skip to main content


Title: History, geography and host use shape genomewide patterns of genetic variation in the redheaded pine sawfly ( Neodiprion lecontei )
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
NSF-PAR ID:
10030710
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
26
Issue:
4
ISSN:
0962-1083
Page Range / eLocation ID:
p. 1022-1044
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Lemurs are among the world's most threatened mammals. The critically endangered black‐and‐white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remainingV. variegatarange. We used 10 polymorphic microsatellite loci and ~550 bp of mtDNAsequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of theMangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNAhaplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high averageFST(0.247) and ΦST(0.544), and followed a pattern of isolation‐by‐distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re‐evaluation of conservation management units moving forward.

     
    more » « less
  2. Abstract

    Identifying drivers of dispersal limitation and genetic differentiation is a key goal in biogeography. We examine patterns of population connectivity and genetic diversity using restriction site‐associatedDNAsequencing (RADseq) in two bumble bee species,Bombus vosnesenskiiandBombus bifarius,across latitude and altitude in mountain ranges from California, Oregon and Washington, U.S.A.Bombus vosnesenskii, which occurs across a broader elevational range at most latitudes, exhibits little population structure whileB. bifarius, which occupies a relatively narrow higher elevation niche across most latitudes, exhibits much stronger population differentiation, although gene flow in both species is best explained by isolation with environmental niche resistance. A relationship between elevational habitat breadth and genetic diversity is also apparent, withB. vosnesenskiiexhibiting relatively consistent levels of genetic diversity across its range, whileB. bifariushas reduced genetic diversity at low latitudes, where it is restricted to high‐elevation habitat. The results of this study highlight the importance of the intersect between elevational range and habitat suitability in influencing population connectivity and suggest that future climate warming will have a fragmenting effect even on populations that are presently well connected, as they track their thermal niches upward in montane systems.

     
    more » « less
  3. Abstract

    Wallace's riverine barrier hypothesis postulates that large rivers, such as the Amazon and its tributaries, reduce or prevent gene flow between populations on opposite banks, leading to allopatry and areas of species endemism occupying interfluvial regions. Several studies have shown that two major tributaries, Rio Branco and Rio Negro, are important barriers to gene flow for birds, amphibians and primates. No botanical studies have considered the potential role of the Rio Branco as a barrier, while a single botanical study has evaluated the Rio Negro as a barrier. We studied an Amazon shrub,Amphirrhox longifolia(A. St.‐Hil.) Spreng (Violaceae), as a model to test the riverine barrier hypothesis. Twenty‐six populations ofA. longifoliawere sampled on both banks of the Rio Branco and Rio Negro in the core Amazon Basin. Double‐digestRADseq was used to identify 8,010 unlinkedSNPmarkers from the nuclear genome of 156 individuals. Data relating to population structure support the hypothesis that the Rio Negro acted as a significant genetic barrier forA. longifolia. On the other hand, no genetic differentiation was detected among populations spanning the narrower Rio Branco, which is a tributary of the Rio Negro. This study shows that the strength of riverine barriers for Amazon plants is dependent on the width of the river separating populations and species‐specific dispersal traits. Future studies of plants with contrasting life history traits will further improve our understanding of the landscape genetics and allopatric speciation history of Amazon plant diversity.

     
    more » « less
  4. Abstract

    Evolutionary radiations have been well documented in plants and insects, and natural selection may often underly these radiations. If radiations are adaptive, the diversity of species could be due to ecological speciation in these lineages. Agromyzid flies exhibit patterns of repeated host‐associated radiations. We investigated whether host‐associated population divergence and evidence of divergent selection exist in the leaf minerPhytomyza glabricolaon its sympatric host plants, the holly species,Ilex coriaceaandI. glabra. UsingAFLPs and nuclear sequence data, we found substantial genetic divergence between host‐associated populations of these flies throughout their geographic range. Genome scans using theAFLPdata identified 13 loci under divergent selection, consistent with processes of ecological speciation.EF‐1αdata suggest that I. glabrais the original host ofP. glabricolaand thatI. coriaceais the novel host, but theAFLPdata are ambiguous with regard to directionality of the host shift.

     
    more » « less
  5. Abstract

    Chromosomal rearrangement can be an important mechanism driving population differentiation and incipient speciation. In the mountain pine beetle (MPB,Dendroctonus ponderosae), deletions on the Y chromosome that are polymorphic among populations are associated with reproductive incompatibility. Here, we usedRADsequencing across the entireMPBrange in western North America to reveal the extent of the phylogeographic differences between Y haplotypes compared to autosomal and X‐linked loci. Clustering and geneflow analyses revealed three distinct Y haplogroups geographically positioned within and on either side of the Great Basin Desert. Despite close geographic proximity between populations on the boundaries of each Y haplogroup, there was extremely low Y haplogroup mixing among populations, and gene flow on the autosomes was reduced across Y haplogroup boundaries. These results are consistent with a previous study suggesting that independent degradation of a recently evolved neo‐Y chromosome in previously isolated populations causes male sterility or inviability among Y haplotype lineages. Phylogeographic results supported historic contraction ofMPBinto three separate Pleistocene glacial refugia followed by postglacial range expansion and secondary contact. Distinct sets ofSNPs were statistically associated with environmental data among the most genetically distinct sets of geographic populations. This finding suggests that the process of adaptation to local climatic conditions is influenced by population genetic structure, with evidence for largely independent evolution in the most genetically isolated Y haplogroup.

     
    more » « less