Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis.

Eva L Koch,E Moriarty Lemmon,Roger K Butlin,Anja M Westram,Rui Faria,Jenny Larsson,Alan R Lemmon,Hernán E Morales,Kerstin Johannesson

doi:10.1002/evl3.227

Abstract

Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on phenotypes under divergent selection. For this, the marine snail Littorina saxatilis provides an ideal study system. Divergent ecotypes adapted to wave action and crab predation occur in close proximity on intertidal shores with gene flow between them. Here, we used F2 individuals obtained from crosses between the ecotypes to test for associations between genomic regions and traits distinguishing the Crab‐/Wave‐adapted ecotypes including size, shape, shell thickness, and behavior. We show that most of these traits are influenced by two previously detected inversion regions that are divergent between ecotypes. We thus gain a better understanding of one important underlying mechanism responsible for the rapid and repeated formation of ecotypes: divergent selection acting on inversions. We also found that some inversions contributed to more than one trait suggesting that they may contain several loci involved in adaptation, consistent with the hypothesis that suppression of recombination within inversions facilitates differentiation in the presence of gene flow.

Highlights

Understanding the mechanisms that promote phenotypic diversification is of central interest in evolutionary biology
Consistent with the expectation of suppressed recombination when parents are heterozygous for alternative arrangements, we found that many markers within these regions shared the same position in our QTL map (Supporting information Fig. S1)
Some Linkage Groups (LG) without any significant QTLs, not even suggestive peaks, explained high proportions of variance in several traits, namely LG 5 and 12. Consistent with this result, we found that inversions of LG 12 had significant influence on several traits (Supporting information Table S7) when we tested inversion genotype effects directly

Summary

Introduction

Understanding the mechanisms that promote phenotypic diversification is of central interest in evolutionary biology. Like assortative mating (Servedio and Boughman 2017) or phenological differences, may contribute to keeping locally adapted entities apart, in many cases some level of gene flow exists (Lenormand 2002; Smadja and Butlin 2011), for instance, in contact zones with frequent hybridization (Wu et al 2008; Harrison and Larson 2016; Schaefer et al 2016; Chhatre et al 2018) These examples have raised questions about the mechanisms maintaining and promoting genetic differentiation despite the homogenizing effects of gene flow (Felsenstein 1981; Pinho and Hey 2010)

Methods

Results

Conclusion