skip to main content


Title: Population genomic evidence of selection on structural variants in a natural hybrid zone
Abstract

Structural variants (SVs) can promote speciation by directly causing reproductive isolation or by suppressing recombination across large genomic regions. Whereas examples of each mechanism have been documented, systematic tests of the role of SVs in speciation are lacking. Here, we take advantage of long‐read (Oxford nanopore) whole‐genome sequencing and a hybrid zone between twoLycaeidesbutterfly taxa (L.melissaand Jackson HoleLycaeides) to comprehensively evaluate genome‐wide patterns of introgression for SVs and relate these patterns to hypotheses about speciation. We found >100,000 SVs segregating within or between the two hybridizing species. SVs and SNPs exhibited similar levels of genetic differentiation between species, with the exception of inversions, which were more differentiated. We detected credible variation in patterns of introgression among SV loci in the hybrid zone, with 562 of 1419 ancestry‐informative SVs exhibiting genomic clines that deviated from null expectations based on genome‐average ancestry. Overall, hybrids exhibited a directional shift towards Jackson HoleLycaeidesancestry at SV loci, consistent with the hypothesis that these loci experienced more selection on average than SNP loci. Surprisingly, we found that deletions, rather than inversions, showed the highest skew towards excess ancestry from Jackson HoleLycaeides. Excess Jackson HoleLycaeidesancestry in hybrids was also especially pronounced for Z‐linked SVs and inversions containing many genes. In conclusion, our results show that SVs are ubiquitous and suggest that SVs in general, but especially deletions, might disproportionately affect hybrid fitness and thus contribute to reproductive isolation.

 
more » « less
Award ID(s):
1844941
NSF-PAR ID:
10401127
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
32
Issue:
6
ISSN:
0962-1083
Format(s):
Medium: X Size: p. 1497-1514
Size(s):
["p. 1497-1514"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Hybrid zones provide unique opportunities to examine reproductive isolation and introgression in nature. We utilized 45,384 single nucleotide polymorphism (SNP) loci to perform association mapping of 14 floral, vegetative and ecological traits that differ betweenIris hexagonaandIris fulva,and to investigate, using a Bayesian genomic cline (BGC) framework, patterns of genomic introgression in a large and phenotypically diverse hybrid zone in southern Louisiana. Many loci of small effect size were consistently found to be associated with phenotypic variation across all traits, and several individual loci were revealed to influence phenotypic variation across multiple traits. Patterns of genomic introgression were quite heterogeneous throughout the Louisiana Iris genome, withI. hexagonaalleles tending to be favoured over those ofI. fulva. Loci that were found to have exceptional patterns of introgression were also found to be significantly associated with phenotypic variation in a small number of morphological traits. However, this was the exception rather than the rule, as most loci that were associated with morphological trait variation were not significantly associated with excess ancestry. These findings provide insights into the complexity of the genomic architecture of phenotypic differences and are a first step towards identifying loci that are associated with both trait variation and reproductive isolation in nature.

     
    more » « less
  2. Abstract

    When organisms experience secondary contact after allopatric divergence, genomic regions can introgress differentially depending on their relationships with adaptation, reproductive isolation, recombination, and drift. Analyses of genome‐wide patterns of divergence and introgression could provide insight into the outcomes of hybridization and the potential relationship between allopatric divergence and reproductive isolation. Here, we generate population genetic data (26,262 SNPs; 353 individuals) using a reduced‐representation sequencing approach to quantify patterns of ancestry, differentiation, and introgression between a pair of ecologically distinct mammals—the desert woodrat (N.lepida) and Bryant's woodrat (N.bryanti)—that hybridize at a sharp ecotone in southern California. Individual ancestry estimates confirmed that hybrids were rare in this bimodal hybrid zone, and entirely consisted of a few F1individuals and a broad range of multigenerational backcrosses. Genomic cline analyses indicated more than half of loci had elevated introgression from one genomic background into the other. However, introgression was not associated with relative or absolute measures of divergence, and loci with extreme values for both were not typically found near detoxification enzymes previously implicated in dietary specialization for woodrats. The decoupling of differentiation and introgression suggests that processes other than adaptation, such as drift, may underlie the extreme clines at this contact zone.

     
    more » « less
  3. Abstract

    Genomic outcomes of hybridization depend on selection and recombination in hybrids. Whether these processes have similar effects on hybrid genome composition in contemporary hybrid zones versus ancient hybrid lineages is unknown. Here we show that patterns of introgression in a contemporary hybrid zone inLycaeidesbutterflies predict patterns of ancestry in geographically adjacent, older hybrid populations. We find a particularly striking lack of ancestry from one of the hybridizing taxa,Lycaeides melissa, on the Z chromosome in both the old and contemporary hybrids. The same pattern of reducedL. melissaancestry on the Z chromosome is seen in two other ancient hybrid lineages. More generally, we find that patterns of ancestry in old or ancient hybrids are remarkably predictable from contemporary hybrids, which suggests selection and recombination affect hybrid genomes in a similar way across disparate time scales and during distinct stages of speciation and species breakdown.

     
    more » « less
  4. Abstract

    Hybrid zones formed between recently diverged populations offer an opportunity to study the mechanisms underlying reproductive isolation and the process of speciation. Here, we use a combination of analytical theory and explicit forward simulations to describe how selection against hybrid genotypes impacts patterns of introgression across genomic and geographic space. By describing how lineages move across the hybrid zone, in a model without coalescence, we add to modern understanding of how clines form and how parental haplotypes are broken up during introgression. Working with lineages makes it easy to see that clines form in about 1/sgenerations, wheresis the strength of selection against hybrids, and linked clines persist over a genomic scale of 1/T, whereTis the age, in generations, of the hybrid zone. Locally disadvantageous alleles tend to exist as small families, whose lineages trace back to the side from which they originated at speeddispersal distances per generation. The lengths of continuous tracts of ancestry provide an additional source of information: blocks of ancestry surrounding incompatibilities can be substantially longer than the genomewide average block length at the same spatial location, an observation that might be used to identify candidate targets of selection.

     
    more » « less
  5. Abstract

    Speciation is the result of an accumulation of reproductive barriers between populations, but pinpointing the factors involved is often difficult. However, hybrid zones can form when these barriers are not complete, especially when lineages come into contact in intermediate or modified habitats. We examine a hybrid zone between two closely related riverine turtle species,Sternotherus depressusandS. peltifer, and use dual‐digest RAD sequencing to understand how this hybrid zone formed and elucidate genomic patterns of reproductive isolation. First, the geographical extent and timing of formation of the hybrid zone is established to provide context for understanding the role of extrinsic and intrinsic reproductive isolating mechanisms in this system. The strength of selection on taxon‐specific contributions to maintenance of the hybrid zone is then inferred using a Bayesian genomic cline model. These analyses identify a role for selection inhibiting introgression in some genomic regions at one end of the hybrid zone and promoting introgression in many loci at the other. When selective pressures necessary to generate outliers to the genomic cline are considered with the geographical and temporal context of this hybrid zone, we conclude that habitat‐specific selection probably limits introgression fromS. depressustoS. peltiferin the direction of river flow. However, selection is mediating rapid, unidirectional introgression fromS. peltifertoS. depressus, which is probably facilitated by anthropogenic habitat alteration. These findings indicate a potentially imminent threat of population‐level genomic extinction for an already imperiled species due to ongoing human‐caused habitat alteration.

     
    more » « less