Pub Date : 2024-09-19DOI: 10.1101/2024.09.15.613121
Laura Meyer, Pierre Barry, Christine Arbiol, Rita Castilho, Carl David Van der Lingen, Malika Chlaïda, Niall J McKeown, Bruno Ernande, Alan Le Moan, François Bonhomme, Pierre-Alexandre Gagnaire, Bruno Guinand
The speciation of ecotypes can unfold in diverse ways and likely depends on multiple processes. The variants involved in ecotype divergence can include new mutations as well as older allelic variation that evolved in different contexts. Among the different types of variants that can contribute to reproductive isolation between ecotypes, structural variants (SVs) represent likely candidates due to their ability to protect divergent haplotypes from recombination and gene flow. The European anchovy (Engraulis encrasicolus) is known to be subdivided into marine and coastal ecotypes, and their divergence shows patterns that are consistent with SVs. Here, we present the first genome-scale study investigating genetic structure in the E. encrasicolus species complex. We generated a reference genome and produced whole-genome resequencing data for anchovies from the North-East Atlantic and Mediterranean Sea, as well as from South Africa. We complemented this approach with the analysis of RAD-seq data in order to study ecotypic structure across the entire distribution range. We found that genetic diversity is not only characterised by the presence of two genetic clusters, namely the marine and coastal ecotypes, but also by a third ancestry which corresponds to a southern Atlantic lineage. This lineage occurs off South Africa but also in southern Morocco and the Canary Islands, and shows a gradient of admixture with northern populations nearing the Atlantic-Mediterranean transition zone. Genomic landscapes of differentiation showed evidence for large regions of high linkage disequilibrium, likely representing SVs that differentiate the three anchovy lineages. We found evidence that three of the SVs contributing to the gene flow barrier between ecotypes originated in the southern lineage, suggesting that the coastal and southern lineages have a partly shared evolutionary history. In addition to these barriers, three other SVs contributing to ecotype differentiation appear to have evolved in situ. Anchovies thus present an interesting case for the study of ecotype speciation, since the barriers involved in reproductive isolation have different origins and have partly diverged in geographic isolation.
{"title":"Ecotype formation in the European anchovy fuelled by structural variants of different origins and genetic interactions with a southern lineage","authors":"Laura Meyer, Pierre Barry, Christine Arbiol, Rita Castilho, Carl David Van der Lingen, Malika Chlaïda, Niall J McKeown, Bruno Ernande, Alan Le Moan, François Bonhomme, Pierre-Alexandre Gagnaire, Bruno Guinand","doi":"10.1101/2024.09.15.613121","DOIUrl":"https://doi.org/10.1101/2024.09.15.613121","url":null,"abstract":"The speciation of ecotypes can unfold in diverse ways and likely depends on multiple processes. The variants involved in ecotype divergence can include new mutations as well as older allelic variation that evolved in different contexts. Among the different types of variants that can contribute to reproductive isolation between ecotypes, structural variants (SVs) represent likely candidates due to their ability to protect divergent haplotypes from recombination and gene flow. The European anchovy (Engraulis encrasicolus) is known to be subdivided into marine and coastal ecotypes, and their divergence shows patterns that are consistent with SVs. Here, we present the first genome-scale study investigating genetic structure in the E. encrasicolus species complex. We generated a reference genome and produced whole-genome resequencing data for anchovies from the North-East Atlantic and Mediterranean Sea, as well as from South Africa. We complemented this approach with the analysis of RAD-seq data in order to study ecotypic structure across the entire distribution range. We found that genetic diversity is not only characterised by the presence of two genetic clusters, namely the marine and coastal ecotypes, but also by a third ancestry which corresponds to a southern Atlantic lineage. This lineage occurs off South Africa but also in southern Morocco and the Canary Islands, and shows a gradient of admixture with northern populations nearing the Atlantic-Mediterranean transition zone. Genomic landscapes of differentiation showed evidence for large regions of high linkage disequilibrium, likely representing SVs that differentiate the three anchovy lineages. We found evidence that three of the SVs contributing to the gene flow barrier between ecotypes originated in the southern lineage, suggesting that the coastal and southern lineages have a partly shared evolutionary history. In addition to these barriers, three other SVs contributing to ecotype differentiation appear to have evolved in situ. Anchovies thus present an interesting case for the study of ecotype speciation, since the barriers involved in reproductive isolation have different origins and have partly diverged in geographic isolation.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264606","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-19DOI: 10.1101/2024.09.16.613311
Lucas J. Albano, Cristina C. Bastias, Aurélien Estarague, Brandon T. Hendrickson, Simon G. Innes, Nevada King, Courtney M. Patterson, Amelia Tudoran, François Vasseur, Adriana Puentes, Cyrille Violle, Nicholas J Kooyers, Marc TJ Johnson
Climate change and the global spread of invasive species are currently two of the most significant threats to biodiversity worldwide. Yet the role of adaptation in organismal responses to changing climates or in facilitating species invasions is still poorly understood. We conducted a large-scale trans-continental common garden experiment to understand adaptation to spatiotemporal variation in climate in the native and introduced ranges of a cosmopolitan plant species. Individuals from 96 populations of Trifolium repens (white clover) from both its native (Europe) and introduced (North America) ranges were planted into four experimental common gardens located in northern (Uppsala, Sweden) and southern (Montpellier, France) Europe, and northern (Mississauga, Canada) and southern (Louisiana, USA) North America. We recorded plant sexual and clonal fitness in each common garden and assessed whether plants are best adapted to local climates, whether the strength of local adaptation differed between the native and introduced ranges, and whether populations show evidence of rapid adaptation to recent climate change. Results show that white clover is locally adapted, particularly in lower latitude locations, but also that the most prominent bioclimatic drivers of local adaptation differed by latitude. We also found that strong local adaptation was only evident when populations were transplanted into common gardens located in the same range (native or introduced) from which they originated, indicating rapid local adaptation across a large latitudinal gradient has occurred in T. repens populations in less than 400 years since its introduction to North America. However, we do find some evidence of an adaptation lag in the northern common garden in the introduced range, with plants from historically slightly warmer climates exhibiting the greatest fitness. This indicates that despite evidence of local adaptation to historic climatic conditions and rapid local adaptation post-introduction, white clover populations may be evolving more slowly than climate change is occurring.
{"title":"Adaptation to climate in the native and introduced ranges of a cosmopolitan plant","authors":"Lucas J. Albano, Cristina C. Bastias, Aurélien Estarague, Brandon T. Hendrickson, Simon G. Innes, Nevada King, Courtney M. Patterson, Amelia Tudoran, François Vasseur, Adriana Puentes, Cyrille Violle, Nicholas J Kooyers, Marc TJ Johnson","doi":"10.1101/2024.09.16.613311","DOIUrl":"https://doi.org/10.1101/2024.09.16.613311","url":null,"abstract":"Climate change and the global spread of invasive species are currently two of the most significant threats to biodiversity worldwide. Yet the role of adaptation in organismal responses to changing climates or in facilitating species invasions is still poorly understood. We conducted a large-scale trans-continental common garden experiment to understand adaptation to spatiotemporal variation in climate in the native and introduced ranges of a cosmopolitan plant species. Individuals from 96 populations of Trifolium repens (white clover) from both its native (Europe) and introduced (North America) ranges were planted into four experimental common gardens located in northern (Uppsala, Sweden) and southern (Montpellier, France) Europe, and northern (Mississauga, Canada) and southern (Louisiana, USA) North America. We recorded plant sexual and clonal fitness in each common garden and assessed whether plants are best adapted to local climates, whether the strength of local adaptation differed between the native and introduced ranges, and whether populations show evidence of rapid adaptation to recent climate change. Results show that white clover is locally adapted, particularly in lower latitude locations, but also that the most prominent bioclimatic drivers of local adaptation differed by latitude. We also found that strong local adaptation was only evident when populations were transplanted into common gardens located in the same range (native or introduced) from which they originated, indicating rapid local adaptation across a large latitudinal gradient has occurred in T. repens populations in less than 400 years since its introduction to North America. However, we do find some evidence of an adaptation lag in the northern common garden in the introduced range, with plants from historically slightly warmer climates exhibiting the greatest fitness. This indicates that despite evidence of local adaptation to historic climatic conditions and rapid local adaptation post-introduction, white clover populations may be evolving more slowly than climate change is occurring.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264605","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-19DOI: 10.1101/2024.09.12.612700
J. Luis Leal, Eva Hodková, Anja Billhardt, D. Magnus Eklund, Gustaf Granath, Pilar Herrera Egoavil, Jun Chen, Pascal Milesi, Jarkko Salojärvi, Martin Lascoux
Autopolyploidy, the result of genome duplication within a single species, is widespread among plant lineages and believed to have played a major role in angiosperm evolution and diversification. Whole genome duplication often triggers significant morphological and ecological changes in autopolyploids vis-a-vis their diploid progenitors, which are induced by subtle changes in gene expression patterns, often of a stochastic nature. Recent results have nonetheless identified specific changes in meiotic, metabolic, and defense response pathways that seem to be commonly shared among autopolyploid species, hinting at convergent evolution. Notably, a set of 12 core meiotic genes, including several genes involved in meiotic crossover formation, has been found to undergo strong selective pressure in the aftermath of autopolyploidization. For the most part these findings have been based on the study of Arabidopsis arenosa and A. lyrata autotetraploids and the question has remained as to whether the evolutionary forces shaping the establishment and evolution of autopolyploidy in the Arabidopsis model system extend more broadly across angiosperms, an area where our knowledge is still limited. In order to address these questions, we conducted a comparative transcriptome analysis of Betula pubescens, a highly introgressed autotetraploid, and its diploid sister species, B. pendula, two birch species belonging to the Fagales order that diverged from Brassicales 120-140 Mya. Our results reveal significant changes in the expression patterns of B. pubescens in genes involved in secondary metabolic processes and the regulation of stress response to pathogens, in agreement with results obtained in other autopolyploid plant complexes. Allele-specific expression analysis identified 16 meiotic genes in B. pubescens with constrained expression patterns, strongly favoring alleles introgressed from B. humilis or B. nana, a set that includes 8 meiotic genes − ASY1, ASY3, PDS5B, PRD3, SYN1, SMC3, SHOC1 and SCC4 − previously found to be under selection in Arabidopsis autopolyploids. These results provide support to the hypothesis that whole genome duplication triggers similar genomic responses across flowering plants, and that the evolutionary path available to autopolyploids for regaining meiotic stability is highly conserved and dependent on a small group of core meiotic genes.
{"title":"Conserved Evolutionary Response to Whole Genome Duplication in Angiosperms Revealed Using High Resolution Gene Expression Profiling","authors":"J. Luis Leal, Eva Hodková, Anja Billhardt, D. Magnus Eklund, Gustaf Granath, Pilar Herrera Egoavil, Jun Chen, Pascal Milesi, Jarkko Salojärvi, Martin Lascoux","doi":"10.1101/2024.09.12.612700","DOIUrl":"https://doi.org/10.1101/2024.09.12.612700","url":null,"abstract":"Autopolyploidy, the result of genome duplication within a single species, is widespread among plant lineages and believed to have played a major role in angiosperm evolution and diversification. Whole genome duplication often triggers significant morphological and ecological changes in autopolyploids vis-a-vis their diploid progenitors, which are induced by subtle changes in gene expression patterns, often of a stochastic nature. Recent results have nonetheless identified specific changes in meiotic, metabolic, and defense response pathways that seem to be commonly shared among autopolyploid species, hinting at convergent evolution. Notably, a set of 12 core meiotic genes, including several genes involved in meiotic crossover formation, has been found to undergo strong selective pressure in the aftermath of autopolyploidization. For the most part these findings have been based on the study of <em>Arabidopsis arenosa</em> and <em>A. lyrata</em> autotetraploids and the question has remained as to whether the evolutionary forces shaping the establishment and evolution of autopolyploidy in the Arabidopsis model system extend more broadly across angiosperms, an area where our knowledge is still limited. In order to address these questions, we conducted a comparative transcriptome analysis of <em>Betula pubescens</em>, a highly introgressed autotetraploid, and its diploid sister species, <em>B. pendula</em>, two birch species belonging to the Fagales order that diverged from Brassicales 120-140 Mya. Our results reveal significant changes in the expression patterns of <em>B. pubescens</em> in genes involved in secondary metabolic processes and the regulation of stress response to pathogens, in agreement with results obtained in other autopolyploid plant complexes. Allele-specific expression analysis identified 16 meiotic genes in <em>B. pubescens</em> with constrained expression patterns, strongly favoring alleles introgressed from <em>B. humilis</em> or <em>B. nana</em>, a set that includes 8 meiotic genes − ASY1, ASY3, PDS5B, PRD3, SYN1, SMC3, SHOC1 and SCC4 − previously found to be under selection in Arabidopsis autopolyploids. These results provide support to the hypothesis that whole genome duplication triggers similar genomic responses across flowering plants, and that the evolutionary path available to autopolyploids for regaining meiotic stability is highly conserved and dependent on a small group of core meiotic genes.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264474","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-19DOI: 10.1101/2024.09.15.613113
Jan-Niklas Runge, Kristian Ullrich, Anna K. Lindholm
Supergenes are linked clusters of DNA that are transmitted together due to rare or absent recombination. They undergo co-adaptation, allowing evolution to work on several genes to refine complex phenotypes, giving supergenes a competitive edge. Yet, due to their lack of recombination, supergenes are susceptible to deterioration as they cannot efficiently purge deleterious DNA. Few examples outside of sex chromosomes have been available for study. Here, we present the first assembly of the t haplotype, a 33.4 Mb supergene in house mice that 'selfishly' transmits itself at non-Mendelian frequencies. We characterize the four large non-overlapping inversions that make up the t haplotype. We compare in a t/t individual two different t variants with different recessive lethal phenotypes (age at death). Despite that difference, they differ much less from each other than the rest of the chromosome. However, the differences that they have were much more likely to be deleterious than the differences between the two variants of the rest of the chromosome. We interpret this marked difference as evidence of the accumulation of deleterious variants, a hallmark of deterioration. The t region of chromosome 17 is more distant to the reference than the rest of the chromosome, and has a higher fraction of impactful differences here as well. Thus, we conclude that the t appears as a quickly spreading and deteriorating selfish supergene, a rare example of Muller's ratchet outside of sex chromosomes. Furthermore, we aim for our assembly to provide a resource for comparative work on the t haplotype, such as its evolutionary history.
超级基因是由于罕见或不存在重组而共同传播的DNA连接簇。它们进行共同适应,使进化能够在多个基因上发挥作用,完善复杂的表型,从而使超级基因具有竞争优势。然而,由于缺乏重组,超级基因无法有效清除有害 DNA,因此容易退化。除性染色体外,很少有其他例子可供研究。在这里,我们首次组装了家鼠的 t 单倍型,这是一个 33.4 Mb 的超级基因,它以非孟德尔频率 "自私 "地传播自己。我们描述了构成 t 单倍型的四个大的非重叠倒位。我们比较了 t/t 个体中两种不同的 t 变体,它们具有不同的隐性致死表型(死亡年龄)。尽管存在差异,但它们之间的差异比染色体其他部分的差异要小得多。然而,它们之间的差异比染色体其他部分的两个变体之间的差异更有可能造成有害影响。我们将这种明显的差异解释为有害变体积累的证据,这是退化的标志。与其他染色体相比,17 号染色体的 t 区与参照区的距离更远,这里有影响的差异比例也更高。因此,我们得出结论:t 是一个迅速扩散和退化的自私超级基因,是性染色体之外穆勒棘轮现象的一个罕见例子。此外,我们的目标是为 t 单倍型的比较工作(如进化史)提供资源。
{"title":"De novo assembly of the selfish t supergene reveals a deleterious evolutionary trajectory","authors":"Jan-Niklas Runge, Kristian Ullrich, Anna K. Lindholm","doi":"10.1101/2024.09.15.613113","DOIUrl":"https://doi.org/10.1101/2024.09.15.613113","url":null,"abstract":"Supergenes are linked clusters of DNA that are transmitted together due to rare or absent recombination. They undergo co-adaptation, allowing evolution to work on several genes to refine complex phenotypes, giving supergenes a competitive edge. Yet, due to their lack of recombination, supergenes are susceptible to deterioration as they cannot efficiently purge deleterious DNA. Few examples outside of sex chromosomes have been available for study. Here, we present the first assembly of the t haplotype, a 33.4 Mb supergene in house mice that 'selfishly' transmits itself at non-Mendelian frequencies. We characterize the four large non-overlapping inversions that make up the t haplotype. We compare in a t/t individual two different t variants with different recessive lethal phenotypes (age at death). Despite that difference, they differ much less from each other than the rest of the chromosome. However, the differences that they have were much more likely to be deleterious than the differences between the two variants of the rest of the chromosome. We interpret this marked difference as evidence of the accumulation of deleterious variants, a hallmark of deterioration. The t region of chromosome 17 is more distant to the reference than the rest of the chromosome, and has a higher fraction of impactful differences here as well. Thus, we conclude that the t appears as a quickly spreading and deteriorating selfish supergene, a rare example of Muller's ratchet outside of sex chromosomes. Furthermore, we aim for our assembly to provide a resource for comparative work on the t haplotype, such as its evolutionary history.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264609","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-19DOI: 10.1101/2024.09.14.613092
Brooke M Allen, Rytas Vilgalys, Jason D Hoeksema
After species introductions and subsequent invasions, organisms often encounter intense selection pressures from biotic and abiotic aspects of novel environments, driving rapid evolutionary changes that potentially lead to local adaptation. This study aimed to investigate how invasion has influenced symbiotic interactions through rapid evolution in exotic isolates of the ectomycorrhizal (EcM) fungus Suillus luteus, which was co-introduced with obligately symbiotic pine trees into the Southern Hemisphere. We conducted a cross-inoculation experiment testing the compatibility of sympatric and allopatric pairings between pines and isolates of S. luteus from native and introduced populations. Our results showed that plant and fungal performance were substantially affected by these pairings, largely supporting a hypothesis of local maladaptation. Several performance metrics indicated stronger outcomes in allopatric pairings compared to sympatric ones. This suggests that fungal isolates may have evolved traits that are less beneficial or even somewhat harmful to their local host plants. These findings highlight the complex dynamics of coevolution and emphasize the necessity of considering both local adaptation and maladaptation in understanding species interactions.
{"title":"An Experimental Test of Local Adaptation in Native and Introduced Populations of an Ectomycorrhizal Fungus, Suillus luteus","authors":"Brooke M Allen, Rytas Vilgalys, Jason D Hoeksema","doi":"10.1101/2024.09.14.613092","DOIUrl":"https://doi.org/10.1101/2024.09.14.613092","url":null,"abstract":"After species introductions and subsequent invasions, organisms often encounter intense selection pressures from biotic and abiotic aspects of novel environments, driving rapid evolutionary changes that potentially lead to local adaptation. This study aimed to investigate how invasion has influenced symbiotic interactions through rapid evolution in exotic isolates of the ectomycorrhizal (EcM) fungus Suillus luteus, which was co-introduced with obligately symbiotic pine trees into the Southern Hemisphere. We conducted a cross-inoculation experiment testing the compatibility of sympatric and allopatric pairings between pines and isolates of S. luteus from native and introduced populations. Our results showed that plant and fungal performance were substantially affected by these pairings, largely supporting a hypothesis of local maladaptation. Several performance metrics indicated stronger outcomes in allopatric pairings compared to sympatric ones. This suggests that fungal isolates may have evolved traits that are less beneficial or even somewhat harmful to their local host plants. These findings highlight the complex dynamics of coevolution and emphasize the necessity of considering both local adaptation and maladaptation in understanding species interactions.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264608","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-19DOI: 10.1101/2024.09.16.613218
Beth Shapiro, Jonas Oppenheimer, Michael P Heaton, Kristen L Kuhn, Ed Green, Harvey D Blackburn, Timothy P.L. Smith
Hybridization is common among lineages in the genus Bos, often mediated through human management for the selection of adaptive or desirable traits. A recent example is the American Beefalo cattle breed, which was developed in the 1970s and defined as a hybrid between American bison (Bison bison) and cattle (Bos taurus). The American Beefalo Association typically require 3/8 bison ancestry to qualify as Beefalo. Here, we sought to characterize admixed ancestry among Beefalo as a component of a larger project to understand the role of hybridization in shaping present-day diversity in bison and cattle. We generated genomic data from 50 historical and present-day Beefalo and bison hybrids, including several important founding animals, as well as from 10 bison originating from commercial herds that represent potential sources of bison ancestry in Beefalo. We found that most Beefalo did not contain detectable bison ancestry. No individual Beefalo within our data set satisfies the ancestry requirements specified by the American Beefalo Association (ABA), although several Beefalo had smaller proportions of bison ancestry (2-18%). Some beefalo had detectable indicine cattle ancestry (2-38%), suggesting that hybridization of taurine and zebu cattle may contribute to morphological similarity between some Beefalo and bison. Overall, ancestry profiles of Beefalo and bison hybrid genomes are consistent with repeated backcrossing to either parental species rather than the breeding between hybrids themselves, implying significant barriers to gene flow between bison and cattle. Our results call into question the 3/8 bison ancestry targeted by the breed association and demonstrate the value of genomic information in examining claims of interspecies gene flow among Bos species.
{"title":"Most Beefalo cattle have no detectable bison genetic ancestry","authors":"Beth Shapiro, Jonas Oppenheimer, Michael P Heaton, Kristen L Kuhn, Ed Green, Harvey D Blackburn, Timothy P.L. Smith","doi":"10.1101/2024.09.16.613218","DOIUrl":"https://doi.org/10.1101/2024.09.16.613218","url":null,"abstract":"Hybridization is common among lineages in the genus Bos, often mediated through human management for the selection of adaptive or desirable traits. A recent example is the American Beefalo cattle breed, which was developed in the 1970s and defined as a hybrid between American bison (Bison bison) and cattle (Bos taurus). The American Beefalo Association typically require 3/8 bison ancestry to qualify as Beefalo. Here, we sought to characterize admixed ancestry among Beefalo as a component of a larger project to understand the role of hybridization in shaping present-day diversity in bison and cattle. We generated genomic data from 50 historical and present-day Beefalo and bison hybrids, including several important founding animals, as well as from 10 bison originating from commercial herds that represent potential sources of bison ancestry in Beefalo. We found that most Beefalo did not contain detectable bison ancestry. No individual Beefalo within our data set satisfies the ancestry requirements specified by the American Beefalo Association (ABA), although several Beefalo had smaller proportions of bison ancestry (2-18%). Some beefalo had detectable indicine cattle ancestry (2-38%), suggesting that hybridization of taurine and zebu cattle may contribute to morphological similarity between some Beefalo and bison. Overall, ancestry profiles of Beefalo and bison hybrid genomes are consistent with repeated backcrossing to either parental species rather than the breeding between hybrids themselves, implying significant barriers to gene flow between bison and cattle. Our results call into question the 3/8 bison ancestry targeted by the breed association and demonstrate the value of genomic information in examining claims of interspecies gene flow among Bos species.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264607","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-18DOI: 10.1101/2024.06.17.599025
Leon Hilgers, Shenglin Liu, Axel Jensen, Thomas Brown, Trevor Cousins, Regev Schweiger, Katerina Guschanski, Michael Hiller
Inferring historical population sizes is key to identify drivers of ecological and evolutionary change, and crucial to predict the future of species on our rapidly changing planet. The pairwise sequentially Markovian coalescent (PSMC) method provided a revolutionary framework to reconstruct species demographic histories over millions of years based on the genome sequence of a single individual 1. Here, we detected and solved a common artifact in PSMC and related methods: recent population peaks followed by population collapses. Combining real and simulated genomes, we show that these peaks do not represent true population dynamics. Instead, ill-set default parameters cause false peaks in our own and published data, which can be avoided by adjusted parameter settings. Furthermore, we show that certain population structure changes can cause similar patterns. Newer methods like Beta-PSMC perform better, but do not always avoid this artifact. Our results suggest testing multiple parameters before interpreting recent population peaks followed by collapses, and call for the development of robust methods.
{"title":"Avoidable false PSMC population size peaks occur across numerous studies","authors":"Leon Hilgers, Shenglin Liu, Axel Jensen, Thomas Brown, Trevor Cousins, Regev Schweiger, Katerina Guschanski, Michael Hiller","doi":"10.1101/2024.06.17.599025","DOIUrl":"https://doi.org/10.1101/2024.06.17.599025","url":null,"abstract":"Inferring historical population sizes is key to identify drivers of ecological and evolutionary change, and crucial to predict the future of species on our rapidly changing planet. The pairwise sequentially Markovian coalescent (PSMC) method provided a revolutionary framework to reconstruct species demographic histories over millions of years based on the genome sequence of a single individual 1. Here, we detected and solved a common artifact in PSMC and related methods: recent population peaks followed by population collapses. Combining real and simulated genomes, we show that these peaks do not represent true population dynamics. Instead, ill-set default parameters cause false peaks in our own and published data, which can be avoided by adjusted parameter settings. Furthermore, we show that certain population structure changes can cause similar patterns. Newer methods like Beta-PSMC perform better, but do not always avoid this artifact. Our results suggest testing multiple parameters before interpreting recent population peaks followed by collapses, and call for the development of robust methods.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264612","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-18DOI: 10.1101/2024.09.16.613318
Alyssa Lyn Fortier, Jonathan K Pritchard
Gene families are groups of evolutionarily-related genes. One large gene family that has experienced rapid evolution is the Major Histocompatibility Complex (MHC), whose proteins serve critical roles in innate and adaptive immunity. Across the ~60 million year history of the primates, some MHC genes have turned over completely, some have changed function, some have converged in function, and others have remained essentially unchanged. Past work has typically focused on identifying MHC alleles within particular species or comparing gene content, but more work is needed to understand the overall evolution of the gene family across species. Thus, despite the immunologic importance of the MHC and its peculiar evolutionary history, we lack a complete picture of MHC evolution in the primates. We readdress this question using sequences from dozens of MHC genes and pseudogenes spanning the entire primate order, building a comprehensive set of gene and allele trees with modern methods. Overall, we find that the Class I gene subfamily is evolving much more quickly than the Class II gene subfamily, with the exception of the Class II MHC-DRB genes. We also pay special attention to the often-ignored pseudogenes, which we use to reconstruct different events in the evolution of the Class I region. We find that despite the shared function of the MHC across species, different species employ different genes, haplotypes, and patterns of variation to achieve a successful immune response. Our trees and extensive literature review represent the most comprehensive look into MHC evolution to date.
基因家族是由进化相关的基因组成的群体。主要组织相容性复合体(MHC)就是一个经历了快速进化的大型基因家族,其蛋白质在先天性免疫和适应性免疫中发挥着关键作用。在灵长类动物长达约 6000 万年的历史中,一些 MHC 基因完全改变,一些改变了功能,一些功能趋同,还有一些则基本保持不变。过去的工作通常侧重于识别特定物种内的 MHC 等位基因或比较基因含量,但要了解该基因家族在不同物种间的整体进化情况,还需要做更多的工作。因此,尽管 MHC 在免疫学上非常重要,而且其进化历史也很奇特,但我们对灵长类动物中 MHC 的进化缺乏完整的了解。我们利用横跨整个灵长类的数十个 MHC 基因和假基因的序列重新解决了这个问题,并用现代方法建立了一套全面的基因和等位基因树。总体而言,我们发现除了 II 类 MHC-DRB 基因外,I 类基因亚家族的进化速度远远快于 II 类基因亚家族。我们还特别关注了经常被忽视的假基因,并利用它们来重建 I 类区进化过程中的不同事件。我们发现,尽管不同物种的 MHC 具有共同的功能,但不同物种采用不同的基因、单体型和变异模式来实现成功的免疫反应。我们的研究树和广泛的文献综述是迄今为止对 MHC 进化最全面的研究。
{"title":"The Primate Major Histocompatibility Complex: An Illustrative Example of Gene Family Evolution","authors":"Alyssa Lyn Fortier, Jonathan K Pritchard","doi":"10.1101/2024.09.16.613318","DOIUrl":"https://doi.org/10.1101/2024.09.16.613318","url":null,"abstract":"Gene families are groups of evolutionarily-related genes. One large gene family that has experienced rapid evolution is the Major Histocompatibility Complex (MHC), whose proteins serve critical roles in innate and adaptive immunity. Across the ~60 million year history of the primates, some MHC genes have turned over completely, some have changed function, some have converged in function, and others have remained essentially unchanged. Past work has typically focused on identifying MHC alleles within particular species or comparing gene content, but more work is needed to understand the overall evolution of the gene family across species. Thus, despite the immunologic importance of the MHC and its peculiar evolutionary history, we lack a complete picture of MHC evolution in the primates. We readdress this question using sequences from dozens of MHC genes and pseudogenes spanning the entire primate order, building a comprehensive set of gene and allele trees with modern methods. Overall, we find that the Class I gene subfamily is evolving much more quickly than the Class II gene subfamily, with the exception of the Class II MHC-DRB genes. We also pay special attention to the often-ignored pseudogenes, which we use to reconstruct different events in the evolution of the Class I region. We find that despite the shared function of the MHC across species, different species employ different genes, haplotypes, and patterns of variation to achieve a successful immune response. Our trees and extensive literature review represent the most comprehensive look into MHC evolution to date.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264611","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-18DOI: 10.1101/2024.08.31.610610
Marcial Quiroga-Carmona, Schuyler Liphardt, Naim M Bautista, Pablo Jayat, Pablo Teta, Jason L Malaney, Tabitha McFarland, Joseph A Cook, Moritz Blumer, Nathanael D Herrera, Zachary A Cheviron, Jeffrey Good, Guillermo D'Elia, Jay Storz
Leaf-eared mice (genus Phyllotis) are among the most widespread and abundant small mammals in the Andean Altiplano, but species boundaries and distributional limits are often poorly delineated due to sparse survey data from remote mountains and high-elevation deserts. Here we report a combined analysis of mitochondrial DNA variation and whole-genome sequence (WGS) variation in Phyllotis mice to delimit species boundaries, to assess the timescale of diversification of the group, and to examine evidence for interspecific hybridization. Estimates of divergence dates suggest that most diversification of Phyllotis occurred during the past 3 million years. Consistent with the Pleistocene Aridification hypothesis, our results suggest that diversification of Phyllotis largely coincided with climatically induced environmental changes in the mid- to late Pleistocene. Contrary to the Montane Uplift hypothesis, most diversification in the group occurred well after the major phase of uplift of the Central Andean Plateau. Species delimitation analyses revealed surprising patterns of cryptic diversity within several nominal forms, suggesting the presence of much undescribed alpha diversity in the genus. Results of genomic analyses revealed evidence of ongoing hybridization between the sister species Phyllotis limatus and P. vaccarum and suggest that the contemporary zone of range overlap between the two species represents an active hybrid zone.
{"title":"Species limits and hybridization in Andean leaf-eared mice (Phyllotis)","authors":"Marcial Quiroga-Carmona, Schuyler Liphardt, Naim M Bautista, Pablo Jayat, Pablo Teta, Jason L Malaney, Tabitha McFarland, Joseph A Cook, Moritz Blumer, Nathanael D Herrera, Zachary A Cheviron, Jeffrey Good, Guillermo D'Elia, Jay Storz","doi":"10.1101/2024.08.31.610610","DOIUrl":"https://doi.org/10.1101/2024.08.31.610610","url":null,"abstract":"Leaf-eared mice (genus Phyllotis) are among the most widespread and abundant small mammals in the Andean Altiplano, but species boundaries and distributional limits are often poorly delineated due to sparse survey data from remote mountains and high-elevation deserts. Here we report a combined analysis of mitochondrial DNA variation and whole-genome sequence (WGS) variation in Phyllotis mice to delimit species boundaries, to assess the timescale of diversification of the group, and to examine evidence for interspecific hybridization. Estimates of divergence dates suggest that most diversification of Phyllotis occurred during the past 3 million years. Consistent with the Pleistocene Aridification hypothesis, our results suggest that diversification of Phyllotis largely coincided with climatically induced environmental changes in the mid- to late Pleistocene. Contrary to the Montane Uplift hypothesis, most diversification in the group occurred well after the major phase of uplift of the Central Andean Plateau. Species delimitation analyses revealed surprising patterns of cryptic diversity within several nominal forms, suggesting the presence of much undescribed alpha diversity in the genus. Results of genomic analyses revealed evidence of ongoing hybridization between the sister species Phyllotis limatus and P. vaccarum and suggest that the contemporary zone of range overlap between the two species represents an active hybrid zone.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264613","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-09-18DOI: 10.1101/2024.09.17.613452
Jozsef Garay, Inmaculada Lopez, Zoltan Varga, Villo Csiszar, Tamas F. Mori
Background: We focus on familial selection of Haldane in monogamous families in a diploid population, where the survival probability of each sibling is determined by altruistic food sharing with its siblings during starvation. An autosomal recessive-dominant or intermediate allele pair uniquely determines the altruistic or selfish behavior, which are coded by homozygotes. We focus on the case when additive cost and benefit functions determine the survival probability of each full sibling. Results: We provide conditions for the existence of the altruistic and selfish homozygote. We show that the condition of evolutionary stability of altruism depends on the genotype-phenotype mapping. Furthermore, if the offspring size increases then the condition of evolutionary stability of altruism becomes stricter. Contrary to that, for the evolutionary stability of selfish behavior it is enough if the classical rule of Hamilton does not hold. Moreover, when the classical rule of Hamilton holds and the condition of evolutionarily stability of altruism does not hold, then the selfish and altruistic phenotypes coexist. Conclusions: In summary, the classical rule of Hamilton is a sufficient condition for the existence of altruism, but it alone does not imply the evolutionary stability of the pure altruistic homozygote population when the altruistic siblings share the cost of altruism.
{"title":"Survival cost sharing among altruistic full siblings in Mendelian population","authors":"Jozsef Garay, Inmaculada Lopez, Zoltan Varga, Villo Csiszar, Tamas F. Mori","doi":"10.1101/2024.09.17.613452","DOIUrl":"https://doi.org/10.1101/2024.09.17.613452","url":null,"abstract":"Background: We focus on familial selection of Haldane in monogamous families in a diploid population, where the survival probability of each sibling is determined by altruistic food sharing with its siblings during starvation. An autosomal recessive-dominant or intermediate allele pair uniquely determines the altruistic or selfish behavior, which are coded by homozygotes. We focus on the case when additive cost and benefit functions determine the survival probability of each full sibling.\u0000Results: We provide conditions for the existence of the altruistic and selfish homozygote. We show that the condition of evolutionary stability of altruism depends on the genotype-phenotype mapping. Furthermore, if the offspring size increases then the condition of evolutionary stability of altruism becomes stricter. Contrary to that, for the evolutionary stability of selfish behavior it is enough if the classical rule of Hamilton does not hold. Moreover, when the classical rule of Hamilton holds and the condition of evolutionarily stability of altruism does not hold, then the selfish and altruistic phenotypes coexist. Conclusions: In summary, the classical rule of Hamilton is a sufficient condition for the existence of altruism, but it alone does not imply the evolutionary stability of the pure altruistic homozygote population when the altruistic siblings share the cost of altruism.","PeriodicalId":501183,"journal":{"name":"bioRxiv - Evolutionary Biology","volume":null,"pages":null},"PeriodicalIF":0.0,"publicationDate":"2024-09-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142264565","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}