skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Microgeographic population structuring in a genus of California trapdoor spiders and discovery of an enigmatic new species (Euctenizidae: Promyrmekiaphila korematsui sp. nov.)
Abstract The recognition and delineation of cryptic species remains a perplexing problem in systematics, evolution, and species delimitation. Once recognized as such, cryptic species complexes provide fertile ground for studying genetic divergence within the context of phenotypic and ecological divergence (or lack thereof). Herein we document the discovery of a new cryptic species of trapdoor spider,Promyrmekiaphila korematsuisp. nov. Using subgenomic data obtained via target enrichment, we document the phylogeography of the California endemic genusPromyrmekiaphilaand its constituent species, which also includesP. clathrataandP. winnemem. Based on these data we show a pattern of strong geographic structuring among populations but cannot entirely discount recent gene flow among populations that are parapatric, particularly for deeply diverged lineages withinP. clathrata. The genetic data, in addition to revealing a new undescribed species, also allude to a pattern of potential phenotypic differentiation where species likely come into close contact. Alternatively, phenotypic cohesion among genetically divergentP. clathratalineages suggests that some level of gene flow is ongoing or occurred in the recent past. Despite considerable field collection efforts over many years, additional sampling in potential zones of contact for both species and lineages is needed to completely resolve the dynamics of divergence inPromyrmekiaphilaat the population–species interface.  more » « less
Award ID(s):
1937604
PAR ID:
10493503
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
14
Issue:
3
ISSN:
2045-7758
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. 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
  3. PremiseDivergence depends on the strength of selection and frequency of gene flow between taxa, while reproductive isolation relies on mating barriers and geographic distance. Less is known about how these processes interact at early stages of speciation. Here, we compared population‐level differentiation in floral phenotype and genetic sequence variation among recently divergedCastillejato explore patterns of diversification under different scenarios of reproductive isolation. MethodsUsing target enrichment enabled by the Angiosperms353 probe set, we assessed genetic distance among 50 populations of fourCastillejaspecies. We investigated whether patterns of genetic divergence are explained by floral trait variation or geographic distance in two focal groups: the widespreadC. sessilifloraand the more restrictedC. purpureaspecies complex. ResultsWe document thatC. sessilifloraand theC. purpureacomplex are characterized by high diversity in floral color across varying geographic scales. Despite phenotypic divergence, groups were not well supported in phylogenetic analyses, and little genetic differentiation was found across targeted Angiosperms353 loci. Nonetheless, a principal coordinate analysis of single nucleotide polymorphisms revealed differentiation withinC. sessilifloraacross floral morphs and geography and less differentiation among species of theC. purpureacomplex. ConclusionsPatterns of genetic distance inC. sessiliflorasuggest species cohesion maintained over long distances despite variation in floral traits. In theC. purpureacomplex, divergence in floral color across narrow geographic clines may be driven by recent selection on floral color. These contrasting patterns of floral and genetic differentiation reveal that divergence can arise via multiple eco‐evolutionary paths. 
    more » « less
  4. Abstract Divergence is often ephemeral, and populations that diverge in response to regional topographic and climatic factors may not remain reproductively isolated when they come into secondary contact. We investigated the geographical structure and evolutionary history of population divergence withinSceloporus occidentalis(western fence lizard), a habitat generalist with a broad distribution that spans the major biogeographical regions of Western North America. We used double digest RAD sequencing to infer population structure, phylogeny and demography. Population genetic structure is hierarchical and geographically structured with evidence for gene flow between biogeographical regions. Consistent with the isolation–expansion model of divergence during Quaternary glacial–interglacial cycles, gene flow and secondary contact are supported as important processes explaining the demographic histories of populations. Although populations may have diverged as they spread northward in a ring‐like manner around the Sierra Nevada and southern Cascade Ranges, there is strong evidence for gene flow among populations at the northern terminus of the ring. We propose the concept of an “ephemeral ring species” and contrastS. occidentaliswith the classic North American ring species,Ensatina eschscholtzii. Contrary to expectations of lower genetic diversity at northern latitudes following post‐Quaternary‐glaciation expansion, the ephemeral nature of divergence inS. occidentalishas produced centres of high genetic diversity for different reasons in the south (long‐term stability) vs. the north (secondary contact). 
    more » « less
  5. 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