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.

Keywords: clines; hybrid zones; inversions; local adaptation; molluscs; speciation.

Figure 1

A) Map of the sampled shore area. Habitat points in the boulder field are shown in black, and points on bedrock in grey. Each sampled snail is represented by a yellow point, and the one‐dimensional path through the sampled area is indicated in orange. There are two main habitat transitions: arrow 1, from the boulder field to the rock platform; and arrow 2, from the rock platform to the steep cliff. The orange arrow indicates the average center of all non‐neutral clines (see Fig. 4). Note that the two large sampling gaps in the “Crab” and the “Wave” area represent intentional breaks in the sampling, while the small gap coinciding with the average cline center (orange arrow) represents a gap in the snail distribution. Insert: satellite image from Google Earth (Image © 2017 DigitalGlobe). B) Examples of phenotypic and genetic clines. The x‐axis represents the path through the sampled transect shown in (A). Vertical lines indicate the positions of the arrows in (A). The top panel shows five different phenotypic clines. Thick lines represent frequencies of different colors/patterns (beige, black, and banded); thin lines represent size and shape (scaled to vary between 0 and 1. Note that for analyses, scaling was done so that it ensured an increase from Crab to Wave. In this figure the size cline is reverted to show that the Crab ecotype is larger). The second panel shows examples of genetic clines, with grey curves representing clines consistent with neutrality and orange curves representing non‐neutral clines.

Figure 2

Variation in cline parameters. A) Comparison of variance explained (var.ex) between simulated selected SNPs (light orange), simulated neutral SNPs (grey), and observed SNPs (light blue). The orange line indicates the 99% quantile of the simulated neutral distribution. The right plot is restricted to var.ex values above this threshold, and shows observed and simulated neutral distributions only, to highlight the difference in the distribution tails. B) Observed neutral (grey) and non‐neutral SNPs (i.e., var.ex above threshold in A; orange). Note that there were many more neutral than non‐neutral SNPs; here, values in each class are expressed as percentages of all SNPs in that class.

Figure 3

(A) Proportion of SNPs that were non‐neutral in each of the 17 LGs (sorted from 1 to 17 on the x‐axis). SNPs within three large regions of high linkage disequilibrium (“nnBlocks”) are shown in color. B) Variation in the proportion of non‐neutral SNPs among map positions in the three LGs with large numbers of non‐neutral SNPs. nnBlocks are again indicated in colour. All 17 LGs are shown in Supporting Information Appendix, Fig. S4.

Figure 4

Distribution of cline slopes versus cline centers of non‐neutral SNPs. Non‐neutral SNPs in nnBlocks are shown in colors analogous to previous figures. All other non‐neutral SNPs are shown in orange. The vertical orange line indicates the average of all non‐neutral cline centers. Blue lines indicate habitat transitions as in Fig. 1.