensity. Temporal trends of these genetic metrics do not align with incidence rates, suggesting that changes in genetic metrics may not straightforwardly reflect changes in transmission intensity, particularly in low transmission settings where genetic drift and importation have a substantial impact. While 88% of samples are genetically linked, continuous turnover in genetic clusters and changes in drug-resistance haplotypes are observed. Principal component analysis reveals some STP samples are genetically similar to those from Central and West Africa, indicating possible importation. CONCLUSIONS These findings highlight the need to prioritize several interventions, such as targeted interventions against transmission hotspots, reactive case detection, and strategies to reduce the introduction of new parasites into this island nation as it approaches elimination. This study also serves as a case study for implementing genetic surveillance in a low transmission setting.
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Affiliation(s)
- Ying-An Chen
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, CA, USA
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan, ROC
| | - Peng-Yin Ng
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan, ROC
| | - Daniel Garcia-Ruiz
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan, ROC
- Bioinformatics Program, Institute of Statistical Science, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan, ROC
| | - Aaron Elliot
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, CA, USA
| | - Brian Palmer
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, CA, USA
| | | | - Lien-Fen Tseng
- Taiwan Anti-Malarial Advisory Mission, São Tomé, São Tomé and Príncipe
| | - Cheng-Sheng Lee
- Institute of Molecular and Cellular Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan, ROC
| | - Kun-Hsien Tsai
- Taiwan Anti-Malarial Advisory Mission, São Tomé, São Tomé and Príncipe
- Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei, Taiwan, ROC
| | - Bryan Greenhouse
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, CA, USA
| | - Hsiao-Han Chang
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan, ROC.
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2
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Bursell M, Rohilla M, Ramirez L, Cheng Y, Schwarzkopf EJ, Guerrero RF, Smukowski Heil C. Mixed Outcomes in Recombination Rates After Domestication: Revisiting Theory and Data. Mol Ecol 2025:e17773. [PMID: 40271548 DOI: 10.1111/mec.17773] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/01/2024] [Revised: 04/07/2025] [Accepted: 04/14/2025] [Indexed: 04/25/2025]
Abstract
The process of domestication has altered many phenotypes. Selection on these phenotypes has long been hypothesised to indirectly select for increases in the genome-wide recombination rate. This hypothesis is potentially consistent with theory on the evolution of the recombination rate, but empirical support has been unclear. We review relevant theory, lab-based experiments, and data comparing recombination rates in wild progenitors and their domesticated counterparts. We utilise population sequencing data and a deep learning method to infer genome-wide recombination rates for new comparisons of chicken/red junglefowl, sheep/mouflon, and goat/bezoar. We find evidence of increased recombination in domesticated goats compared to bezoars but more mixed results in chicken and generally decreased recombination in domesticated sheep compared to mouflon. Our results add to a growing body of literature in plants and animals that finds no consistent evidence of an increase in genome-wide recombination with domestication.
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Affiliation(s)
- Madeline Bursell
- Department of Plant Pathology and Entomology, North Carolina State University, Raleigh, North Carolina, USA
- Bioinformatics Research Center, North Carolina State University, Raleigh, North Carolina, USA
| | - Manav Rohilla
- Bioinformatics Research Center, North Carolina State University, Raleigh, North Carolina, USA
| | - Lucia Ramirez
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA
| | - Yuhuan Cheng
- Bioinformatics Research Center, North Carolina State University, Raleigh, North Carolina, USA
- Department of Statistics, North Carolina State University, Raleigh, North Carolina, USA
| | - Enrique J Schwarzkopf
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA
| | - Rafael F Guerrero
- Bioinformatics Research Center, North Carolina State University, Raleigh, North Carolina, USA
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA
| | - Caiti Smukowski Heil
- Department of Biological Sciences, North Carolina State University, Raleigh, North Carolina, USA
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3
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Bian Z, Xu Z, Peer A, Choi Y, Priest SJ, Akritidou K, Dasgupta A, Dahlmann TA, Kück U, Nowrousian M, Sachs MS, Sun S, Heitman J. Essential genes encoded by the mating-type locus of the human fungal pathogen Cryptococcus neoformans. mBio 2025; 16:e0022325. [PMID: 39998264 PMCID: PMC11980393 DOI: 10.1128/mbio.00223-25] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/17/2025] [Accepted: 02/03/2025] [Indexed: 02/26/2025] Open
Abstract
Fungal sexual reproduction is controlled by the mating-type (MAT) locus. In contrast to a majority of species in the phylum Basidiomycota that have tetrapolar mating-type systems, the opportunistic human pathogen Cryptococcus neoformans employs a bipolar mating-type system, with two mating types (a and α) determined by a single MAT locus that is unusually large (~120 kb) and contains more than 20 genes. While several MAT genes are associated with mating and sexual development, others control conserved cellular processes (e.g., cargo transport and protein synthesis), of which five (MYO2, PRT1, RPL22, RPL39, and RPO41) have been hypothesized to be essential. In this study, through genetic analysis involving sporulation of heterozygous diploid deletion mutants, as well as in some cases construction and analyses of conditional expression alleles of these genes, we confirmed that with the exception of MYO2, both alleles of the other four MAT genes are indeed essential for cell viability. We further showed that while MYO2 is not essential, its function is critical for infectious spore production, faithful cytokinesis, adaptation for growth at high temperature, and pathogenicity in vivo. Our results demonstrate the presence of essential genes in the MAT locus that are divergent between cells of opposite mating types. We discuss possible mechanisms to maintain functional alleles of these essential genes in a rapidly evolving genomic region in the context of fungal sexual reproduction and mating-type evolution.IMPORTANCESexual reproduction is essential for long-term evolutionary success. Fungal cell-type identity is governed by the MAT locus, which is typically rapidly evolving and highly divergent between different mating types. In this study, we show that the a and α alleles of four genes encoded in the MAT locus of the opportunistic human fungal pathogen C. neoformans are essential. We demonstrate that a fifth gene, MYO2, which had been predicted to be essential, is in fact dispensable for cell viability. However, a functional MYO2 allele is important for cytokinesis and fungal pathogenicity. Our study highlights the need for careful genetic analyses in determining essential genes, which is complementary to high-throughput approaches. Additionally, the presence of essential genes in the MAT locus of C. neoformans provides insights into the function, maintenance, and evolution of these fast-evolving genomic regions.
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Affiliation(s)
- Zhuyun Bian
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Ziyan Xu
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Anushka Peer
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Yeseul Choi
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Shelby J. Priest
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Konstantina Akritidou
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Ananya Dasgupta
- Department of Biology, Texas A&M University, College Station, Texas, USA
| | - Tim A. Dahlmann
- Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, Bochum, Germany
| | - Ulrich Kück
- Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, Bochum, Germany
| | - Minou Nowrousian
- Lehrstuhl für Molekulare und Zelluläre Botanik, Ruhr-Universität Bochum, Bochum, Germany
| | - Matthew S. Sachs
- Department of Biology, Texas A&M University, College Station, Texas, USA
| | - Sheng Sun
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Joseph Heitman
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
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4
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Talbi M, Turner GF, Malinsky M. Rapid evolution of recombination landscapes during the divergence of cichlid ecotypes in Lake Masoko. Evolution 2025; 79:364-379. [PMID: 39589917 DOI: 10.1093/evolut/qpae169] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/30/2024] [Revised: 11/06/2024] [Accepted: 11/25/2024] [Indexed: 11/28/2024]
Abstract
Variation of recombination rate along the genome is of crucial importance to rapid adaptation and organismal diversification. Many unknowns remain regarding how and why recombination landscapes evolve in nature. Here, we reconstruct recombination maps based on linkage disequilibrium and use subsampling and simulations to derive a new measure of recombination landscape evolution: the Population Recombination Divergence Index (PRDI). Using PRDI, we show that fine-scale recombination landscapes differ substantially between two cichlid fish ecotypes of Astatotilapia calliptera that diverged only ~2,500 generations ago. Perhaps surprisingly, recombination landscape differences are not driven by divergence in terms of allele frequency (FST) and nucleotide diversity (Δ(π)): although there is some association, we observe positive PRDI in regions where FST and Δ(π) are zero. We found a stronger association between the evolution of recombination and 47 large haplotype blocks that are polymorphic in Lake Masoko, cover 21% of the genome, and appear to include multiple inversions. Among haplotype blocks, there is a strong and clear association between the degree of recombination divergence and differences between ecotypes in heterozygosity, consistent with recombination suppression in heterozygotes. Overall, our work provides a holistic view of changes in population recombination landscapes during the early stages of speciation with gene flow.
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Affiliation(s)
- Marion Talbi
- Biology Department, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
- Department of Fish Ecology and Evolution, EAWAG, Kastanienbaum, Switzerland
| | - George F Turner
- School of Natural & Environmental Sciences, Bangor University, Bangor, United Kingdom
| | - Milan Malinsky
- Biology Department, Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
- Department of Fish Ecology and Evolution, EAWAG, Kastanienbaum, Switzerland
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5
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Parée T, Noble L, Roze D, Teotónio H. Selection Can Favor a Recombination Landscape That Limits Polygenic Adaptation. Mol Biol Evol 2025; 42:msae273. [PMID: 39776196 PMCID: PMC11739800 DOI: 10.1093/molbev/msae273] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/26/2024] [Revised: 12/05/2024] [Accepted: 12/13/2024] [Indexed: 01/11/2025] Open
Abstract
Modifiers of recombination rates have been described but the selective pressures acting on them and their effect on adaptation to novel environments remain unclear. We performed experimental evolution in the nematode Caenorhabditis elegans using alternative rec-1 alleles modifying the position of meiotic crossovers along chromosomes without detectable direct fitness effects. We show that adaptation to a novel environment is impaired by the allele that decreases recombination rates in the genomic regions containing fitness variation. However, the allele that impairs adaptation is indirectly favored by selection, because it increases recombination rates and reduces the associations among beneficial and deleterious variation located in its chromosomal vicinity. These results validate theoretical expectations about the evolution of recombination but suggest that genome-wide polygenic adaptation is of little consequence to indirect selection on recombination rate modifiers.
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Affiliation(s)
- Tom Parée
- Institut de Biologie, École Normale Supérieure, CNRS UMR 8197, Inserm U1024, PSL Research University, Paris 75005, France
- Department of Biology, New York University, New York, NY 10003, USA
| | - Luke Noble
- Institut de Biologie, École Normale Supérieure, CNRS UMR 8197, Inserm U1024, PSL Research University, Paris 75005, France
- EnviroDNA, 95 Albert St Brunswick, Melbourne, Victoria 3065, Australia
| | - Denis Roze
- Adaptation et Diversité en Milieu Marin CNRS UMR 7144, Station Biologique de Roscoff, Sorbonne University, Roscoff 29688, France
| | - Henrique Teotónio
- Institut de Biologie, École Normale Supérieure, CNRS UMR 8197, Inserm U1024, PSL Research University, Paris 75005, France
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6
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Bian Z, Xu Z, Peer A, Choi Y, Priest SJ, Akritidou K, Dasgupta A, Dahlmann TA, Kück U, Nowrousian M, Sachs MS, Sun S, Heitman J. Essential genes encoded by the mating-type locus of the human fungal pathogen Cryptococcus neoformans. BIORXIV : THE PREPRINT SERVER FOR BIOLOGY 2024:2024.12.02.626420. [PMID: 39677606 PMCID: PMC11642766 DOI: 10.1101/2024.12.02.626420] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Download PDF] [Subscribe] [Scholar Register] [Indexed: 12/17/2024]
Abstract
Fungal sexual reproduction is controlled by the mating-type (MAT) locus. In contrast to a majority of species in the phylum Basidiomycota that have tetrapolar mating-type systems, the opportunistic human pathogen Cryptococcus neoformans employs a bipolar mating-type system, with two mating types (a and α) determined by a single MAT locus that is unusually large (~120 kb) and contains more than 20 genes. While several MAT genes are associated with mating and sexual development, others control conserved cellular processes (e.g. cargo transport and protein synthesis), of which five (MYO2, PRT1, RPL22, RPL39, and RPO41) have been hypothesized to be essential. In this study, through genetic analysis involving sporulation of heterozygous diploid deletion mutants, as well as in some cases construction and analyses of conditional expression alleles of these genes, we confirmed that with the exception of MYO2, both alleles of the other four MAT genes are indeed essential for cell viability. We further showed that while MYO2 is not essential, its function is critical for infectious spore production, faithful cytokinesis, adaptation for growth at high temperature, and pathogenicity in vivo. Our results demonstrate the presence of essential genes in the MAT locus that are divergent between cells of opposite mating types. We discuss possible mechanisms to maintain functional alleles of these essential genes in a rapidly-evolving genomic region in the context of fungal sexual reproduction and mating-type evolution.
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Affiliation(s)
- Zhuyun Bian
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Ziyan Xu
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Anushka Peer
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Yeseul Choi
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Shelby J. Priest
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Konstantina Akritidou
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Ananya Dasgupta
- Department of Biology, Texas A&M University, College Station, Texas, USA
| | - Tim A. Dahlmann
- Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, Bochum, Germany
| | - Ulrich Kück
- Allgemeine und Molekulare Botanik, Ruhr-Universität Bochum, Bochum, Germany
| | - Minou Nowrousian
- Lehrstuhl für Molekulare und Zelluläre Botanik, Ruhr-Universität Bochum, Germany
| | - Matthew S. Sachs
- Department of Biology, Texas A&M University, College Station, Texas, USA
| | - Sheng Sun
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
| | - Joseph Heitman
- Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, USA
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7
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Chaparro-Pedraza PC, Roth G, Melián CJ. Ecological diversification in sexual and asexual lineages. Sci Rep 2024; 14:30369. [PMID: 39638813 PMCID: PMC11621406 DOI: 10.1038/s41598-024-81770-8] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/28/2024] [Accepted: 11/28/2024] [Indexed: 12/07/2024] Open
Abstract
The presence or absence of sex can have a strong influence on the processes whereby species arise. Yet, the mechanistic underpinnings of this influence are poorly understood. To gain insights into the mechanisms whereby the reproductive mode may influence ecological diversification, we investigate how natural selection, genetic mixing, and the reproductive mode interact and how this interaction affects the evolutionary dynamics of diversifying lineages. To do so, we analyze models of ecological diversification for sexual and asexual lineages, in which diversification is driven by intraspecific resource competition. We find that the reproductive mode strongly influences the diversification rate and, thus, the ensuing diversity of a lineage. Our results reveal that ecologically-based selection is stronger in asexual lineages because asexual organisms have a higher reproductive potential than sexual ones. This promotes faster diversification in asexual lineages. However, a small amount of genetic mixing accelerates the trait expansion process in sexual lineages, overturning the effect of ecologically-based selection alone and enabling a faster niche occupancy than asexual lineages. As a consequence, sexual lineages can occupy more ecological niches, eventually resulting in higher diversity. This suggests that sexual reproduction may be widespread among species because it increases the rate of diversification.
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Affiliation(s)
- P Catalina Chaparro-Pedraza
- Department of Fish Ecology and Evolution, Swiss Federal Institute of Aquatic Science and Technology (EAWAG), Kastanienbaum, Switzerland.
- Department Systems Analysis, Integrated Assessment and Modelling, Swiss Federal Institute of Aquatic Science and Technology (EAWAG), Dübendorf, Switzerland.
- Inst. of Ecology and Evolution, University of Bern, Bern, Switzerland.
- Swiss Institute of Bioinformatics, Lausanne, Switzerland.
| | - Gregory Roth
- Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland
| | - Carlos J Melián
- Department of Fish Ecology and Evolution, Swiss Federal Institute of Aquatic Science and Technology (EAWAG), Kastanienbaum, Switzerland
- Inst. of Ecology and Evolution, University of Bern, Bern, Switzerland
- Inst. de Física Interdisciplinar y Sistemas Complejos IFISC (CSIC-UIB), Palma de Mallorca, Spain
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8
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Chen Y, Ng PY, Garcia D, Elliot A, Palmer B, Assunção Carvalho RMCD, Tseng LF, Lee CS, Tsai KH, Greenhouse B, Chang HH. Genetic surveillance reveals low, sustained malaria transmission with clonal replacement in Sao Tome and Principe. MEDRXIV : THE PREPRINT SERVER FOR HEALTH SCIENCES 2024:2024.07.15.24309968. [PMID: 39072035 PMCID: PMC11275696 DOI: 10.1101/2024.07.15.24309968] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 07/30/2024]
Abstract
Despite efforts to eliminate malaria in Sao Tome and Principe (STP), cases have recently increased. Understanding residual transmission structure is crucial for developing effective elimination strategies. This study collected surveillance data and generated amplicon sequencing data from 980 samples between 2010 and 2016 to examine the genetic structure of the parasite population. The mean multiplicity of infection (MOI) was 1.3, with 11% polyclonal infections, indicating low transmission intensity. Temporal trends of these genetic metrics did not align with incidence rates, suggesting that changes in genetic metrics may not straightforwardly reflect changes in transmission intensity, particularly in low transmission settings where genetic drift and importation have a substantial impact. While 88% of samples were genetically linked, continuous turnover in genetic clusters and changes in drug-resistance haplotypes were observed. Principal component analysis revealed some STP samples were genetically similar to those from Central and West Africa, indicating possible importation. These findings highlight the need to prioritize several interventions such as targeted interventions against transmission hotspots, reactive case detection, and strategies to reduce the introduction of new parasites into this island nation as it approaches elimination. This study also serves as a case study for implementing genetic surveillance in a low transmission setting.
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Affiliation(s)
- Ying‑An Chen
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, United States
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan
| | - Peng-Yin Ng
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan
| | - Daniel Garcia
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan
- Bioinformatics Program, Institute of Statistical Science, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan
| | - Aaron Elliot
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, United States
| | - Brian Palmer
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, United States
| | | | - Lien-Fen Tseng
- Taiwan Anti-Malarial Advisory Mission, São Tomé, Democratic Republic of São Tomé and Príncipe
| | - Cheng-Sheng Lee
- Institute of Molecular and Cellular Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan
| | - Kun-Hsien Tsai
- Taiwan Anti-Malarial Advisory Mission, São Tomé, Democratic Republic of São Tomé and Príncipe
- Institute of Environmental and Occupational Health Sciences, College of Public Health, National Taiwan University, Taipei, Taiwan
| | - Bryan Greenhouse
- EPPIcenter Research Program, Division of HIV, Infectious Diseases and Global Medicine, Department of Medicine, University of California, San Francisco, United States
| | - Hsiao-Han Chang
- Institute of Bioinformatics and Structural Biology, College of Life Sciences and Medicine, National Tsing Hua University, Hsinchu, Taiwan
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9
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Selection-enriched genomic loci (SEGL) reveals genetic loci for environmental adaptation and photosynthetic productivity in Chlamydomonas reinhardtii. ALGAL RES 2022. [DOI: 10.1016/j.algal.2022.102709] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/19/2022]
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10
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Tamrat S, Borrell JS, Shiferaw E, Wondimu T, Kallow S, Davies RM, Dickie JB, Nuraga GW, White O, Woldeyes F, Demissew S, Wilkin P. Reproductive biology of wild and domesticated Ensete ventricosum: Further evidence for maintenance of sexual reproductive capacity in a vegetatively propagated perennial crop. PLANT BIOLOGY (STUTTGART, GERMANY) 2022; 24:482-491. [PMID: 35137516 PMCID: PMC9303740 DOI: 10.1111/plb.13390] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 06/21/2021] [Accepted: 12/22/2021] [Indexed: 06/14/2023]
Abstract
Loss of sexual reproductive capacity has been proposed as a syndrome of domestication in vegetatively propagated crops, but there are relatively few examples from agricultural systems. In this study, we compare sexual reproductive capacity in wild (sexual) and domesticated (vegetative) populations of enset (Ensete ventricosum (Welw.) Cheesman), a tropical banana relative and Ethiopian food security crop. We examined floral and seed morphology and germination ecology across 35 wild and domesticated enset. We surveyed variation in floral and seed traits, including seed weight, viability and internal morphology, and germinated seeds across a range of constant and alternating temperature regimes to characterize optimum germination requirements. We report highly consistent floral allometry, seed viability, internal morphology and days to germination in wild and domesticated enset. However, seeds from domesticated plants responded to cooler temperatures with greater diurnal range. Shifts in germination behaviour appear concordant with a climatic envelope shift in the domesticated distribution. Our findings provide evidence that sexual reproductive capacity has been maintained despite long-term near-exclusive vegetative propagation in domesticated enset. Furthermore, certain traits such as germination behaviour and floral morphology may be under continued selection, presumably through rare sexually reproductive events. Compared to sexually propagated crops banked as seeds, vegetative crop diversity is typically conserved in living collections that are more costly and insecure. Improved understanding of sexual propagation in vegetative crops may have applications in germplasm conservation and plant breeding.
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Affiliation(s)
- S. Tamrat
- Department of Plant Biology and Biodiversity ManagementAddis Ababa UniversityAddis AbabaEthiopia
- Department of BiologyDilla UniversityDillaSouthern Ethiopia
| | | | - E. Shiferaw
- Ethiopian Biodiversity InstituteAddis AbabaEthiopia
| | - T. Wondimu
- Department of Plant Biology and Biodiversity ManagementAddis Ababa UniversityAddis AbabaEthiopia
| | - S. Kallow
- Royal Botanic Gardens KewMillennium Seed BankWakehurst, ArdinglySussexUK
- Department of BiosystemsKatholieke Universiteit LeuvenLeuvenBelgium
| | - R. M. Davies
- Royal Botanic Gardens KewMillennium Seed BankWakehurst, ArdinglySussexUK
| | - J. B. Dickie
- Royal Botanic Gardens KewMillennium Seed BankWakehurst, ArdinglySussexUK
| | - G. W. Nuraga
- Department of Plant Biology and Biodiversity ManagementAddis Ababa UniversityAddis AbabaEthiopia
| | - O. White
- Royal Botanic GardensKew, RichmondSurreyUK
| | - F. Woldeyes
- Ethiopian Biodiversity InstituteAddis AbabaEthiopia
| | - S. Demissew
- Department of Plant Biology and Biodiversity ManagementAddis Ababa UniversityAddis AbabaEthiopia
| | - P. Wilkin
- Royal Botanic GardensKew, RichmondSurreyUK
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11
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Keaney TA, Jones TM, Holman L. Sexual selection can partly explain low frequencies of Segregation Distorter alleles. Proc Biol Sci 2021; 288:20211190. [PMID: 34583584 PMCID: PMC8479333 DOI: 10.1098/rspb.2021.1190] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/02/2021] [Accepted: 09/02/2021] [Indexed: 11/12/2022] Open
Abstract
The Segregation Distorter (SD) allele found in Drosophila melanogaster distorts Mendelian inheritance in heterozygous males by causing developmental failure of non-SD spermatids, such that greater than 90% of the surviving sperm carry SD. This within-individual advantage should cause SD to fix, and yet SD is typically rare in wild populations. Here, we explore whether this paradox can be resolved by sexual selection, by testing if males carrying three different variants of SD suffer reduced pre- or post-copulatory reproductive success. We find that males carrying the SD allele are just as successful at securing matings as control males, but that one SD variant (SD-5) reduces sperm competitive ability and increases the likelihood of female remating. We then used these results to inform a theoretical model; we found that sexual selection could limit SD to natural frequencies when sperm competitive ability and female remating rate equalled the values observed for SD-5. However, sexual selection was unable to explain natural frequencies of the SD allele when the model was parameterized with the values found for two other SD variants, indicating that sexual selection alone is unlikely to explain the rarity of SD.
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Affiliation(s)
- Thomas A. Keaney
- School of Biosciences, The University of Melbourne, Melbourne, VIC 3010, Australia
| | - Therésa M. Jones
- School of Biosciences, The University of Melbourne, Melbourne, VIC 3010, Australia
| | - Luke Holman
- School of Applied Sciences, Edinburgh Napier University, Edinburgh, UK
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12
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Catchpole S, Barría EM, González PS, Rivera R. Population and reproductive structure in the endangered and highly endemic freshwater crab
Aegla concepcionensis
(Decapoda:Pleocyemata:Aeglidae) from Chile. ACTA ZOOL-STOCKHOLM 2021. [DOI: 10.1111/azo.12408] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.3] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/27/2022]
Affiliation(s)
| | - Erwin M. Barría
- Centro de Investigación e Innovación Para el Cambio Climático (CiiCC) Facultad de Ciencias Universidad Santo Tomás Osorno Chile
- Departamento de Ciencias Básicas Facultad de Ciencias Universidad Santo Tomás Osorno Chile
- Laboratorio de Ecología Evolutiva y Filoinformática Departamento de Zoología Facultad de Ciencias Naturales y Oceanográficas Universidad de Concepción Concepción Chile
- Programa de Doctorado en Sistemática y Biodiversidad Facultad de Ciencias Naturales y Oceanográficas Universidad de Concepción Concepción Chile
| | - Pablo S. González
- Centro Regional de Estudios Ambientales (CREA) Universidad Católica de la Santísima Concepción Concepción Chile
- Programa de Doctorado en Ciencias Ambientales con Mención en Sistemas Acuáticos Continentales Facultad de Ciencias Ambientales Universidad de Concepción Concepción Chile
| | - Reinaldo Rivera
- Laboratorio de Ecología Evolutiva y Filoinformática Departamento de Zoología Facultad de Ciencias Naturales y Oceanográficas Universidad de Concepción Concepción Chile
- Centro de Investigación en Biodiversidad y Ambientes Sustentables (CIBAS) Universidad Católica de la Santísima Concepción Concepción Chile
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13
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Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination. Nat Commun 2019; 10:4310. [PMID: 31541084 PMCID: PMC6754367 DOI: 10.1038/s41467-019-12209-2] [Citation(s) in RCA: 40] [Impact Index Per Article: 6.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/12/2018] [Accepted: 08/19/2019] [Indexed: 12/12/2022] Open
Abstract
Meiotic crossovers (COs) ensure proper chromosome segregation and redistribute the genetic variation that is transmitted to the next generation. Large populations and the demand for genome-wide, fine-scale resolution challenge existing methods for CO identification. Taking advantage of linked-read sequencing, we develop a highly efficient method for genome-wide identification of COs at kilobase resolution in pooled recombinants. We first test this method using a pool of Arabidopsis F2 recombinants, and recapitulate results obtained from the same plants using individual whole-genome sequencing. By applying this method to a pool of pollen DNA from an F1 plant, we establish a highly accurate CO landscape without generating or sequencing a single recombinant plant. The simplicity of this approach enables the simultaneous generation and analysis of multiple CO landscapes, accelerating the pace at which mechanisms for the regulation of recombination can be elucidated through efficient comparisons of genotypic and environmental effects on recombination. Meiotic crossovers (COs) generate genetic variation and ensure proper chromosome segregation. Here, the authors develop a method for identifying COs at kilobase resolution in pooled recombinants using linked-read sequencing data, and apply it to investigate genome-wide CO landscapes of Arabidopsis thaliana.
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14
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Sun H, Rowan BA, Flood PJ, Brandt R, Fuss J, Hancock AM, Michelmore RW, Huettel B, Schneeberger K. Linked-read sequencing of gametes allows efficient genome-wide analysis of meiotic recombination. Nat Commun 2019. [PMID: 31541084 DOI: 10.1101/484022] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/11/2023] Open
Abstract
Meiotic crossovers (COs) ensure proper chromosome segregation and redistribute the genetic variation that is transmitted to the next generation. Large populations and the demand for genome-wide, fine-scale resolution challenge existing methods for CO identification. Taking advantage of linked-read sequencing, we develop a highly efficient method for genome-wide identification of COs at kilobase resolution in pooled recombinants. We first test this method using a pool of Arabidopsis F2 recombinants, and recapitulate results obtained from the same plants using individual whole-genome sequencing. By applying this method to a pool of pollen DNA from an F1 plant, we establish a highly accurate CO landscape without generating or sequencing a single recombinant plant. The simplicity of this approach enables the simultaneous generation and analysis of multiple CO landscapes, accelerating the pace at which mechanisms for the regulation of recombination can be elucidated through efficient comparisons of genotypic and environmental effects on recombination.
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Affiliation(s)
- Hequan Sun
- Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany
| | - Beth A Rowan
- The Genome Center and Department of Plant Sciences, University of California, Davis, 451 East Health Sciences Drive, Davis, CA, 95616, USA.
| | - Pádraic J Flood
- Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany
| | - Ronny Brandt
- Max Planck-Genome-Center Cologne, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany
| | - Janina Fuss
- Max Planck-Genome-Center Cologne, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany
| | - Angela M Hancock
- Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany
| | - Richard W Michelmore
- The Genome Center and Department of Plant Sciences, University of California, Davis, 451 East Health Sciences Drive, Davis, CA, 95616, USA
| | - Bruno Huettel
- Max Planck-Genome-Center Cologne, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany
| | - Korbinian Schneeberger
- Department of Chromosome Biology, Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany.
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15
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Deegan DF, Karbalaei R, Madzo J, Kulathinal RJ, Engel N. The developmental origins of sex-biased expression in cardiac development. Biol Sex Differ 2019; 10:46. [PMID: 31488212 PMCID: PMC6727560 DOI: 10.1186/s13293-019-0259-1] [Citation(s) in RCA: 33] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/12/2019] [Accepted: 08/20/2019] [Indexed: 12/23/2022] Open
Abstract
BACKGROUND Expression patterns between males and females vary in every adult tissue, even in organs with no conspicuous dimorphisms such as the heart. While studies of male and female differences have traditionally focused on the influence of sex hormones, these do not account for all the differences at the molecular and epigenetic levels. We previously reported that a substantial number of genes were differentially expressed in male and female mouse embryonic stem (ES) cells and revealed dose-dependent enhancer activity in response to Prdm14, a key pluripotency factor expressed more highly in female ES cells. In this work, we investigated the role of Prdm14 in establishing sex-specific gene expression networks. We surveyed the sex-specific landscape in early embryogenesis with special reference to cardiac development. We generated sex-specific co-expression networks from mouse ES cells, examined the presence of sex-specific chromatin domains, and analyzed previously published datasets from different developmental time points to characterize how sex-biased gene expression waxes and wanes to evaluate whether sex-biased networks are detectable throughout heart development. RESULTS We performed ChIP-seq on male and female mouse ES cells to determine differences in chromatin status. Our study reveals sex-biased histone modifications, underscoring the potential for the sex chromosome complement to prime the genome differently in early development with consequences for later expression biases. Upon differentiation of ES cells to cardiac precursors, we found sex-biased expression of key transcription and epigenetic factors, some of which persisted from the undifferentiated state. Using network analyses, we also found that Prdm14 plays a prominent role in regulating a subset of dimorphic expression patterns. To determine whether sex-biased expression is present throughout cardiogenesis, we re-analyzed data from two published studies that sampled the transcriptomes of mouse hearts from 8.5 days post-coitum embryos to neonates and adults. We found sex-biased expression at every stage in heart development, and interestingly, identified a subset of genes that exhibit the same bias across multiple cardiogenic stages. CONCLUSIONS Overall, our results support the existence of sexually dimorphic gene expression profiles and regulatory networks at every stage of cardiac development, some of which may be established in early embryogenesis and epigenetically perpetuated.
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Affiliation(s)
- Daniel F. Deegan
- Fels Institute for Cancer Research, Lewis Katz School of Medicine, Temple University, 3400 N. Broad St, Philadelphia, PA 19140 USA
| | - Reza Karbalaei
- Department of Biology, College of Science and Technology, Temple University, 1900 N. 12th St, Philadelphia, PA 19122 USA
| | - Jozef Madzo
- Fels Institute for Cancer Research, Lewis Katz School of Medicine, Temple University, 3400 N. Broad St, Philadelphia, PA 19140 USA
| | - Rob J. Kulathinal
- Department of Biology, College of Science and Technology, Temple University, 1900 N. 12th St, Philadelphia, PA 19122 USA
| | - Nora Engel
- Fels Institute for Cancer Research, Lewis Katz School of Medicine, Temple University, 3400 N. Broad St, Philadelphia, PA 19140 USA
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16
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Van den Bergh B, Swings T, Fauvart M, Michiels J. Experimental Design, Population Dynamics, and Diversity in Microbial Experimental Evolution. Microbiol Mol Biol Rev 2018; 82:e00008-18. [PMID: 30045954 PMCID: PMC6094045 DOI: 10.1128/mmbr.00008-18] [Citation(s) in RCA: 105] [Impact Index Per Article: 15.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/14/2022] Open
Abstract
In experimental evolution, laboratory-controlled conditions select for the adaptation of species, which can be monitored in real time. Despite the current popularity of such experiments, nature's most pervasive biological force was long believed to be observable only on time scales that transcend a researcher's life-span, and studying evolution by natural selection was therefore carried out solely by comparative means. Eventually, microorganisms' propensity for fast evolutionary changes proved us wrong, displaying strong evolutionary adaptations over a limited time, nowadays massively exploited in laboratory evolution experiments. Here, we formulate a guide to experimental evolution with microorganisms, explaining experimental design and discussing evolutionary dynamics and outcomes and how it is used to assess ecoevolutionary theories, improve industrially important traits, and untangle complex phenotypes. Specifically, we give a comprehensive overview of the setups used in experimental evolution. Additionally, we address population dynamics and genetic or phenotypic diversity during evolution experiments and expand upon contributing factors, such as epistasis and the consequences of (a)sexual reproduction. Dynamics and outcomes of evolution are most profoundly affected by the spatiotemporal nature of the selective environment, where changing environments might lead to generalists and structured environments could foster diversity, aided by, for example, clonal interference and negative frequency-dependent selection. We conclude with future perspectives, with an emphasis on possibilities offered by fast-paced technological progress. This work is meant to serve as an introduction to those new to the field of experimental evolution, as a guide to the budding experimentalist, and as a reference work to the seasoned expert.
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Affiliation(s)
- Bram Van den Bergh
- Laboratory of Symbiotic and Pathogenic Interactions, Centre of Microbial and Plant Genetics, KU Leuven-University of Leuven, Leuven, Belgium
- Michiels Lab, Center for Microbiology, VIB, Leuven, Belgium
- Douglas Lab, Department of Entomology, Cornell University, Ithaca, New York, USA
| | - Toon Swings
- Laboratory of Symbiotic and Pathogenic Interactions, Centre of Microbial and Plant Genetics, KU Leuven-University of Leuven, Leuven, Belgium
- Michiels Lab, Center for Microbiology, VIB, Leuven, Belgium
| | - Maarten Fauvart
- Laboratory of Symbiotic and Pathogenic Interactions, Centre of Microbial and Plant Genetics, KU Leuven-University of Leuven, Leuven, Belgium
- Michiels Lab, Center for Microbiology, VIB, Leuven, Belgium
- imec, Leuven, Belgium
| | - Jan Michiels
- Laboratory of Symbiotic and Pathogenic Interactions, Centre of Microbial and Plant Genetics, KU Leuven-University of Leuven, Leuven, Belgium
- Michiels Lab, Center for Microbiology, VIB, Leuven, Belgium
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17
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Christie JR, Beekman M. Uniparental Inheritance Promotes Adaptive Evolution in Cytoplasmic Genomes. Mol Biol Evol 2017; 34:677-691. [PMID: 28025277 PMCID: PMC5896580 DOI: 10.1093/molbev/msw266] [Citation(s) in RCA: 16] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/08/2023] Open
Abstract
Eukaryotes carry numerous asexual cytoplasmic genomes (mitochondria and plastids). Lacking recombination, asexual genomes should theoretically suffer from impaired adaptive evolution. Yet, empirical evidence indicates that cytoplasmic genomes experience higher levels of adaptive evolution than predicted by theory. In this study, we use a computational model to show that the unique biology of cytoplasmic genomes-specifically their organization into host cells and their uniparental (maternal) inheritance-enable them to undergo effective adaptive evolution. Uniparental inheritance of cytoplasmic genomes decreases competition between different beneficial substitutions (clonal interference), promoting the accumulation of beneficial substitutions. Uniparental inheritance also facilitates selection against deleterious cytoplasmic substitutions, slowing Muller's ratchet. In addition, uniparental inheritance generally reduces genetic hitchhiking of deleterious substitutions during selective sweeps. Overall, uniparental inheritance promotes adaptive evolution by increasing the level of beneficial substitutions relative to deleterious substitutions. When we assume that cytoplasmic genome inheritance is biparental, decreasing the number of genomes transmitted during gametogenesis (bottleneck) aids adaptive evolution. Nevertheless, adaptive evolution is always more efficient when inheritance is uniparental. Our findings explain empirical observations that cytoplasmic genomes-despite their asexual mode of reproduction-can readily undergo adaptive evolution.
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Affiliation(s)
- Joshua R Christie
- School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia
| | - Madeleine Beekman
- School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia
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18
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Sex initiates adaptive evolution by recombination between beneficial loci. PLoS One 2017; 12:e0177895. [PMID: 28575015 PMCID: PMC5456038 DOI: 10.1371/journal.pone.0177895] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/28/2016] [Accepted: 05/04/2017] [Indexed: 11/19/2022] Open
Abstract
Current theory proposes that sex can increase genetic variation and produce high fitness genotypes if genetic associations between alleles at different loci are non-random. In case beneficial and deleterious alleles at different loci are in linkage disequilibrium, sex may i) recombine beneficial alleles of different loci, ii) liberate beneficial alleles from genetic backgrounds of low fitness, or iii) recombine deleterious mutations for more effective elimination. In our study, we found that the first mechanism dominated the initial phase of adaptive evolution in Brachionus calyciflorus rotifers during a natural selection experiment. We used populations that had been locally adapted to two environments previously, creating a linkage disequilibrium between beneficial and deleterious alleles at different loci in a combined environment. We observed the highest fitness increase when several beneficial alleles of different loci could be recombined, while the other mechanisms were ineffective. Our study thus provides evidence for the hypothesis that sex can speed up adaptation by recombination between beneficial alleles of different loci, in particular during early stages of adaptive evolution in our system. We also suggest that the benefits of sex might change over time and state of adaptive progress.
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19
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Dubé CE, Boissin E, Maynard JA, Planes S. Fire coral clones demonstrate phenotypic plasticity among reef habitats. Mol Ecol 2017; 26:3860-3869. [DOI: 10.1111/mec.14165] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/01/2016] [Revised: 03/02/2017] [Accepted: 04/24/2017] [Indexed: 11/29/2022]
Affiliation(s)
- Caroline E. Dubé
- PSL Research University; EPHE-UPVD-CNRS; USR 3278 CRIOBE; Université de Perpignan; Perpignan France
- Laboratoire d'Excellence “CORAIL”; Perpignan France
| | - Emilie Boissin
- PSL Research University; EPHE-UPVD-CNRS; USR 3278 CRIOBE; Université de Perpignan; Perpignan France
- Laboratoire d'Excellence “CORAIL”; Perpignan France
| | - Jeffrey A. Maynard
- Laboratoire d'Excellence “CORAIL”; Perpignan France
- SymbioSeas and Marine Applied Research Center; Wilmington NC USA
| | - Serge Planes
- PSL Research University; EPHE-UPVD-CNRS; USR 3278 CRIOBE; Université de Perpignan; Perpignan France
- Laboratoire d'Excellence “CORAIL”; Perpignan France
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20
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Ledón-Rettig CC, Zattara EE, Moczek AP. Asymmetric interactions between doublesex and tissue- and sex-specific target genes mediate sexual dimorphism in beetles. Nat Commun 2017; 8:14593. [PMID: 28239147 PMCID: PMC5333360 DOI: 10.1038/ncomms14593] [Citation(s) in RCA: 52] [Impact Index Per Article: 6.5] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/22/2016] [Accepted: 01/11/2017] [Indexed: 12/29/2022] Open
Abstract
Sexual dimorphisms fuel significant intraspecific variation and evolutionary diversification. Yet the developmental-genetic mechanisms underlying sex-specific development remain poorly understood. Here, we focus on the conserved sex-determination gene doublesex (dsx) and the mechanisms by which it mediates sex-specific development in a horned beetle species by combining systemic dsx knockdown, high-throughput sequencing of diverse tissues and a genome-wide analysis of Dsx-binding sites. We find that Dsx regulates sex-biased expression predominantly in males, that Dsx's target repertoires are highly sex- and tissue-specific and that Dsx can exercise its regulatory role via two distinct mechanisms: as a sex-specific modulator by regulating strictly sex-specific targets, or as a switch by regulating the same genes in males and females in opposite directions. More generally, our results suggest Dsx can rapidly acquire new target gene repertoires to accommodate evolutionarily novel traits, evidenced by the large and unique repertoire identified in head horns, a recent morphological innovation.
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Affiliation(s)
- C. C. Ledón-Rettig
- Department of Biology, Indiana University, 915 E. Third Street, Myers Hall 150, Bloomington, Indiana 47405-7107, USA
| | - E. E. Zattara
- Department of Biology, Indiana University, 915 E. Third Street, Myers Hall 150, Bloomington, Indiana 47405-7107, USA
| | - A. P. Moczek
- Department of Biology, Indiana University, 915 E. Third Street, Myers Hall 150, Bloomington, Indiana 47405-7107, USA
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21
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Chauhan P, Wellenreuther M, Hansson B. Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression. BMC Genomics 2016; 17:985. [PMID: 27905879 PMCID: PMC5131402 DOI: 10.1186/s12864-016-3334-6] [Citation(s) in RCA: 23] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/17/2016] [Accepted: 11/23/2016] [Indexed: 12/25/2022] Open
Abstract
Background Sexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-limited colour polymorphism with two female-like gynochrome morphs and one male-mimicking, androchrome morph. Whole-organism transcriptome profiling and sex-biased gene expression analysis was conducted on adults of both sexes (pooling all females as well as separating the three morphs) to gain insights into genes and pathways potentially associated with sexual development and sexual conflict. Results The de novo transcriptome assembly was of high quality and completeness (54 k transcripts; 99.6% CEGMA score; 55% annotated). We identified transcripts of several relevant pathways, including transcripts involved in sex determination, hormone biosynthesis, pigmentation and innate immune signalling. A total of 1,683 genes were differentially expressed (DE) between males and all females (1,173 were female-biased; 510 male-biased). The DE genes were associated with sex-specific physiological and reproductive processes, olfaction, pigmentation (ommochrome and melanin), hormone (ecdysone) biosynthesis and innate immunity signalling pathways. Comparisons between males and each female morph category showed that the gynochromes differed more from males than the androchrome morph. Conclusions This is the first study to characterize sex-biased gene expression in odonates, one of the most ancient extant insect orders. Comparison between I. elegans sexes revealed expression differences in several genes related to sexual differences in behaviour and development as well as morphology. The differential expression of several olfactory genes suggests interesting sexual components in the detection of odours, pheromones and environmental volatiles. Up-regulation of pigmentation pathways in females indicates a prominent role of ommochrome pigments in the formation of the genetically controlled female colour polymorphism. Finally, the female-biased expression of several immunity genes suggests a stronger immune response in females, possibly related to the high levels of male mating harassment and recurrent matings in this species, both of which have been shown to injure females and expose them to sexually transmitted diseases and toxins contained in seminal fluids. Electronic supplementary material The online version of this article (doi:10.1186/s12864-016-3334-6) contains supplementary material, which is available to authorized users.
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Affiliation(s)
| | - Maren Wellenreuther
- Department of Biology, Lund University, Lund, Sweden.,Institute for Plant and Food Research, Nelson, New Zealand
| | - Bengt Hansson
- Department of Biology, Lund University, Lund, Sweden.
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22
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Klastersky J, Paesmans M, Aoun M, Georgala A, Loizidou A, Lalami Y, Dal Lago L. Clinical research in febrile neutropenia in cancer patients: Past achievements and perspectives for the future. World J Clin Infect Dis 2016; 6:37-60. [DOI: 10.5495/wjcid.v6.i3.37] [Citation(s) in RCA: 6] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 06/30/2015] [Revised: 12/02/2015] [Accepted: 06/03/2016] [Indexed: 02/06/2023] Open
Abstract
Febrile neutropenia (FN) is responsible for significant morbidity and mortality. It can also be the reason for delaying or changing potentially effective treatments and generates substantial costs. It has been recognized for more than 50 years that empirical administration of broad spectrum antibiotics to patients with FN was associated with much improved outcomes; that has become a paradigm of management. Increase in the incidence of microorganisms resistant to many antibiotics represents a challenge for the empirical antimicrobial treatment and is a reason why antibiotics should not be used for the prevention of neutropenia. Prevention of neutropenia is best performed with the use of granulocyte colony-stimulating factors (G-CSFs). Prophylactic administration of G-CSFs significantly reduces the risk of developing FN and consequently the complications linked to that condition; moreover, the administration of G-CSF is associated with few complications, most of which are not severe. The most common reason for not using G-CSF as a prophylaxis of FN is the relatively high cost. If FN occurs, in spite of prophylaxis, empirical therapy with broad spectrum antibiotics is mandatory. However it should be adjusted to the risk of complications as established by reliable predictive instruments such as the Multinational Association for Supportive Care in Cancer. Patients predicted at a low level of risk of serious complications, can generally be treated with orally administered antibiotics and as out-patients. Patients with a high risk of complications should be hospitalized and treated intravenously. A short period of time between the onset of FN and beginning of empirical therapy is crucial in those patients. Persisting fever in spite of antimicrobial therapy in neutropenic patients requires a special diagnostic attention, since invasive fungal infection is a possible cause for it and might require the use of empirical antifungal therapy.
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23
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McDonald MJ, Rice DP, Desai MM. Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 2016; 531:233-6. [PMID: 26909573 PMCID: PMC4855304 DOI: 10.1038/nature17143] [Citation(s) in RCA: 210] [Impact Index Per Article: 23.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 05/21/2015] [Accepted: 01/20/2016] [Indexed: 12/30/2022]
Abstract
Sex and recombination are pervasive throughout nature despite their substantial costs1. Understanding the evolutionary forces that maintain these phenomena is a central challenge in biology2,3. One longstanding hypothesis argues that sex is beneficial because recombination speeds adaptation4. Theory has proposed a number of distinct population genetic mechanisms that could underlie this advantage. For example, sex can promote the fixation of beneficial mutations either by alleviating interference competition (the Fisher-Muller effect)5,6 or by separating them from deleterious load (the ruby in the rubbish effect)7,8. Previous experiments confirm that sex can increase the rate of adaptation9–17, but these studies did not observe the evolutionary dynamics that drive this effect at the genomic level. Here, we present the first comparison between the sequence-level dynamics of adaptation in experimental sexual and asexual populations, which allows us to identify the specific mechanisms by which sex speeds adaptation. We find that sex alters the molecular signatures of evolution by changing the spectrum of mutations that fix, and confirm theoretical predictions that it does so by alleviating clonal interference. We also show that substantially deleterious mutations hitchhike to fixation in adapting asexual populations. In contrast, recombination prevents such mutations from fixing. Our results demonstrate that sex both speeds adaptation and alters its molecular signature by allowing natural selection to more efficiently sort beneficial from deleterious mutations.
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Affiliation(s)
- Michael J McDonald
- Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.,FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA
| | - Daniel P Rice
- Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.,FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA
| | - Michael M Desai
- Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA.,FAS Center for Systems Biology, Harvard University, Cambridge, Massachusetts 02138, USA.,Department of Physics, Harvard University, Cambridge, Massachusetts 02138, USA
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24
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Aggarwal DD, Rashkovetsky E, Michalak P, Cohen I, Ronin Y, Zhou D, Haddad GG, Korol AB. Experimental evolution of recombination and crossover interference in Drosophila caused by directional selection for stress-related traits. BMC Biol 2015; 13:101. [PMID: 26614097 PMCID: PMC4661966 DOI: 10.1186/s12915-015-0206-5] [Citation(s) in RCA: 24] [Impact Index Per Article: 2.4] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2015] [Accepted: 10/27/2015] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Population genetics predicts that tight linkage between new and/or pre-existing beneficial and deleterious alleles should decrease the efficiency of natural selection in finite populations. By decoupling beneficial and deleterious alleles and facilitating the combination of beneficial alleles, recombination accelerates the formation of high-fitness genotypes. This may impose indirect selection for increased recombination. Despite the progress in theoretical understanding, interplay between recombination and selection remains a controversial issue in evolutionary biology. Even less satisfactory is the situation with crossover interference, which is a deviation of double-crossover frequency in a pair of adjacent intervals from the product of recombination rates in the two intervals expected on the assumption of crossover independence. Here, we report substantial changes in recombination and interference in three long-term directional selection experiments with Drosophila melanogaster: for desiccation (~50 generations), hypoxia, and hyperoxia tolerance (>200 generations each). RESULTS For all three experiments, we found a high interval-specific increase of recombination frequencies in selection lines (up to 40-50% per interval) compared to the control lines. We also discovered a profound effect of selection on interference as expressed by an increased frequency of double crossovers in selection lines. Our results show that changes in interference are not necessarily coupled with increased recombination. CONCLUSIONS Our results support the theoretical predictions that adaptation to a new environment can promote evolution toward higher recombination. Moreover, this is the first evidence of selection for different recombination-unrelated traits potentially leading, not only to evolution toward increased crossover rates, but also to changes in crossover interference, one of the fundamental features of recombination.
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Affiliation(s)
| | | | - Pawel Michalak
- Virginia Bioinformatics Institute, Virginia Tech, Washington Street, MC 0477, Blacksburg, VA, 24061-0477, USA
| | - Irit Cohen
- Institute of Evolution, University of Haifa, Haifa, 3498838, Israel
| | - Yefim Ronin
- Institute of Evolution, University of Haifa, Haifa, 3498838, Israel
| | - Dan Zhou
- University of California, San Diego, USA
| | - Gabriel G Haddad
- University of California, San Diego, USA
- Rady Children's Hospital, San Diego, USA
| | - Abraham B Korol
- Institute of Evolution, University of Haifa, Haifa, 3498838, Israel.
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25
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Reding L, Cummings ME. Does sensory expansion benefit asexual species? An olfactory discrimination test in Amazon mollies. Behav Ecol 2015. [DOI: 10.1093/beheco/arv168] [Citation(s) in RCA: 5] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/13/2022] Open
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Carranza J, Polo V. Sexual reproduction with variable mating systems can resist asexuality in a rock-paper-scissors dynamics. ROYAL SOCIETY OPEN SCIENCE 2015; 2:140383. [PMID: 26587254 PMCID: PMC4632567 DOI: 10.1098/rsos.140383] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Figures] [Subscribe] [Scholar Register] [Received: 10/29/2014] [Accepted: 06/18/2015] [Indexed: 06/05/2023]
Abstract
While sex can be advantageous for a lineage in the long term, we still lack an explanation for its maintenance with the twofold cost per generation. Here we model an infinite diploid population where two autosomal loci determine, respectively, the reproductive mode, sexual versus asexual and the mating system, polygynous (costly sex) versus monogamous (assuming equal contribution of parents to offspring, i.e. non-costly sex). We show that alleles for costly sex can spread when non-costly sexual modes buffer the interaction between asexual and costly sexual strategies, even without twofold benefit of recombination with respect to asexuality. The three interacting strategies have intransitive fitness relationships leading to a rock-paper-scissors dynamics, so that alleles for costly sex cannot be eliminated by asexuals in most situations throughout the parameter space. Our results indicate that sexual lineages with variable mating systems can resist the invasion of asexuals and allow for long-term effects to accumulate, thus providing a solution to the persisting theoretical question of why sex was not displaced by asexuality along evolution.
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Affiliation(s)
- Juan Carranza
- Department of Zoology, CRCP Research Center, University of Córdoba, Córdoba 14071, Spain
- Biology and Ethology Unit, University of Extremadura, Cáceres 10071, Spain
| | - Vicente Polo
- Departamento de Biología y Geología del Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y Tecnología (ESCET), Universidad Rey Juan Carlos, Madrid, Spain
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Kleiman M, Hadany L. The evolution of obligate sex: the roles of sexual selection and recombination. Ecol Evol 2015; 5:2572-83. [PMID: 26257871 PMCID: PMC4523354 DOI: 10.1002/ece3.1516] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.7] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/02/2015] [Revised: 04/20/2015] [Accepted: 04/23/2015] [Indexed: 11/20/2022] Open
Abstract
The evolution of sex is one of the greatest mysteries in evolutionary biology. An even greater mystery is the evolution of obligate sex, particularly when competing with facultative sex and not with complete asexuality. Here, we develop a stochastic simulation of an obligate allele invading a facultative population, where males are subject to sexual selection. We identify a range of parameters where sexual selection can contribute to the evolution of obligate sex: Especially when the cost of sex is low, mutation rate is high, and the facultative individuals do not reproduce sexually very often. The advantage of obligate sex becomes larger in the absence of recombination. Surprisingly, obligate sex can take over even when the population has a lower mean fitness as a result. We show that this is due to the high success of obligate males that can compensate the cost of sex.
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Affiliation(s)
- Maya Kleiman
- Department of Chemistry, Ben-Gurion University of the Negev Be'er-Sheva, 8410501, Israel
| | - Lilach Hadany
- Department of Molecular Biology and Ecology of Plants, Faculty of Life Sciences, Tel Aviv University Ramat Aviv, 69978, Israel
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Abstract
Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28 °C (current ambient mean spawning temperature) and 33 °C (projected for the year 2100). The EDC selected was clotrimazole (at 2 μg/L and 10 μg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced male-skewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.
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29
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Mitrokhin Y. Two faces of entropy and information in biological systems. J Theor Biol 2014; 359:192-8. [DOI: 10.1016/j.jtbi.2014.06.018] [Citation(s) in RCA: 7] [Impact Index Per Article: 0.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/14/2014] [Revised: 05/30/2014] [Accepted: 06/12/2014] [Indexed: 10/25/2022]
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Cao K, Zheng Z, Wang L, Liu X, Zhu G, Fang W, Cheng S, Zeng P, Chen C, Wang X, Xie M, Zhong X, Wang X, Zhao P, Bian C, Zhu Y, Zhang J, Ma G, Chen C, Li Y, Hao F, Li Y, Huang G, Li Y, Li H, Guo J, Xu X, Wang J. Comparative population genomics reveals the domestication history of the peach, Prunus persica, and human influences on perennial fruit crops. Genome Biol 2014; 15:415. [PMID: 25079967 PMCID: PMC4174323 DOI: 10.1186/s13059-014-0415-1] [Citation(s) in RCA: 75] [Impact Index Per Article: 6.8] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 02/25/2014] [Accepted: 07/15/2014] [Indexed: 12/24/2022] Open
Abstract
Background Recently, many studies utilizing next generation sequencing have investigated
plant evolution and domestication in annual crops. Peach, Prunus persica, is a typical perennial fruit crop that has
ornamental and edible varieties. Unlike other fruit crops, cultivated peach
includes a large number of phenotypes but few polymorphisms. In this study, we
explore the genetic basis of domestication in peach and the influence of humans on
its evolution. Results We perform large-scale resequencing of 10 wild and 74 cultivated peach
varieties, including 9 ornamental, 23 breeding, and 42 landrace lines. We identify
4.6 million SNPs, a large number of which could explain the phenotypic variation
in cultivated peach. Population analysis shows a single domestication event, the
speciation of P. persica from wild peach.
Ornamental and edible peach both belong to P.
persica, along with another geographically separated subgroup,
Prunus ferganensis. We identify 147 and 262 genes under edible and ornamental selection,
respectively. Some of these genes are associated with important biological
features. We perform a population heterozygosity analysis in different plants that
indicates that free recombination effects could affect domestication history. By
applying artificial selection during the domestication of the peach and
facilitating its asexual propagation, humans have caused a sharp decline of the
heterozygote ratio of SNPs. Conclusions Our analyses enhance our knowledge of the domestication history of perennial
fruit crops, and the dataset we generated could be useful for future research on
comparative population genomics. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0415-1) contains supplementary material, which is available to authorized
users.
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31
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Moradigaravand D, Kouyos R, Hinkley T, Haddad M, Petropoulos CJ, Engelstädter J, Bonhoeffer S. Recombination accelerates adaptation on a large-scale empirical fitness landscape in HIV-1. PLoS Genet 2014; 10:e1004439. [PMID: 24967626 PMCID: PMC4072600 DOI: 10.1371/journal.pgen.1004439] [Citation(s) in RCA: 32] [Impact Index Per Article: 2.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/07/2014] [Accepted: 04/30/2014] [Indexed: 01/18/2023] Open
Abstract
Recombination has the potential to facilitate adaptation. In spite of the substantial body of theory on the impact of recombination on the evolutionary dynamics of adapting populations, empirical evidence to test these theories is still scarce. We examined the effect of recombination on adaptation on a large-scale empirical fitness landscape in HIV-1 based on in vitro fitness measurements. Our results indicate that recombination substantially increases the rate of adaptation under a wide range of parameter values for population size, mutation rate and recombination rate. The accelerating effect of recombination is stronger for intermediate mutation rates but increases in a monotonic way with the recombination rates and population sizes that we examined. We also found that both fitness effects of individual mutations and epistatic fitness interactions cause recombination to accelerate adaptation. The estimated epistasis in the adapting populations is significantly negative. Our results highlight the importance of recombination in the evolution of HIV-I. One of the most challenging issues in evolutionary biology concerns the question of why most organisms exchange genetic material with each other, e.g. during sexual reproduction. Gene shuffling can create genetic diversity that facilitates adaptation to new environments, but theory shows that this effect is highly dependent on how different genes interact in determining the fitness of an organism. Using a large data set of fitness values based on HIV-1, we provide evidence that shuffling of genetic material indeed raises the level of genetic diversity, and as a result accelerates adaptation. Our results also propose genetic shuffling as a mechanism utilized by HIV to accelerate the evolution of multi-drug-resistant strains.
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Affiliation(s)
- Danesh Moradigaravand
- Institute of Biogeochemistry and Pollutant Dynamics, ETH Zürich, Zürich, Switzerland
- * E-mail: (DM); (SB)
| | - Roger Kouyos
- Division of Infectious Diseases and Hospital Epidemiology, University Hospital Zürich, University of Zürich, Zürich, Switzerland
| | - Trevor Hinkley
- WestCHEM, School of Chemistry, The University of Glasgow, Glasgow, Scotland, United Kingdom
| | - Mojgan Haddad
- Monogram Biosciences, South San Francisco, California, United States of America
| | | | - Jan Engelstädter
- School of Biological Sciences, The University of Queensland, Brisbane, Queensland, Australia
| | - Sebastian Bonhoeffer
- Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland
- * E-mail: (DM); (SB)
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Chelo IM, Nédli J, Gordo I, Teotónio H. An experimental test on the probability of extinction of new genetic variants. Nat Commun 2014; 4:2417. [PMID: 24030070 PMCID: PMC3778522 DOI: 10.1038/ncomms3417] [Citation(s) in RCA: 21] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/01/2012] [Accepted: 08/08/2013] [Indexed: 11/09/2022] Open
Abstract
In 1927, J.B.S. Haldane reasoned that the probability of fixation of new beneficial alleles is twice their fitness effect. This result, later generalized by M. Kimura, has since become the cornerstone of modern population genetics. There is no experimental test of Haldane's insight that new beneficial alleles are lost with high probability. Here we demonstrate that extinction rates decrease with increasing initial numbers of beneficial alleles, as expected, by performing invasion experiments with inbred lines of the nematode Caenorhabditis elegans. We further show that the extinction rates of deleterious alleles are higher than those of beneficial alleles, also as expected. Interestingly, we also find that for these inbred lines, when at intermediate frequencies, the fate of invaders might not result in their ultimate fixation or loss but on their maintenance. Our study confirms the key results from classical population genetics and highlights that the nature of adaptation can be complex.
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Affiliation(s)
- Ivo M Chelo
- Instituto Gulbenkian de Ciência, Apartado 14, P-2781-901 Oeiras, Portugal
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33
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Neher RA. Genetic Draft, Selective Interference, and Population Genetics of Rapid Adaptation. ANNUAL REVIEW OF ECOLOGY EVOLUTION AND SYSTEMATICS 2013. [DOI: 10.1146/annurev-ecolsys-110512-135920] [Citation(s) in RCA: 134] [Impact Index Per Article: 11.2] [Reference Citation Analysis] [Track Full Text] [Subscribe] [Scholar Register] [Indexed: 11/09/2022]
Affiliation(s)
- Richard A. Neher
- Max Planck Institute for Developmental Biology, Tübingen 72070, Germany;
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34
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Tarka M, Akesson M, Hasselquist D, Hansson B. Intralocus sexual conflict over wing length in a wild migratory bird. Am Nat 2013; 183:62-73. [PMID: 24334736 DOI: 10.1086/674072] [Citation(s) in RCA: 49] [Impact Index Per Article: 4.1] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/04/2022]
Abstract
Intralocus sexual conflict (ISC) occurs when males and females have different adaptive peaks but are constrained from evolving sexual dimorphism because of shared genes. Implications of this conflict on evolutionary dynamics in wild populations have not been investigated in detail. In comprehensive analyses of selection, heritability, and genetic correlations, we found evidence for an ISC over wing length, a key trait for flight performance and migration, in a long-term study of wild great reed warblers (Acrocephalus arundinaceus). We found moderate sexual dimorphism, high heritability, moderate sexually antagonistic selection, and strong positive cross-sex genetic correlation in wing length, together supporting the presence of ISC. A negative genetic correlation between male wing length and female fitness indicated that females inheriting alleles for longer wings from their male relatives also inherited lower fitness. Moreover, cross-sex genetic correlations imposed constraint on the predicted microevolutionary trajectory of wing length (based on selection gradients), especially in females where the predicted response was reversed. The degree of sexual dimorphism in wing length did not change over time, suggesting no sign of conflict resolution. Our study provides novel insight into how an ISC over a fitness trait can affect microevolution in a wild population under natural selection.
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Affiliation(s)
- Maja Tarka
- Department of Biology, Lund University, SE-223 62 Lund, Sweden
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35
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Dennehy JJ, Duffy S, O'Keefe KJ, Edwards SV, Turner PE. Frequent Coinfection Reduces RNA Virus Population Genetic Diversity. J Hered 2013; 104:704-12. [DOI: 10.1093/jhered/est038] [Citation(s) in RCA: 17] [Impact Index Per Article: 1.4] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/14/2022] Open
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36
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Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration. Nat Rev Genet 2013; 14:113-24. [PMID: 23329112 DOI: 10.1038/nrg3366] [Citation(s) in RCA: 545] [Impact Index Per Article: 45.4] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 12/24/2022]
Abstract
The human Y chromosome is intriguing not only because it harbours the master-switch gene that determines gender but also because of its unusual evolutionary history. The Y chromosome evolved from an autosome, and its evolution has been characterized by massive gene decay. Recent whole-genome and transcriptome analyses of Y chromosomes in humans and other primates, in Drosophila species and in plants have shed light on the current gene content of the Y chromosome, its origins and its long-term fate. Furthermore, comparative analysis of young and old Y chromosomes has given further insights into the evolutionary and molecular forces triggering Y-chromosome degeneration and into the evolutionary destiny of the Y chromosome.
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Abstract
The evolution of sex is one of the most important and controversial problems in evolutionary biology. Although sex is almost universal in higher animals and plants, its inherent costs have made its maintenance difficult to explain. The most famous of these is the twofold cost of males, which can greatly reduce the fecundity of a sexual population, compared to a population of asexual females. Over the past century, multiple hypotheses, along with experimental evidence to support these, have been put forward to explain widespread costly sex. In this review, we outline some of the most prominent theories, along with the experimental and observational evidence supporting these. Historically, there have been 4 classes of theories: the ability of sex to fix multiple novel advantageous mutants (Fisher-Muller hypothesis); sex as a mechanism to stop the build-up of deleterious mutations in finite populations (Muller's ratchet); recombination creating novel genotypes that can resist infection by parasites (Red Queen hypothesis); and the ability of sex to purge bad genomes if deleterious mutations act synergistically (mutational deterministic hypothesis). Current theoretical and experimental evidence seems to favor the hypothesis that sex breaks down selection interference between new mutants, or it acts as a mechanism to shuffle genotypes in order to repel parasitic invasion. However, there is still a need to collect more data from natural populations and experimental studies, which can be used to test different hypotheses.
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Affiliation(s)
- Matthew Hartfield
- Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, UK
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38
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Abstract
The spirochetes in the Borrelia burgdorferi sensu lato genospecies group cycle in nature between tick vectors and vertebrate hosts. The current assemblage of B. burgdorferi sensu lato, of which three species cause Lyme disease in humans, originated from a rapid species radiation that occurred near the origin of the clade. All of these species share a unique genome structure that is highly segmented and predominantly composed of linear replicons. One of the circular plasmids is a prophage that exists as several isoforms in each cell and can be transduced to other cells, likely contributing to an otherwise relatively anemic level of horizontal gene transfer, which nevertheless appears to be adequate to permit strong natural selection and adaptation in populations of B. burgdorferi. Although the molecular genetic toolbox is meager, several antibiotic-resistant mutants have been isolated, and the resistance alleles, as well as some exogenous genes, have been fashioned into markers to dissect gene function. Genetic studies have probed the role of the outer membrane lipoprotein OspC, which is maintained in nature by multiple niche polymorphisms and negative frequency-dependent selection. One of the most intriguing genetic systems in B. burgdorferi is vls recombination, which generates antigenic variation during infection of mammalian hosts.
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MESH Headings
- Alleles
- Animals
- Antigenic Variation
- Antigens, Bacterial/genetics
- Antigens, Bacterial/immunology
- Antigens, Bacterial/metabolism
- Bacterial Outer Membrane Proteins/genetics
- Bacterial Outer Membrane Proteins/metabolism
- Bacterial Proteins/genetics
- Bacterial Proteins/immunology
- Bacterial Proteins/metabolism
- Bacteriophages/genetics
- Bacteriophages/metabolism
- Bacteriophages/pathogenicity
- Borrelia burgdorferi/genetics
- Borrelia burgdorferi/immunology
- Borrelia burgdorferi/pathogenicity
- Borrelia burgdorferi/virology
- DNA, Bacterial/genetics
- DNA, Bacterial/metabolism
- Electroporation
- Evolution, Molecular
- Genes, Bacterial
- Genetic Variation
- Humans
- Ixodes/microbiology
- Linkage Disequilibrium
- Lipoproteins/genetics
- Lipoproteins/immunology
- Lipoproteins/metabolism
- Lyme Disease/microbiology
- Plasmids/genetics
- Plasmids/metabolism
- Prophages/genetics
- Prophages/metabolism
- Recombination, Genetic
- Selection, Genetic
- Species Specificity
- Transduction, Genetic
- Transformation, Genetic
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Affiliation(s)
- Dustin Brisson
- Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104
| | - Dan Drecktrah
- Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
| | - Christian H. Eggers
- Department of Biomedical Sciences, Quinnipiac University, Hamden, Connecticut 06518
| | - D. Scott Samuels
- Division of Biological Sciences, The University of Montana, Missoula, Montana 59812
- Center for Biomolecular Structure and Dynamics, The University of Montana, Missoula, Montana 59812
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39
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Becks L, Agrawal AF. The evolution of sex is favoured during adaptation to new environments. PLoS Biol 2012; 10:e1001317. [PMID: 22563299 PMCID: PMC3341334 DOI: 10.1371/journal.pbio.1001317] [Citation(s) in RCA: 91] [Impact Index Per Article: 7.0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/17/2011] [Accepted: 03/20/2012] [Indexed: 11/18/2022] Open
Abstract
Both theory and experiments have demonstrated that sex can facilitate adaptation, potentially yielding a group-level advantage to sex. However, it is unclear whether this process can help solve the more difficult problem of the maintenance of sex within populations. Using experimental populations of the facultatively sexual rotifer Brachionus calyciflorus, we show that rates of sex evolve to higher levels during adaptation but then decline as fitness plateaus. To assess the fitness consequences of genetic mixing, we directly compare the fitnesses of sexually and asexually derived genotypes that naturally occur in our experimental populations. Sexually derived genotypes are more fit than asexually derived genotypes when adaptive pressures are strong, but this pattern reverses as the pace of adaptation slows, matching the pattern of evolutionary change in the rate of sex. These fitness assays test the net effect of sex but cannot be used to disentangle whether selection on sex arises because highly sexual lineages become associated with different allele combinations or with different allele frequencies than less sexual lineages (i.e., "short-" or "long-term" effects, respectively). We infer which of these mechanisms provides an advantage to sex by performing additional manipulations to obtain fitness distributions of sexual and asexual progeny arrays from unbiased parents (rather than from naturally occurring, and thereby evolutionarily biased, parents). We find evidence that sex breaks down adaptive gene combinations, resulting in lower average fitness of sexual progeny (i.e., a short-term disadvantage to sex). As predicted by theory, the advantage to sex arises because sexually derived progeny are more variable in fitness, allowing for faster adaptation. This "long-term advantage" builds over multiple generations, eventually resulting in higher fitness of sexual types.
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Affiliation(s)
- Lutz Becks
- Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada.
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40
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Gray JC, Goddard MR. Sex enhances adaptation by unlinking beneficial from detrimental mutations in experimental yeast populations. BMC Evol Biol 2012; 12:43. [PMID: 22462622 PMCID: PMC3342131 DOI: 10.1186/1471-2148-12-43] [Citation(s) in RCA: 49] [Impact Index Per Article: 3.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 10/20/2011] [Accepted: 03/30/2012] [Indexed: 11/11/2022] Open
Abstract
BACKGROUND The maintenance of sexuality is a classic problem in evolutionary biology because it is a less efficient mode of reproduction compared with asexuality; however, many organisms are sexual. Theoretical work suggests sex facilitates natural selection, and experimental data support this. However, there are fewer experimental studies that have attempted to determine the mechanisms underlying the advantage of sex. Two main classes of hypotheses have been proposed to explain its advantage: detrimental mutation clearance and beneficial mutation accumulation. Here we attempt to experimentally differentiate between these two classes by evolving Saccharomyces cerevisiae populations that differ only in their ability to undergo sex, and also manipulate mutation rate. We cannot manipulate the types of mutation that occur, but instead propagate populations in both stressful and permissive environments and assume that the extent of detrimental mutation clearance and beneficial mutation incorporation differs between them. RESULTS After 300 mitotic generations interspersed with 11 rounds of sex we found there was no change or difference in fitness between sexuals and asexuals propagated in the permissive environment, regardless of mutation rate. Sex conferred a greater extent of adaptation in the stressful environment, and wild-type and elevated mutation rate sexual populations adapted equivalently. However, the asexual populations with an elevated mutation rate appeared more retarded in their extent of adaptation compared to asexual wild-type populations. CONCLUSIONS Sex provided no advantage in the permissive environment where beneficial mutations were rare. We could not evaluate if sex functioned to clear detrimental mutations more effectively or not here as no additional fitness load was observed in the mutator populations. However, in the stressful environment, where detrimental mutations were likely of more consequence, and where beneficial mutations were apparent, sex provided an advantage. In the stressful environment asexuals were increasingly constrained in their extent of adaptation with increasing mutation rate. Sex appeared to facilitate adaptation not just by more rapidly combining beneficial mutations, but also by unlinking beneficial from detrimental mutations: sex allowed selection to operate on both types of mutations more effectively compared to asexual populations.
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Affiliation(s)
- Jeremy C Gray
- School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland Mail Centre, Auckland 1142, New Zealand
| | - Matthew R Goddard
- School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland Mail Centre, Auckland 1142, New Zealand
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41
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Melián CJ, Alonso D, Allesina S, Condit RS, Etienne RS. Does sex speed up evolutionary rate and increase biodiversity? PLoS Comput Biol 2012; 8:e1002414. [PMID: 22412362 PMCID: PMC3297559 DOI: 10.1371/journal.pcbi.1002414] [Citation(s) in RCA: 15] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/04/2011] [Accepted: 01/20/2012] [Indexed: 01/22/2023] Open
Abstract
Most empirical and theoretical studies have shown that sex increases the rate of evolution, although evidence of sex constraining genomic and epigenetic variation and slowing down evolution also exists. Faster rates with sex have been attributed to new gene combinations, removal of deleterious mutations, and adaptation to heterogeneous environments. Slower rates with sex have been attributed to removal of major genetic rearrangements, the cost of finding a mate, vulnerability to predation, and exposure to sexually transmitted diseases. Whether sex speeds or slows evolution, the connection between reproductive mode, the evolutionary rate, and species diversity remains largely unexplored. Here we present a spatially explicit model of ecological and evolutionary dynamics based on DNA sequence change to study the connection between mutation, speciation, and the resulting biodiversity in sexual and asexual populations. We show that faster speciation can decrease the abundance of newly formed species and thus decrease long-term biodiversity. In this way, sex can reduce diversity relative to asexual populations, because it leads to a higher rate of production of new species, but with lower abundances. Our results show that reproductive mode and the mechanisms underlying it can alter the link between mutation, evolutionary rate, speciation and biodiversity and we suggest that a high rate of evolution may not be required to yield high biodiversity. The role of sex in driving genetic variation and the speed at which new species emerge has been debated for over a century. There is experimental and theoretical evidence that sex increases genetic variation and the speed at which new species emerge, although evidence that sex reduces variation and slows the formation of new species also exists. Surprisingly, given the link between sex and genetic variation, little work has been done on the impact of sex on biodiversity. In the present theoretical study we show that a faster evolutionary rate can decrease the abundance of newly formed species and thus decrease long-term biodiversity. This leads to the paradoxical result that sexual reproduction can increase genetic variation but reduce species diversity. These results suggest that reducing the rate of appearance of genetic variation and the speed at which new species emerge may increase biodiversity in the long-term. This unexpected link between reproductive mode, the speed of evolution and biodiversity suggests that a high evolutionary rate may not be required to yield a large number of species in natural ecosystems.
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Affiliation(s)
- Carlos J Melián
- National Center for Ecological Analysis and Synthesis, University of California, Santa Barbara, California, United States of America.
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42
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Dal Grande F, Widmer I, Wagner HH, Scheidegger C. Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol Ecol 2012; 21:3159-72. [PMID: 22384938 DOI: 10.1111/j.1365-294x.2012.05482.x] [Citation(s) in RCA: 87] [Impact Index Per Article: 6.7] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/28/2022]
Abstract
Lichens are widespread symbioses and play important roles in many terrestrial ecosystems. The genetic structure of lichens is the result of the association between fungal and algal populations constituting the lichen thallus. Using eight fungus- and seven alga-specific highly variable microsatellite markers on within-population spatial genetic data from 62 replicate populations across Europe, North America, Asia and Africa, we investigated the contributions of vertical and horizontal transmission of the photobiont to the genetic structure of the epiphytic lichen Lobaria pulmonaria. Based on pairwise comparisons of multilocus genotypes defined separately for the mycobiont and for the photobiont, we inferred the transmission mode of the photobiont and the relative contribution of somatic mutation and recombination. After constraining the analysis of one symbiont to pairs of individuals with genetically identical symbiotic partners, we found that 77% of fungal and 70% of algal pairs were represented by clones. Thus, the predominant dispersal mode was by means of symbiotic vegetative propagules (vertical transmission), which dispersed fungal and algal clones co-dependently over a short distance, thus shaping the spatial genetic structure up to distances of 20m. Evidence for somatic mutation generating genetic diversity was found in both symbionts, accounting for 30% of pairwise comparisons in the alga and 15% in the fungus. While the alga did not show statistically significant evidence of recombination, recombination accounted for 7.7% of fungal pairs with identical algae. This implies that, even in a mostly vegetatively reproducing species, horizontal transmission plays a role in shaping the symbiotic association, as shown in many coral and other symbioses in nature.
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Affiliation(s)
- F Dal Grande
- Biodiversity and Conservation Biology, WSL Swiss Federal Research Institute, 8903 Birmensdorf, Switzerland.
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43
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Abbott JK, Morrow EH. Obtaining snapshots of genetic variation using hemiclonal analysis. Trends Ecol Evol 2011; 26:359-68. [DOI: 10.1016/j.tree.2011.03.011] [Citation(s) in RCA: 36] [Impact Index Per Article: 2.6] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/26/2011] [Revised: 03/10/2011] [Accepted: 03/13/2011] [Indexed: 11/30/2022]
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Rodríguez-Casuriaga R, Geisinger A, Santiñaque FF, López-Carro B, Folle GA. High-purity flow sorting of early meiocytes based on DNA analysis of guinea pig spermatogenic cells. Cytometry A 2011; 79:625-34. [PMID: 21520399 DOI: 10.1002/cyto.a.21067] [Citation(s) in RCA: 14] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/01/2010] [Revised: 03/01/2011] [Accepted: 03/24/2011] [Indexed: 01/14/2023]
Abstract
Mammalian spermatogenesis is still nowadays poorly understood at the molecular level. Testis cellular heterogeneity is a major drawback for spermatogenic gene expression studies, especially when research is focused on stages that are usually very short and poorly represented at the cellular level such as initial meiotic prophase I (i.e., leptotene [L] and zygotene [Z]). Presumably, genes whose products are involved in critical meiotic events such as alignment, pairing and recombination of homologous chromosomes are expressed during the short stages of early meiotic prophase. Aiming to characterize mammalian early meiotic gene expression, we have found the guinea pig (Cavia porcellus) as an especially attractive model. A detailed analysis of its first spermatogenic wave by flow cytometry (FCM) and optical microscopy showed that guinea pig testes exhibit a higher representation of early meiotic stages compared to other studied rodents, partly because of their longer span, and also as a result of the increased number of cells entering meiosis. Moreover, we have found that adult guinea pig testes exhibit a peculiar 4C DNA content profile, with a bimodal peak for L/Z and P spermatocytes that is absent in other rodents. Besides, we show that this unusual 4C peak allows the separation by FCM of highly pure L/Z spermatocyte populations aside from pachytene ones, even from adult individuals. To our knowledge, this is the first report on an accurate and suitable method for highly pure early meiotic prophase cell isolation from adult mammals, and thus sets an interesting approach for gene expression studies aiming at a deeper understanding of the molecular groundwork underlying male gamete production.
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Affiliation(s)
- Rosana Rodríguez-Casuriaga
- Departamento de Biología Molecular, Instituto de Investigaciones Biológicas Clemente Estable (IIBCE), Montevideo, Uruguay.
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Uncoupling of sexual reproduction from homologous recombination in homozygous Oenothera species. Heredity (Edinb) 2011; 107:87-94. [PMID: 21448231 PMCID: PMC3186113 DOI: 10.1038/hdy.2010.171] [Citation(s) in RCA: 22] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/25/2022] Open
Abstract
Salient features of the first meiotic division are independent segregation of chromosomes and homologous recombination (HR). In non-sexually reproducing, homozygous species studied to date HR is absent. In this study, we constructed the first linkage maps of homozygous, bivalent-forming Oenothera species and provide evidence that HR was exclusively confined to the chromosome ends of all linkage groups in our population. Co-segregation of complementary DNA-based markers with the major group of AFLP markers indicates that HR has only a minor role in generating genetic diversity of this taxon despite its efficient adaptation capability. Uneven chromosome condensation during meiosis in Oenothera may account for restriction of HR. The use of plants with ancient chromosomal arm arrangement demonstrates that limitation of HR occurred before and independent from species hybridizations and reciprocal translocations of chromosome arms—a phenomenon, which is widespread in the genus. We propose that consecutive loss of HR favored the evolution of reciprocal translocations, beneficial superlinkage groups and ultimately permanent translocation heterozygosity.
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Arguello JR, Zhang Y, Kado T, Fan C, Zhao R, Innan H, Wang W, Long M. Recombination yet inefficient selection along the Drosophila melanogaster subgroup's fourth chromosome. Mol Biol Evol 2010; 27:848-61. [PMID: 20008457 PMCID: PMC2877538 DOI: 10.1093/molbev/msp291] [Citation(s) in RCA: 47] [Impact Index Per Article: 3.1] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 11/12/2022] Open
Abstract
A central goal of evolutionary genetics is an understanding of the forces responsible for the observed variation, both within and between species. Theoretical and empirical work have demonstrated that genetic recombination contributes to this variation by breaking down linkage between nucleotide sites, thus allowing them to behave independently and for selective forces to act efficiently on them. The Drosophila fourth chromosome, which is believed to experience no-or very low-rates of recombination has been an important model for investigating these effects. Despite previous efforts, central questions regarding the extent of recombination and the predominant modes of selection acting on it remain open. In order to more comprehensively test hypotheses regarding recombination and its potential influence on selection along the fourth chromosome, we have resequenced regions from most of its genes from Drosophila melanogaster, D. simulans, and D. yakuba. These data, along with available outgroup sequence, demonstrate that recombination is low but significantly greater than zero for the three species. Despite there being recombination, there is strong evidence that its frequency is low enough to have rendered selection relatively inefficient. The signatures of relaxed constraint can be detected at both the level of polymorphism and divergence.
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Affiliation(s)
- J. Roman Arguello
- Committee on Evolutionary Biology, University of Chicago
- Department of Ecology and Evolution, University of Chicago
| | - Yue Zhang
- State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China
| | - Tomoyuki Kado
- Hayama Center for Advanced Studies, The Graduate University for Advanced Studies, Hayama, Kanagawa, Japan
| | - Chuanzhu Fan
- Department of Ecology and Evolution, University of Chicago
| | - Ruoping Zhao
- State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China
| | - Hideki Innan
- Hayama Center for Advanced Studies, The Graduate University for Advanced Studies, Hayama, Kanagawa, Japan
| | - Wen Wang
- State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, Yunnan, China
| | - Manyuan Long
- Committee on Evolutionary Biology, University of Chicago
- Department of Ecology and Evolution, University of Chicago
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Hartfield M, Otto SP, Keightley PD. The role of advantageous mutations in enhancing the evolution of a recombination modifier. Genetics 2010; 184:1153-64. [PMID: 20139345 PMCID: PMC2865915 DOI: 10.1534/genetics.109.112920] [Citation(s) in RCA: 42] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/10/2009] [Accepted: 02/03/2010] [Indexed: 11/18/2022] Open
Abstract
Although the evolution of recombination is still a major problem in evolutionary genetics, recent theoretical studies have shown that recombination can evolve by breaking down interference ("Hill-Robertson effects") among multiple loci. This leads to selection on a recombination modifier in a population subject to recurrent deleterious mutation. Here, we use computer simulations to investigate the evolution of a recombination modifier under three different scenarios of recurrent mutation in a finite population: (1) mutations are deleterious only, (2) mutations are advantageous only, and (3) there is a mixture of deleterious and advantageous mutations. We also investigate how linkage disequilibrium, the strength of selection acting on a modifier, and effective population size change under the different scenarios. We observe that adding even a small number of advantageous mutations increases the fixation rate of modifiers that increase recombination, especially if the effects of deleterious mutations are weak. However, the strength of selection on a modifier is less than the summed strengths had there been deleterious mutations only and advantageous mutations only.
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Affiliation(s)
- Matthew Hartfield
- Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United Kingdom.
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Benatti TR, Valicente FH, Aggarwal R, Zhao C, Walling JG, Chen MS, Cambron SE, Schemerhorn BJ, Stuart JJ. A neo-sex chromosome that drives postzygotic sex determination in the hessian fly (Mayetiola destructor). Genetics 2010; 184:769-77. [PMID: 20026681 PMCID: PMC2845344 DOI: 10.1534/genetics.109.108589] [Citation(s) in RCA: 28] [Impact Index Per Article: 1.9] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 08/13/2009] [Accepted: 12/11/2009] [Indexed: 11/18/2022] Open
Abstract
Two nonoverlapping autosomal inversions defined unusual neo-sex chromosomes in the Hessian fly (Mayetiola destructor). Like other neo-sex chromosomes, these were normally heterozygous, present only in one sex, and suppressed recombination around a sex-determining master switch. Their unusual properties originated from the anomalous Hessian fly sex determination system in which postzygotic chromosome elimination is used to establish the sex-determining karyotypes. This system permitted the evolution of a master switch (Chromosome maintenance, Cm) that acts maternally. All of the offspring of females that carry Cm-associated neo-sex chromosomes attain a female-determining somatic karyotype and develop as females. Thus, the chromosomes act as maternal effect neo-W's, or W-prime (W') chromosomes, where ZW' females mate with ZZ males to engender female-producing (ZW') and male-producing (ZZ) females in equal numbers. Genetic mapping and physical mapping identified the inversions. Their distribution was determined in nine populations. Experimental matings established the association of the inversions with Cm and measured their recombination suppression. The inversions are the functional equivalent of the sciarid X-prime chromosomes. We speculate that W' chromosomes exist in a variety of species that produce unisexual broods.
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Affiliation(s)
- Thiago R. Benatti
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Fernando H. Valicente
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Rajat Aggarwal
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Chaoyang Zhao
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Jason G. Walling
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Ming-Shun Chen
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Sue E. Cambron
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Brandon J. Schemerhorn
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
| | - Jeffrey J. Stuart
- Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089, U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Kansas State University, Manhattan, Kansas 66506 and U.S. Department of Agriculture–Agricultural Research Service and Department of Entomology, Purdue University, West Lafayette, Indiana 47907-2089
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Cooper TF, Lenski RE. Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol Biol 2010; 10:11. [PMID: 20070898 PMCID: PMC2827396 DOI: 10.1186/1471-2148-10-11] [Citation(s) in RCA: 89] [Impact Index Per Article: 5.9] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/28/2009] [Accepted: 01/13/2010] [Indexed: 12/11/2023] Open
Abstract
BACKGROUND Environmental conditions affect the topology of the adaptive landscape and thus the trajectories followed by evolving populations. For example, a heterogeneous environment might lead to a more rugged adaptive landscape, making it more likely that replicate populations would evolve toward distinct adaptive peaks, relative to a uniform environment. To date, the influence of environmental variability on evolutionary dynamics has received relatively little experimental study. RESULTS We report findings from an experiment designed to test the effects of environmental variability on the adaptation and divergence of replicate populations of E. coli. A total of 42 populations evolved for 2000 generations in 7 environmental regimes that differed in the number, identity, and presentation of the limiting resource. Regimes were organized in two sets, having the sugars glucose and maltose singly and in combination, or glucose and lactose singly and in combination. Combinations of sugars were presented either simultaneously or as temporally fluctuating resource regimes. This design allowed us to compare the effects of resource identity and presentation on the evolutionary trajectories followed by replicate populations. After 2000 generations, the fitness of all populations had increased relative to the common ancestor, but to different extents. Populations evolved in glucose improved the least, whereas populations evolving in maltose or lactose increased the most in their respective sets. Among-population divergence also differed across regimes, with variation higher in those groups that evolved in fluctuating environments than in those that faced constant resource regimens. This divergence under the fluctuating conditions increased between 1000 and 2000 generations, consistent with replicate populations evolving toward distinct adaptive peaks. CONCLUSIONS These results support the hypothesis that environmental heterogeneity can give rise to more rugged adaptive landscapes, which in turn promote evolutionary diversification. These results also demonstrate that this effect depends on the form of environmental heterogeneity, with greater divergence when the pairs of resources fluctuated temporally rather than being presented simultaneously.
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Affiliation(s)
- Tim F Cooper
- Department of Biology and Biochemistry, University of Houston, Houston, TX 77204, USA.
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Park JM, Muñoz E, Deem MW. Quasispecies theory for finite populations. PHYSICAL REVIEW. E, STATISTICAL, NONLINEAR, AND SOFT MATTER PHYSICS 2010; 81:011902. [PMID: 20365394 PMCID: PMC4479305 DOI: 10.1103/physreve.81.011902] [Citation(s) in RCA: 24] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 10/30/2008] [Revised: 10/26/2009] [Indexed: 05/25/2023]
Abstract
We present stochastic, finite-population formulations of the Crow-Kimura and Eigen models of quasispecies theory, for fitness functions that depend in an arbitrary way on the number of mutations from the wild type. We include back mutations in our description. We show that the fluctuation of the population numbers about the average values is exceedingly large in these physical models of evolution. We further show that horizontal gene transfer reduces by orders of magnitude the fluctuations in the population numbers and reduces the accumulation of deleterious mutations in the finite population due to Muller's ratchet. Indeed, the population sizes needed to converge to the infinite population limit are often larger than those found in nature for smooth fitness functions in the absence of horizontal gene transfer. These analytical results are derived for the steady state by means of a field-theoretic representation. Numerical results are presented that indicate horizontal gene transfer speeds up the dynamics of evolution as well.
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Affiliation(s)
- Jeong-Man Park
- Department of Physics & Astronomy, Rice University, Houston, Texas 77005-1892, USA
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