Danielle K Herrig, Ryan D Ridenbaugh, Kim L Vertacnik, Kathryn M Everson, Sheina B Sim, Scott M Geib, David W Weisrock, Catherine R Linnen
{"title":"全基因组揭示 Neodiprion 锯蝇基因树不一致的进化关系和机制","authors":"Danielle K Herrig, Ryan D Ridenbaugh, Kim L Vertacnik, Kathryn M Everson, Sheina B Sim, Scott M Geib, David W Weisrock, Catherine R Linnen","doi":"10.1093/sysbio/syae036","DOIUrl":null,"url":null,"abstract":"<p><p>Rapidly evolving taxa are excellent models for understanding the mechanisms that give rise to biodiversity. However, developing an accurate historical framework for comparative analysis of such lineages remains a challenge due to ubiquitous incomplete lineage sorting (ILS) and introgression. Here, we use a whole-genome alignment, multiple locus-sampling strategies, and summary-tree and single nucleotide polymorphism-based species-tree methods to infer a species tree for eastern North American Neodiprion species, a clade of pine-feeding sawflies (Order: Hymenopteran; Family: Diprionidae). We recovered a well-supported species tree that-except for three uncertain relationships-was robust to different strategies for analyzing whole-genome data. Nevertheless, underlying gene-tree discordance was high. To understand this genealogical variation, we used multiple linear regression to model site concordance factors estimated in 50-kb windows as a function of several genomic predictor variables. We found that site concordance factors tended to be higher in regions of the genome with more parsimony-informative sites, fewer singletons, less missing data, lower GC content, more genes, lower recombination rates, and lower D-statistics (less introgression). Together, these results suggest that ILS, introgression, and genotyping error all shape the genomic landscape of gene-tree discordance in Neodiprion. More generally, our findings demonstrate how combining phylogenomic analysis with knowledge of local genomic features can reveal mechanisms that produce topological heterogeneity across genomes.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"839-860"},"PeriodicalIF":6.1000,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Whole Genomes Reveal Evolutionary Relationships and Mechanisms Underlying Gene-Tree Discordance in Neodiprion Sawflies.\",\"authors\":\"Danielle K Herrig, Ryan D Ridenbaugh, Kim L Vertacnik, Kathryn M Everson, Sheina B Sim, Scott M Geib, David W Weisrock, Catherine R Linnen\",\"doi\":\"10.1093/sysbio/syae036\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>Rapidly evolving taxa are excellent models for understanding the mechanisms that give rise to biodiversity. However, developing an accurate historical framework for comparative analysis of such lineages remains a challenge due to ubiquitous incomplete lineage sorting (ILS) and introgression. Here, we use a whole-genome alignment, multiple locus-sampling strategies, and summary-tree and single nucleotide polymorphism-based species-tree methods to infer a species tree for eastern North American Neodiprion species, a clade of pine-feeding sawflies (Order: Hymenopteran; Family: Diprionidae). We recovered a well-supported species tree that-except for three uncertain relationships-was robust to different strategies for analyzing whole-genome data. Nevertheless, underlying gene-tree discordance was high. To understand this genealogical variation, we used multiple linear regression to model site concordance factors estimated in 50-kb windows as a function of several genomic predictor variables. We found that site concordance factors tended to be higher in regions of the genome with more parsimony-informative sites, fewer singletons, less missing data, lower GC content, more genes, lower recombination rates, and lower D-statistics (less introgression). Together, these results suggest that ILS, introgression, and genotyping error all shape the genomic landscape of gene-tree discordance in Neodiprion. More generally, our findings demonstrate how combining phylogenomic analysis with knowledge of local genomic features can reveal mechanisms that produce topological heterogeneity across genomes.</p>\",\"PeriodicalId\":22120,\"journal\":{\"name\":\"Systematic Biology\",\"volume\":\" \",\"pages\":\"839-860\"},\"PeriodicalIF\":6.1000,\"publicationDate\":\"2024-10-30\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Systematic Biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1093/sysbio/syae036\",\"RegionNum\":1,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"EVOLUTIONARY BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Systematic Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/sysbio/syae036","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"EVOLUTIONARY BIOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
快速进化的类群是了解生物多样性产生机制的绝佳模型。然而,由于无处不在的不完全世系分类和引入,为这类世系的比较分析建立一个准确的历史框架仍然是一个挑战。在本文中,我们使用全基因组比对、多位点取样策略以及基于总结树和 SNP 的物种树方法来推断北美东部 Neodiprion 物种的物种树,这是一个食松锯蝇支系(目:膜翅目;科:双翅目)。我们恢复了一个支持良好的物种树,除了三个不确定的关系外,该物种树对不同的全基因组数据分析策略都很稳健。然而,潜在基因树的不一致性很高。为了了解这种谱系变异,我们使用多元线性回归方法,将 50-kb 窗口中估计的位点一致性因子作为几个基因组预测变量的函数来建模。我们发现,在基因组中具有更多解析信息的位点、更少的单子、更少的缺失数据、更低的 GC 含量、更多的基因、更低的重组率和更低的 D 统计量(更少的引入)的区域,位点一致性系数往往更高。这些结果表明,不完全的世系分选、引入和基因分型错误都会造成新地鸟基因组中基因树不一致的情况。更广泛地说,我们的研究结果证明了如何将系统发生组分析与对局部基因组特征的了解相结合,从而揭示产生跨基因组拓扑异质性的机制。
Whole Genomes Reveal Evolutionary Relationships and Mechanisms Underlying Gene-Tree Discordance in Neodiprion Sawflies.
Rapidly evolving taxa are excellent models for understanding the mechanisms that give rise to biodiversity. However, developing an accurate historical framework for comparative analysis of such lineages remains a challenge due to ubiquitous incomplete lineage sorting (ILS) and introgression. Here, we use a whole-genome alignment, multiple locus-sampling strategies, and summary-tree and single nucleotide polymorphism-based species-tree methods to infer a species tree for eastern North American Neodiprion species, a clade of pine-feeding sawflies (Order: Hymenopteran; Family: Diprionidae). We recovered a well-supported species tree that-except for three uncertain relationships-was robust to different strategies for analyzing whole-genome data. Nevertheless, underlying gene-tree discordance was high. To understand this genealogical variation, we used multiple linear regression to model site concordance factors estimated in 50-kb windows as a function of several genomic predictor variables. We found that site concordance factors tended to be higher in regions of the genome with more parsimony-informative sites, fewer singletons, less missing data, lower GC content, more genes, lower recombination rates, and lower D-statistics (less introgression). Together, these results suggest that ILS, introgression, and genotyping error all shape the genomic landscape of gene-tree discordance in Neodiprion. More generally, our findings demonstrate how combining phylogenomic analysis with knowledge of local genomic features can reveal mechanisms that produce topological heterogeneity across genomes.
期刊介绍:
Systematic Biology is the bimonthly journal of the Society of Systematic Biologists. Papers for the journal are original contributions to the theory, principles, and methods of systematics as well as phylogeny, evolution, morphology, biogeography, paleontology, genetics, and the classification of all living things. A Points of View section offers a forum for discussion, while book reviews and announcements of general interest are also featured.