Genome‐wide association analyses reveal polygenic genomic architecture underlying divergent shell morphology in SpanishLittorina saxatilisecotypes

Abstract

Gene flow between diverging populations experiencing dissimilar ecological conditions can theoretically constrain adaptive evolution. To minimize the effect of gene flow, alleles underlying traits essential for local adaptation are predicted to be located in linked genome regions with reduced recombination. Local reduction in gene flow caused by selection is expected to produce elevated divergence in these regions. The highly divergent crab‐adapted and wave‐adapted ecotypes of the marine snail Littorina saxatilis present a model system to test these predictions. We used genome‐wide association (GWA) analysis of geometric morphometric shell traits associated with microgeographic divergence between the two L. saxatilis ecotypes within three separate sampling sites. A total of 477 snails that had individual geometric morphometric data and individual genotypes at 4,066 single nucleotide polymorphisms (SNPs) were analyzed using GWA methods that corrected for population structure among the three sites. This approach allowed dissection of the genomic architecture of shell shape divergence between ecotypes across a wide geographic range, spanning two glacial lineages. GWA revealed 216 quantitative trait loci (QTL) with shell size or shape differences between ecotypes, with most loci explaining a small proportion of phenotypic variation. We found that QTL were evenly distributed across 17 linkage groups, and exhibited elevated interchromosomal linkage, suggesting a genome‐wide response to divergent selection on shell shape between the two ecotypes. Shell shape trait‐associated loci showed partial overlap with previously identified outlier loci under divergent selection between the two ecotypes, supporting the hypothesis of diversifying selection on these genomic regions. These results suggest that divergence in shell shape between the crab‐adapted and wave‐adapted ecotypes is produced predominantly by a polygenic genomic architecture with positive linkage disequilibrium among loci of small effect.

Putative chromosomal rearrangements are associated primarily with ecotype divergence rather than geographic separation in an intertidal, poorly dispersing snail

“…Another recent GWA study using SNP loci called without a reference genome (Kess & Boulding, 2019) also found genome‐wide trait association signals across regions of varying levels of differentiation, but higher overall ecotype divergence among trait‐associated loci. However, here we uncover greater enrichment of trait‐associated loci in genomic regions with putative rearrangements compared with Kess and Boulding (2019).…”

“…However, here we uncover greater enrichment of trait‐associated loci in genomic regions with putative rearrangements compared with Kess and Boulding (2019). Previous genome‐wide association analyses with this morphometric data set (Kess & Boulding, 2019) used aligned shell landmark coordinates in addition to relative warps and did not include shell ornamentation traits. Many individual landmark coordinates in Kess and Boulding (2019) likely did not covary with ecotype, and therefore, many loci identified would not be expected to overlap with rearrangement regions.…”

“…We scored shell photos for five measures of shell ornamentation: banding pattern, tessellation pattern, presence of ridging, intensity of pattern colour and intensity of shell base colour. Sampled individuals had been previously photographed for geometric morphometric comparisons (Kess & Boulding, 2019). Tessellation pattern, shell ridging and shell banding were each measured for presence (0) or absence (1), ( Figure S1).…”

“…Recent studies of L. saxatilis have begun investigating the genomic basis of trait divergence between crab and wave ecotypes (Kess & Boulding, 2019; Westram et al., 2018), and high‐ and low‐shore environmental exposures across the species range (Morales et al., 2019). Inference of genomic architecture associated with shell traits has been conducted at a Swedish site and identified a role for large divergent genomic regions potentially representing chromosomal inversions or rearrangements (Westram et al., 2018).…”

“…Comparison of whole‐genome sequences from across the Northeast Atlantic identified genomic divergence coinciding with a subset of these putative rearrangements, suggesting polymorphism of these genomic regions across the species range along environmental clines (Morales et al., 2019). Investigations of divergence specifically in Spanish localities with restriction‐associated DNA sequencing (RADseq) and whole‐genome sequencing have revealed varying degrees of parallelism associated with geography (Kess et al., 2018), with elevated sharing of outliers in putative chromosomal rearrangements (Morales et al., 2019), and high differentiation at trait‐associated loci (Kess & Boulding, 2019). However, comparison of the relationship between these putative chromosomal rearrangements and replicate ecological conditions and site‐specific variation has yet to be characterized at Spanish sites.…”