The Multispecies Coalescent Over-Splits Species in the Case of Geographically Widespread Taxa

2019 ◽  
Vol 69 (1) ◽  
pp. 184-193 ◽  
Author(s):  
E Anne Chambers ◽  
David M Hillis
Keyword(s):  
Species Delimitation ◽  
Isolation By Distance ◽  
A Priori ◽  
Genetic Data ◽  
Species Group ◽  
Recent Analysis ◽  
Multispecies Coalescent ◽  
Species Complexes ◽  
Taxonomic Changes ◽  
Recent Species

AbstractMany recent species delimitation studies rely exclusively on limited analyses of genetic data analyzed under the multispecies coalescent (MSC) model, and results from these studies often are regarded as conclusive support for taxonomic changes. However, most MSC-based species delimitation methods have well-known and often unmet assumptions. Uncritical application of these genetic-based approaches (without due consideration of sampling design, the effects of a priori group designations, isolation by distance, cytoplasmic–nuclear mismatch, and population structure) can lead to over-splitting of species. Here, we argue that in many common biological scenarios, researchers must be particularly cautious regarding these limitations, especially in cases of well-studied, geographically variable, and parapatrically distributed species complexes. We consider these points with respect to a historically controversial species group, the American milksnakes (Lampropeltis triangulum complex), using genetic data from a recent analysis (Ruane et al. 2014). We show that over-reliance on the program Bayesian Phylogenetics and Phylogeography, without adequate consideration of its assumptions and of sampling limitations, resulted in over-splitting of species in this study. Several of the hypothesized species of milksnakes instead appear to represent arbitrary slices of continuous geographic clines. We conclude that the best available evidence supports three, rather than seven, species within this complex. More generally, we recommend that coalescent-based species delimitation studies incorporate thorough analyses of geographic variation and carefully examine putative contact zones among delimited species before making taxonomic changes.

scholarly journals The challenge of delimiting cryptic species, and a supervised machine learning solution

2021 ◽  
Author(s):  
Shahan Derkarabetian ◽  
James Starrett ◽  
Marshal Hedin
Keyword(s):  
Machine Learning ◽  
Cryptic Species ◽  
Species Delimitation ◽  
Genetic Data ◽  
Biological Characteristics ◽  
Supervised Machine Learning ◽  
Training Dataset ◽  
Dispersal Ability ◽  
Data Types ◽  
Multispecies Coalescent

The diversity of biological and ecological characteristics of organisms, and the underlying genetic patterns and processes of speciation, makes the development of universally applicable genetic species delimitation methods challenging. Many approaches, like those incorporating the multispecies coalescent, sometimes delimit populations and overestimate species numbers. This issue is exacerbated in taxa with inherently high population structure due to low dispersal ability, and in cryptic species resulting from nonecological speciation. These taxa present a conundrum when delimiting species: analyses rely heavily, if not entirely, on genetic data which over split species, while other lines of evidence lump. We showcase this conundrum in the harvester Theromaster brunneus, a low dispersal taxon with a wide geographic distribution and high potential for cryptic species. Integrating morphology, mitochondrial, and sub-genomic (double-digest RADSeq and ultraconserved elements) data, we find high discordance across analyses and data types in the number of inferred species, with further evidence that multispecies coalescent approaches over split. We demonstrate the power of a supervised machine learning approach in effectively delimiting cryptic species by creating a "custom" training dataset derived from a well-studied lineage with similar biological characteristics as Theromaster. This novel approach uses known taxa with particular biological characteristics to inform unknown taxa with similar characteristics, and uses modern computational tools ideally suited for species delimitation while also considering the biology and natural history of organisms to make more biologically informed species delimitation decisions. In principle, this approach is universally applicable for species delimitation of any taxon with genetic data, particularly for cryptic species.

scholarly journals Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

2020 ◽  
Author(s):  
Jelmer W Poelstra ◽  
Jordi Salmona ◽  
George P Tiley ◽  
Dominik Schüßler ◽  
Marina B Blanco ◽  
...  
Keyword(s):  
Species Delimitation ◽  
Isolation By Distance ◽  
Divergence Time ◽  
Taxonomic Revision ◽  
Mouse Lemur ◽  
Effective Population ◽  
Separate Species ◽  
Divergence Time Estimates ◽  
Multispecies Coalescent ◽  
Mouse Lemurs

Abstract Mouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic revision has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we investigate mouse lemur diversity in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for two pairs of sister lineages that include three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among the two pairs of lineages. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported—a result that is particularly striking when using the genealogical discordance index (gdi). Nonsister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated relaxed-clock estimates. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case. [Cryptic species; effective population size; microendemism; multispecies coalescent; speciation; species delimitation.]

scholarly journals Incorporating the speciation process into species delimitation

2021 ◽  
Vol 17 (5) ◽  
pp. e1008924
Author(s):  
Jeet Sukumaran ◽  
Mark T. Holder ◽  
L. Lacey Knowles
Keyword(s):  
Gene Flow ◽  
Species Delimitation ◽  
Subsequent Development ◽  
Genetic Data ◽  
Distinct Species ◽  
Species Boundaries ◽  
Multispecies Coalescent ◽  
Speciation Process ◽  
Other Information ◽  
Species Population

The “multispecies” coalescent (MSC) model that underlies many genomic species-delimitation approaches is problematic because it does not distinguish between genetic structure associated with species versus that of populations within species. Consequently, as both the genomic and spatial resolution of data increases, a proliferation of artifactual species results as within-species population lineages, detected due to restrictions in gene flow, are identified as distinct species. The toll of this extends beyond systematic studies, getting magnified across the many disciplines that rely upon an accurate framework of identified species. Here we present the first of a new class of approaches that addresses this issue by incorporating an extended speciation process for species delimitation. We model the formation of population lineages and their subsequent development into independent species as separate processes and provide for a way to incorporate current understanding of the species boundaries in the system through specification of species identities of a subset of population lineages. As a result, species boundaries and within-species lineages boundaries can be discriminated across the entire system, and species identities can be assigned to the remaining lineages of unknown affinities with quantified probabilities. In addition to the identification of species units in nature, the primary goal of species delimitation, the incorporation of a speciation model also allows us insights into the links between population and species-level processes. By explicitly accounting for restrictions in gene flow not only between, but also within, species, we also address the limits of genetic data for delimiting species. Specifically, while genetic data alone is not sufficient for accurate delimitation, when considered in conjunction with other information we are able to not only learn about species boundaries, but also about the tempo of the speciation process itself.

scholarly journals Validation and description of two new north-western Australian Rainbow skinks with multispecies coalescent methods and morphology

PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3724 ◽  
Author(s):  
Ana C. Afonso Silva ◽  
Natali Santos ◽  
Huw A. Ogilvie ◽  
Craig Moritz
Keyword(s):  
Species Delimitation ◽  
A Priori ◽  
Integrated Approach ◽  
Morphological Characters ◽  
Integrative Taxonomy ◽  
Gene Trees ◽  
Separate Species ◽  
Data Set ◽  
Multispecies Coalescent ◽  
Alternative Species

While methods for genetic species delimitation have noticeably improved in the last decade, this remains a work in progress. Ideally, model based approaches should be applied and considered jointly with other lines of evidence, primarily morphology and geography, in an integrative taxonomy framework. Deep phylogeographic divergences have been reported for several species ofCarliaskinks, but only for some eastern taxa have species boundaries been formally tested. The present study does this and revises the taxonomy for two species from northern Australia,Carlia johnstoneiandC. triacantha. We introduce an approach that is based on the recently published method StarBEAST2, which uses multilocus data to explore the support for alternative species delimitation hypotheses using Bayes Factors (BFD). We apply this method, jointly with two other multispecies coalescent methods, using an extensive (from 2,163 exons) data set along with measures of 11 morphological characters. We use this integrated approach to evaluate two new candidate species previously revealed in phylogeographic analyses of rainbow skinks (genusCarlia) in Western Australia. The results based on BFD StarBEAST2, BFD* SNAPP and BPP genetic delimitation, together with morphology, support each of the four recently identifiedCarlialineages as separate species. The BFD StarBEAST2 approach yielded results highly congruent with those from BFD* SNAPP and BPP. This supports use of the robust multilocus multispecies coalescent StarBEAST2 method for species delimitation, which does not requirea prioriresolved species or gene trees. Compared to the situation inC. triacantha, morphological divergence was greater between the two lineages within Kimberley endemicC. johnstonei, which also had deeper divergent histories. This congruence supports recognition of two species withinC. johnstonei. Nevertheless, the combined evidence also supports recognition of two taxa within the more widespreadC. triacantha. With this work, we describe two new species,Carlia insularissp. nov andCarlia isostriacanthasp. nov. in the northwest of Australia. This contributes to increasing recognition that this region of tropical Australia has a rich and unique fauna.

scholarly journals Species limits in butterflies (Lepidoptera: Nymphalidae): Reconciling classical taxonomy with the multispecies coalescent

2018 ◽  
Author(s):  
Pável Matos-Maraví ◽  
Niklas Wahlberg ◽  
Alexandre Antonelli ◽  
Carla M. Penz
Keyword(s):  
Species Delimitation ◽  
Single Gene ◽  
A Priori ◽  
Structured Populations ◽  
Taxonomic Assignment ◽  
Multispecies Coalescent ◽  
Synergistic Approach ◽  
Taxonomic Uncertainty ◽  
Traditional Taxonomy ◽  
The Impact

AbstractSpecies delimitation is at the core of biological sciences. During the last decade, molecular-based approaches have advanced the field by providing additional sources of evidence to classical, morphology-based taxonomy. However, taxonomy has not yet fully embraced molecular species delimitation beyond threshold-based, single-gene approaches, and taxonomic knowledge is not commonly integrated to multi-locus species delimitation models. Here we aim to bridge empirical data (taxonomic and genetic) with recently developed coalescent-based species delimitation approaches. We use the multispecies coalescent model as implemented in two Bayesian methods (DISSECT/STACEY and BP&P) to infer species hypotheses. In both cases, we account for phylogenetic uncertainty (by not using any guide tree) and taxonomic uncertainty (by measuring the impact of using or not a priori taxonomic assignment to specimens). We focus on an entire Neotropical tribe of butterflies, the Haeterini (Nymphalidae: Satyrinae). We contrast divergent taxonomic opinion—splitting, lumping and misclassifying species—in the light of different phenotypic classifications proposed to date. Our results provide a solid background for the recognition of 22 species. The synergistic approach presented here overcomes limitations in both traditional taxonomy (e.g. by recognizing cryptic species) and molecular-based methods (e.g. by recognizing structured populations, and not raise them to species). Our framework provides a step forward towards standardization and increasing reproducibility of species delimitations.

scholarly journals Species delimitation and phylogeny estimation under the multispecies coalescent

2014 ◽  
Author(s):  
Graham R Jones
Keyword(s):  
Dna Sequences ◽  
Species Delimitation ◽  
A Priori ◽  
Simulated Data ◽  
Species Trees ◽  
Data Set ◽  
Multispecies Coalescent ◽  
Multiple Loci ◽  
Population Sizes ◽  
Phylogeny Estimation

This article describes a Bayesian method for inferring both species delimitations and species trees under the multispecies coalescent model using DNA sequences from multiple loci. The focus here is on species delimitation with no a priori assignment of individuals to species, and no guide tree. The method uses a new model for the population sizes along the branches of the species tree, and three new operators for sampling from the posterior using the Markov chain Monte Carlo (MCMC) algorithm. The correctness of the moves is demonstrated both by proofs and by tests of the implementation. Current practice, using a pipeline approach to species delimitation under the multispecies coalescent, has been shown to have major problems on simulated data (Olave et al, 2014). The same simulated data set is used to demonstrate the accuracy and efficiency of the present method. The method is implemented in a package called STACEY for BEAST2.

Species Delimitation

2022 ◽  
Keyword(s):  
Species Delimitation ◽  
Genetic Data ◽  
Species Boundaries ◽  
Dna Barcodes ◽  
Multispecies Coalescent ◽  
Statistical Framework ◽  
Dramatic Rise ◽  
Invaluable Tool ◽  
Taxonomic Groups ◽  
Over Time

Species delimitation is the process of determining whether a group of sampled individuals belong to the same species or to different species. The criteria used to delimit species differ across taxonomic groups, and the methods for delimiting species have changed over time, with a dramatic rise in the popularity of genomic approaches recently. Because inferred species boundaries have ramifications that extend beyond systematics, affecting all fields that rely upon species as a foundational unit, controversy has unsurprisingly surrounded not only the practices used to delimit species boundaries, but also the idea of what species are, which varies across taxa (e.g., the use of subspecies varies across the tree of life). This lack of consensus has no doubt contributed to the appeal of genetic-based delimitation. Specifically, genomic data can be collected from any taxon. Moreover, it can be analyzed in a common statistical framework (as popularized by the multispecies coalescent as a model for species delimitation). With the ease of collecting genetic data, the power of genomics, and the purported standardization for diagnosing species limits, genetic-based species delimitation is displacing traditional time-honored (albeit time-consuming) taxonomic practices of species diagnosis. It has also become an invaluable tool for discovering species in understudied groups, and genetic-based approaches are the foundation of international endeavors to generate a catalogue of DNA barcodes to illuminate biodiversity for all of life on the planet. Yet, genomic applications, and especially the sole reliance upon genetic data for inferring species boundaries, are not without their own set of challenges.

scholarly journals Cryptic Patterns of Speciation in Cryptic Primates: Microendemic Mouse Lemurs and the Multispecies Coalescent

2019 ◽  
Author(s):  
Jelmer Poelstra ◽  
Jordi Salmona ◽  
George P. Tiley ◽  
Dominik Schüßler ◽  
Marina B. Blanco ◽  
...  
Keyword(s):  
Species Delimitation ◽  
Isolation By Distance ◽  
Divergence Time ◽  
Mouse Lemur ◽  
Integrative Approach ◽  
Effective Population ◽  
Separate Species ◽  
Divergence Time Estimates ◽  
Multispecies Coalescent ◽  
Mouse Lemurs

AbstractMouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic explosion has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we take an integrative approach to investigate species diversity in two pairs of sister lineages that occur in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among them. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported – a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC and calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated concatenated likelihood estimates, however. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.

Species Delimitation and evolutionary history of tree frogs in the Hyla chinensis-group (Hylidae, Amphibian)

2019 ◽  
Author(s):  
Tao Pan ◽  
Guiyou Wu ◽  
Xing Kang ◽  
Peng Yan ◽  
Izaz Ali ◽  
...  
Keyword(s):  
Species Delimitation ◽  
Divergence Time ◽  
Distinct Species ◽  
Species Group ◽  
Early Miocene ◽  
Evolutionary Divergence ◽  
Dabie Mountains ◽  
Ancestral Area ◽  
Ancestral Area Reconstruction ◽  
History Of

Abstract Background Species are the cornerstone in many domains of biology research, which made the accurate species delimitation became critically important. In this study, the systematics and biogeography of the Hyla chinensis -group were analyzed based on phylogeny, species delimitation and ancestral area reconstruction methods.Results The phylogenetic results showed six specific clusters existed in the H. chinensis- group. BPP analysis indicated that six distinct species exist due to the high probability values (>0.95), which were also supported by the BF analysis. The divergence time of the H. chinensis -group is estimated to date back to 18.84 Mya in the early Miocene. Combining the results of ancestral area reconstruction, the H. chinensis -group might have originated from Guangxi-Hainan, then spread eastwardly and reached Nanling mountains, Wuyi mountains, Huangshan mountains and Taiwan. In rightabout colonization, it is gradually extended to the Yunnan-Guizhou Plateau, Sichuan basin, Qinling mountains and Dabie mountains. Considering the geological movement from early Miocene to Pliocene, the colonization pattern of the H. chinensis -group maybe closely related to the progressive uplift of Qinghai-Tibetan Plateau (QTP) and historical climate change.Conclusions Our study provides evidence for species delimitation and speciation process within the H. chinensis -group. Our study supports the hypothesis that the evolutionary divergence in this species group was a consequence of the progressive uplift of QTP and environmental change.

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