Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution

Abstract

Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination betweenalternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence.

The genomic landscape of adaptation to a new host plant

“…The genomic basis conferring mimicry on different host plants in Timema walking consists of few loci of large effects, and the background genomic divergence is lower (Villoutreix et al 2020). The genomic basis of the Littorina ecotypes is similar to that in T. conura in that variants within inversions contribute to approximately half of the ecotype divergence (Koch et al 2022). Compared to those systems, the study races in T. conura have relatively high levels of genetic divergence and strong reproductive isolation, arising from the combination of preference, phenology and performance in the alternative niche (Diegisser et al 2006a;Diegisser et al 2006bDiegisser et al , 2007Diegisser et al 2008;Nilsson et al 2022).…”

Predicting rapid adaptation in time from adaptation in space: a 30-year field experiment in marine snails

“…For inversions, we predicted an increase in frequency of arrangements that are common in Wave ecotype populations. We predicted a tendency to fix arrangements that appear favoured in the Wave ecotype ( 18, 23 ). We predicted non-fixation for inversions that are maintained polymorphic in the Wave ecotype, likely by balancing selection ( 24 ).…”

“…At the phenotypic level, we anticipated a transition from Crab ecotype to Wave ecotype morphology: the averages of quantitative traits (e.g., shell length, and shell thickness) and the proportions of qualitative traits (e.g., shell colour, patterning, and roughness) were expected to approach the values typically observed in the Wave ecotype present in the area. We formulated our prediction on the basis of the polygenicity of phenotypes ( 23, 29 ) that can reach Wave optima through different pathways (both genetic and plastic) and are often under strong selection in space ( 30 ). For SNPs, we predicted an allele frequency shift over time beyond the effect of drift and neutral gene flow in at least a subset of “spatial outliers” (candidate SNPs associated with ecotype divergence in space in previous studies; see supplementary materials and methods) towards the frequencies observed in undisturbed Wave ecotype population.…”

“…Previous estimates of additive genetic variance and plastic effects of the environment for size and shell-shape traits allowed us to estimate the strength of selection required to explain the observed phenotypic ( 23 ) changes in these quantitative traits. Assuming an initial plastic response in the transplanted population, followed by Gaussian stabilizing selection towards an optimum defined by the phenotype of the Wave reference population (supplementary materials and methods), the strength of stabilizing selection (V S /V P , the variance of the fitness function relative to the phenotypic variance) ranged from 1.65 to 7.84, depending on the trait, assuming one generation per year (supplementary text).…”

“…For example, the Wave ecotype is small, has a thin shell that often shows Wave-specific colours and patterns, a large and rounded aperture, and bold behaviour, while the Crab ecotype is large, has a thick shell without patterns, a relatively smaller and more elongated aperture, and wary behaviour (Figure 1B, Figure S1D). At the level of individual SNPs (single-nucleotide polymorphisms), highly differentiated loci likely contributing to adaptation or linked to adaptive loci are scattered across the whole genome (18,23). At the level of large chromosomal rearrangements, several inversions differ in frequency between ecotypes (24)(25)(26) and explain variation in divergent traits between ecotypes (23,26).…”