skip to main content


Title: Assessing models of speciation under different biogeographic scenarios; an empirical study using multi‐locus and RNA ‐seq analyses
Abstract

Evolutionary biology often seeks to decipher the drivers of speciation, and much debate persists over the relative importance of isolation and gene flow in the formation of new species. Genetic studies of closely related species can assess if gene flow was present during speciation, because signatures of past introgression often persist in the genome. We test hypotheses on which mechanisms of speciation drove diversity among three distinct lineages of desert tortoise in the genusGopherus. These lineages offer a powerful system to study speciation, because different biogeographic patterns (physical vs. ecological segregation) are observed at opposing ends of their distributions. We use 82 samples collected from 38 sites, representing the entire species' distribution and generate sequence data for mtDNAand four nuclear loci. A multilocus phylogenetic analysis in *BEAST estimates the species tree.RNA‐seq data yield 20,126 synonymous variants from 7665 contigs from two individuals of each of the three lineages. Analyses of these data using the demographic inference package ∂a∂i serve to test the null hypothesis of no gene flow during divergence. The best‐fit demographic model for the three taxa is concordant with the *BEAST species tree, and the ∂a∂i analysis does not indicate gene flow among any of the three lineages during their divergence. These analyses suggest that divergence among the lineages occurred in the absence of gene flow and in this scenario the genetic signature of ecological isolation (parapatric model) cannot be differentiated from geographic isolation (allopatric model).

 
more » « less
NSF-PAR ID:
10196924
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
6
Issue:
2
ISSN:
2045-7758
Page Range / eLocation ID:
p. 379-396
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Divergent host use has long been suspected to drive population differentiation and speciation in plant‐feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as dispersal limitation and population structure may also influence patterns of genetic variation. In this study, we use double‐digest restriction‐associatedDNA(ddRAD) sequencing to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiplePinushosts throughout its range in eastern North America. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model‐based and model‐free clustering methods and identify three geographically distinct genetic clusters. Next, using a composite‐likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linkedRADmarkers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge ofPinusrefugia, estimated demographic parameters and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario forN. lecontei. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters, and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, dispersal limitation and ecological divergence all contribute to genomewide differentiation in this species and support the hypothesis that host use is a common driver of population divergence in host‐specialized insects.

     
    more » « less
  2. Abstract

    Rapid speciation events, with taxa generated over a short time period, are among the most investigated biological phenomena. However, molecular systematics often reveals contradictory results compared with morphological/phenotypical diagnoses of species under scenarios of recent and rapid diversification. In this study, we used molecular data from an average of over 29 000 loci per sample from RADseq to reconstruct the diversification history and delimit the species boundary in a short‐winged grasshopper species complex (Melanoplus scudderigroup), where Pleistocene diversification has been hypothesized to generate more than 20 putative species with distinct male genitalic shapes. We found that, based on a maximum likelihood molecular phylogeny, each morphological species indeed forms a monophyletic group, contrary to the result from a previous mitochondrial DNA sequence study. By dating the diversification events, the species complex is estimated to have diversified during the Late Pleistocene, supporting the recent radiation hypothesis. Furthermore, coalescent‐based species delimitation analyses provide quantitative support for independent genetic lineages, which corresponds to the morphologically defined species. Our results also showed that male genitalic shape may not be predicted by evolutionary distance among species, not only indicating that this trait is labile, but also implying that selection may play a role in character divergence. Additionally, our findings suggest that the rapid speciation events in this flightless grasshopper complex might be primarily associated with the fragmentation of their grassland habitats during the Late Pleistocene. Collectively, our study highlights the importance of integrating multiple sources of information to delineate species, especially for a species complex that diversified rapidly, and whose divergence may be linked to ecological processes that create geographic isolation (i.e. fragmented habitats), as well as selection acting on characters with direct consequences for reproductive isolation (i.e. genitalic divergence).

     
    more » « less
  3. Abstract Aim

    The “sexy shrimp”Thor amboinensisis currently considered a single circumtropical species. However, the tropical oceans are partitioned by hard and soft barriers to dispersal, providing ample opportunity for allopatric speciation. Herein, we test the null hypothesis thatT. amboinensisis a single global species, reconstruct its global biogeographical history, and comment on population‐level patterns throughout the Tropical Western Atlantic.

    Location

    Coral reefs in all tropical oceans.

    Methods

    Specimens ofThor amboinensiswere obtained through field collection and museum holdings. We used one mitochondrial (COI) and two nuclear (NaK, enolase) gene fragments for global species delimitation and phylogenetic analyses (n = 83 individuals, 30 sample localities), while phylogeographical reconstruction in theTWAwas based onCOIonly (n = 303 individuals, 10 sample localities).

    Results

    We found evidence for at least five cryptic lineages (9%–22%COIpairwise sequence divergence): four in the Indo‐West Pacific and one in the Tropical Western Atlantic. Phylogenetic reconstruction revealed that endemic lineages from Japan and the South Central Pacific are more closely related to the Tropical Western Atlantic lineage than to a co‐occurring lineage that is widespread throughout the Indo‐West Pacific. Concatenated and species tree phylogenetic analyses differ in the placement of an endemic Red Sea lineage and suggest alternate dispersal pathways into the Atlantic. Phylogeographical reconstruction throughout the Tropical Western Atlantic reveals little genetic structure over more than 3,000 km.

    Main conclusions

    Thor amboinensisis a species complex that has undergone a series of allopatric speciation events and whose members are in secondary contact in the Indo‐West Pacific. Nuclear‐ and mitochondrial‐ gene phylogenies show evidence of introgression between lineages inferred to have been separated more than 20 Ma. Phylogenetic discordance between multi‐locus analyses suggest thatT. amboinensisoriginated in the Tethys sea and dispersed into the Atlantic and Indo‐West Pacific through the Tethys seaway or, alternatively, originated in the Indo‐West Pacific and dispersed into the Atlantic around South Africa. Population‐level patterns in the Caribbean indicate extensive gene flow across the region.

     
    more » « less
  4. Abstract Aim

    To test the importance of alternative diversification drivers and biogeographical processes for the evolution of Amazonian upland forest birds through a densely sampled analysis of diversification of the endemic Amazonian genusRhegmatorhinaat multiple taxonomic and temporal scales.

    Location

    Amazonia.

    Taxon

    Antbirds (Thamnophilidae).

    Methods

    We sequenced four mtDNAand nuclear gene regions of 120 individuals from 50 localities representing all recognized species and subspecies of the genus. We performed molecular phylogenetic analyses using both gene tree and species tree methods, molecular dating analysis and estimated population demographic history and gene flow.

    Results

    Dense sampling throughout the distribution ofRhegmatorhinarevealed that the main Amazonian rivers delimit the geographic distribution of taxa as inferred from mtDNAlineages. Molecular phylogenetic analyses resulted in a strongly supported phylogenetic hypothesis for the genus, with two main clades currently separated by the Madeira River. Molecular dating analysis indicated diversification during the Quaternary. Reconstruction of recent demographic history of populations revealed a trend for population expansion in eastern Amazonia and stability in the west. Estimates of gene flow corroborate the possibility that migration after divergence had some influence on the current patterns of diversity.

    Main Conclusions

    Based on broad‐scale sampling, a clarification of taxonomic boundaries, and strongly supported phylogenetic relationships, we confirm that, first, mitochondrial lineages within this upland forest Amazonian bird genus agree with spatial patterns known for decades based on phenotypes, and second, that most lineages are geographically delimited by the large Amazonian rivers. The association between past demographic changes related to palaeoclimatic cycles and the historically varying strength and size of rivers as barriers to dispersal may be the path to the answer to the long‐standing question of identifying the main drivers of Amazonian diversification.

     
    more » « less
  5. Abstract Aim

    To investigate the structure and rate of gene flow among populations of habitat‐specialized species to understand the ecological and evolutionary processes underpinning their population dynamics and historical demography, including speciation and extinction.

    Location

    Peruvian and Argentine Andes.

    Taxon

    Two subspecies of torrent duck (Merganetta armata).

    Methods

    We sampled 156 individuals in Peru (M. a. leucogenis;Chillón River,n = 57 and Pachachaca River,n = 49) and Argentina (M. a. armata;Arroyo Grande River,n = 33 and Malargüe River,n = 17), and sequenced the mitochondrial DNA (mtDNA) control region to conduct coarse and fine‐scale demographic analyses of population structure. Additionally, to test for differences between subspecies, and across genetic markers with distinct inheritance patterns, a subset of individuals (Peru,n = 10 and Argentina,n = 9) was subjected to partial genome resequencing, obtaining 4,027 autosomal and 189 Z‐linked double‐digest restriction‐associated DNA sequences.

    Results

    Haplotype and nucleotide diversities were higher in Peru than Argentina across all markers. Peruvian and Argentine subspecies showed concordant species‐level differences (ΦSTmtDNA = 0.82; ΦSTautosomal = 0.30; ΦSTZ chromosome = 0.45), including no shared mtDNA haplotypes. Demographic parameters estimated for mtDNA using IM and IMa2 analyses, and for autosomal markers using∂a∂i(isolation‐with‐migration model), supported an old divergence (mtDNA = 600,000 years before present (ybp), 95% HPD range = 1.2 Mya to 200,000 ybp; and autosomal∂a∂i = 782,490 ybp), between the two subspecies, characteristic of deeply diverged lineages. The populations were well‐differentiated in Argentina but moderately differentiated in Peru, with low unidirectional gene flow in each country.

    Main conclusions

    We suggest that the South American Arid Diagonal was preexisting and remains a current phylogeographic barrier between the ranges of the two torrent duck subspecies, and the adult territoriality and breeding site fidelity to the rivers define their population structure.

     
    more » « less