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

Abstract

Littorina saxatilis is becoming a model system for understanding the genomic basis of ecological speciation. The parallel formation of crab-adapted ecotypes that exhibit partial reproductive isolation from wave-adapted ecotypes has enabled genomic investigation of conspicuous shell traits. Recent genomic studies suggest that chromosomal rearrangements may enable ecotype divergence by reducing gene flow. However, the genomic architecture of traits that are divergent between ecotypes remains poorly understood. Here, we use 11,504 single nucleotide polymorphism (SNP) markers called using the recently released L. saxatilis genome to genotype 462 crab ecotype, wave ecotype and phenotypically intermediate Spanish L. saxatilis individuals with scored phenotypes. We used redundancy analysis to study the genetic architecture of loci associated with shell shape, shape corrected for size, shell size and shell ornamentation, and to compare levels of co-association among different traits. We discovered 341 SNPs associated with shell traits. Loci associated with trait divergence between ecotypes were often located inside putative chromosomal rearrangements recently characterized in Swedish L. saxatilis. In contrast, we found that shell shape corrected for size varied primarily by geographic site rather than by ecotype and showed little association with these putative rearrangements. We conclude that genomic regions of elevated divergence inside putative rearrangements were associated with divergence of L. saxatilis ecotypes along steep environmental axes-consistent with models of adaptation with gene flow-but were not associated with divergence among the three geographical sites. Our findings support predictions from models indicating the importance of genomic regions of reduced recombination allowing co-association of loci during ecological speciation with ongoing gene flow.

Speciation in marine environments: Diving under the surface

“…For example, mussels of the genus Mytilus form a complex system with multiple hybrid zones between various species that have been intensively studied (Bierne et al., 2003; Popovic et al., 2021; Simon et al., 2021). Another taxon that has become a model in the study of ecotype evolution and ecological speciation comprises the gastropods of the genus Littorina (Galindo et al., 2021; Johannesson, 2015; Kess et al., 2021; Stankowski et al., 2020; Westram et al., 2018). Some species of corals, seaweeds, seagrasses or sea squirts have also been important targets for studies focusing on genetic divergence and species evolution (Monteiro et al., 2016; Olsen et al., 2004; Pereyra et al., 2013; see also Hudson et al., 2021; Prada & Hellberg, 2021), as have a few species of microalgae and bacteria (Johnson et al., 2006).…”

“…Data recently gathered from some marine fish species support that inversions might play a central role in local adaptation, population divergence and potentially also speciation (Barth et al., 2019; Cayuela et al., 2020; Han et al., 2020; Le Moan et al., 2020). Notably, several large putative inversions recently detected in the marine snail Littorina saxatilis (Faria et al., 2019) are enriched for loci involved in divergence between ecotypes across the species’ distribution (Kess et al., 2021; Morales et al., 2019; Westram et al., 2018). Something similar could shape ecotype divergence in the related species L. fabalis (Galindo et al., 2021; Tatarenkov & Johannesson, 1999).…”

“…Littorina (Galindo et al, 2021;Johannesson, 2015;Kess et al, 2021;Stankowski et al, 2020;Westram et al, 2018). Some species of corals, seaweeds, seagrasses or sea squirts have also been important targets for studies focusing on genetic divergence and species evolution (Monteiro et al, 2016;Olsen et al, 2004;Pereyra et al, 2013; see also Hudson et al, 2021;Prada & Hellberg, 2021), as have a few species of microalgae and bacteria (Johnson et al, 2006 (Table 1).…”

“…The biggest technical challenge for most systems is the need to produce and rear large mapping families in the laboratory, an issue that is especially pertinent to the study of marine organisms, as previously mentioned. When this cannot be done, genome‐wide association studies (GWAS) may provide an alternative means for inferring the architecture of isolating traits from natural populations (Kess et al., 2021). However, GWAS methods usually require a high‐quality reference genome, resequencing data for many individuals and are based on assumptions that are unlikely to hold in many cases of speciation, such as absence of population structure and high levels of historical recombination.…”

“…Johannesson et al., 2020; Westram et al., 2018) (also, see Section 2.5 ) . Although not very frequent, detailed studies of hybrid zones in marine environments have provided important information about the role of local adaptation in speciation (Kess et al., 2021; Leder et al., 2021; Prada & Hellberg, 2021; Westram et al., 2018), the presence of genetic incompatibilities (Simon et al., 2021) or the coupling between these two types of barriers (Bierne, 2011). Extensive mixing in hybrid zones may also make it possible to identify candidate SNPs or genomic regions underlying reproductive barriers through genome‐wide association tests (Duranton et al., 2020).…”