Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow

Abstract

Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system‐specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome‐wide SNP set from an ideally suited study organism, the intertidal snail Littorina saxatilis, which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non‐neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non‐neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasizes that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.

Is embryo abortion a post‐zygotic barrier to gene flow between Littorina ecotypes?

“…Genotyping of female L. saxatilis was primarily used to identify female hybrid status. Importantly, however, earlier results indicate that hybrid zones are populated by later generation hybrids and backcrosses rather than F1 and F2 generation hybrids (Westram et al, ). Furthermore, as both males and females usually only disperse 1–2 m during their life‐time (Westram et al, ), a female's genotype will in most cases also reflect the average hybrid status of the ~20 males that sired her brood of embryos (Panova et al, ), and consequently also the average hybrid status of the embryos.…”

“…The Wave ecotype has a small adult size (3–7 mm), thin shell and a bold behaviour: traits that are favoured in wave‐exposed patches (Johannesson, ; Le Pennec et al, ). Contact zones are frequent, and over a Swedish contact zone divergent selection affects ~1.4% of SNPs (single nucleotide polymorphisms) over less than 50 metres, with most of the differentiated loci allocated to three large inversions which also contained many of the loci associated with the phenotypic differences (Westram et al, ). Notably, mark–recapture experiments at the same site suggested hybrid phenotypes to be superior to the parental phenotypes in the contact zone centre (Janson, ), thus showing no clear signs of hybrid maladaptation.…”

“…A random subset of the 600 sampled snails per site was genotyped using capture sequencing (Illumina sequencing based on 40,000 randomly distributed probes, see Westram et al, for details). This generated genotype information for 172, 192 and 180 of the analysed females from the three islands after appropriate filtering of the genetic data.…”

“…This generated genotype information for 172, 192 and 180 of the analysed females from the three islands after appropriate filtering of the genetic data. The sequencing generated 69,386 SNP loci (methods as in Westram et al, ) from which a hybrid index (HI) was calculated by summing reads over loci for the reference allele and dividing by the sum of total reads across both alleles. The reference allele was defined as the allele that was more common in the Wave ecotype than the Crab ecotype, and loci were only included if the allele frequency difference between the Wave and Crab ends of the transect was >0.1.…”

Genomic signatures of host‐associated divergence and adaptation in a coral‐eating snail, Coralliophila violacea (Kiener, 1836)

“…While encouraging, there are gaps in our knowledge that with the expansion of genomic technologies, we are now in a position to begin to fill. Detecting signatures of natural selection in populations where there is likely ongoing gene flow is now possible using genome-wide data, lending insight into the mechanisms of ecological speciation (Bernal, Gaither, Simison, & Rocha, 2017;Campbell, Poelstra, & Yoder, 2018;Puebla, Bermingham, & McMillan, 2014;Westram et al, 2018). To date, however, no studies examining the genomic signatures of ecological divergence in marine host-parasite systems have been conducted.…”