An official website of the United States government
Abstract Most new cryptic species are described using conventional tree‐ and distance‐based species delimitation methods (SDMs), which rely on phylogenetic arrangements and measures of genetic divergence. However, although numerous factors such as population structure and gene flow are known to confound phylogenetic inference and species delimitation, the influence of these processes is not frequently evaluated. Using large numbers of exons, introns, and ultraconserved elements obtained using the FrogCap sequence‐capture protocol, we compared conventional SDMs with more robust genomic analyses that assess population structure and gene flow to characterize species boundaries in a Southeast Asian frog complex (Pulchrana picturata). Our results showed that gene flow and introgression can produce phylogenetic patterns and levels of divergence that resemble distinct species (up to 10% divergence in mitochondrial DNA). Hybrid populations were inferred as independent (singleton) clades that were highly divergent from adjacent populations (7%–10%) and unusually similar (<3%) to allopatric populations. Such anomalous patterns are not uncommon in Southeast Asian amphibians, which brings into question whether the high levels of cryptic diversity observed in other amphibian groups reflect distinct cryptic species—or, instead, highly admixed and structured metapopulation lineages. Our results also provide an alternative explanation to the conundrum of divergent (sometimes nonsister) sympatric lineages—a pattern that has been celebrated as indicative of true cryptic speciation. Based on these findings, we recommend that species delimitation of continuously distributed “cryptic” groups should not rely solely on conventional SDMs, but should necessarily examine population structure and gene flow to avoid taxonomic inflation.
more »
« less
Incorporating the speciation process into species delimitation
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.
more »
« less
- Award ID(s):
- 1655607
- PAR ID:
- 10229731
- Editor(s):
- Barraclough, Timothy G.
- Date Published:
- Journal Name:
- PLoS computational biology
- Volume:
- 17
- Issue:
- 5
- ISSN:
- 1553-734X
- Page Range / eLocation ID:
- e1008924
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Genomic‐scale datasets, sophisticated analytical techniques, and conceptual advances have disproportionately failed to resolve species boundaries in some groups relative to others. To understand the processes that underlie taxonomic intractability, we dissect the speciation history of an Australian lizard clade that arguably represents a “worst‐case” scenario for species delimitation within vertebrates: theCtenotus inornatusspecies group, a clade beset with decoupled genetic and phenotypic breaks, uncertain geographic ranges, and parallelism in purportedly diagnostic morphological characters. We sampled hundreds of localities to generate a genomic perspective on population divergence, structure, and admixture. Our results revealed rampant paraphyly of nominate taxa in the group, with lineages that are either morphologically cryptic or polytypic. Isolation‐by‐distance patterns reflect spatially continuous differentiation among certain pairs of putative species, yet genetic and geographic distances are decoupled in other pairs. Comparisons of mitochondrial and nuclear gene trees, tests of nuclear introgression, and historical demographic modelling identified gene flow between divergent candidate species. Levels of admixture are decoupled from phylogenetic relatedness; gene flow is often higher between sympatric species than between parapatric populations of the same species. Such idiosyncratic patterns of introgression contribute to species boundaries that are fuzzy while also varying in fuzziness. Our results suggest that “taxonomic disaster zones” like theC. inornatusspecies group result from spatial variation in the porosity of species boundaries and the resulting patterns of genetic and phenotypic variation. This study raises questions about the origin and persistence of hybridizing species and highlights the unique insights provided by taxa that have long eluded straightforward taxonomic categorization.more » « less
-
Carstens, Bryan (Ed.)Gene flow between diverging lineages challenges the resolution of species boundaries and the understanding of evolutionary history in recent radiations. Here, we integrate phylogenetic and coalescent tools to resolve reticulate patterns of diversification and use a perspective focused on evolutionary mechanisms to distinguish interspecific and intraspecific taxonomic variation. We use this approach to resolve the systematics for one of the most intensively studied but difficult to understand groups of reptiles: the spotted whiptail lizards of the genus Aspidoscelis (A. gularis complex). Whiptails contain the largest number of unisexual species known within any vertebrate group and the spotted whiptail complex has played a key role in the generation of this diversity through hybrid speciation. Understanding lineage boundaries and the evolutionary history of divergence and reticulation within this group is therefore key to understanding the generation of unisexual diversity in whiptails. Despite this importance, long-standing confusion about their systematics has impeded understanding of which gonochoristic species have contributed to the formation of unisexual lineages. Using reduced representation genomic data, we resolve patterns of divergence and gene flow within the spotted whiptails and clarify patterns of hybrid speciation. We find evidence that biogeographically structured ecological and environmental variation has been important in morphological and genetic diversification, as well as the maintenance of species boundaries in this system. Our study elucidates how gene flow among lineages and the continuous nature of speciation can bias the practice of species delimitation and lead taxonomists operating under different frameworks to different conclusions (here we propose that a 2 species arrangement best reflects our current understanding). In doing so, this study provides conceptual and methodological insights into approaches to resolving diversification patterns and species boundaries in rapid radiations with complex histories, as well as long-standing taxonomic challenges in the field of systematic biology.more » « less
-
Burbrink, Frank (Ed.)Abstract In cryptic amphibian complexes, there is a growing trend to equate high levels of genetic structure with hidden cryptic species diversity. Typically, phylogenetic structure and distance-based approaches are used to demonstrate the distinctness of clades and justify the recognition of new cryptic species. However, this approach does not account for gene flow, spatial, and environmental processes that can obfuscate phylogenetic inference and bias species delimitation. As a case study, we sequenced genome-wide exons and introns to evince the processes that underlie the diversification of Philippine Puddle Frogs—a group that is widespread, phenotypically conserved, and exhibits high levels of geographically based genetic structure. We showed that widely adopted tree- and distance-based approaches inferred up to 20 species, compared to genomic analyses that inferred an optimal number of five distinct genetic groups. Using a suite of clustering, admixture, and phylogenetic network analyses, we demonstrate extensive admixture among the five groups and elucidate two specific ways in which gene flow can cause overestimations of species diversity: 1) admixed populations can be inferred as distinct lineages characterized by long branches in phylograms; and 2) admixed lineages can appear to be genetically divergent, even from their parental populations when simple measures of genetic distance are used. We demonstrate that the relationship between mitochondrial and genome-wide nuclear $$p$$-distances is decoupled in admixed clades, leading to erroneous estimates of genetic distances and, consequently, species diversity. Additionally, genetic distance was also biased by spatial and environmental processes. Overall, we showed that high levels of genetic diversity in Philippine Puddle Frogs predominantly comprise metapopulation lineages that arose through complex patterns of admixture, isolation-by-distance, and isolation-by-environment as opposed to species divergence. Our findings suggest that speciation may not be the major process underlying the high levels of hidden diversity observed in many taxonomic groups and that widely adopted tree- and distance-based methods overestimate species diversity in the presence of gene flow. [Cryptic species; gene flow; introgression; isolation-by-distance; isolation-by-environment; phylogenetic network; species delimitation.]more » « less
-
Abstract Species delimitation is an imperative first step toward understanding Earth's biodiversity, yet what constitutes a species and the relative importance of the various processes by which new species arise continue to be debatable. Species delimitation in spiders has traditionally used morphological characters; however, certain mygalomorph spiders exhibit morphological homogeneity despite long periods of population‐level isolation, absence of gene flow, and consequent high degrees of molecular divergence. Studies have shown strong geographic structuring and significant genetic divergence among several species complexes within the trapdoor spider genusAptostichus, most of which are restricted to the California Floristic Province (CAFP) biodiversity hotspot. Specifically, theAptostichus icenogleicomplex, which comprises the three sibling species,A. barackobamai,A. isabella, andA. icenoglei, exhibits evidence of cryptic mitochondrial DNA diversity throughout their ranges in Northern, Central, and Southern California. Our study aimed to explicitly test species hypotheses within this assemblage by implementing a cohesion species‐based approach. We used genomic‐scale data (ultraconserved elements, UCEs) to first evaluate genetic exchangeability and then assessed ecological interchangeability of genetic lineages. Biogeographical analysis was used to assess the likelihood of dispersal versus vicariance events that may have influenced speciation pattern and process across the CAFP's complex geologic and topographic landscape. Considering the lack of congruence across data types and analyses, we take a more conservative approach by retaining species boundaries withinA. icenoglei.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/doi.org/10.1371/journal.pcbi.1008924
