The acknowledgment of evolutionary dependence among species has fundamentally changed how we ask biological questions. Phylogenetic models became the standard approach for studies with 3 or more lineages, in particular those using extant species. Most phylogenetic comparative methods (PCMs) translate relatedness into covariance, meaning that evolutionary changes before lineages split should be interpreted together whereas after the split lineages are expected to change independently. This clever realization has shaped decades of research. Here, we discuss one element of the comparative method often ignored or assumed as unimportant: if nodes of a phylogeny represent the dissolution of the ancestral lineage into two new ones or if the ancestral lineage can survive speciation events (i.e., budding). Budding speciation is often reported in paleontological studies, due to the nature of the evidence for budding in the fossil record, but it is surprisingly absent in comparative methods. Here, we show that many PCMs assume that divergence happens as a symmetric split, even if these methods do not explicitly mention this assumption. We discuss the properties of trait evolution models for continuous and discrete traits and their adequacy under a scenario of budding speciation. We discuss the effects of budding speciation under a series of plausible evolutionary scenarios and show when and how these can influence our estimates. We also propose that long-lived lineages that have survived through a series of budding speciation events and given birth to multiple new lineages can produce evolutionary patterns that challenge our intuition about the most parsimonious history of trait changes in a clade. We hope our discussion can help bridge comparative approaches in paleontology and neontology as well as foster awareness about the assumptions we make when we use phylogenetic trees.
{"title":"How Important Is Budding Speciation for Comparative Studies?","authors":"Daniel S Caetano, Tiago B Quental","doi":"10.1093/sysbio/syad050","DOIUrl":"10.1093/sysbio/syad050","url":null,"abstract":"<p><p>The acknowledgment of evolutionary dependence among species has fundamentally changed how we ask biological questions. Phylogenetic models became the standard approach for studies with 3 or more lineages, in particular those using extant species. Most phylogenetic comparative methods (PCMs) translate relatedness into covariance, meaning that evolutionary changes before lineages split should be interpreted together whereas after the split lineages are expected to change independently. This clever realization has shaped decades of research. Here, we discuss one element of the comparative method often ignored or assumed as unimportant: if nodes of a phylogeny represent the dissolution of the ancestral lineage into two new ones or if the ancestral lineage can survive speciation events (i.e., budding). Budding speciation is often reported in paleontological studies, due to the nature of the evidence for budding in the fossil record, but it is surprisingly absent in comparative methods. Here, we show that many PCMs assume that divergence happens as a symmetric split, even if these methods do not explicitly mention this assumption. We discuss the properties of trait evolution models for continuous and discrete traits and their adequacy under a scenario of budding speciation. We discuss the effects of budding speciation under a series of plausible evolutionary scenarios and show when and how these can influence our estimates. We also propose that long-lived lineages that have survived through a series of budding speciation events and given birth to multiple new lineages can produce evolutionary patterns that challenge our intuition about the most parsimonious history of trait changes in a clade. We hope our discussion can help bridge comparative approaches in paleontology and neontology as well as foster awareness about the assumptions we make when we use phylogenetic trees.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10004968","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Evan Twomey, Paulo Melo-Sampaio, Lisa M Schulte, Franky Bossuyt, Jason L Brown, Santiago Castroviejo-Fisher
Convergent evolution is defined as the independent evolution of similar phenotypes in different lineages. Its existence underscores the importance of external selection pressures in evolutionary history, revealing how functionally similar adaptations can evolve in response to persistent ecological challenges through a diversity of evolutionary routes. However, many examples of convergence, particularly among closely related species, involve parallel changes in the same genes or developmental pathways, raising the possibility that homology at deeper mechanistic levels is an important facilitator of phenotypic convergence. Using the genus Ranitomeya, a young, color-diverse radiation of Neotropical poison frogs, we set out to 1) provide a phylogenetic framework for this group, 2) leverage this framework to determine if color phenotypes are convergent, and 3) to characterize the underlying coloration mechanisms to test whether color convergence occurred through the same or different physical mechanisms. We generated a phylogeny for Ranitomeya using ultraconserved elements and investigated the physical mechanisms underlying bright coloration, focusing on skin pigments. Using phylogenetic comparative methods, we identified several instances of color convergence, involving several gains and losses of carotenoid and pterin pigments. We also found a compelling example of nonparallel convergence, where, in one lineage, red coloration evolved through the red pterin pigment drosopterin, and in another lineage through red ketocarotenoids. Additionally, in another lineage, "reddish" coloration evolved predominantly through structural color mechanisms. Our study demonstrates that, even within a radiation of closely related species, convergent evolution can occur through both parallel and nonparallel mechanisms, challenging the assumption that similar phenotypes among close relatives evolve through the same mechanisms.
{"title":"Multiple Routes to Color Convergence in a Radiation of Neotropical Poison Frogs.","authors":"Evan Twomey, Paulo Melo-Sampaio, Lisa M Schulte, Franky Bossuyt, Jason L Brown, Santiago Castroviejo-Fisher","doi":"10.1093/sysbio/syad051","DOIUrl":"10.1093/sysbio/syad051","url":null,"abstract":"<p><p>Convergent evolution is defined as the independent evolution of similar phenotypes in different lineages. Its existence underscores the importance of external selection pressures in evolutionary history, revealing how functionally similar adaptations can evolve in response to persistent ecological challenges through a diversity of evolutionary routes. However, many examples of convergence, particularly among closely related species, involve parallel changes in the same genes or developmental pathways, raising the possibility that homology at deeper mechanistic levels is an important facilitator of phenotypic convergence. Using the genus Ranitomeya, a young, color-diverse radiation of Neotropical poison frogs, we set out to 1) provide a phylogenetic framework for this group, 2) leverage this framework to determine if color phenotypes are convergent, and 3) to characterize the underlying coloration mechanisms to test whether color convergence occurred through the same or different physical mechanisms. We generated a phylogeny for Ranitomeya using ultraconserved elements and investigated the physical mechanisms underlying bright coloration, focusing on skin pigments. Using phylogenetic comparative methods, we identified several instances of color convergence, involving several gains and losses of carotenoid and pterin pigments. We also found a compelling example of nonparallel convergence, where, in one lineage, red coloration evolved through the red pterin pigment drosopterin, and in another lineage through red ketocarotenoids. Additionally, in another lineage, \"reddish\" coloration evolved predominantly through structural color mechanisms. Our study demonstrates that, even within a radiation of closely related species, convergent evolution can occur through both parallel and nonparallel mechanisms, challenging the assumption that similar phenotypes among close relatives evolve through the same mechanisms.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10924724/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10021110","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Phylogenetic comparative methods use random processes, such as the Brownian Motion, to model the evolution of continuous traits on phylogenetic trees. Growing evidence for non-gradual evolution motivated the development of complex models, often based on Lévy processes. However, their statistical inference is computationally intensive and currently relies on approximations, high-dimensional sampling, or numerical integration. We consider here the Cauchy Process (CP), a particular pure-jump Lévy process in which the trait increment along each branch follows a centered Cauchy distribution with a dispersion proportional to its length. In this work, we derive an exact algorithm to compute both the joint probability density of the tip trait values of a phylogeny under a CP and the ancestral trait values and branch increments posterior densities in quadratic time. A simulation study shows that the CP generates patterns in comparative data that are distinct from any Gaussian process, and that restricted maximum likelihood parameter estimates and root trait reconstruction are unbiased and accurate for trees with 200 tips or less. The CP has only two parameters but is rich enough to capture complex-pulsed evolution. It can reconstruct posterior ancestral trait distributions that are multimodal, reflecting the uncertainty associated with the inference of the evolutionary history of a trait from extant taxa only. Applied on empirical datasets taken from the Evolutionary Ecology and Virology literature, the CP suggests nuanced scenarios for the body size evolution of Greater Antilles Lizards and for the geographical spread of the West Nile Virus epidemics in North America, both consistent with previous studies using more complex models. The method is efficiently implemented in C with an R interface in package cauphy, which is open source and freely available online.
系统进化比较方法使用随机过程(如布朗运动)来模拟系统进化树上连续性状的进化。非渐进进化的证据越来越多,促使人们开发复杂的模型,这些模型通常基于莱维过程。然而,这些模型的统计推断需要大量计算,目前依赖于近似、高维采样或数值积分。我们在这里考虑的是考奇过程(CP),这是一种特殊的纯跳跃莱维过程,其中每个分支的性状增量都遵循一个居中的考奇分布,其离散度与长度成正比。在这项研究中,我们推导出一种精确算法,可以在二次时间内计算 CP 下系统发育顶端性状值的联合概率密度以及祖先性状值和分支增量的后验密度。一项模拟研究表明,CP 在比较数据中产生的模式不同于任何高斯过程,而且对于树梢数不超过 200 个的树来说,受限最大似然参数估计和根性状重建是无偏和准确的。CP只有两个参数,但其丰富程度足以捕捉复杂的脉冲演化。它可以重建多模态的后代祖先性状分布,反映了仅从现生类群推断性状进化史的不确定性。在对来自进化生态学和病毒学文献的经验数据集的应用中,CP 为大安的列斯蜥蜴的体型进化和西尼罗河病毒在北美的地理分布提出了微妙的方案,这两个方案都与之前使用更复杂模型的研究相一致。该方法用 C 语言高效实现,并在 cauphy 软件包中提供了 R 接口,该软件包开源并可在网上免费获取。
{"title":"The Cauchy Process on Phylogenies: A Tractable Model for Pulsed Evolution.","authors":"Paul Bastide, Gilles Didier","doi":"10.1093/sysbio/syad053","DOIUrl":"10.1093/sysbio/syad053","url":null,"abstract":"<p><p>Phylogenetic comparative methods use random processes, such as the Brownian Motion, to model the evolution of continuous traits on phylogenetic trees. Growing evidence for non-gradual evolution motivated the development of complex models, often based on Lévy processes. However, their statistical inference is computationally intensive and currently relies on approximations, high-dimensional sampling, or numerical integration. We consider here the Cauchy Process (CP), a particular pure-jump Lévy process in which the trait increment along each branch follows a centered Cauchy distribution with a dispersion proportional to its length. In this work, we derive an exact algorithm to compute both the joint probability density of the tip trait values of a phylogeny under a CP and the ancestral trait values and branch increments posterior densities in quadratic time. A simulation study shows that the CP generates patterns in comparative data that are distinct from any Gaussian process, and that restricted maximum likelihood parameter estimates and root trait reconstruction are unbiased and accurate for trees with 200 tips or less. The CP has only two parameters but is rich enough to capture complex-pulsed evolution. It can reconstruct posterior ancestral trait distributions that are multimodal, reflecting the uncertainty associated with the inference of the evolutionary history of a trait from extant taxa only. Applied on empirical datasets taken from the Evolutionary Ecology and Virology literature, the CP suggests nuanced scenarios for the body size evolution of Greater Antilles Lizards and for the geographical spread of the West Nile Virus epidemics in North America, both consistent with previous studies using more complex models. The method is efficiently implemented in C with an R interface in package cauphy, which is open source and freely available online.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10096345","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
The bootstrap method is based on resampling sequence alignments and re-estimating trees. Felsenstein's bootstrap proportions (FBP) are the most common approach to assess the reliability and robustness of sequence-based phylogenies. However, when increasing taxon sampling (i.e., the number of sequences) to hundreds or thousands of taxa, FBP tend to return low support for deep branches. The transfer bootstrap expectation (TBE) has been recently suggested as an alternative to FBP. TBE is measured using a continuous transfer index in [0,1] for each bootstrap tree, instead of the binary {0,1} index used in FBP to measure the presence/absence of the branch of interest. TBE has been shown to yield higher and more informative supports while inducing a very low number of falsely supported branches. Nonetheless, it has been argued that TBE must be used with care due to sampling issues, especially in datasets with a high number of closely related taxa. In this study, we conduct multiple experiments by varying taxon sampling and comparing FBP and TBE support values on different phylogenetic depths, using empirical datasets. Our results show that the main critique of TBE stands in extreme cases with shallow branches and highly unbalanced sampling among clades, but that TBE is still robust in most cases, while FBP is inescapably negatively impacted by high taxon sampling. We suggest guidelines and good practices in TBE (and FBP) computing and interpretation.
{"title":"Robustness of Felsenstein's Versus Transfer Bootstrap Supports With Respect to Taxon Sampling.","authors":"Paul Zaharias, Frédéric Lemoine, Olivier Gascuel","doi":"10.1093/sysbio/syad052","DOIUrl":"10.1093/sysbio/syad052","url":null,"abstract":"<p><p>The bootstrap method is based on resampling sequence alignments and re-estimating trees. Felsenstein's bootstrap proportions (FBP) are the most common approach to assess the reliability and robustness of sequence-based phylogenies. However, when increasing taxon sampling (i.e., the number of sequences) to hundreds or thousands of taxa, FBP tend to return low support for deep branches. The transfer bootstrap expectation (TBE) has been recently suggested as an alternative to FBP. TBE is measured using a continuous transfer index in [0,1] for each bootstrap tree, instead of the binary {0,1} index used in FBP to measure the presence/absence of the branch of interest. TBE has been shown to yield higher and more informative supports while inducing a very low number of falsely supported branches. Nonetheless, it has been argued that TBE must be used with care due to sampling issues, especially in datasets with a high number of closely related taxa. In this study, we conduct multiple experiments by varying taxon sampling and comparing FBP and TBE support values on different phylogenetic depths, using empirical datasets. Our results show that the main critique of TBE stands in extreme cases with shallow branches and highly unbalanced sampling among clades, but that TBE is still robust in most cases, while FBP is inescapably negatively impacted by high taxon sampling. We suggest guidelines and good practices in TBE (and FBP) computing and interpretation.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10939309/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41110434","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Dezhi Zhang, Huishang She, Shangyu Wang, Haitao Wang, Shi Li, Yalin Cheng, Gang Song, Chenxi Jia, Yanhua Qu, Frank E Rheindt, Urban Olsson, Per Alström, Fumin Lei
Different genomic regions may reflect conflicting phylogenetic topologies primarily due to incomplete lineage sorting and/or gene flow. Genomic data are necessary to reconstruct the true species tree and explore potential causes of phylogenetic conflict. Here, we investigate the phylogenetic relationships of four Emberiza species (Aves: Emberizidae) and discuss the potential causes of the observed mitochondrial non-monophyly of Emberiza godlewskii (Godlewski's bunting) using phylogenomic analyses based on whole genome resequencing data from 41 birds. Analyses based on both the whole mitochondrial genome and ~39 kilobases from the non-recombining W chromosome reveal sister relationships between each the northern and southern populations of E. godlewskii with E. cioides and E. cia, respectively. In contrast, the monophyly of E. godlewskii is reflected by the phylogenetic signal of autosomal and Z chromosomal sequence data as well as demographic inference analyses, which – in combination – support the following tree topology: (((E. godlewskii, E. cia), E. cioides), E. jankowskii). Using D-statistics, we detected multiple gene flow events among different lineages, indicating pervasive introgressive hybridization within this clade. Introgression from an unsampled lineage that is sister to E. cioides or introgression from an unsampled mitochondrial + W chromosomal lineage of E. cioides into northern E. godlewskii may explain the phylogenetic conflict between the species tree estimated from genome-wide data versus mtDNA/W tree topologies. These results underscore the importance of using genomic data for phylogenetic reconstruction and species delimitation.
不同的基因组区域可能反映出相互冲突的系统发生拓扑结构,这主要是由于不完全的品系分类和/或基因流动造成的。要重建真正的物种树并探索系统发生冲突的潜在原因,基因组数据是必要的。在此,我们基于41种鸟类的全基因组重测序数据,研究了4种Emberiza(鸟类:Emberizidae)的系统发生关系,并讨论了Emberiza godlewskii(戈德勒夫斯基鹀)线粒体非单系的潜在原因。基于整个线粒体基因组和约 39 千碱基的非重组 W 染色体的分析表明,E. godlewskii 的北部和南部种群分别与 E. cioides 和 E. cia 是姊妹关系。与此相反,常染色体和 Z 染色体序列数据以及人口推断分析的系统发生信号反映了 E. godlewskii 的单系性,它们共同支持以下树拓结构:((E. godlewskii, E. cia), E. cioides), E. jankowskii)。利用 D 统计法,我们在不同品系之间检测到多个基因流事件,表明该支系内部存在普遍的内向杂交。cioides 的姊妹系或未取样的线粒体 + W 染色体的 E. cioides 系向北部 E. godlewskii 的引入可能解释了全基因组数据估计的物种树与 mtDNA/W 树拓扑之间的系统发生冲突。这些结果强调了利用基因组数据进行系统发育重建和物种划分的重要性。
{"title":"Phylogenetic conflict between species tree and maternally inherited gene trees in a clade of Emberiza buntings (Aves: Emberizidae)","authors":"Dezhi Zhang, Huishang She, Shangyu Wang, Haitao Wang, Shi Li, Yalin Cheng, Gang Song, Chenxi Jia, Yanhua Qu, Frank E Rheindt, Urban Olsson, Per Alström, Fumin Lei","doi":"10.1093/sysbio/syad078","DOIUrl":"https://doi.org/10.1093/sysbio/syad078","url":null,"abstract":"Different genomic regions may reflect conflicting phylogenetic topologies primarily due to incomplete lineage sorting and/or gene flow. Genomic data are necessary to reconstruct the true species tree and explore potential causes of phylogenetic conflict. Here, we investigate the phylogenetic relationships of four Emberiza species (Aves: Emberizidae) and discuss the potential causes of the observed mitochondrial non-monophyly of Emberiza godlewskii (Godlewski's bunting) using phylogenomic analyses based on whole genome resequencing data from 41 birds. Analyses based on both the whole mitochondrial genome and ~39 kilobases from the non-recombining W chromosome reveal sister relationships between each the northern and southern populations of E. godlewskii with E. cioides and E. cia, respectively. In contrast, the monophyly of E. godlewskii is reflected by the phylogenetic signal of autosomal and Z chromosomal sequence data as well as demographic inference analyses, which – in combination – support the following tree topology: (((E. godlewskii, E. cia), E. cioides), E. jankowskii). Using D-statistics, we detected multiple gene flow events among different lineages, indicating pervasive introgressive hybridization within this clade. Introgression from an unsampled lineage that is sister to E. cioides or introgression from an unsampled mitochondrial + W chromosomal lineage of E. cioides into northern E. godlewskii may explain the phylogenetic conflict between the species tree estimated from genome-wide data versus mtDNA/W tree topologies. These results underscore the importance of using genomic data for phylogenetic reconstruction and species delimitation.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139060877","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Time-scaled phylogenetic trees are an ultimate goal of evolutionary biology and a necessary ingredient in comparative studies. The accumulation of genomic data has resolved the tree of life to a great extent, yet timing evolutionary events remains challenging if not impossible without external information such as fossil ages and morphological characters. Methods for incorporating morphology in tree estimation have lagged behind their molecular counterparts, especially in the case of continuous characters. Despite recent advances, such tools are still direly needed as we approach the limits of what molecules can teach us. Here, we implement a suite of state-of-the-art methods for leveraging continuous morphology in phylogenetics, and by conducting extensive simulation studies we thoroughly validate and explore our methods’ properties. While retaining model generality and scalability, we make it possible to estimate absolute and relative divergence times from multiple continuous characters while accounting for uncertainty. We compile and analyze one of the most data-type diverse data sets to date, comprised of contemporaneous and ancient molecular sequences, and discrete and continuous characters from living and extinct Carnivora taxa. We conclude by synthesizing lessons about our method’s behavior, and suggest future research venues.
{"title":"Fast Bayesian inference of phylogenies from multiple continuous characters","authors":"Rong Zhang, Alexei J Drummond, Fábio K Mendes","doi":"10.1093/sysbio/syad067","DOIUrl":"https://doi.org/10.1093/sysbio/syad067","url":null,"abstract":"Time-scaled phylogenetic trees are an ultimate goal of evolutionary biology and a necessary ingredient in comparative studies. The accumulation of genomic data has resolved the tree of life to a great extent, yet timing evolutionary events remains challenging if not impossible without external information such as fossil ages and morphological characters. Methods for incorporating morphology in tree estimation have lagged behind their molecular counterparts, especially in the case of continuous characters. Despite recent advances, such tools are still direly needed as we approach the limits of what molecules can teach us. Here, we implement a suite of state-of-the-art methods for leveraging continuous morphology in phylogenetics, and by conducting extensive simulation studies we thoroughly validate and explore our methods’ properties. While retaining model generality and scalability, we make it possible to estimate absolute and relative divergence times from multiple continuous characters while accounting for uncertainty. We compile and analyze one of the most data-type diverse data sets to date, comprised of contemporaneous and ancient molecular sequences, and discrete and continuous characters from living and extinct Carnivora taxa. We conclude by synthesizing lessons about our method’s behavior, and suggest future research venues.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138578430","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Julia V Tejada, Pierre-Olivier Antoine, Philippe Münch, Guillaume Billet, Lionel Hautier, Frédéric Delsuc, Fabien L Condamine
Combining morphological and molecular characters through Bayesian total-evidence dating allows inferring the phylogenetic and timescale framework of both extant and fossil taxa, while accounting for the stochasticity and incompleteness of the fossil record. Such an integrative approach is particularly needed when dealing with clades such as sloths (Mammalia: Folivora), for which developmental and biomechanical studies have shown high levels of morphological convergence whereas molecular data can only account for a limited percentage of their total species richness. Here, we propose an alternative hypothesis of sloth evolution that emphasizes the pervasiveness of morphological convergence and the importance of considering the fossil record and an adequate taxon sampling in both phylogenetic and biogeographic inferences. Regardless of different clock models and morphological datasets, the extant sloth Bradypus is consistently recovered as a megatherioid, and Choloepus as a mylodontoid, in agreement with molecular-only analyses. The recently extinct Caribbean sloths (Megalocnoidea) are found to be a monophyletic sister-clade of Megatherioidea, in contrast to previous phylogenetic hypotheses. Our results contradict previous morphological analyses and further support the polyphyly of “Megalonychidae”, whose members were found in five different clades. Regardless of taxon sampling and clock models, the Caribbean colonization of sloths is compatible with the exhumation of islands along Aves Ridge and its geological time frame. Overall, our total-evidence analysis illustrates the difficulty of positioning highly incomplete fossils, although a robust phylogenetic framework was recovered by an a posteriori removal of taxa with high percentages of missing characters. Elimination of these taxa improved topological resolution by reducing polytomies and increasing node support. However, it introduced a systematic and geographic bias because most of these incomplete specimens are from northern South America. This is evident in biogeographic reconstructions, which suggest Patagonia as the area of origin of many clades when taxa are underrepresented, but Amazonia and/or Central and Southern Andes when all taxa are included. More generally, our analyses demonstrate the instability of topology and divergence time estimates when using different morphological datasets and clock models, and thus caution against making macroevolutionary inferences when node support is weak or when uncertainties in the fossil record are not considered.
{"title":"Bayesian total-evidence dating revisits sloth phylogeny and biogeography: a cautionary tale on morphological clock analyses","authors":"Julia V Tejada, Pierre-Olivier Antoine, Philippe Münch, Guillaume Billet, Lionel Hautier, Frédéric Delsuc, Fabien L Condamine","doi":"10.1093/sysbio/syad069","DOIUrl":"https://doi.org/10.1093/sysbio/syad069","url":null,"abstract":"Combining morphological and molecular characters through Bayesian total-evidence dating allows inferring the phylogenetic and timescale framework of both extant and fossil taxa, while accounting for the stochasticity and incompleteness of the fossil record. Such an integrative approach is particularly needed when dealing with clades such as sloths (Mammalia: Folivora), for which developmental and biomechanical studies have shown high levels of morphological convergence whereas molecular data can only account for a limited percentage of their total species richness. Here, we propose an alternative hypothesis of sloth evolution that emphasizes the pervasiveness of morphological convergence and the importance of considering the fossil record and an adequate taxon sampling in both phylogenetic and biogeographic inferences. Regardless of different clock models and morphological datasets, the extant sloth Bradypus is consistently recovered as a megatherioid, and Choloepus as a mylodontoid, in agreement with molecular-only analyses. The recently extinct Caribbean sloths (Megalocnoidea) are found to be a monophyletic sister-clade of Megatherioidea, in contrast to previous phylogenetic hypotheses. Our results contradict previous morphological analyses and further support the polyphyly of “Megalonychidae”, whose members were found in five different clades. Regardless of taxon sampling and clock models, the Caribbean colonization of sloths is compatible with the exhumation of islands along Aves Ridge and its geological time frame. Overall, our total-evidence analysis illustrates the difficulty of positioning highly incomplete fossils, although a robust phylogenetic framework was recovered by an a posteriori removal of taxa with high percentages of missing characters. Elimination of these taxa improved topological resolution by reducing polytomies and increasing node support. However, it introduced a systematic and geographic bias because most of these incomplete specimens are from northern South America. This is evident in biogeographic reconstructions, which suggest Patagonia as the area of origin of many clades when taxa are underrepresented, but Amazonia and/or Central and Southern Andes when all taxa are included. More generally, our analyses demonstrate the instability of topology and divergence time estimates when using different morphological datasets and clock models, and thus caution against making macroevolutionary inferences when node support is weak or when uncertainties in the fossil record are not considered.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-12-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138475677","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jennifer C Girón, Sergei Tarasov, Luis Antonio González Montaña, Nicolas Matentzoglu, Aaron D Smith, Markus Koch, Brendon E Boudinot, Patrice Bouchard, Roger Burks, Lars Vogt, Matthew Yoder, David Osumi-Sutherland, Frank Friedrich, Rolf G Beutel, István Mikó
The spectacular radiation of insects has produced a stunning diversity of phenotypes. During the past 250 years, research on insect systematics has generated hundreds of terms for naming and comparing them. In its current form, this terminological diversity is presented in natural language and lacks formalization, which prohibits computer-assisted comparison using semantic web technologies. Here we propose a Model for Describing Cuticular Anatomical Structures (MoDCAS) which incorporates structural properties and positional relationships for standardized, consistent, and reproducible descriptions of arthropod phenotypes. We applied the MoDCAS framework in creating the ontology for the Anatomy of the Insect Skeleto-Muscular system (AISM). The AISM is the first general insect ontology that aims to cover all taxa by providing generalized, fully logical, and queryable, definitions for each term. It was built using the Ontology Development Kit (ODK), which maximizes interoperability with Uberon (Uberon multispecies anatomy ontology) and other basic ontologies, enhancing the integration of insect anatomy into the broader biological sciences. A template system for adding new terms, extending, and linking the AISM to additional anatomical, phenotypic, genetic, and chemical ontologies is also introduced. The AISM is proposed as the backbone for taxon-specific insect ontologies and has potential applications spanning systematic biology and biodiversity informatics, allowing users to: 1) use controlled vocabularies and create semiautomated computer-parsable insect morphological descriptions; 2) integrate insect morphology into broader fields of research, including ontology-informed phylogenetic methods, logical homology hypothesis testing, evo-devo studies, and genotype to phenotype mapping; and 3) automate the extraction of morphological data from the literature, enabling the generation of large-scale phenomic data, by facilitating the production and testing of informatic tools able to extract, link, annotate, and process morphological data. This descriptive model and its ontological applications will allow for clear and semantically interoperable integration of arthropod phenotypes in biodiversity studies.
{"title":"Formalizing Invertebrate Morphological Data: A Descriptive Model for Cuticle-Based Skeleto-Muscular Systems, an Ontology for Insect Anatomy, and their Potential Applications in Biodiversity Research and Informatics.","authors":"Jennifer C Girón, Sergei Tarasov, Luis Antonio González Montaña, Nicolas Matentzoglu, Aaron D Smith, Markus Koch, Brendon E Boudinot, Patrice Bouchard, Roger Burks, Lars Vogt, Matthew Yoder, David Osumi-Sutherland, Frank Friedrich, Rolf G Beutel, István Mikó","doi":"10.1093/sysbio/syad025","DOIUrl":"10.1093/sysbio/syad025","url":null,"abstract":"<p><p>The spectacular radiation of insects has produced a stunning diversity of phenotypes. During the past 250 years, research on insect systematics has generated hundreds of terms for naming and comparing them. In its current form, this terminological diversity is presented in natural language and lacks formalization, which prohibits computer-assisted comparison using semantic web technologies. Here we propose a Model for Describing Cuticular Anatomical Structures (MoDCAS) which incorporates structural properties and positional relationships for standardized, consistent, and reproducible descriptions of arthropod phenotypes. We applied the MoDCAS framework in creating the ontology for the Anatomy of the Insect Skeleto-Muscular system (AISM). The AISM is the first general insect ontology that aims to cover all taxa by providing generalized, fully logical, and queryable, definitions for each term. It was built using the Ontology Development Kit (ODK), which maximizes interoperability with Uberon (Uberon multispecies anatomy ontology) and other basic ontologies, enhancing the integration of insect anatomy into the broader biological sciences. A template system for adding new terms, extending, and linking the AISM to additional anatomical, phenotypic, genetic, and chemical ontologies is also introduced. The AISM is proposed as the backbone for taxon-specific insect ontologies and has potential applications spanning systematic biology and biodiversity informatics, allowing users to: 1) use controlled vocabularies and create semiautomated computer-parsable insect morphological descriptions; 2) integrate insect morphology into broader fields of research, including ontology-informed phylogenetic methods, logical homology hypothesis testing, evo-devo studies, and genotype to phenotype mapping; and 3) automate the extraction of morphological data from the literature, enabling the generation of large-scale phenomic data, by facilitating the production and testing of informatic tools able to extract, link, annotate, and process morphological data. This descriptive model and its ontological applications will allow for clear and semantically interoperable integration of arthropod phenotypes in biodiversity studies.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9382918","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Wade R Roberts, Elizabeth C Ruck, Kala M Downey, Eveline Pinseel, Andrew J Alverson
Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation and extinction. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic data set of genomes and transcriptomes for 59 diatom taxa to resolve freshwater transitions in one lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. Evidence from gene trees, protein alignments, and diatom life history together suggest that habitat transitions were largely the product of homoplasy rather than hemiplasy, a condition where transitions occur on branches in gene trees not shared with the species tree. Nevertheless, we identified a set of putatively hemiplasious genes, many of which have been associated with shifts to low salinity, indicating that hemiplasy played a small but potentially important role in freshwater adaptation. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help further distinguish different sources of adaptive mutation in freshwater diatoms.
{"title":"Resolving Marine-Freshwater Transitions by Diatoms Through a Fog of Gene Tree Discordance.","authors":"Wade R Roberts, Elizabeth C Ruck, Kala M Downey, Eveline Pinseel, Andrew J Alverson","doi":"10.1093/sysbio/syad038","DOIUrl":"10.1093/sysbio/syad038","url":null,"abstract":"<p><p>Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation and extinction. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic data set of genomes and transcriptomes for 59 diatom taxa to resolve freshwater transitions in one lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. Evidence from gene trees, protein alignments, and diatom life history together suggest that habitat transitions were largely the product of homoplasy rather than hemiplasy, a condition where transitions occur on branches in gene trees not shared with the species tree. Nevertheless, we identified a set of putatively hemiplasious genes, many of which have been associated with shifts to low salinity, indicating that hemiplasy played a small but potentially important role in freshwater adaptation. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help further distinguish different sources of adaptive mutation in freshwater diatoms.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9662988","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Paschalia Kapli, Ioanna Kotari, Maximilian J Telford, Nick Goldman, Ziheng Yang
Inference of deep phylogenies has almost exclusively used protein rather than DNA sequences based on the perception that protein sequences are less prone to homoplasy and saturation or to issues of compositional heterogeneity than DNA sequences. Here, we analyze a model of codon evolution under an idealized genetic code and demonstrate that those perceptions may be misconceptions. We conduct a simulation study to assess the utility of protein versus DNA sequences for inferring deep phylogenies, with protein-coding data generated under models of heterogeneous substitution processes across sites in the sequence and among lineages on the tree, and then analyzed using nucleotide, amino acid, and codon models. Analysis of DNA sequences under nucleotide-substitution models (possibly with the third codon positions excluded) recovered the correct tree at least as often as analysis of the corresponding protein sequences under modern amino acid models. We also applied the different data-analysis strategies to an empirical dataset to infer the metazoan phylogeny. Our results from both simulated and real data suggest that DNA sequences may be as useful as proteins for inferring deep phylogenies and should not be excluded from such analyses. Analysis of DNA data under nucleotide models has a major computational advantage over protein-data analysis, potentially making it feasible to use advanced models that account for among-site and among-lineage heterogeneity in the nucleotide-substitution process in inference of deep phylogenies.
{"title":"DNA Sequences Are as Useful as Protein Sequences for Inferring Deep Phylogenies.","authors":"Paschalia Kapli, Ioanna Kotari, Maximilian J Telford, Nick Goldman, Ziheng Yang","doi":"10.1093/sysbio/syad036","DOIUrl":"10.1093/sysbio/syad036","url":null,"abstract":"<p><p>Inference of deep phylogenies has almost exclusively used protein rather than DNA sequences based on the perception that protein sequences are less prone to homoplasy and saturation or to issues of compositional heterogeneity than DNA sequences. Here, we analyze a model of codon evolution under an idealized genetic code and demonstrate that those perceptions may be misconceptions. We conduct a simulation study to assess the utility of protein versus DNA sequences for inferring deep phylogenies, with protein-coding data generated under models of heterogeneous substitution processes across sites in the sequence and among lineages on the tree, and then analyzed using nucleotide, amino acid, and codon models. Analysis of DNA sequences under nucleotide-substitution models (possibly with the third codon positions excluded) recovered the correct tree at least as often as analysis of the corresponding protein sequences under modern amino acid models. We also applied the different data-analysis strategies to an empirical dataset to infer the metazoan phylogeny. Our results from both simulated and real data suggest that DNA sequences may be as useful as proteins for inferring deep phylogenies and should not be excluded from such analyses. Analysis of DNA data under nucleotide models has a major computational advantage over protein-data analysis, potentially making it feasible to use advanced models that account for among-site and among-lineage heterogeneity in the nucleotide-substitution process in inference of deep phylogenies.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":null,"pages":null},"PeriodicalIF":6.5,"publicationDate":"2023-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10627555/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10063438","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}