Jennifer R Hodge,Danielle S Adams,Keiffer L Williams,Laura R V Alencar,Benjamin Camper,Olivier Larouche,Mason A Thurman,Katerina Zapfe,Samantha A Price
Understanding the ecological drivers and limitations of adaptive convergence is a fundamental challenge. Here, we explore how adaptive convergence of planktivorous fishes has been influenced by multiple ecological factors, evolutionary history, and chance. Using ecomorphological data for over 1600 marine species, we integrate pattern-based metrics of convergence with evolutionary model fitting to test whether phenotypic similarities among specialist planktivores exceed expectations under null models and whether ecology, evolutionary history, or their combined effects best explain trait evolution. We find that planktivores are significantly more similar in phenotype than expected. Traits with functional relevance for prey detection and capture, such as eye diameter and lower jaw length, are strongly convergent, while general body size and shape are constrained by deep divisions between clades where the effects of evolutionary history are most pronounced. Since not all traits undergo strong selection toward a convergent ecomorph, their evolutionary trajectories have not entirely overcome ancestral differences in the multivariate trait space, resulting in a specific form of convergence termed conservatism. We show how adaptive responses to feeding ecology intertwine with other ecological pressures (i.e., light environment) and historical contingency to shape fish phenotype evolution over deep time, offering key insights into the generality of phenotypic evolution.
{"title":"Unravelling the Effects of Ecology and Evolutionary History in the Phenotypic Convergence of Fishes.","authors":"Jennifer R Hodge,Danielle S Adams,Keiffer L Williams,Laura R V Alencar,Benjamin Camper,Olivier Larouche,Mason A Thurman,Katerina Zapfe,Samantha A Price","doi":"10.1093/sysbio/syaf034","DOIUrl":"https://doi.org/10.1093/sysbio/syaf034","url":null,"abstract":"Understanding the ecological drivers and limitations of adaptive convergence is a fundamental challenge. Here, we explore how adaptive convergence of planktivorous fishes has been influenced by multiple ecological factors, evolutionary history, and chance. Using ecomorphological data for over 1600 marine species, we integrate pattern-based metrics of convergence with evolutionary model fitting to test whether phenotypic similarities among specialist planktivores exceed expectations under null models and whether ecology, evolutionary history, or their combined effects best explain trait evolution. We find that planktivores are significantly more similar in phenotype than expected. Traits with functional relevance for prey detection and capture, such as eye diameter and lower jaw length, are strongly convergent, while general body size and shape are constrained by deep divisions between clades where the effects of evolutionary history are most pronounced. Since not all traits undergo strong selection toward a convergent ecomorph, their evolutionary trajectories have not entirely overcome ancestral differences in the multivariate trait space, resulting in a specific form of convergence termed conservatism. We show how adaptive responses to feeding ecology intertwine with other ecological pressures (i.e., light environment) and historical contingency to shape fish phenotype evolution over deep time, offering key insights into the generality of phenotypic evolution.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"1 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143945477","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}
Fernando Alda,S Elizabeth Alter,Naoko P Kurata,Prosanta Chakrabarty,Melanie L J Stiassny
Understanding the drivers of diversification is a central goal in evolutionary biology but can be challenging when lineages radiate quickly and/or hybridize frequently. Cichlids in the tribe Lamprologini, an exceptionally diverse clade found in the Congo basin, exemplify these issues: their evolutionary history has been difficult to untangle with previous datasets, particularly with regard to river-dwelling lineages in the genus Lamprologus. This clade notably includes the only known blind and depigmented cichlid, L. lethops. Here, we reconstructed the evolutionary, population, and biogeographic history of a Lamprologus clade from the Congo River by leveraging genomic data and sampling over 50 lamprologine species from the entire Lake Tanganyika radiation. This study provides the most comprehensive species-level coverage to date of the riverine taxa within this lacustrine-origin clade. We found that in the mid-late Pliocene, two lineages of Lake Tanganyika lamprologines independently colonized the Congo River, where they subsequently hybridized and diversified, forming the current monophyletic group of riverine Lamprologus. Our estimates for divergence time and introgression align with the region's geological history and suggest rapid speciation in Lamprologus species from the Congo River marked by rapids-driven vicariance and water level fluctuations, and repeated episodes of secondary contact and reticulation. As a result of our analyses, we propose the taxonomic restriction of the genus Lamprologus to Congo River taxa only. The complex evolutionary history of this group-characterized by introgressive hybridization followed by a rapid series of isolation and reconnection-illustrates the multifaceted dynamics of speciation that have shaped the rich biodiversity of this region. [African cichlids; Congo River; diversification; hybridization; Lamprologini; phylogenomics; UCEs; ultraconserved elements].
{"title":"Phylogenomic and Population Genomic Analyses of Ultraconserved Elements Reveal Deep Coalescence and Introgression Shaped Diversification Patterns in Lamprologine Cichlids of the Congo River.","authors":"Fernando Alda,S Elizabeth Alter,Naoko P Kurata,Prosanta Chakrabarty,Melanie L J Stiassny","doi":"10.1093/sysbio/syaf032","DOIUrl":"https://doi.org/10.1093/sysbio/syaf032","url":null,"abstract":"Understanding the drivers of diversification is a central goal in evolutionary biology but can be challenging when lineages radiate quickly and/or hybridize frequently. Cichlids in the tribe Lamprologini, an exceptionally diverse clade found in the Congo basin, exemplify these issues: their evolutionary history has been difficult to untangle with previous datasets, particularly with regard to river-dwelling lineages in the genus Lamprologus. This clade notably includes the only known blind and depigmented cichlid, L. lethops. Here, we reconstructed the evolutionary, population, and biogeographic history of a Lamprologus clade from the Congo River by leveraging genomic data and sampling over 50 lamprologine species from the entire Lake Tanganyika radiation. This study provides the most comprehensive species-level coverage to date of the riverine taxa within this lacustrine-origin clade. We found that in the mid-late Pliocene, two lineages of Lake Tanganyika lamprologines independently colonized the Congo River, where they subsequently hybridized and diversified, forming the current monophyletic group of riverine Lamprologus. Our estimates for divergence time and introgression align with the region's geological history and suggest rapid speciation in Lamprologus species from the Congo River marked by rapids-driven vicariance and water level fluctuations, and repeated episodes of secondary contact and reticulation. As a result of our analyses, we propose the taxonomic restriction of the genus Lamprologus to Congo River taxa only. The complex evolutionary history of this group-characterized by introgressive hybridization followed by a rapid series of isolation and reconnection-illustrates the multifaceted dynamics of speciation that have shaped the rich biodiversity of this region. [African cichlids; Congo River; diversification; hybridization; Lamprologini; phylogenomics; UCEs; ultraconserved elements].","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"44 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143945478","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}
Holly M Robertson, Joseph F Walker, Edwige Moyroud
Phenotypic convergence is found across the tree of life, and morphological similarities in distantly related species are often presumed to have evolved independently. However, clarifying the origins of traits has recently highlighted the complex nature of evolution, as apparent convergent features often share similar genetic foundations. Hence, the tree topology of genes that underlie such traits frequently conflicts with the overall history of species relationships. This conflict, which usually results from incomplete lineage sorting, introgression or horizontal gene transfer, creates both a challenge for systematists and an exciting opportunity to investigate the rich, complex network of information that connects molecular trajectories with trait evolution. Here we present a novel conflict identification program named CAnDI (Conflict And Duplication Identifier), which enables the analysis of conflict in homologous gene trees rather than inferred orthologs. We demonstrate that the analysis of conflicts in homologous trees using CAnDI yields more comparisons than in ortholog trees in six datasets from across the eukaryotic tree of life. Using the carnivorous trap of Caryophyllales, a charismatic group of flowering plants, as a case study we demonstrate that analysing conflict on entire homolog trees can aid in inferring the contribution of standing genetic variation to trait evolution: by dissecting all gene relationships within homolog trees, we find genomic evidence that the molecular basis of the pleisiomorphic mucilaginous sticky trap was likely present in the ancestor of all carnivorous Caryophyllales. We also show that many genes whose evolutionary trajectories group species with similar trap devices code for proteins contributing to plant carnivory and identify a LATERAL ORGAN BOUNDARY DOMAIN transcription factor as a possible candidate for regulating sticky trap development.
{"title":"CAnDI: a new tool to investigate conflict in homologous gene trees and explain convergent trait evolution","authors":"Holly M Robertson, Joseph F Walker, Edwige Moyroud","doi":"10.1093/sysbio/syaf028","DOIUrl":"https://doi.org/10.1093/sysbio/syaf028","url":null,"abstract":"Phenotypic convergence is found across the tree of life, and morphological similarities in distantly related species are often presumed to have evolved independently. However, clarifying the origins of traits has recently highlighted the complex nature of evolution, as apparent convergent features often share similar genetic foundations. Hence, the tree topology of genes that underlie such traits frequently conflicts with the overall history of species relationships. This conflict, which usually results from incomplete lineage sorting, introgression or horizontal gene transfer, creates both a challenge for systematists and an exciting opportunity to investigate the rich, complex network of information that connects molecular trajectories with trait evolution. Here we present a novel conflict identification program named CAnDI (Conflict And Duplication Identifier), which enables the analysis of conflict in homologous gene trees rather than inferred orthologs. We demonstrate that the analysis of conflicts in homologous trees using CAnDI yields more comparisons than in ortholog trees in six datasets from across the eukaryotic tree of life. Using the carnivorous trap of Caryophyllales, a charismatic group of flowering plants, as a case study we demonstrate that analysing conflict on entire homolog trees can aid in inferring the contribution of standing genetic variation to trait evolution: by dissecting all gene relationships within homolog trees, we find genomic evidence that the molecular basis of the pleisiomorphic mucilaginous sticky trap was likely present in the ancestor of all carnivorous Caryophyllales. We also show that many genes whose evolutionary trajectories group species with similar trap devices code for proteins contributing to plant carnivory and identify a LATERAL ORGAN BOUNDARY DOMAIN transcription factor as a possible candidate for regulating sticky trap development.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"27 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143920035","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}
Loïs Rancilhac, Stacey G de Souza, Sifiso M Lukhele, Matteo Sebastianelli, Bridget O Ogolowa, Michaella Moysi, Christos Nikiforou, Tsyon Asfaw, Colleen T Downs, Alan Brelsford, Bridgett M vonHoldt, Alexander N G Kirschel
Genomic analyses of hybrid zones provide excellent opportunities to investigate the consequences of introgression in nature. In combination with phylogenomics analyses, hybrid zone studies may illuminate the role of ancient and contemporary gene flow in shaping variation of phylogenetic signals across the genome, but this avenue has not been explored yet. We combined phylogenomic and geographic cline analyses in a Pogoniulus tinkerbird clade to determine whether contemporary introgression through hybrid zones contributes to gene-tree heterogeneity across the species ranges. We found diverse phylogenetic signals across the genome with the most common topologies supporting monophyly among taxa connected by secondary contact zones. Remarkably, these systematic conflicts were also recovered when selecting only individuals from each taxon's core range. Using analyses of derived allele sharing and “recombination aware” phylogenomics, we found that introgression shapes gene-tree heterogeneity, and the species tree most likely supports monophyletic red-fronted tinkerbirds, as recovered in previous reconstructions based on mitochondrial DNA. Furthermore, by fitting geographic clines across two secondary contact zones, we found that introgression rates were lower in genomic regions supporting the putative species tree compared to those supporting the two taxa in contact as monophyletic. This demonstrates that introgression through narrow contact zones shapes gene-tree heterogeneity even in allopatric populations. Finally, we did not find evidence that mitochondria-interacting nuclear genes acted as barrier loci. Our results show that species can withstand important amounts of introgression while maintaining their phenotypic integrity and ecological separation, raising questions regarding the genomic architecture of adaptation and barriers to gene flow.
{"title":"Introgression across narrow contact zones shapes the genomic landscape of phylogenetic variation in an African bird clade","authors":"Loïs Rancilhac, Stacey G de Souza, Sifiso M Lukhele, Matteo Sebastianelli, Bridget O Ogolowa, Michaella Moysi, Christos Nikiforou, Tsyon Asfaw, Colleen T Downs, Alan Brelsford, Bridgett M vonHoldt, Alexander N G Kirschel","doi":"10.1093/sysbio/syaf033","DOIUrl":"https://doi.org/10.1093/sysbio/syaf033","url":null,"abstract":"Genomic analyses of hybrid zones provide excellent opportunities to investigate the consequences of introgression in nature. In combination with phylogenomics analyses, hybrid zone studies may illuminate the role of ancient and contemporary gene flow in shaping variation of phylogenetic signals across the genome, but this avenue has not been explored yet. We combined phylogenomic and geographic cline analyses in a Pogoniulus tinkerbird clade to determine whether contemporary introgression through hybrid zones contributes to gene-tree heterogeneity across the species ranges. We found diverse phylogenetic signals across the genome with the most common topologies supporting monophyly among taxa connected by secondary contact zones. Remarkably, these systematic conflicts were also recovered when selecting only individuals from each taxon's core range. Using analyses of derived allele sharing and “recombination aware” phylogenomics, we found that introgression shapes gene-tree heterogeneity, and the species tree most likely supports monophyletic red-fronted tinkerbirds, as recovered in previous reconstructions based on mitochondrial DNA. Furthermore, by fitting geographic clines across two secondary contact zones, we found that introgression rates were lower in genomic regions supporting the putative species tree compared to those supporting the two taxa in contact as monophyletic. This demonstrates that introgression through narrow contact zones shapes gene-tree heterogeneity even in allopatric populations. Finally, we did not find evidence that mitochondria-interacting nuclear genes acted as barrier loci. Our results show that species can withstand important amounts of introgression while maintaining their phenotypic integrity and ecological separation, raising questions regarding the genomic architecture of adaptation and barriers to gene flow.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"119 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143920036","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}
Methods for rapidly inferring the evolutionary history of species or populations with, genome-wide data are progressing, but computational constraints still limit our abilities in, this area. We developed an alignment-free method to infer genome-wide phylogenies and, implemented it in the Python package TopicContml. The method uses probabilistic, topic modeling (specifically, Latent Dirichlet Allocation or LDA) to extract ‘topic’, frequencies from k-mers, which are derived from multilocus DNA sequences. These, extracted frequencies then serve as an input for the program Contml in the PHYLIP, package, which is used to generate a species tree. We evaluated the performance of, TopicContml on simulated datasets with gaps and three biological datasets: (1) 14 DNA, sequence loci from two Australian bird species distributed across nine populations, (2), 5162 loci from 80 mammal species, and (3) raw, unaligned, non-orthologous PacBio, sequences from 12 bird species. We also assessed the uncertainty of the estimated, relationships among clades using a bootstrap procedure. Our empirical results and, simulated data suggest that our method is efficient and statistically robust.
{"title":"Estimating Genome-wide Phylogenies Using Probabilistic Topic Modeling","authors":"Marzieh Khodaei, Scott V Edwards, Peter Beerli","doi":"10.1093/sysbio/syaf015","DOIUrl":"https://doi.org/10.1093/sysbio/syaf015","url":null,"abstract":"Methods for rapidly inferring the evolutionary history of species or populations with, genome-wide data are progressing, but computational constraints still limit our abilities in, this area. We developed an alignment-free method to infer genome-wide phylogenies and, implemented it in the Python package TopicContml. The method uses probabilistic, topic modeling (specifically, Latent Dirichlet Allocation or LDA) to extract ‘topic’, frequencies from k-mers, which are derived from multilocus DNA sequences. These, extracted frequencies then serve as an input for the program Contml in the PHYLIP, package, which is used to generate a species tree. We evaluated the performance of, TopicContml on simulated datasets with gaps and three biological datasets: (1) 14 DNA, sequence loci from two Australian bird species distributed across nine populations, (2), 5162 loci from 80 mammal species, and (3) raw, unaligned, non-orthologous PacBio, sequences from 12 bird species. We also assessed the uncertainty of the estimated, relationships among clades using a bootstrap procedure. Our empirical results and, simulated data suggest that our method is efficient and statistically robust.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"50 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143910412","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}
Joseph Rusinko, Yu Cai, Allison Crysler, Katherine Thompson, Julien Boutte, Mark Fishbein, Shannon C K Straub
After collecting large data sets for phylogenomics studies, researchers must decide which, genes or samples to include when reconstructing a species tree. Incomplete or unreliable, data sets make the empiricist’s decision more difficult. Researchers rely on ad hoc, strategies to maximize sampling while ensuring sufficient data for accurate inferences. An, algorithm called PickMe formalizes the sample selection process, assuming that the, samples evolved under the Tree Multispecies Coalescent model. We propose a Bayesian, framework for selecting samples for species tree analysis. Given a collection of gene trees, we compute a posterior probability for each quartet, describing the likelihood that the, species tree displays this topology. From this, we assign individual samples reliability, scores computed as the average of a scaled version of the posterior probabilities. PickMe, uses these weights to recommend which samples to include in a species tree analysis., Analysis of simulated data showed that including the samples suggested by Pickme, produced species trees closer to the true species trees than both unfiltered data sets and, data sets with ad hoc gene occupancy cut-offs applied. To further illustrate the efficacy of, this tool, we apply PickMe to gene trees generated from target capture data from, milkweeds. PickMe indicates more samples could have reliably been included in a previous, milkweed phylogenomic analysis than the authors analyzed without access to a formal, methodology for sample selection. Using simulated and empirical data, we also compare, PickMe to existing sample selection methods. Inclusion of PickMe will enhance, phylogenomics data analysis pipelines by providing a formal structure for sample selection.
{"title":"PickMe: Sample selection for species tree reconstruction using coalescent weighted quartets","authors":"Joseph Rusinko, Yu Cai, Allison Crysler, Katherine Thompson, Julien Boutte, Mark Fishbein, Shannon C K Straub","doi":"10.1093/sysbio/syaf017","DOIUrl":"https://doi.org/10.1093/sysbio/syaf017","url":null,"abstract":"After collecting large data sets for phylogenomics studies, researchers must decide which, genes or samples to include when reconstructing a species tree. Incomplete or unreliable, data sets make the empiricist’s decision more difficult. Researchers rely on ad hoc, strategies to maximize sampling while ensuring sufficient data for accurate inferences. An, algorithm called PickMe formalizes the sample selection process, assuming that the, samples evolved under the Tree Multispecies Coalescent model. We propose a Bayesian, framework for selecting samples for species tree analysis. Given a collection of gene trees, we compute a posterior probability for each quartet, describing the likelihood that the, species tree displays this topology. From this, we assign individual samples reliability, scores computed as the average of a scaled version of the posterior probabilities. PickMe, uses these weights to recommend which samples to include in a species tree analysis., Analysis of simulated data showed that including the samples suggested by Pickme, produced species trees closer to the true species trees than both unfiltered data sets and, data sets with ad hoc gene occupancy cut-offs applied. To further illustrate the efficacy of, this tool, we apply PickMe to gene trees generated from target capture data from, milkweeds. PickMe indicates more samples could have reliably been included in a previous, milkweed phylogenomic analysis than the authors analyzed without access to a formal, methodology for sample selection. Using simulated and empirical data, we also compare, PickMe to existing sample selection methods. Inclusion of PickMe will enhance, phylogenomics data analysis pipelines by providing a formal structure for sample selection.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"29 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143910413","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}
A relationship between the rate of molecular change and diversification has long been, discussed, on both theoretical and empirical grounds. However, the effect on our, understanding of evolutionary patterns is yet to be fully explored. Here we develop a new, model, the Covariant Evolutionary Tempo (CET) model, with the aim of integrating, patterns of diversification and molecular evolution within a framework of a continuously, changing ‘tempo’ variable that acts as a master control for molecular, morphological and, diversification rates. Importantly, tempo itself is treated as being variable at a rate, proportional to its own value. This model predicts that diversity is dominated by a small, number of extremely large clades at any historical epoch including the present; that these, large clades are expected to be characterised by explosive early radiations accompanied by, elevated rates of molecular evolution; and that extant organisms are likely to have evolved, from species with unusually fast evolutionary rates. Under such a model, the amount of, molecular change along a particular lineage is essentially independent of its height, which, weakens the molecular clock hypothesis. Finally, our model explains the existence of ‘living, fossil’ sister groups to large clades that are species poor and exhibit slow rates of, morphological and molecular change. Our results demonstrate that the observed historical, patterns of evolution can be modelled without invoking special evolutionary mechanisms or, innovations that are unique to specific times or taxa, even when they are highly, non-uniform
{"title":"Evolutionary Tempo, Supertaxa and Living Fossils","authors":"Graham E Budd, Richard P Mann","doi":"10.1093/sysbio/syaf020","DOIUrl":"https://doi.org/10.1093/sysbio/syaf020","url":null,"abstract":"A relationship between the rate of molecular change and diversification has long been, discussed, on both theoretical and empirical grounds. However, the effect on our, understanding of evolutionary patterns is yet to be fully explored. Here we develop a new, model, the Covariant Evolutionary Tempo (CET) model, with the aim of integrating, patterns of diversification and molecular evolution within a framework of a continuously, changing ‘tempo’ variable that acts as a master control for molecular, morphological and, diversification rates. Importantly, tempo itself is treated as being variable at a rate, proportional to its own value. This model predicts that diversity is dominated by a small, number of extremely large clades at any historical epoch including the present; that these, large clades are expected to be characterised by explosive early radiations accompanied by, elevated rates of molecular evolution; and that extant organisms are likely to have evolved, from species with unusually fast evolutionary rates. Under such a model, the amount of, molecular change along a particular lineage is essentially independent of its height, which, weakens the molecular clock hypothesis. Finally, our model explains the existence of ‘living, fossil’ sister groups to large clades that are species poor and exhibit slow rates of, morphological and molecular change. Our results demonstrate that the observed historical, patterns of evolution can be modelled without invoking special evolutionary mechanisms or, innovations that are unique to specific times or taxa, even when they are highly, non-uniform","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"25 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143910414","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}
Yuezheng Tu, Xuankun Li, Fumio Hayashi, Feng Zhang, Ding Yang, Fabien L Condamine, Xingyue Liu
Evolutionary radiations are considered key processes underlying the origin of biodiversity. Notably, the mechanisms driving these radiations can vary across organisms and often involve a complex interplay of abiotic and biotic factors. Empirical studies on evolutionary history are crucial for validation of multiple hypothesis regarding the mode of evolutionary radiations. Within the aquatic insect order Megaloptera, the genus Protohermes is the most speciose clade with 90 described species, accounting for around 22% of the total ordinal diversity. Protohermes species are featured by the limited dispersal ability, primarily occurring across the Oriental region, and a range of diversified phenotypes, e.g., highly divergent genital characters, and mimetic coloration alongside shifts in biological rhythm—from nocturnal to diurnal activities. Here we infer the spatiotemporal mode of diversification and associated driving factors of the Protohermes radiation as a test case for exploring the processes and potential mechanisms of evolutionary radiations. We present the first time-calibrated phylogeny of Protohermes using genome-scale data of ultraconserved elements (UCEs) and mitochondrial genes with a comprehensive taxon sampling. Our results reveal a mid-Cretaceous stem age of Protohermes, followed by a recent and steady diversification during the Neogene. Estimation of historical biogeography suggests the genus likely originated from a broad range including the Himalayas-Hengduan Mountains + Indochina + Borneo, with the first two areas serving as the center of early diversification. Our results further suggest that vicariance events, likely attributed to the Cenozoic Himalayan orogeny as well as climate change in East Asia, triggered speciation that coincided with the accumulation of genital divergence. Further enhancement of genital and phenotypic diversification may have been promoted by secondary contacts of allopatric or parapatric lineages following the build-up of species richness, likely facilitating species coexistence and lineage accumulation. We argue that the current species diversity of Protohermes likely resulted from a non-adaptive radiation. Our results highlight the role of geographic vicariance and sexual selection in driving the species and phenotypic diversification in insects.
{"title":"Non-adaptive Radiation Promotes Phenotypic Diversification and Convergent Evolution of Aposematic Mimicry in a Highly Diverse Genus of Megaloptera","authors":"Yuezheng Tu, Xuankun Li, Fumio Hayashi, Feng Zhang, Ding Yang, Fabien L Condamine, Xingyue Liu","doi":"10.1093/sysbio/syaf030","DOIUrl":"https://doi.org/10.1093/sysbio/syaf030","url":null,"abstract":"Evolutionary radiations are considered key processes underlying the origin of biodiversity. Notably, the mechanisms driving these radiations can vary across organisms and often involve a complex interplay of abiotic and biotic factors. Empirical studies on evolutionary history are crucial for validation of multiple hypothesis regarding the mode of evolutionary radiations. Within the aquatic insect order Megaloptera, the genus Protohermes is the most speciose clade with 90 described species, accounting for around 22% of the total ordinal diversity. Protohermes species are featured by the limited dispersal ability, primarily occurring across the Oriental region, and a range of diversified phenotypes, e.g., highly divergent genital characters, and mimetic coloration alongside shifts in biological rhythm—from nocturnal to diurnal activities. Here we infer the spatiotemporal mode of diversification and associated driving factors of the Protohermes radiation as a test case for exploring the processes and potential mechanisms of evolutionary radiations. We present the first time-calibrated phylogeny of Protohermes using genome-scale data of ultraconserved elements (UCEs) and mitochondrial genes with a comprehensive taxon sampling. Our results reveal a mid-Cretaceous stem age of Protohermes, followed by a recent and steady diversification during the Neogene. Estimation of historical biogeography suggests the genus likely originated from a broad range including the Himalayas-Hengduan Mountains + Indochina + Borneo, with the first two areas serving as the center of early diversification. Our results further suggest that vicariance events, likely attributed to the Cenozoic Himalayan orogeny as well as climate change in East Asia, triggered speciation that coincided with the accumulation of genital divergence. Further enhancement of genital and phenotypic diversification may have been promoted by secondary contacts of allopatric or parapatric lineages following the build-up of species richness, likely facilitating species coexistence and lineage accumulation. We argue that the current species diversity of Protohermes likely resulted from a non-adaptive radiation. Our results highlight the role of geographic vicariance and sexual selection in driving the species and phenotypic diversification in insects.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"42 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143902886","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}
Rowan J Schley, Rosalía Piñeiro, James A Nicholls, Flávia Fonseca Pezzini, Audrey Farbos, Gwilym P Lewis, Jens J Ringelberg, Catherine Kidner, Alex D Twyford, Kyle G Dexter, R Toby Pennington
Evolutionary radiations underlie much of the species diversity of life on Earth, particularly within the world’s most species-rich tree flora – that of the Amazon rainforest. Hybridisation occurs in many radiations, with effects ranging from homogenisation of divergent species to the generation of genetic and phenotypic novelty that fuels speciation. However, the influence of hybridisation on Amazonian tree radiations has been little studied. We address this using the ubiquitous, species-rich, neotropical tree genus Inga, which typifies rapid radiations of rainforest trees. We assess patterns of gene tree incongruence to ascertain whether hybridisation was associated with rapid radiation in Inga. Given the importance of insect herbivory in structuring rainforest tree communities (and hence the potential for hybridisation to promote adaptation through admixture of defence traits), we also test whether introgression of loci underlying chemical defences against herbivory occurred during the radiation of Inga. Our phylogenomic analyses of 189/288 Inga species using >1300 target capture loci showed widespread introgression in Inga. Specifically, we found widespread phylogenetic incongruence explained by introgression, with phylogenetic networks recovering multiple introgression events across Inga and up to 20% of shared, likely introgressed, genetic variation between some species. In addition, most defence chemistry loci showed evidence of positive selection and marginally higher levels of introgression. Overall, our results suggest that introgression has occurred widely over the course of Inga’s history, possibly in a syngameon scenario, likely facilitated by extensive dispersal across Amazonia. Furthermore, in some cases introgression of chemical defence loci may influence adaptation in Inga.
{"title":"Rampant Reticulation in a Rapid Radiation of Tropical Trees -Insights from Inga (Fabaceae)","authors":"Rowan J Schley, Rosalía Piñeiro, James A Nicholls, Flávia Fonseca Pezzini, Audrey Farbos, Gwilym P Lewis, Jens J Ringelberg, Catherine Kidner, Alex D Twyford, Kyle G Dexter, R Toby Pennington","doi":"10.1093/sysbio/syaf027","DOIUrl":"https://doi.org/10.1093/sysbio/syaf027","url":null,"abstract":"Evolutionary radiations underlie much of the species diversity of life on Earth, particularly within the world’s most species-rich tree flora – that of the Amazon rainforest. Hybridisation occurs in many radiations, with effects ranging from homogenisation of divergent species to the generation of genetic and phenotypic novelty that fuels speciation. However, the influence of hybridisation on Amazonian tree radiations has been little studied. We address this using the ubiquitous, species-rich, neotropical tree genus Inga, which typifies rapid radiations of rainforest trees. We assess patterns of gene tree incongruence to ascertain whether hybridisation was associated with rapid radiation in Inga. Given the importance of insect herbivory in structuring rainforest tree communities (and hence the potential for hybridisation to promote adaptation through admixture of defence traits), we also test whether introgression of loci underlying chemical defences against herbivory occurred during the radiation of Inga. Our phylogenomic analyses of 189/288 Inga species using >1300 target capture loci showed widespread introgression in Inga. Specifically, we found widespread phylogenetic incongruence explained by introgression, with phylogenetic networks recovering multiple introgression events across Inga and up to 20% of shared, likely introgressed, genetic variation between some species. In addition, most defence chemistry loci showed evidence of positive selection and marginally higher levels of introgression. Overall, our results suggest that introgression has occurred widely over the course of Inga’s history, possibly in a syngameon scenario, likely facilitated by extensive dispersal across Amazonia. Furthermore, in some cases introgression of chemical defence loci may influence adaptation in Inga.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"35 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-05-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143902885","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}
Ivan Lorca-Alonso, Otero-de-Navascues Fernando, Miguel Arenas, Ugo Bastolla
In previous studies, we presented our site-specific Stability Constrained substitution models of Protein Evolution (Stab-CPE) that define fitness as the probability of finding a protein folded in its native state but ignore changes in the native structure. Stab-CPE models can be used to predict a more realistic evolutionary variability across protein sites, nevertheless they still qualitatively differ from observed data and appear too tolerant to mutations. Here we present novel structurally constrained substitution models (Str-CPE) that define fitness based on the structural deformation produced by a mutation, which we predict adopting an extension of Juli’an Echaveás linearly forced elastic network model. Compared to our previous Stab-CPE models, the novel Str-CPE models are more stringent (they predict lower sequence entropy and substitution rate), provide higher likelihood to multiple sequence alignments (MSAs) that include one or more known structures, and better predict the observed conservation across sites. The models that combine Str-CPE and Stab-CPE models are even more stringent and fit the empirical MSAs better. We collectively refer to our models as Structure and Stability Constrained substitution models of Protein Evolution (SSCPE). When using distantly-related proteins, we find that more similar phylogenies are inferred under the SSCPE models than under traditional empirical substitution models if compared to the corresponding reference phylogenies inferred using structural distances. Therefore, SSCPE models seem to be much better-fitting substitution models for deep phylogeny inference. The SSCPE models have been implemented in the PERL-based program SSCPE.pl, which uses RAxML-NG to infer phylogenies under the SSCPE model given a concatenated MSA and a list of protein structures that match the sequences in the MSA.
{"title":"Site-specific structure and stability constrained substitution models improve phylogenetic inference","authors":"Ivan Lorca-Alonso, Otero-de-Navascues Fernando, Miguel Arenas, Ugo Bastolla","doi":"10.1093/sysbio/syaf007","DOIUrl":"https://doi.org/10.1093/sysbio/syaf007","url":null,"abstract":"In previous studies, we presented our site-specific Stability Constrained substitution models of Protein Evolution (Stab-CPE) that define fitness as the probability of finding a protein folded in its native state but ignore changes in the native structure. Stab-CPE models can be used to predict a more realistic evolutionary variability across protein sites, nevertheless they still qualitatively differ from observed data and appear too tolerant to mutations. Here we present novel structurally constrained substitution models (Str-CPE) that define fitness based on the structural deformation produced by a mutation, which we predict adopting an extension of Juli’an Echaveás linearly forced elastic network model. Compared to our previous Stab-CPE models, the novel Str-CPE models are more stringent (they predict lower sequence entropy and substitution rate), provide higher likelihood to multiple sequence alignments (MSAs) that include one or more known structures, and better predict the observed conservation across sites. The models that combine Str-CPE and Stab-CPE models are even more stringent and fit the empirical MSAs better. We collectively refer to our models as Structure and Stability Constrained substitution models of Protein Evolution (SSCPE). When using distantly-related proteins, we find that more similar phylogenies are inferred under the SSCPE models than under traditional empirical substitution models if compared to the corresponding reference phylogenies inferred using structural distances. Therefore, SSCPE models seem to be much better-fitting substitution models for deep phylogeny inference. The SSCPE models have been implemented in the PERL-based program SSCPE.pl, which uses RAxML-NG to infer phylogenies under the SSCPE model given a concatenated MSA and a list of protein structures that match the sequences in the MSA.","PeriodicalId":22120,"journal":{"name":"Systematic Biology","volume":"5 1","pages":""},"PeriodicalIF":6.5,"publicationDate":"2025-04-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"143866191","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}