Alison R Irwin, Nicholas W Roberts, Ellen E Strong, Yasunori Kano, Daniel I Speiser, Elizabeth M Harper, Suzanne T Williams
Eyes within the marine gastropod superfamily Stromboidea range widely in size, from 0.2 to 2.3 mm-the largest eyes known in any gastropod. Despite this interesting variation, the underlying evolutionary pressures remain unknown. Here, we use the wealth of material available in museum collections to explore the evolution of stromboid eye size and structure. Our results suggest that depth is a key light-limiting factor in stromboid eye evolution; here, increasing water depth is correlated with increasing aperture width relative to lens diameter, and therefore an increasing investment in sensitivity in dim light environments. In the major clade containing all large-eyed stromboid families, species observed active during the day and the night had wider eye apertures relative to lens sizes than species observed active during the day only, thereby prioritizing sensitivity over resolution. Species with no consistent diel activity pattern also had smaller body sizes than exclusively day-active species, which may suggest that smaller animals are more vulnerable to shell-crushing predators, and avoid the higher predation pressure experienced by animals active during the day. Within the same major clade, ancestral state reconstruction suggests that absolute eye size increased above 1 mm twice. The unresolved position of Varicospira, however, weakens this hypothesis and further work with additional markers is needed to confirm this result.
{"title":"Evolution of Large Eyes in Stromboidea (Gastropoda): Impact of Photic Environment and Life History Traits.","authors":"Alison R Irwin, Nicholas W Roberts, Ellen E Strong, Yasunori Kano, Daniel I Speiser, Elizabeth M Harper, Suzanne T Williams","doi":"10.1093/sysbio/syae063","DOIUrl":"10.1093/sysbio/syae063","url":null,"abstract":"<p><p>Eyes within the marine gastropod superfamily Stromboidea range widely in size, from 0.2 to 2.3 mm-the largest eyes known in any gastropod. Despite this interesting variation, the underlying evolutionary pressures remain unknown. Here, we use the wealth of material available in museum collections to explore the evolution of stromboid eye size and structure. Our results suggest that depth is a key light-limiting factor in stromboid eye evolution; here, increasing water depth is correlated with increasing aperture width relative to lens diameter, and therefore an increasing investment in sensitivity in dim light environments. In the major clade containing all large-eyed stromboid families, species observed active during the day and the night had wider eye apertures relative to lens sizes than species observed active during the day only, thereby prioritizing sensitivity over resolution. Species with no consistent diel activity pattern also had smaller body sizes than exclusively day-active species, which may suggest that smaller animals are more vulnerable to shell-crushing predators, and avoid the higher predation pressure experienced by animals active during the day. Within the same major clade, ancestral state reconstruction suggests that absolute eye size increased above 1 mm twice. The unresolved position of Varicospira, however, weakens this hypothesis and further work with additional markers is needed to confirm this result.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"301-322"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142584383","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}
Théo Gaboriau, Joseph A Tobias, Daniele Silvestro, Nicolas Salamin
Popular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions assume that, at speciation, a trait value is inherited identically by 2 descendant species. This assumption contrasts with models of speciation at a micro-evolutionary scale where descendants' phenotypic distributions are sub-samples of the ancestral distribution. Different speciation mechanisms can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of ancestral phenotypic distribution at speciation. Here, we develop an Asymmetric Brownian Motion model (ABM) that relaxes the assumption of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also infers the mode of phenotypic inheritance at speciation, which can range from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.
{"title":"Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation.","authors":"Théo Gaboriau, Joseph A Tobias, Daniele Silvestro, Nicolas Salamin","doi":"10.1093/sysbio/syae043","DOIUrl":"10.1093/sysbio/syae043","url":null,"abstract":"<p><p>Popular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions assume that, at speciation, a trait value is inherited identically by 2 descendant species. This assumption contrasts with models of speciation at a micro-evolutionary scale where descendants' phenotypic distributions are sub-samples of the ancestral distribution. Different speciation mechanisms can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of ancestral phenotypic distribution at speciation. Here, we develop an Asymmetric Brownian Motion model (ABM) that relaxes the assumption of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also infers the mode of phenotypic inheritance at speciation, which can range from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"267-281"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11958934/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141752781","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}
Despite their extensive diversity and ecological importance, the history of diversification for most groups of parasitic organisms remains relatively understudied. Elucidating broad macroevolutionary patterns of parasites is challenging, often limited by the availability of samples, genetic resources, and knowledge about ecological relationships with their hosts. In this study, we explore the macroevolutionary history of parasites by focusing on parasitic body lice from doves. Building on extensive knowledge of ecological relationships and previous phylogenomic studies of their avian hosts, we tested specific questions about the evolutionary origins of the body lice of doves, leveraging whole genome data sets for phylogenomics. Specifically, we sequenced whole genomes from 68 samples of dove body lice, including representatives of all body louse genera from 51 host taxa. From these data, we assembled > 2300 nuclear genes to estimate dated phylogenetic relationships among body lice and several outgroup taxa. The resulting phylogeny of body lice was well supported, although some branches had conflicting signals across the genome. We then reconstructed ancestral biogeographic ranges of body lice and compared the body louse phylogeny to the phylogeny of doves, and also to a previously published phylogeny of the wing lice of doves. Divergence estimates placed the origin of body lice in the late Oligocene. Body lice likely originated in Australasia and dispersed with their hosts during the early Miocene, with subsequent codivergence and host switching throughout the world. Notably, this evolutionary history is very similar to that of dove wing lice, despite the stronger dispersal capabilities of wing lice compared to body lice. Our results highlight the central role of the biogeographic history of host organisms in driving the evolutionary history of their parasites across time and geographic space.
{"title":"Biogeographic History of Pigeons and Doves Drives the Origin and Diversification of Their Parasitic Body Lice.","authors":"Andrew D Sweet, Jorge Doña, Kevin P Johnson","doi":"10.1093/sysbio/syae038","DOIUrl":"10.1093/sysbio/syae038","url":null,"abstract":"<p><p>Despite their extensive diversity and ecological importance, the history of diversification for most groups of parasitic organisms remains relatively understudied. Elucidating broad macroevolutionary patterns of parasites is challenging, often limited by the availability of samples, genetic resources, and knowledge about ecological relationships with their hosts. In this study, we explore the macroevolutionary history of parasites by focusing on parasitic body lice from doves. Building on extensive knowledge of ecological relationships and previous phylogenomic studies of their avian hosts, we tested specific questions about the evolutionary origins of the body lice of doves, leveraging whole genome data sets for phylogenomics. Specifically, we sequenced whole genomes from 68 samples of dove body lice, including representatives of all body louse genera from 51 host taxa. From these data, we assembled > 2300 nuclear genes to estimate dated phylogenetic relationships among body lice and several outgroup taxa. The resulting phylogeny of body lice was well supported, although some branches had conflicting signals across the genome. We then reconstructed ancestral biogeographic ranges of body lice and compared the body louse phylogeny to the phylogeny of doves, and also to a previously published phylogeny of the wing lice of doves. Divergence estimates placed the origin of body lice in the late Oligocene. Body lice likely originated in Australasia and dispersed with their hosts during the early Miocene, with subsequent codivergence and host switching throughout the world. Notably, this evolutionary history is very similar to that of dove wing lice, despite the stronger dispersal capabilities of wing lice compared to body lice. Our results highlight the central role of the biogeographic history of host organisms in driving the evolutionary history of their parasites across time and geographic space.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"198-214"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141734980","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}
Mathilde Barthe, Loïs Rancilhac, Maria C Arteaga, Anderson Feijó, Marie-Ka Tilak, Fabienne Justy, William J Loughry, Colleen M McDonough, Benoit de Thoisy, François Catzeflis, Guillaume Billet, Lionel Hautier, Nabholz Benoit, Frédéric Delsuc
The nine-banded armadillo (Dasypus novemcinctus) is the most widespread xenarthran species across the Americas. Recent studies have suggested it is composed of 4 morphologically and genetically distinct lineages of uncertain taxonomic status. To address this issue, we used a museomic approach to sequence 80 complete mitogenomes and capture 997 nuclear loci for 71 Dasypus individuals sampled across the entire distribution. We carefully cleaned up potential genotyping errors and cross-contaminations that could blur species boundaries by mimicking gene flow. Our results unambiguously support 4 distinct lineages within the D. novemcinctus complex. We found cases of mito-nuclear phylogenetic discordance but only limited contemporary gene flow confined to the margins of the lineage distributions. All available evidence including the restricted gene flow, phylogenetic reconstructions based on both mitogenomes and nuclear loci, and phylogenetic delimitation methods consistently supported the 4 lineages within D. novemcinctus as 4 distinct species. Comparable genetic differentiation values to other recognized Dasypus species further reinforced their status as valid species. Considering congruent morphological results from previous studies, we provide an integrative taxonomic view to recognize 4 species within the D. novemcinctus complex: D. novemcinctus, D. fenestratus, D. mexicanus, and D. guianensis sp. nov., a new species endemic of the Guiana Shield that we describe here. The 2 available individuals of D. mazzai and D. sabanicola were consistently nested within D. novemcinctus lineage and their status remains to be assessed. The present work offers a case study illustrating the power of museomics to reveal cryptic species diversity within a widely distributed and emblematic species of mammals.
九带犰狳(Dasypus novemcinctus)是美洲分布最广的异种。最近的研究表明,九带犰狳由四个形态和基因上不同的品系组成,其分类地位尚不确定。为了解决这个问题,我们采用了一种 museomic 方法,对整个分布区的 71 个 Dasypus 个体进行了 80 个完整的有丝分裂基因组测序,并捕获了 997 个核基因位点。我们仔细清除了潜在的基因分型错误和交叉污染,这些错误和污染可能会通过模拟基因流模糊物种界限。我们的研究结果明确支持在 D. novemcinctus 复合物中存在四个不同的品系。我们发现了有丝分裂-核系统发育不一致的情况,但当代基因流动仅局限于各系分布的边缘。所有可用的证据,包括受限的基因流动、基于有丝分裂基因组和核基因位点的系统发育重建以及系统发育定界方法,都一致支持将新鳞蟾蜍的四个品系视为四个不同的物种。与其他公认的 Dasypus 物种相似的遗传分化值进一步加强了它们作为有效物种的地位。考虑到先前研究中一致的形态学结果,我们提供了一个综合的分类学观点,以确认新月豚复合种中的四个物种:D. novemcinctus、D. fenestratus、D. mexicanus,以及我们在此描述的圭亚那盾地区特有的新种 D. guianensis sp.现有的两个 D. mazzai 和 D. sabanicola 个体一直被归入 D. novemcinctus 系,它们的地位仍有待评估。本研究提供了一个案例研究,说明了 museomics 在广泛分布的代表性哺乳动物物种中揭示隐性物种多样性的能力。
{"title":"Exon Capture Museomics Deciphers the Nine-Banded Armadillo Species Complex and Identifies a New Species Endemic to the Guiana Shield.","authors":"Mathilde Barthe, Loïs Rancilhac, Maria C Arteaga, Anderson Feijó, Marie-Ka Tilak, Fabienne Justy, William J Loughry, Colleen M McDonough, Benoit de Thoisy, François Catzeflis, Guillaume Billet, Lionel Hautier, Nabholz Benoit, Frédéric Delsuc","doi":"10.1093/sysbio/syae027","DOIUrl":"10.1093/sysbio/syae027","url":null,"abstract":"<p><p>The nine-banded armadillo (Dasypus novemcinctus) is the most widespread xenarthran species across the Americas. Recent studies have suggested it is composed of 4 morphologically and genetically distinct lineages of uncertain taxonomic status. To address this issue, we used a museomic approach to sequence 80 complete mitogenomes and capture 997 nuclear loci for 71 Dasypus individuals sampled across the entire distribution. We carefully cleaned up potential genotyping errors and cross-contaminations that could blur species boundaries by mimicking gene flow. Our results unambiguously support 4 distinct lineages within the D. novemcinctus complex. We found cases of mito-nuclear phylogenetic discordance but only limited contemporary gene flow confined to the margins of the lineage distributions. All available evidence including the restricted gene flow, phylogenetic reconstructions based on both mitogenomes and nuclear loci, and phylogenetic delimitation methods consistently supported the 4 lineages within D. novemcinctus as 4 distinct species. Comparable genetic differentiation values to other recognized Dasypus species further reinforced their status as valid species. Considering congruent morphological results from previous studies, we provide an integrative taxonomic view to recognize 4 species within the D. novemcinctus complex: D. novemcinctus, D. fenestratus, D. mexicanus, and D. guianensis sp. nov., a new species endemic of the Guiana Shield that we describe here. The 2 available individuals of D. mazzai and D. sabanicola were consistently nested within D. novemcinctus lineage and their status remains to be assessed. The present work offers a case study illustrating the power of museomics to reveal cryptic species diversity within a widely distributed and emblematic species of mammals.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"177-197"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11958936/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141440907","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}
Philipp Mitteroecker, Michael L Collyer, Dean C Adams
Due to the hierarchical structure of the tree of life, closely related species often resemble each other more than distantly related species; a pattern termed phylogenetic signal. Numerous univariate statistics have been proposed as measures of phylogenetic signal for single phenotypic traits, but the study of phylogenetic signal for multivariate data, as is common in modern biology, remains challenging. Here, we introduce a new method to explore phylogenetic signal in multivariate phenotypes. Our approach decomposes the data into linear combinations with maximal (or minimal) phylogenetic signal, as measured by Blomberg's K. The loading vectors of these phylogenetic components or K-components can be biologically interpreted, and scatterplots of the scores can be used as a low-dimensional ordination of the data that maximally (or minimally) preserves phylogenetic signal. We present algebraic and statistical properties, along with 2 new summary statistics, KA and KG, of phylogenetic signal in multivariate data. Simulation studies showed that KA and KG have higher statistical power than the previously suggested statistic Kmult, especially if phylogenetic signal is low or concentrated in a few trait dimensions. In 2 empirical applications to vertebrate cranial shape (crocodyliforms and papionins), we found statistically significant phylogenetic signal concentrated in a few trait dimensions. The finding that phylogenetic signal can be highly variable across the dimensions of multivariate phenotypes has important implications for current maximum likelihood approaches to phylogenetic signal in multivariate data.
由于生命树的层次结构,近缘物种往往比远缘物种更相似;这种模式被称为系统发生信号。人们提出了许多单变量统计量来衡量单一表型性状的系统发生信号,但对于现代生物学中常见的多变量数据的系统发生信号研究仍具有挑战性。在此,我们介绍一种探索多元表型系统发生信号的新方法。我们的方法将数据分解成具有最大(或最小)系统发生信号的线性组合,以布隆伯格 K 值衡量。这些系统发生成分或 K 成分的载荷向量可以从生物学角度进行解释,分数的散点图可以用作数据的低维排序,从而最大(或最小)地保留系统发生信号。我们介绍了多元数据中系统发生信号的代数和统计特性,以及两个新的汇总统计量 KA 和 KG。模拟研究表明,KA 和 KG 比之前建议的统计量 Kmult 具有更高的统计能力,尤其是当系统发生信号较低或集中在几个性状维度时。在对脊椎动物颅骨形状(鳄形目和乳头状目)的两个经验应用中,我们发现具有统计意义的系统发生信号集中在几个性状维度上。系统发生学信号在多变量表型的各个维度上都可能存在很大的差异,这一发现对目前在多变量数据中系统发生学信号的最大似然法有重要影响。
{"title":"Exploring Phylogenetic Signal in Multivariate Phenotypes by Maximizing Blomberg's K.","authors":"Philipp Mitteroecker, Michael L Collyer, Dean C Adams","doi":"10.1093/sysbio/syae035","DOIUrl":"10.1093/sysbio/syae035","url":null,"abstract":"<p><p>Due to the hierarchical structure of the tree of life, closely related species often resemble each other more than distantly related species; a pattern termed phylogenetic signal. Numerous univariate statistics have been proposed as measures of phylogenetic signal for single phenotypic traits, but the study of phylogenetic signal for multivariate data, as is common in modern biology, remains challenging. Here, we introduce a new method to explore phylogenetic signal in multivariate phenotypes. Our approach decomposes the data into linear combinations with maximal (or minimal) phylogenetic signal, as measured by Blomberg's K. The loading vectors of these phylogenetic components or K-components can be biologically interpreted, and scatterplots of the scores can be used as a low-dimensional ordination of the data that maximally (or minimally) preserves phylogenetic signal. We present algebraic and statistical properties, along with 2 new summary statistics, KA and KG, of phylogenetic signal in multivariate data. Simulation studies showed that KA and KG have higher statistical power than the previously suggested statistic Kmult, especially if phylogenetic signal is low or concentrated in a few trait dimensions. In 2 empirical applications to vertebrate cranial shape (crocodyliforms and papionins), we found statistically significant phylogenetic signal concentrated in a few trait dimensions. The finding that phylogenetic signal can be highly variable across the dimensions of multivariate phenotypes has important implications for current maximum likelihood approaches to phylogenetic signal in multivariate data.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"215-229"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11958371/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141545292","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}
Muthukumaran Panchaksaram, Lucas Freitas, Mario Dos Reis
In Bayesian molecular-clock dating of species divergences, rate models are used to construct the prior on the molecular evolutionary rates for branches in the phylogeny, with independent and autocorrelated rate models being commonly used. The two classes of models, however, can result in markedly different divergence time estimates for the same data set, and thus selecting the best rate model appears important for obtaining reliable inferences of divergence times. However, the properties of Bayesian rate model selection are not well understood, in particular when the number of sequence partitions analyzed increases and when age calibrations (such as fossil calibrations) are misspecified. Furthermore, Bayesian rate model selection is computationally expensive as it requires the calculation of marginal likelihoods by Markov Chain Monte Carlo sampling, and therefore, methods that can speed up the model selection procedure without compromising its accuracy are desirable. In this study, we use a combination of computer simulations and real data analysis to investigate the statistical behavior of Bayesian rate model selection and we also explore approximations of the likelihood to improve computational efficiency in large phylogenomic data sets. Our simulations demonstrate that the posterior probability for the correct rate model converges to one as more molecular sequence partitions are analyzed and when no calibrations are used, as expected due to asymptotic Bayesian model selection theory. Furthermore, we also show the model selection procedure is robust to slight misspecification of calibrations, and reliable inference of the correct rate model is possible in this case. However, we show that when calibrations are seriously misspecified, calculated model probabilities are completely wrong and may converge to one for the wrong rate model. Finally, we demonstrate that approximating the phylogenetic likelihood under an arcsine branch-length transform can dramatically reduce the computational cost of rate model selection without compromising accuracy. We test the approximate procedure on two large phylogenies of primates (372 species) and flowering plants (644 species), replicating results obtained on smaller data sets using exact likelihood. Our findings and methodology can assist users in selecting the optimal rate model for estimating times and rates along the Tree of Life.
{"title":"Bayesian Selection of Relaxed-Clock Models: Distinguishing between Independent and Autocorrelated Rates.","authors":"Muthukumaran Panchaksaram, Lucas Freitas, Mario Dos Reis","doi":"10.1093/sysbio/syae066","DOIUrl":"10.1093/sysbio/syae066","url":null,"abstract":"<p><p>In Bayesian molecular-clock dating of species divergences, rate models are used to construct the prior on the molecular evolutionary rates for branches in the phylogeny, with independent and autocorrelated rate models being commonly used. The two classes of models, however, can result in markedly different divergence time estimates for the same data set, and thus selecting the best rate model appears important for obtaining reliable inferences of divergence times. However, the properties of Bayesian rate model selection are not well understood, in particular when the number of sequence partitions analyzed increases and when age calibrations (such as fossil calibrations) are misspecified. Furthermore, Bayesian rate model selection is computationally expensive as it requires the calculation of marginal likelihoods by Markov Chain Monte Carlo sampling, and therefore, methods that can speed up the model selection procedure without compromising its accuracy are desirable. In this study, we use a combination of computer simulations and real data analysis to investigate the statistical behavior of Bayesian rate model selection and we also explore approximations of the likelihood to improve computational efficiency in large phylogenomic data sets. Our simulations demonstrate that the posterior probability for the correct rate model converges to one as more molecular sequence partitions are analyzed and when no calibrations are used, as expected due to asymptotic Bayesian model selection theory. Furthermore, we also show the model selection procedure is robust to slight misspecification of calibrations, and reliable inference of the correct rate model is possible in this case. However, we show that when calibrations are seriously misspecified, calculated model probabilities are completely wrong and may converge to one for the wrong rate model. Finally, we demonstrate that approximating the phylogenetic likelihood under an arcsine branch-length transform can dramatically reduce the computational cost of rate model selection without compromising accuracy. We test the approximate procedure on two large phylogenies of primates (372 species) and flowering plants (644 species), replicating results obtained on smaller data sets using exact likelihood. Our findings and methodology can assist users in selecting the optimal rate model for estimating times and rates along the Tree of Life.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"323-334"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142682823","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}
Bernat Burriel-Carranza, Héctor Tejero-Cicuéndez, Albert Carné, Gabriel Mochales-Riaño, Adrián Talavera, Saleh Al Saadi, Johannes Els, Jiří Šmíd, Karin Tamar, Pedro Tarroso, Salvador Carranza
Advances in genomics have greatly enhanced our understanding of mountain biodiversity, providing new insights into the complex and dynamic mechanisms that drive the formation of mountain biotas. These span from broad biogeographic patterns to population dynamics and adaptations to these environments. However, significant challenges remain in integrating large-scale and fine-scale findings to develop a comprehensive understanding of mountain biodiversity. One significant challenge is the lack of genomic data, especially in historically understudied arid regions where reptiles are a particularly diverse vertebrate group. In the present study, we assembled a de novo genome-wide SNP dataset for the complete endemic reptile fauna of a mountain range (19 described species with more than 600 specimens sequenced), and integrated state-of-the-art biogeographic analyses at the population, species, and community level. Thus, we provide a holistic integration of how a whole endemic reptile community has originated, diversified and dispersed through a mountain system. Our results show that reptiles independently colonized the Hajar Mountains of southeastern Arabia 11 times. After colonization, species delimitation methods suggest high levels of within-mountain diversification, supporting up to 49 deep lineages. This diversity is strongly structured following local topography, with the highest peaks acting as a broad barrier to gene flow among the entire community. Interestingly, orogenic events do not seem key drivers of the biogeographic history of reptiles in this system. Instead, past climatic events seem to have had a major role in this community assemblage. We observe an increase of vicariant events from Late Pliocene onwards, coinciding with an unstable climatic period of rapid shifts between hyper-arid and semiarid conditions that led to the ongoing desertification of Arabia. We conclude that paleoclimate, and particularly extreme aridification, acted as a main driver of diversification in arid mountain systems which is tangled with the generation of highly adapted endemicity. Overall, our study does not only provide a valuable contribution to understanding the evolution of mountain biodiversity, but also offers a flexible and scalable approach that can be reproduced into any taxonomic group and at any discrete environment.
基因组学的进步极大地促进了我们对山区生物多样性的了解,为我们提供了对推动山区生物群落形成的复杂动态机制的新见解。这些机制包括广泛的生物地理格局、种群动态以及对这些环境的适应。然而,在整合大规模和精细规模的研究结果以全面了解山区生物多样性方面仍存在重大挑战。其中一个重大挑战是缺乏基因组数据,尤其是在历史上研究不足的干旱地区,而爬行动物是一个特别多样化的脊椎动物类群。在本研究中,我们为一个山脉的完整特有爬行动物群(19 个描述物种,600 多个标本测序)建立了一个全新的全基因组 SNP 数据集,并在种群、物种和群落层面整合了最先进的生物地理学分析。因此,我们对整个特有爬行动物群落如何在山脉系统中起源、多样化和扩散进行了整体整合。我们的研究结果表明,爬行动物在阿拉伯东南部的哈杰尔山脉独立殖民了 11 次。定殖之后,物种划分方法表明,山地内的多样性水平很高,支持多达 49 个深系。这种多样性是根据当地地形形成的,最高的山峰成为整个群落基因流动的巨大障碍。有趣的是,造山运动似乎并不是该系统中爬行动物生物地理历史的关键驱动因素。相反,过去的气候事件似乎在这一群落组合中发挥了重要作用。我们观察到,从上新世晚期开始,沧海桑田的事件越来越多,而这一时期的气候并不稳定,在极度干旱和半干旱条件之间快速转换,导致了阿拉伯地区的持续沙漠化。我们的结论是,古气候,尤其是极端干旱化,是干旱山地系统多样化的主要驱动力,它与高度适应性地方性的产生纠缠在一起。总之,我们的研究不仅为了解山区生物多样性的演变做出了宝贵贡献,而且提供了一种灵活、可扩展的方法,可用于任何分类群和任何离散环境。
{"title":"Integrating Genomics and Biogeography to Unravel the Origin of a Mountain Biota: The Case of a Reptile Endemicity Hotspot in Arabia.","authors":"Bernat Burriel-Carranza, Héctor Tejero-Cicuéndez, Albert Carné, Gabriel Mochales-Riaño, Adrián Talavera, Saleh Al Saadi, Johannes Els, Jiří Šmíd, Karin Tamar, Pedro Tarroso, Salvador Carranza","doi":"10.1093/sysbio/syae032","DOIUrl":"10.1093/sysbio/syae032","url":null,"abstract":"<p><p>Advances in genomics have greatly enhanced our understanding of mountain biodiversity, providing new insights into the complex and dynamic mechanisms that drive the formation of mountain biotas. These span from broad biogeographic patterns to population dynamics and adaptations to these environments. However, significant challenges remain in integrating large-scale and fine-scale findings to develop a comprehensive understanding of mountain biodiversity. One significant challenge is the lack of genomic data, especially in historically understudied arid regions where reptiles are a particularly diverse vertebrate group. In the present study, we assembled a de novo genome-wide SNP dataset for the complete endemic reptile fauna of a mountain range (19 described species with more than 600 specimens sequenced), and integrated state-of-the-art biogeographic analyses at the population, species, and community level. Thus, we provide a holistic integration of how a whole endemic reptile community has originated, diversified and dispersed through a mountain system. Our results show that reptiles independently colonized the Hajar Mountains of southeastern Arabia 11 times. After colonization, species delimitation methods suggest high levels of within-mountain diversification, supporting up to 49 deep lineages. This diversity is strongly structured following local topography, with the highest peaks acting as a broad barrier to gene flow among the entire community. Interestingly, orogenic events do not seem key drivers of the biogeographic history of reptiles in this system. Instead, past climatic events seem to have had a major role in this community assemblage. We observe an increase of vicariant events from Late Pliocene onwards, coinciding with an unstable climatic period of rapid shifts between hyper-arid and semiarid conditions that led to the ongoing desertification of Arabia. We conclude that paleoclimate, and particularly extreme aridification, acted as a main driver of diversification in arid mountain systems which is tangled with the generation of highly adapted endemicity. Overall, our study does not only provide a valuable contribution to understanding the evolution of mountain biodiversity, but also offers a flexible and scalable approach that can be reproduced into any taxonomic group and at any discrete environment.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":"230-249"},"PeriodicalIF":6.1,"publicationDate":"2025-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11958937/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141493496","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}
Ants are a globally distributed and highly diverse group of eusocial animals, playing key ecological roles in most of the world’s terrestrial ecosystems. Our understanding of the processes involved in the evolution of this diverse family is contingent upon our knowledge of the phylogeny of the ants. While relationships among most subfamilies have come into resolution recently, several of the tribal relationships within the hyperdiverse subfamily Myrmicinae persistently conflict between or within studies, mirroring the controversial relationships of the Leptanillinae and Martialinae to the remaining ant subfamilies. Another persistent issue of debate in ant phylogenetics is the timing of major evolutionary events as inferred via divergence dating. Here, we test the topology of the myrmicine tribes using genome scale data, inspect gene tree-species tree concordance, and use posterior predictive checks and tests of compositional heterogeneity to infer sequence characteristics which potentially introduce systematic bias in myrmicine tribal topology. Furthermore, we test the placement of the Baltic amber fossil †Manica andrannae by integrating phylogenomic and morphological data from nearly all species within the genus Manica, and a broad sampling of its sister genus Myrmica. Subsequently, we demonstrate the effect of fossil placement on overall divergence times in the Myrmicinae. We then re-evaluate the historical biogeography of the Myrmicini and Pogonomyrmecini considering newly generated genetic data and insights from our phylogenomic results. We find that our current understanding of tribal topology in the Myrmicinae is strongly supported, but this topology is highly sensitive to compositional heterogeneity and gene-tree species-tree conflict. Our fossil placement analyses strongly suggest that †Manica andrannae is a stem Manica species, and analysis of this fossil in context of the Myrmicinae demonstrates that a single fossil calibration point can have broad-scale cascading effects on divergence dates within the entire subfamily. The results of our biogeographic reconstructions indicate a South American origin for the Pogonomyrmecini + Myrmicini. Additionally, our results suggest that the MRCA of Myrmica may have inhabited the western Nearctic in the early Miocene prior to repeated dispersal across Beringia throughout the Miocene and Pliocene. The MRCA of Manica, on the other hand, was inferred to have a Holarctic range prior to vicariance during the Pliocene. Unexpectedly, we found strong support in the Pogonomyrmecini for three coordinated dispersal events from South to Central America during the early Miocene, which has been previously proposed as an early biotic interchange event prior to the more commonly accepted 3.5 Ma closure of the Isthmus of Panama.
{"title":"Phylogenomics resolve the systematics and biogeography of the ant tribe Myrmicini and tribal relationships within the hyperdiverse ant subfamily Myrmicinae","authors":"Matthew Prebus, Christian Rabeling","doi":"10.1093/sysbio/syaf022","DOIUrl":"https://doi.org/10.1093/sysbio/syaf022","url":null,"abstract":"Ants are a globally distributed and highly diverse group of eusocial animals, playing key ecological roles in most of the world’s terrestrial ecosystems. Our understanding of the processes involved in the evolution of this diverse family is contingent upon our knowledge of the phylogeny of the ants. While relationships among most subfamilies have come into resolution recently, several of the tribal relationships within the hyperdiverse subfamily Myrmicinae persistently conflict between or within studies, mirroring the controversial relationships of the Leptanillinae and Martialinae to the remaining ant subfamilies. Another persistent issue of debate in ant phylogenetics is the timing of major evolutionary events as inferred via divergence dating. Here, we test the topology of the myrmicine tribes using genome scale data, inspect gene tree-species tree concordance, and use posterior predictive checks and tests of compositional heterogeneity to infer sequence characteristics which potentially introduce systematic bias in myrmicine tribal topology. Furthermore, we test the placement of the Baltic amber fossil †Manica andrannae by integrating phylogenomic and morphological data from nearly all species within the genus Manica, and a broad sampling of its sister genus Myrmica. Subsequently, we demonstrate the effect of fossil placement on overall divergence times in the Myrmicinae. We then re-evaluate the historical biogeography of the Myrmicini and Pogonomyrmecini considering newly generated genetic data and insights from our phylogenomic results. We find that our current understanding of tribal topology in the Myrmicinae is strongly supported, but this topology is highly sensitive to compositional heterogeneity and gene-tree species-tree conflict. Our fossil placement analyses strongly suggest that †Manica andrannae is a stem Manica species, and analysis of this fossil in context of the Myrmicinae demonstrates that a single fossil calibration point can have broad-scale cascading effects on divergence dates within the entire subfamily. The results of our biogeographic reconstructions indicate a South American origin for the Pogonomyrmecini + Myrmicini. Additionally, our results suggest that the MRCA of Myrmica may have inhabited the western Nearctic in the early Miocene prior to repeated dispersal across Beringia throughout the Miocene and Pliocene. The MRCA of Manica, on the other hand, was inferred to have a Holarctic range prior to vicariance during the Pliocene. Unexpectedly, we found strong support in the Pogonomyrmecini for three coordinated dispersal events from South to Central America during the early Miocene, which has been previously proposed as an early biotic interchange event prior to the more commonly accepted 3.5 Ma closure of the Isthmus of Panama.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"183 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-03-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143736827","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}
Lucas D Fernandes, Rogier E Hintzen, Samuel E D Thompson, Tatsiana Barychka, Derek Tittensor, Michael Harfoot, Tim Newbold, James Rosindell
The total number of species on earth and the rate at which new species are created are fundamental questions for ecology, evolution and conservation. These questions have typically been approached separately, despite their obvious interconnection. In this study, we approach both questions in conjunction, for all terrestrial animals. To do this, we combine two previously unconnected bodies of theory: general ecosystem models and individual-based ecological neutral theory. General ecosystem models provide us with estimated numbers of individual organisms, separated by functional group and body size. Neutral theory, applied within a guild of functionally similar individuals, connects species richness, speciation rate, and number of individual organisms. In combination, for terrestrial endotherms where species numbers are known, they provide us with estimates for speciation rates as a function of body size and diet class. Extrapolating the same rates to guilds of ectotherms enables us to estimate the species richness of those groups, including species yet to be described. We find that speciation rates per species per million years decrease with increasing body size. Rates are also higher for carnivores compared to omnivores or herbivores of the same body size. Our estimate for the total number of terrestrial species of animals is in the range 1.03-2.92 million species, a value consistent with estimates from previous studies, despite having used a fundamentally new approach. Perhaps what is most remarkable about these results is that they have been obtained using only limited data from larger endotherms and their speciation rates, with the predictive process being based on mechanistic theory. This work illustrates the potential of a new approach to classic eco-evolutionary questions, while also adding weight to existing predictions. As we now face an era of dramatic biological change, new methods will be needed to mechanistically model global biodiversity at the species and individual organism level. This will be a huge challenge but the combination of general ecosystem models and neutral theory that we introduce here is a way to tractably achieve it.
{"title":"Species Richness and Speciation Rates for all Terrestrial Animals Emerge from a Synthesis of Ecological Theories.","authors":"Lucas D Fernandes, Rogier E Hintzen, Samuel E D Thompson, Tatsiana Barychka, Derek Tittensor, Michael Harfoot, Tim Newbold, James Rosindell","doi":"10.1093/sysbio/syaf006","DOIUrl":"https://doi.org/10.1093/sysbio/syaf006","url":null,"abstract":"<p><p>The total number of species on earth and the rate at which new species are created are fundamental questions for ecology, evolution and conservation. These questions have typically been approached separately, despite their obvious interconnection. In this study, we approach both questions in conjunction, for all terrestrial animals. To do this, we combine two previously unconnected bodies of theory: general ecosystem models and individual-based ecological neutral theory. General ecosystem models provide us with estimated numbers of individual organisms, separated by functional group and body size. Neutral theory, applied within a guild of functionally similar individuals, connects species richness, speciation rate, and number of individual organisms. In combination, for terrestrial endotherms where species numbers are known, they provide us with estimates for speciation rates as a function of body size and diet class. Extrapolating the same rates to guilds of ectotherms enables us to estimate the species richness of those groups, including species yet to be described. We find that speciation rates per species per million years decrease with increasing body size. Rates are also higher for carnivores compared to omnivores or herbivores of the same body size. Our estimate for the total number of terrestrial species of animals is in the range 1.03-2.92 million species, a value consistent with estimates from previous studies, despite having used a fundamentally new approach. Perhaps what is most remarkable about these results is that they have been obtained using only limited data from larger endotherms and their speciation rates, with the predictive process being based on mechanistic theory. This work illustrates the potential of a new approach to classic eco-evolutionary questions, while also adding weight to existing predictions. As we now face an era of dramatic biological change, new methods will be needed to mechanistically model global biodiversity at the species and individual organism level. This will be a huge challenge but the combination of general ecosystem models and neutral theory that we introduce here is a way to tractably achieve it.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":""},"PeriodicalIF":6.1,"publicationDate":"2025-03-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143743968","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}
Sarah H D Santos, Henrique V Figueiró, Tomas Flouri, Emiliano Ramalho, Laury Cullen, Ziheng Yang, William J Murphy, Eduardo Eizirik
Phylogenomic analyses of closely related species allow important glimpses into their evolutionary history. Although recent studies have demonstrated that interspecies hybridization has occurred in several groups, incorporating this process in phylogenetic reconstruction remains challenging. Specifically, the most predominant topology across the genome is often assumed to reflect the speciation tree, but rampant hybridization might overwhelm the genomes, causing that assumption to be violoated. The notoriously challenging phylogeny of the five extant Panthera species (specifically jaguar [P. onca], lion [P. leo], and leopard [P. pardus]) is an interesting system to address this problem. Here we employed a Panthera-wide whole-genome-sequence dataset incorporating three jaguar genomes and two representatives of lions and leopards to dissect the relationships among these three species. Maximum-likelihood trees reconstructed from non-overlapping genomic fragments of four different sizes strongly supported the monophyly of all three species. The most frequent topology (76-95%) united lion+leopard as sister-species (topology 1), followed by lion+jaguar (topology 2: 4-8%) and leopard+jaguar (topology 3: 0-6%). Topology 1 was dominant across the genome, especially in high-recombination regions. Topologies 2 and 3 were enriched in low-recombination segments, likely reflecting the species tree in the face of hybridization. Divergence times between sister-species of each topology, corrected for local recombination rate effects, indicated that the lion-leopard divergence was significantly younger than the alternatives, likely driven by post-speciation admixture. Introgression analyses detected pervasive hybridization between lions and leopards, regardless of the assumed species tree. This inference was strongly supported by multi-species-coalescence-with-introgression (MSci) analyses, which rejected topology 1 or any model without introgression. Interestingly, topologies 2 and 3 with extensive lion-leopard introgression were unidentifiable, highlighting the complexity of this phylogenetic problem. Our results suggest that the dominant genome-wide tree topology is not the true species tree but rather a consequence of overwhelming post-speciation admixture between lion and leopard.
{"title":"Massive inter-species introgression overwhelms phylogenomic relationships among jaguar, lion, and leopard.","authors":"Sarah H D Santos, Henrique V Figueiró, Tomas Flouri, Emiliano Ramalho, Laury Cullen, Ziheng Yang, William J Murphy, Eduardo Eizirik","doi":"10.1093/sysbio/syaf021","DOIUrl":"https://doi.org/10.1093/sysbio/syaf021","url":null,"abstract":"<p><p>Phylogenomic analyses of closely related species allow important glimpses into their evolutionary history. Although recent studies have demonstrated that interspecies hybridization has occurred in several groups, incorporating this process in phylogenetic reconstruction remains challenging. Specifically, the most predominant topology across the genome is often assumed to reflect the speciation tree, but rampant hybridization might overwhelm the genomes, causing that assumption to be violoated. The notoriously challenging phylogeny of the five extant Panthera species (specifically jaguar [P. onca], lion [P. leo], and leopard [P. pardus]) is an interesting system to address this problem. Here we employed a Panthera-wide whole-genome-sequence dataset incorporating three jaguar genomes and two representatives of lions and leopards to dissect the relationships among these three species. Maximum-likelihood trees reconstructed from non-overlapping genomic fragments of four different sizes strongly supported the monophyly of all three species. The most frequent topology (76-95%) united lion+leopard as sister-species (topology 1), followed by lion+jaguar (topology 2: 4-8%) and leopard+jaguar (topology 3: 0-6%). Topology 1 was dominant across the genome, especially in high-recombination regions. Topologies 2 and 3 were enriched in low-recombination segments, likely reflecting the species tree in the face of hybridization. Divergence times between sister-species of each topology, corrected for local recombination rate effects, indicated that the lion-leopard divergence was significantly younger than the alternatives, likely driven by post-speciation admixture. Introgression analyses detected pervasive hybridization between lions and leopards, regardless of the assumed species tree. This inference was strongly supported by multi-species-coalescence-with-introgression (MSci) analyses, which rejected topology 1 or any model without introgression. Interestingly, topologies 2 and 3 with extensive lion-leopard introgression were unidentifiable, highlighting the complexity of this phylogenetic problem. Our results suggest that the dominant genome-wide tree topology is not the true species tree but rather a consequence of overwhelming post-speciation admixture between lion and leopard.</p>","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":" ","pages":""},"PeriodicalIF":6.1,"publicationDate":"2025-03-25","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143701546","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}