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 two
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/
- NSF-PAR ID:
- 10245980
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 25
- Issue:
- 11
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 2559-2576
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract Lycaeides butterfly taxa (L .melissa and 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 HoleLycaeides ancestry 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 HoleLycaeides ancestry 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
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 depressus andS. 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. depressus toS. peltifer in the direction of river flow. However, selection is mediating rapid, unidirectional introgression fromS. peltifer toS. 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
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 in
Lycaeides butterflies 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. melissa ancestry 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
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
Abstract Incompletely isolated species provide an opportunity to investigate the genetic mechanisms and evolutionary forces that maintain distinct species in the face of ongoing gene flow. Here, we use field surveys and reduced representation sequencing to characterize the patterns of reproductive isolation, admixture and genomic divergence between populations of the outcrossing wildflower
Mimulus guttatus and selfingM. nasutus . Focusing on a single site where these two species have come into secondary contact, we find that phenological isolation is strong, although incomplete, and is likely driven by divergence in response to photoperiod. In contrast to previous field studies, which have suggested that F1‐hybrid formation might be rare, we discover patterns of genomic variation consistent with ongoing introgression. Strikingly, admixed individuals vary continuously from highly admixed to nearly pureM. guttatus , demonstrating ongoing hybridization and asymmetric introgression fromM. nasutus intoM. guttatus . Patterns of admixture and divergence across the genome show that levels of introgression are more variable than expected by chance. Some genomic regions show a reduced introgression, including one region that overlaps a critical photoperiodQTL , whereas other regions show elevated levels of interspecific gene flow. In addition, we observe a genome‐wide negative relationship between absolute divergence and the local recombination rate, potentially indicating natural selection againstM. nasutus ancestry inM. guttatus genetic backgrounds. Together, our results suggest thatMimulus speciation is both ongoing and dynamic and that a combination of divergence in phenology and mating system, as well as selection against interspecific alleles, likely maintains these sympatric species.
