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opencc-zeroDec 2015View details →

Data from: Accounting for uncertainty in gene tree estimation: summary-coalescent species tree inference in a challenging radiation of Australian lizards

Accurate gene tree inference is an important aspect of species tree estimation in a summary-coalescent framework. Yet, in empirical studies, inferred gene trees differ in accuracy due to stochastic variation in phylogenetic signal between targeted loci. Empiricists should, therefore, examine the consistency of species tree inference, while accounting for the observed heterogeneity in gene tree resolution of phylogenomic data sets. Here, we assess the impact of gene tree estimation error on summary-coalescent species tree inference by screening ${\sim}2000$ exonic loci based on gene tree resolution prior to phylogenetic inference. We focus on a phylogenetically challenging radiation of Australian lizards (genus Cryptoblepharus, Scincidae) and explore effects on topology and support. We identify a well-supported topology based on all loci and find that a relatively small number of high-resolution gene trees can be sufficient to converge on the same topology. Adding gene trees with decreasing resolution produced a generally consistent topology, and increased confidence for specific bipartitions that were poorly supported when using a small number of informative loci. This corroborates coalescent-based simulation studies that have highlighted the need for a large number of loci to confidently resolve challenging relationships and refutes the notion that low-resolution gene trees introduce phylogenetic noise. Further, our study also highlights the value of quantifying changes in nodal support across locus subsets of increasing size (but decreasing gene tree resolution). Such detailed analyses can reveal anomalous fluctuations in support at some nodes, suggesting the possibility of model violation. By characterizing the heterogeneity in phylogenetic signal among loci, we can account for uncertainty in gene tree estimation and assess its effect on the consistency of the species tree estimate. We suggest that the evaluation of gene tree resolution should be incorporated in the analysis of empirical phylogenomic data sets. This will ultimately increase our confidence in species tree estimation using summary-coalescent methods and enable us to exploit genomic data for phylogenetic inference.

opencc-zeroDec 2017View details →

Data from: What have been and what can be delimited as species using molecular data under the multi-species coalescent model? A case study using Hercules beetles (Dynastes; Dynastidae)

Molecular species delimitation using the multi-species coalescent model has become common for statistically and objectively determining species limits. Empirical examples of how consistently different molecular data sets delimit the same level of divergence as species using coalescent-based methods are still lacking. I applied the method of molecular species delimitation in the Bayesian Phylogenetics and Phylogeography (BPP) program to study species delimitation in the divergence between populations and between putative species across four species of Hercules beetles. The quantity and variability of the molecular data affected species delimitation. A divergence that represented a late stage along the speciation continuum, e.g. between sympatric biological species, could be delimited by BPP by fewer and less variable loci than a recent divergence, e.g. between geographic populations. My results further indicated that the use of genomic data could even over-split geographically continuously distributed populations into species. I compared my results with those from other empirical studies and argue for the need of a thorough review of the kind of evolutionary entities, e.g. geographic populations versus morphologically distinct taxa, that have been designated as species and whether such designations are consistent among studies.

opencc-zeroDec 2013View details →

Data from: Multilocus coalescent analyses reveal the demographic history and speciation patterns of mouse lemur sister species

Background: Debate continues as to whether allopatric speciation or peripatric speciation through a founder effect is the predominant force driving evolution in vertebrates. The mouse lemurs of Madagascar are a system in which evolution has generated a large number of species over a relatively recent time frame. Here, we examine speciation patterns in a pair of sister species of mouse lemur, Microcebus murinus and M. griseorufus. These two species have ranges that are disparately proportioned in size, with M. murinus showing a much more extensive range that marginally overlaps that of M. griseorufus. Given that these two species are sister taxa, the asymmetric but overlapping geographic ranges are consistent with a model of peripatric speciation. To test this hypothesis, we analyze DNA sequence data from four molecular markers using coalescent methods. If the peripatric speciation model is supported, we predict substantially greater genetic diversity in M. murinus, relative to M. griseorufus. Further, we expect a larger effective population size in M. murinus and in the common ancestor of the two species than in M. griseorufus, with a concomitant decrease in gene tree/species tree incongruence in the latter and weak signs of demographic expansion in M. murinus. Results: Our results reject a model of peripatric divergence. Coalescent effective population size estimates were similar for both extant species and larger than that estimated for their most recent common ancestor. Gene tree results show similar levels of incomplete lineage sorting within species with respect to the species tree, and locus-specific estimates of genetic diversity are concordant for both species. Multilocus demographic analyses suggest range expansions for M. murinus, with this species also experiencing more recent population declines over the past 160 thousand years. Conclusions: Results suggest that speciation occurred in allopatry from a common ancestor narrowly distributed throughout southwest Madagascar, with subsequent range expansion for M. murinus. Population decline in M. murinus is likely related to patterns of climate change in Madagascar throughout the Pleistocene, potentially exacerbated by continual anthropogenic perturbation. Genome-level data are needed to quantify the role of niche specialization and adaptation in shaping the current ranges of these species.

opencc-zeroDec 2016View details →

Data from: Impact of model violations on the inference of species boundaries under the multispecies coalescent

The use of genetic data for identifying species-level lineages across the tree of life has received increasing attention in the field of systematics over the past decade. The multispecies coalescent model provides a framework for understanding the process of lineage divergence, and has become widely adopted for delimiting species. However, because these studies lack an explicit assessment of model fit, in many cases, the accuracy of the inferred species boundaries are unknown. This is concerning given the large amount of empirical data and theory that highlight the complexity of the speciation process. Here, we seek to fill this gap by using simulation to characterize the sensitivity of inference under the multispecies coalescent to several violations of model assumptions thought to be common in empirical data. We also assess the fit of the multispecies coalescent model to empirical data in the context of species delimitation. Our results show substantial variation in model fit across datasets. Posterior predictive tests find the poorest model performance in datasets that were hypothesized to be impacted by model violations. We also show that while the inferences assuming the multispecies coalescent are robust to minor model violations, such inferences can be biased under some biologically plausible scenarios. Taken together, these results suggest that researchers can identify individual datasets in which species delimitation under the multispecies coalescent is likely to be problematic, thereby highlighting the cases where additional lines of evidence to identify species boundaries are particularly important to collect. Our study supports a growing body of work highlighting the importance of model checking in phylogenetics, and the usefulness of tailoring tests of model fit to assess the reliability of particular inferences.

opencc-zeroDec 2015View details →

Data from: Species discovery and validation in a cryptic radiation of endangered primates: coalescent-based species delimitation in Madagascar's mouse lemurs

Implementation of the coalescent model in a Bayesian framework is an emerging strength in genetically based species delimitation studies. By providing an objective measure of species diagnosis, these methods represent a quantitative enhancement to the analysis of multilocus data, and complement more traditional methods based on phenotypic and ecological characteristics. Recognized as two species 20 years ago, mouse lemurs (genus Microcebus) now comprise more than 20 species, largely diagnosed from mtDNA sequence data. With each new species description, enthusiasm has been tempered with scientific scepticism. Here, we present a statistically justified and unbiased Bayesian approach towards mouse lemur species delimitation. We perform validation tests using multilocus sequence data and two methodologies: (i) reverse-jump Markov chain Monte Carlo sampling to assess the likelihood of different models defined a priori by a guide tree, and (ii) a Bayes factor delimitation test that compares different species-tree models without a guide tree. We assess the sensitivity of these methods using randomized individual assignments, which has been used in bpp studies, but not with Bayes factor delimitation tests. Our results validate previously diagnosed taxa, as well as new species hypotheses, resulting in support for three new mouse lemur species. As the challenge of multiple researchers using differing criteria to describe diversity is not unique to Microcebus, the methods used here have significant potential for clarifying diversity in other taxonomic groups. We echo previous studies in advocating that multiple lines of evidence, including use of the coalescent model, should be trusted to delimit new species.

opencc-zeroNov 2019View details →

Data from: Model-based species delimitation: are coalescent species reproductively isolated?

A large and growing fraction of systematists define species as independently evolving lineages that may be recognized by analyzing the population genetic history of alleles sampled from individuals belonging to those species. This has motivated the development of increasingly sophisticated statistical models rooted in the multispecies coalescent process. Specifically, these models allow for simultaneous estimation of the number of species present in a sample of individuals and the phylogenetic history of those species using only DNA sequence data from independent loci. These methods hold extraordinary promise for increasing the efficiency of species discovery, but require extensive validation to ensure that they are accurate and precise. Whether the species identified by these methods correspond to the species that would be recognized by alternative species recognition criteria (such as measurements of reproductive isolation) is currently an open question, and a subject of vigorous debate. Here we perform an empirical test of these methods by making use of a classic model system in the history of speciation research, flies of the genus Drosophila. Specifically, we use the uniquely comprehensive data on reproductive isolation that is available for this system, along with DNA sequence data, to ask whether Drosophila species inferred under the multispecies coalescent model correspond to those recognized by many decades of speciation research. We found that coalescent based and reproductive isolation based methods of inferring species boundaries are concordant for 77% of the species pairs. We explore and discuss potential explanations for these discrepancies. We also found that the amount of prezygotic isolation between two species is a strong predictor of the posterior probability of species boundaries based on DNA sequence data, regardless of whether the species pairs are sympatrically or allopatrically distributed.

opencc-zeroDec 2014View details →

Data from: Sky island diversification meets the multispecies coalescent – divergence in the spruce-fir moss spider (Microhexura montivaga, Araneae, Mygalomorphae) on the highest peaks of southern Appalachia

Microhexura montivaga is a miniature tarantula-like spider endemic to the highest peaks of the southern Appalachian mountains and is known only from six allopatric, highly disjunct montane populations. Because of severe declines in spruce-fir forest in the late 20th century, M. montivaga was formally listed as a US federally endangered species in 1995. Using DNA sequence data from one mitochondrial and seven nuclear genes, patterns of multigenic genetic divergence were assessed for six montane populations. Independent mitochondrial and nuclear discovery analyses reveal obvious genetic fragmentation both within and among montane populations, with five to seven primary genetic lineages recovered. Multispecies coalescent validation analyses [guide tree and unguided Bayesian Phylogenetics and Phylogeography (BPP), Bayes factor delimitation (BFD)] using nuclear-only data congruently recover six or seven distinct lineages; BFD analyses using combined nuclear plus mitochondrial data favour seven or eight lineages. In stark contrast to this clear genetic fragmentation, a survey of secondary sexual features for available males indicates morphological conservatism across montane populations. While it is certainly possible that morphologically cryptic speciation has occurred in this taxon, this system may alternatively represent a case where extreme population genetic structuring (but not speciation) leads to an oversplitting of lineage diversity by multispecies coalescent methods. Our results have clear conservation implications for this federally endangered taxon and illustrate a methodological issue expected to become more common as genomic-scale data sets are gathered for taxa found in naturally fragmented habitats.

FIGURE 74 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURE 74. Map of richness in indigenous species of all bumblebees excluding the subgenus Mendacibombus among equalarea grid cells. Map, grid, and grey scale as in Figs 71, 72.

FIGURE 68 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURE 68. Best estimate of phylogeny and absolute chronogram for the species of the subgenus Mendacibombus (as recognised in Figs 11, 12), from a linked-tree BEAST analysis of COI, 16S, PEPCK and opsin genes. Values above nodes of the maximum clade-credibility tree are Bayesian posterior probabilities showing branch support. Numbers below nodes are the estimated ages of events in Ma (millions of years before the present) based on the Mendacibombus root-date estimate of 34 (25–40) Ma from Hines (2008). The grey bars represent the 95% confidence intervals for the estimates of the age of events.

FIGURES 56‒67 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 56‒67. Maps of the global distributions of species of the subgenus Mendacibombus from the material examined, with grey spots for specimen records and black spots for the samples with COI sequences (each species is unknown from regions outside the map boundaries shown); grey crosses for records of all species of Mendacibombus combined. Relief map with hill shading, Cartesian orthonormal projection, grey lines show borders to national administration according to UN maps, north at the top of the map. Image created in ArcGIS using World_Shaded_Relief basemap © 2014 Esri.

FIGURES 69‒70 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 69‒70. Photos of (69) a worker of B. superbus (MD#4123) from (left) the dorsal and (right) the left lateral aspect (scale bar 10 mm), from the sample site (70) in the Tanggula mountains, Xizang, China (16.viii.2014, 32.86142°N 91.91739°E, GPS elevation ca 5220 m). Photos by (69) NHM digital imaging unit and (70) Z.-Y. Miao.

FIGURES 11‒12 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 11‒12. Recognising species from an estimate of phylogeny for 30 unique COI haplotypes of the subgenus Mendacibombus by BEAST, using GMYC models and the PTP procedure. From the GMYC models (11), the single threshold T is shown by the vertical grey bar so that the intersecting lineages are interpreted as indicating 12 separate species (black spots at coalescent nodes; outgroups not shown). Values below the nodes of the maximum clade-credibility tree are Bayesian posterior probabilities showing branch support (groups with values <0.8 are considered unreliable) from the BEAST analysis with two billion MCMC generations and a 1% burn-in. The x-scale axis is calibrated in substitutions per nucleotide site. From the PTP procedure (12), the Bayesian PTP solution with highest support also indicates 12 species. Values above the nodes are PTP Bayesian support values that all daughter haplotypes are parts of a single species; values below the nodes are Bayesian posterior probabilities showing branch support. The scale bar is calibrated in substitutions per nucleotide site. Each unique haplotype is represented by one of the longest available sample sequences, labelled with: the sequence length in number of base pairs, a taxon name or name for an unpublished colour pattern (light/dark/yellow/white/pale), and then a code that consists of a specimen identifier (MD#) from the project database and (after the hyphen) a sample identifier from BOLD or from GenBank, followed with its geographic origin.

FIGURES 24‒35 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 24‒35. Morphology of the male genitalia for species of the subgenus Mendacibombus from the dorsal aspect, anterior to the left of the image, posterior to the right: 24, B. superbus, China MD#339; 25, B. waltoni, China MD#216; 26, B. convexus, China MD#215; 27, B. makarjini, Kazakhstan MD#1240; 28, B. marussinus, Pakistan MD#408; 29, B. avinoviellus, India MD#404; 30, B. himalayanus, India MD#426; 31, B. turkestanicus, China MD#351; 32, B. defector, Kyrgyzstan MD#367; 33, B. margreiteri, China MD#294; 34, B. handlirschianus, Russia MD#835; 35, B. mendax, Spain MD#689.

FIGURES 15‒23 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 15‒23. Morphology of the female (queen) head from the ventral aspect (labrum and mandibles): 15, B. marussinus queen, Pakistan MD#482; 16, B. avinoviellus queen, India MD#598; 17, B. turkestanicus queen, Tajikistan MD#320; 18, B. defector queen, Kyrgyzstan MD#1080; 19, B. margreiteri queen, Mongolia MD#319; 20, B. himalayanus queen, India MD#453. Morphology of the female (queen) left hindleg tibia from the left lateral aspect, dorsal at the top of the image, anterior to the left: 21, B. defector, China MD#1251; 22, B. margreiteri, Mongolia MD#319; 23, B. turkestanicus, Kyrgyzstan MD#324.

FIGURE 14 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURE 14. Assessing morphological characters by assessing groups of species within the subgenus Mendacibombus from three characters of hair colour (characters 1‒3) and 13 characters of male genital morphology (characters 4‒16) by maximum parsimony analysis with TNT. Numbers above the branches of the tree are the character numbers from Table 6; solid squares show unique character-state changes; and open squares show parallel or reverse character-state changes.

FIGURE 10 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURE 10. Plot of (y axis) the number of lineages in the BEAST tree (Fig. 11) of unique COI haplotypes excluding outgroups on a log scale against (x axis) time as substitutions per nucleotide. T, the single threshold at maximum likelihood for the change in branching rate from the GMYC models.

FIGURE 9 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURE 9. Map of the global distribution of sites from which samples of the subgenus Mendacibombus have been examined (these bees are unknown from any other regions). Spots are coloured to show the site elevation above sea level (scale in metres to the left). Image showing vegetation, Cartesian orthonormal projection, with north at the top of the map.

FIGURES 36‒55 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 36‒55. Morphology of parts of the male genitalia from the dorsal aspect of the left side, anterior to the left of the image, posterior to the right, white bars indicating morphological characters referred to in the key to males: 36, B. waltoni; 37, B. mendax; 38, B. superbus; 39, B. convexus; 40, B. waltoni; 41, B. convexus; 42, B. defector; 43, B. mendax; 44, B. mendax; 45, B. turkestanicus; 46, B. avinoviellus; 47, B. mendax; 48, B. mendax; 49, B. makarjini; 50, B. handlirschianus; 51, B. himalayanus; 52, B. turkestanicus; 53, B. himalayanus; 54, B. himalayanus; 55, B. marussinus.

FIGURE 8 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURE 8. Plot of (y axis) terminal branch lengths from a tree for 43 unique COI haplotypes obtained with BEAST against (x axis) lengths of the barcode sequences in numbers of nucleotides.

FIGURES 1‒6 in Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species' gene coalescents and morphology (Hymenoptera, Apidae)

FIGURES 1‒6. Views of perching males of species of the subgenus Mendacibombus, showing the anteriorly extended antennae and laterally extended wings that are characteristic of their form of male mate-searching behaviour: 1, B. waltoni at Diebu ca 3910 m, Minshan mountains, Gansu, China, 29.viii.2009; 2, B. convexus at Diebu ca 3340 m, Minshan mountains, Gansu, China, 29.viii.2009; 3, B. avinoviellus at Gulmarg ca 2700 m, Pir Panjal mountains, Kashmir, India, 16.viii.1985; 4, B. himalayanus at Apharwat ca 4100 m, Pir Panjal mountains, Kashmir, India, 30.viii.1986; 5‒6, B. margreiteri near Dulan ca 3520 m, Burhan Budai mountains, Qinghai, China, 31.viii.2010. Photos by PW (Figs 3–4 are the best available for these species).