skip to main content


Title: Population genomics of divergence among extreme and intermediate color forms in a polymorphic insect
Abstract

Geographic variation in insect coloration is among the most intriguing examples of rapid phenotypic evolution and provides opportunities to study mechanisms of phenotypic change and diversification in closely related lineages. The bumble beeBombus bifariuscomprises two geographically disparate color groups characterized by red‐banded and black‐banded abdominal pigmentation, but with a range of spatially and phenotypically intermediate populations across western North America. Microsatellite analyses have revealed thatB. bifariusin the USA are structured into two major groups concordant with geography and color pattern, but also suggest ongoing gene flow among regional populations. In this study, we better resolve the relationships among major color groups to better understand evolutionary mechanisms promoting and maintaining such polymorphism. We analyze >90,000 and >25,000 single‐nucleotide polymorphisms derived from transcriptome (RNAseq) and double digest restriction site associatedDNAsequencing (ddRAD), respectively, in representative samples from spatial and color pattern extremes inB. bifariusas well as phenotypic and geographic intermediates. Both ddRADandRNAseq data illustrate substantial genome‐wide differentiation of the red‐banded (eastern) color form from both black‐banded (western) and intermediate (central) phenotypes and negligible differentiation among the latter populations, with no obvious admixture among bees from the two major lineages. Results thus indicate much stronger background differentiation amongB. bifariuslineages than expected, highlighting potential challenges for revealing loci underlying color polymorphism from population genetic data alone. These findings will have significance for resolving taxonomic confusion in this species and in future efforts to investigate color‐pattern evolution inB. bifariusand other polymorphic bumble bee species.

 
more » « less
Award ID(s):
1457659
NSF-PAR ID:
10196916
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Volume:
6
Issue:
4
ISSN:
2045-7758
Page Range / eLocation ID:
p. 1075-1091
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. Abstract

    A major goal of speciation research is to reveal the genomic signatures that accompany the speciation process. Genome scans are routinely used to explore genome‐wide variation and identify highly differentiated loci that may contribute to ecological divergence, but they do not incorporate spatial, phenotypic or environmental data that might enhance outlier detection. Geographic cline analysis provides a potential framework for integrating diverse forms of data in a spatially explicit framework, but has not been used to study genome‐wide patterns of divergence. Aided by a first‐draft genome assembly, we combined anFCTscan and geographic cline analysis to characterize patterns of genome‐wide divergence between divergent pollination ecotypes ofMimulus aurantiacus.FCTanalysis of 58 872SNPs generated viaRAD‐seq revealed little ecotypic differentiation (meanFCT = 0.041), although a small number of loci were moderately‐to‐highly diverged. Consistent with our previous results from the geneMaMyb2, which contributes to differences in flower colour, 130 loci have cline shapes that recapitulate the spatial pattern of trait divergence, suggesting that they may reside in or near the genomic regions that contribute to pollinator isolation. In the narrow hybrid zone between the ecotypes, extensive admixture among individuals and low linkage disequilibrium between markers indicate that most outlier loci are scattered throughout the genome, rather than being restricted to one or a few divergent regions. In addition to revealing the genomic consequences of ecological divergence in this system, we discuss how geographic cline analysis is a powerful but under‐utilized framework for studying genome‐wide patterns of divergence.

     
    more » « less
  3. Abstract

    Reproductive isolation can be initiated by changes in one or a few key traits that prevent random mating among individuals in a population. During the early stages of speciation, when isolation is often incomplete, there will be a heterogeneous pattern of differentiation across regions of the genome between diverging populations, with loci controlling these key traits appearing the most distinct as a result of strong diversifying selection. In this study, we used Illumina‐sequenced ddRADtags to identify genomewide patterns of differentiation in three recently diverged island populations of theMonarcha castaneiventrisflycatcher of the Solomon Islands. Populations of this species have diverged in plumage colour, and these differences in plumage colour, in turn, are used in conspecific recognition and likely important in reproductive isolation. Previous candidate gene sequencing identified point mutations inMC1RandASIP, both known pigmentation genes, to be associated with the difference in plumage colour between islands. Here, we show that background levels of genomic differentiation based on over 70,000SNPs are extremely low between populations of distinct plumage colour, with no loci reaching the level of differentiation found in either candidate gene. Further, we found that a phylogenetic analysis based on theseSNPs produced a taxonomy wherein the two melanic populations appear to have evolved convergently, rather than from a single common ancestor, in contrast to their original classification as a single subspecies. Finally, we found evidence that the pattern of low genomic differentiation is the result of both incomplete lineage sorting and gene flow between populations.

     
    more » « less
  4. Premise

    The ability to sequence genome‐scale data from herbarium specimens would allow for the economical development of data sets with broad taxonomic and geographic sampling that would otherwise not be possible. Here, we evaluate the utility of a basic double‐digest restriction site–associatedDNAsequencing (ddRADseq) protocol usingDNAs from four genera extracted from both silica‐dried and herbarium tissue.

    Methods

    DNAs fromDraba,Boechera,Solidago, andIlexwere processed with a ddRADseq protocol. The effects ofDNAdegradation, taxon, and specimen age were assessed.

    Results

    Although taxon, preservation method, and specimen age affected data recovery, large phylogenetically informative data sets were obtained from the majority of samples.

    Discussion

    These results suggest that herbarium samples can be incorporated into ddRADseq project designs, and that specimen age can be used as a rapid on‐site guide for sample choice. The detailed protocol we provide will allow users to pursue herbarium‐based ddRADseq projects that minimize the expenses associated with fieldwork and sample evaluation.

     
    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