Speciation Times Research Articles

Identifiability of speciation times under the multispecies coalescent

The advent of rapid and inexpensive sequencing technologies has necessitated the development of computationally efficient methods for analyzing sequence data for many genes simultaneously in a phylogenetic framework. The coalescent process is the most commonly used model for linking the underlying genealogies of individual genes with the global species-level phylogeny, but inference under the coalescent model is computationally daunting in the typical inference frameworks (e.g., the likelihood and Bayesian frameworks) due to the dimensionality of the space of both gene trees and species trees. Here we consider estimation of the branch lengths in fixed species trees with three or four taxa, and show that these branch lengths are identifiable. We also show that for three and four taxa simple estimators for the branch lengths can be derived based on observed site pattern frequencies. Properties of these estimators, such as their asymptotic variances and large-sample distributions, are examined, and performance of the estimators is assessed using simulation. Finally, we use these estimators to develop a hypothesis test that can be used to delimit species under the coalescent model for three or four putative taxa.

Phylogenomic analyses of all species of swordtail fishes (genus Xiphophorus) show that hybridization preceded speciation

Hybridization has been recognized to play important roles in evolution, however studies of the genetic consequence are still lagging behind in vertebrates due to the lack of appropriate experimental systems. Fish of the genus Xiphophorus are proposed to have evolved with multiple ancient and ongoing hybridization events. They have served as an informative research model in evolutionary biology and in biomedical research on human disease for more than a century. Here, we provide the complete genomic resource including annotations for all described 26 Xiphophorus species and three undescribed taxa and resolve all uncertain phylogenetic relationships. We investigate the molecular evolution of genes related to cancers such as melanoma and for the genetic control of puberty timing, focusing on genes that are predicted to be involved in pre-and postzygotic isolation and thus affect hybridization. We discovered dramatic size-variation of some gene families. These persisted despite reticulate evolution, rapid speciation and short divergence time. Finally, we clarify the hybridization history in the entire genus settling disputed hybridization history of two Southern swordtails. Our comparative genomic analyses revealed hybridization ancestries that are manifested in the mosaic fused genomes and show that hybridization often preceded speciation.

Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation.

Popular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions, assume that, at speciation, a trait value is inherited identically by two 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.

An 8000 years old genome reveals the Neolithic origin of the zoonosis Brucella melitensis

Brucella melitensis is a major livestock bacterial pathogen and zoonosis, causing disease and infection-related abortions in small ruminants and humans. A considerable burden to animal-based economies today, the presence of Brucella in Neolithic pastoral communities has been hypothesised but we lack direct genomic evidence thus far. We report a 3.45X B. melitensis genome preserved in an ~8000 year old sheep specimen from Menteşe Höyük, Northwest Türkiye, demonstrating that the pathogen had evolved and was circulating in Neolithic livestock. The genome is basal with respect to all known B. melitensis and allows the calibration of the B. melitensis speciation time from the primarily cattle-infecting B. abortus to approximately 9800 years Before Present (BP), coinciding with a period of consolidation and dispersal of livestock economies. We use the basal genome to timestamp evolutionary events in B. melitensis, including pseudogenization events linked to erythritol response, the supposed determinant of the pathogen’s placental tropism in goats and sheep. Our data suggest that the development of herd management and multi-species livestock economies in the 11th–9th millennium BP drove speciation and host adaptation of this zoonotic pathogen.

Detecting diversifying selection for a trait from within and between-species genotypes and phenotypes.

To quantify selection acting on a trait, methods have been developed using either within or between-species variation. However, methods using within-species variation do not integrate the changes at the macroevolutionary scale. Conversely, current methods using between-species variation usually discard within-species variation, thus not accounting for processes at the micro-evolutionary scale. The main goal of this study is to define a neutrality index for a quantitative trait, by combining withinand between-species variation. This neutrality index integrates nucleotide polymorphism and divergence for normalizing trait variation. As such, it does not require estimation of population size nor of time of speciation for normalization. Our index can be used to seek deviation from the null model of neutral evolution, and test for diversifying selection. Applied to brain mass and body mass at the mammalian scale, we show that brain mass is under diversifying selection. Finally, we show that our test is not sensitive to the assumption that population sizes, mutation rates and generation time are constant across the phylogeny, and automatically adjust for it.

The Problems of DNA-Barcoding the Shads of Genus Alosa (Alosidae) of the Ponto-Caspian Basin

—Numerous studies show that species identification of representatives of the genus Alosa using various genetic markers is often difficult and the search for more specific biomarkers is required. For the first time we analyzed polymorphism of COI gene fragment of mitochondrial DNA of two representatives of this genus (A. tanaica and A. kessleri), supplemented with new data on A. immaculata, from the waters of the Ponto-Caspian basin in comparative aspect with other representatives of the herring (Clupeoidea) genera Alosa, Clupea, Clupeonella, Sprattus, and Sardinops. The main result was the conclusion that within the genus Alosa, it is not possible to identify species using the marker used. On the one hand, specimens collected from morphologically distinct individuals and identified as different species have the same haplotypes. On the other hand, samples belonging to different species differ from each other by an insignificant number of nucleotide substitutions and do not form independent clades on the phylogram and haplotype network. This indicates the absence of genetic differentiation between the studied samples of herrings of genus Alosa into separate species and species groups when using DNA barcoding based on the COI gene. The reasons for such a phenomenon may be the following: (1) incorrect identification of species in catches, since shads (Alosidae) have high morphological flexibility and in many species, the main external morphological characters often overlap; (2) recent time of speciation by the standards of biological evolution for shads of genus Alosa; (3) difference in proportion of interspecific hybrids, which can vary significantly between populations of the same species.

Speciation patterns of Aedes mosquitoes in the Scutellaris Group: a mitochondrial perspective

The Scutellaris Group of Aedes comprises 47 mosquito species, including Aedes albopictus. While Ae. albopictus is widely distributed, the other species are mostly found in the Asia–Pacific region. Evolutionary history researches of Aedes species within the Scutellaris Group have mainly focused on Ae. albopictus, a species that raises significant public health concerns, neglecting the other species. In this study, we aimed to assess genetic diversity and estimate speciation times of several species within the Scutellaris Group. Mosquitoes were therefore collected from various Asia–Pacific countries. Their mitochondrial cytochrome c oxidase subunit 1 (cox1) and subunit 3 (cox3) sequences were analyzed alongside those of other Scutellaris Group species available in the GenBank database. To estimate the divergence time, we analyzed 1849 cox1 gene sequences from 21 species, using three species (Aedes aegypti, Aedes notoscriptus and Aedes vigilax) as outgroups. We found that most of the speciation dates occurred during the Paleogene and the Neogene periods. A separation between the Scutellaris Subgroup and the Albopictus Subgroup occurred approximately 64–61 million years ago (MYA). We also identified a split between species found in Asia/Micronesia and those collected in Melanesia/Polynesia approximately 36–35 MYA. Our findings suggest that the speciation of Aedes species within the Scutellaris Group may be driven by diversity in mammalian hosts, climate and environmental changes, and geological dynamics rather than human migration.

Infrequent Long-Range Dispersal and Evolution of a Top Terrestrial Arthropod Predator in the Sub-Antarctic.

AbstractThe sub-Antarctic terrestrial ecosystems survive on isolated oceanic islands in the path of circumpolar currents and winds that have raged for more than 30 million years and are shaped by climatic cycles that surpass the tolerance limits of many species. Surprisingly little is known about how these ecosystems assembled their native terrestrial fauna and how such processes have changed over time. Here, we demonstrate the patterns and timing of colonization and speciation in the largest and dominant arthropod predators in the eastern sub-Antarctic: spiders of the genus Myro. Our results indicate that this lineage originated from Australia before the Plio-Pleistocenic glacial cycles and underwent an adaptive radiation on the Crozet archipelago, from where one native species colonized multiple remote archipelagos via the Antarctic circumpolar current across thousands of kilometers. The results indicate limited natural connectivity between terrestrial macroinvertebrate faunas in the eastern sub-Antarctic and partial survival of repeated glaciations in the Plio-Pleistocene. Furthermore, our findings highlight that by integrating arthropod taxa from multiple continents, the climatically more stable volcanic Crozet archipelago played a critical role in the evolution and distribution of arthropod life in the sub-Antarctic.

TRAILS: Tree reconstruction of ancestry using incomplete lineage sorting.

Genome-wide genealogies of multiple species carry detailed information about demographic and selection processes on individual branches of the phylogeny. Here, we introduce TRAILS, a hidden Markov model that accurately infers time-resolved population genetics parameters, such as ancestral effective population sizes and speciation times, for ancestral branches using a multi-species alignment of three species and an outgroup. TRAILS leverages the information contained in incomplete lineage sorting fragments by modelling genealogies along the genome as rooted three-leaved trees, each with a topology and two coalescent events happening in discretized time intervals within the phylogeny. Posterior decoding of the hidden Markov model can be used to infer the ancestral recombination graph for the alignment and details on demographic changes within a branch. Since TRAILS performs posterior decoding at the base-pair level, genome-wide scans based on the posterior probabilities can be devised to detect deviations from neutrality. Using TRAILS on a human-chimp-gorilla-orangutan alignment, we recover speciation parameters and extract information about the topology and coalescent times at high resolution.

Tropical Origin, Global Diversification, and Dispersal in the Pond Damselflies (Coenagrionoidea) Revealed by a New Molecular Phylogeny.

The processes responsible for the formation of Earth's most conspicuous diversity pattern, the latitudinal diversity gradient (LDG), remain unexplored for many clades in the Tree of Life. Here, we present a densely sampled and dated molecular phylogeny for the most speciose clade of damselflies worldwide (Odonata: Coenagrionoidea) and investigate the role of time, macroevolutionary processes, and biome-shift dynamics in shaping the LDG in this ancient insect superfamily. We used process-based biogeographic models to jointly infer ancestral ranges and speciation times and to characterize within-biome dispersal and biome-shift dynamics across the cosmopolitan distribution of Coenagrionoidea. We also investigated temporal and biome-dependent variation in diversification rates. Our results uncover a tropical origin of pond damselflies and featherlegs ~105 Ma, while highlighting the uncertainty of ancestral ranges within the tropics in deep time. Even though diversification rates have declined since the origin of this clade, global climate change and biome-shifts have slowly increased diversity in warm- and cold-temperate areas, where lineage turnover rates have been relatively higher. This study underscores the importance of biogeographic origin and time to diversify as important drivers of the LDG in pond damselflies and their relatives, while diversification dynamics have instead resulted in the formation of ephemeral species in temperate regions. Biome-shifts, although limited by tropical niche conservatism, have been the main factor reducing the steepness of the LDG in the last 30 Myr. With ongoing climate change and increasing northward range expansions of many damselfly taxa, the LDG may become less pronounced. Our results support recent calls to unify biogeographic and macroevolutionary approaches to improve our understanding of how latitudinal diversity gradients are formed and why they vary across time and among taxa.

A microbial perspective on speciation

Abstract Understanding what a microbial species is and the process of speciation in microbes has been and still is a puzzle with many challenges. But there is now emerging consensus that speciation in microbes does follow certain rules and limitations. Just like in macrobes, it can be driven by divergent natural selection and is maintained by barriers to gene flow, either genetic or ecological in nature. However, whether microbial speciation mirrors that of sexually reproducing eukaryotes is up for debate, as extensive horizontal gene flow can blur patterns and processes. Here, I provide intriguing examples of speciation in bacteria, viruses, and yeast, which are arguably similar to what we see in eukaryotes. I synthesize recent insights from microbial evolutionary genomics, which may mitigate the traditional view that microbes are ‘messy’ and do not fit eukaryotic species concepts and speciation models. Finally, I highlight the benefits of microbial experimental evolution to answer fundamental questions in speciation research (especially why, how, and when speciation occurs). Speciation research with microbes, as opposed to the organisms traditionally used in this field, may suffer less from observational bias and the experimental control we have over selection types, gene flow, and reproductive modes in microbial systems may allow us to determine the mechanisms and timing of ecological divergence, reproductive isolation, and speciation.

Time-resolved, integrated analysis of clonally evolving genomes.

Clonal genome evolution is a key feature of asexually reproducing species and human cancer development. While many studies have described the landscapes of clonal genome evolution in cancer, few determine the underlying evolutionary parameters from molecular data, and even fewer integrate theory with data. We derived theoretical results linking mutation rate, time, expansion dynamics, and biological/clinical parameters. Subsequently, we inferred time-resolved estimates of evolutionary parameters from mutation accumulation, mutational signatures and selection. We then applied this framework to predict the time of speciation of the marbled crayfish, an enigmatic, globally invasive parthenogenetic freshwater crayfish. The results predict that speciation occurred between 1986 and 1990, which is consistent with biological records. We also used our framework to analyze whole-genome sequencing datasets from primary and relapsed glioblastoma, an aggressive brain tumor. The results identified evolutionary subgroups and showed that tumor cell survival could be inferred from genomic data that was generated during the resection of the primary tumor. In conclusion, our framework allowed a time-resolved, integrated analysis of key parameters in clonally evolving genomes, and provided novel insights into the evolutionary age of marbled crayfish and the progression of glioblastoma.

Same process, different patterns: pervasive effect of evolutionary time on species richness in freshwater fishes.

Tropical lands harbour the highest number of species, resulting in the ubiquitous latitudinal diversity gradient (LDG). However, exceptions to this pattern have been observed in some taxa, explained by the interaction between the evolutionary histories and environmental factors that constrain species' physiological and ecological requirements. Here, we applied a deconstruction approach to map the detailed species richness patterns of Actinopterygian freshwater fishes at the class and order levels and to disentangle their drivers using geographical ranges and a phylogeny, comprising 77% (12 557) of all described species. We jointly evaluated seven evolutionary and ecological hypotheses posited to explain the LDG: diversification rate, time for speciation, species-area relationship, environmental heterogeneity, energy, temperature seasonality and past temperature stability. We found distinct diversity gradients across orders, including expected, bimodal and inverse LDGs. Despite these differences, the positive effect of evolutionary time explained patterns for all orders, where species-rich regions are inhabited by older species compared to species-poor regions. Overall, the LDG of each order has been shaped by a unique combination of factors, highlighting the importance of performing a joint evaluation of evolutionary, historical and ecological factors at different taxonomic levels to reach a comprehensive understanding on the causes driving global species richness patterns.

Pervasive incomplete lineage sorting illuminates speciation and selection in primates.

Incomplete lineage sorting (ILS) causes the phylogeny of some parts of the genome to differ from the species tree. In this work, we investigate the frequencies and determinants of ILS in 29 major ancestral nodes across the entire primate phylogeny. We find up to 64% of the genome affected by ILS at individual nodes. We exploit ILS to reconstruct speciation times and ancestral population sizes. Estimated speciation times are much more recent than genomic divergence times and are in good agreement with the fossil record. We show extensive variation of ILS along the genome, mainly driven by recombination but also by the distance to genes, highlighting a major impact of selection on variation along the genome. In many nodes, ILS is reduced more on the X chromosome compared with autosomes than expected under neutrality, which suggests higher impacts of natural selection on the X chromosome. Finally, we show an excess of ILS in genes with immune functions and a deficit of ILS in housekeeping genes. The extensive ILS in primates discovered in this study provides insights into the speciation times, ancestral population sizes, and patterns of natural selection that shape primate evolution.

Analysis of intrinsic evolutionary factors leading to microendemic distributions in New Caledonian leaf beetles

Microendemicity, or the condition of some species having local ranges, is a relatively common pattern in nature. However, the factors that lead to this pattern are still largely unknown. Most studies addressing this issue tend to focus on extrinsic factors associated with microendemic distributions, such as environmental conditions, hypothesising a posteriori about underlying potential speciation mechanisms, linked or not to these conditions. Here, we use a multi-faceted approach mostly focusing on intrinsic factors instead, namely diversification dynamics and speciation modes in two endemic sibling genera of leaf beetles with microendemic distributions, Taophila and Tricholapita, in a microendemicity hotspot, New Caledonia. Results suggest that the diversification rate in this lineage slowed down through most of the Neogene and consistently with a protracted speciation model possibly combined with several ecological and environmental factors potentially adding rate-slowing effects through time. In turn, species accumulated following successive allopatric speciation cycles, possibly powered by marked geological and climatic changes in the region in the last 25 million years, with daughter species ranges uncorrelated with the time of speciation. In this case, microendemicity seems to reflect a mature state for the system, rather than a temporary condition for recent species, as suggested for many microendemic organisms.

Evolutionary history and global angiosperm species richness–climate relationships

AbstractAimClimate has been regarded as an important explanation for large‐scale species richness patterns. However, the mechanisms underlying the significant variations in species richness–climate relationships across different clades remain to be tested. We explored how niche conservatism, diversification rates and time for speciation influenced species richness–climate relationships between clades.LocationThe globe.Time PeriodPresent day.Major Taxa StudiedAngiosperms.MethodsBased on a newly complied database of the global distributions of 288,735 angiosperm species, we used generalized linear models to assess the relationships between species richness of different angiosperm families and climatic factors. We also conducted phylogenetic comparative analysis to test whether niche conservatism, diversification rates and time for speciation affect the variations in species richness–climate relationships.ResultsWe found that temperature seasonality dominated the global angiosperm diversity patterns. Closely related families had more similar species richness–climate relationships than distantly related ones. The discrepancy between the current and ancestral niches of different clades had much stronger effects on variations in species richness–climate relationships than diversification rates and time for speciation. With the increase in the discrepancy between current and ancestral niches, the explanatory power (i.e., R2) of contemporary temperature and precipitation in explaining species richness patterns increased.Main ConclusionsOverall, our findings strongly support that niche conservatism dominates the variations in species richness–climate relationships across taxonomic groups. These findings allow better understanding on how large‐scale species diversity patterns are formed.

Isolation and endemism in the subterranean aquatic snails of the genus Belgrandiella A. J. Wagner, 1928 (Caenogastropoda: Truncatelloidea: Hydrobiidae)

The Western Balkans hosts the richest subterranean aquatic gastropod fauna in the world. The main factors shaping intraspecies diversity are thought to be isolation and endemism. In the genus Belgrandiella, minute snails inhabiting subterranean waters and springs in Central Europe and Balkans, molecular studies have shown much fewer valid species than previously anticipated. The present study applies mitochondrial cytochrome c oxidase subunit I, histone 3, and RAPD analysis, to check the inter- and intraspecies genetic diversity in 36 Belgrandiella populations from caves, springs and interstitial aquifers. The level of gene flow is assessed to check if these snails form a widespread genetically uniform metapopulation or rather follow the highly endemic pattern. The studied populations have been assigned to six species. In the most widely distributed B. kusceri from 21 populations, 60 sequenced specimens represent 16 haplotypes. While the same haplotypes are present in distant populations, gene flow between the other populations is low. Nei distances for RAPD show no geographic pattern. The interspecies differences in COI evidently confirm the time of speciation in Pleistocene, before karstification, which rejects speciation within isolated caves. The pattern observed in Belgrandiella seems more similar to the one described in Montenegrospeum than in Kerkia.

The origins of climate-diversity relationships and richness patterns in Chinese plants.

A major goal of ecology and evolutionary biology is to explain geographic patterns of species richness. Richness is often correlated with climatic variables. However, the processes underlying these climate-diversity relationships remain poorly understood. Two potential hypotheses to explain these relationships involve: (i) faster diversification rates (speciation minus extinction) in high-richness climates and (ii) earlier colonization of high-richness climates, allowing more time for speciation to build up richness. Few studies have tested these hypotheses directly, and most focused on animal clades with limited richness. In this study, we test these hypotheses in Chinese angiosperms, encompassing ~10% of Earth's plant species, using large-scale phylogenetic, climatic, and distributional data including 26,977 species. We find that climatic zones that were colonized earlier have higher species richness. By contrast, relationships between diversification rates and richness of climatic zones are often nonsignificant or negative. Our study reveals that even when richness is strongly correlated with climate, the underlying explanation may still be rooted in phylogenetic history. Thus, climate may not be a competing explanation for richness patterns relative to colonization times and diversification rates. We also show that the timing of colonization can be crucial for explaining richness patterns. Yet, many recent studies have ignored this explanation and instead have focused solely on rates of speciation and diversification as drivers of diversity gradients.

Intraspecific variation in reproductive barriers between two closely related Arabidopsis sister species.

Reproductive isolation (RI) is a critical component of speciation and varies strongly in timing and strength among different sister taxa, depending on, for example the geography of speciation and divergence time. However, these factors may also produce variation in timing and strength among populations within species. Here we tested for variation in the expression of RI among replicate population pairs between the sister taxa Arabidopsis lyrata subsp. lyrata and A. arenicola. While the former is predominantly outcrossing, the latter is predominantly selfing. We focused on intrinsic prezygotic and postzygotic RI as both species occur largely in allopatry. We assessed RI by performing within-population crosses and interspecific between-population crosses, and by raising offspring. RI was generally high between all interspecific population pairs, but it varied in timing and strength depending on population history. Prezygotic isolation was strongest between the closest-related population pair, while early postzygotic isolation was high for all other population pairs. Furthermore, the timing and strength of RI depended strongly on cross direction. Our study provides empirical support that reproductive barriers between species are highly variable among population pairs and asymmetric within population pairs, and this variation seems to follow patterns typically described across species pairs.

On the effects of selection and mutation on species tree inference

The effect of selection acting on regions of the genome on the accuracy of species-level phylogenetic inference using methods that do not explicitly model selection is an open question that is relevant to most, if not all, phylogenomic studies. To address this, we derive a mathematical approximation to the Wright-Fisher model with mutation and selection in the limit as the population size becomes large. In contrast to previous approximations based on diffusion processes, our approximation can be used to study the distribution of coalescent times for an arbitrary number of lineages, allowing calculation of the probability distribution of gene genealogies under the coalescent model. We use these calculations to show that direct selection at strengths typically encountered in practice has only a small effect on the distribution of coalescent times, and hence on the distribution of gene trees. This implies that many coalescent-based methods for estimating the species tree topology will be robust to the presence of selection in a subset of the underlying genes. Selection will, however, bias the estimation of speciation times, causing them to underestimate the true speciation times. Our model captures the effects of selection on the genealogies that generate the observed sequence data, but does not model selective pressures that act only on the subsequent sequences or that negatively impact gene tree estimation.