Historical Biogeography of the Marine Snail Littorina saxatilis Inferred from Haplotype and Shell Morphology Evolution in NW Spain

Abstract

The marine snail Littorina saxatilis exhibits extreme morphological variation between and within geographical regions and represents an excellent model for assessing local adaptation. Previous studies support the hypothesis of parallel evolution in sympatry of two morphologically different ecotypes (named as RB and SU) that co-inhabit different habitats from Galician rocky shores (NW Spain), and which are interrupted by sheltered areas inhabited by a different morph never studied before (named as SRB). Here, we use morphological and mitochondrial DNA (mtDNA) sequence data to test hypotheses on the origin and diversification of SRB snails and to assess their evolutionary relationships with RB and SU ecotypes. Our results show that the SRB morph displays the largest size and shell elongation and the smallest relative shell aperture, representing an extreme type of the RB vs. SU polymorphism, which has been linked to adaptation to sheltered ecological factors. Phylogenetic analysis shows that the SRB morph shares ancestry with RB and SU ecotypes, rejecting the hypothesis that the SRB morph marks relict populations from which these ecotypes evolved in Galician coasts. Our data support that genetic differentiation among SRB, RB and SU morphs results from a general pattern of restricted gene flow and isolation by distance linked to the colonization of Galician coasts by two independent mtDNA lineages, rather than from a random fragmentation of the initial distributional range. Therefore, the confinement of distinct lineages to specific geographical areas denote evident limits to the distances these snails can disperse. Morphological analysis indicates no association between mtDNA lineage and a specific morphotype, and suggests the independent gain of convergent morphological patterns within each mtDNA lineage in populations occupying contrasting habitats following the colonization of Galician coasts.

Whole-genome phylogeography of the intertidal snail Littorina saxatilis

“…2). This is in agreement with another previously described genetic discontinuity around Burela (Quesada et al, 2007;Doellman et al, 2011;Tirado et al, 2016). Further sampling in southern France and the north of the Iberian Peninsula may help refine the geographic location of these discontinuities and test for potential contact between these lineages.…”

Genomic divergence between Spanish Littorina saxatilis ecotypes unravels limited admixture and extensive parallelism associated with population history

“…Our phylogenetic and genetic differentiation analyses of neutral loci suggest a large degree of genetic independence of ecotypes in each site. Repeated observation of mitochondrial phylogenies that cluster by sampling site rather than ecotype, including between southern sites (Quesada et al., ; Tirado et al., ), and support for independent ecotype origin between northern and southern sites using demographic modeling (Butlin et al., ), together provide strong evidence for local emergence of ecotype pairs. Although this scenario cannot be completely rejected between southern sites, the observation of separate neutral SNP phylogenies in the present study and the occurrence of high between‐ecotype levels of divergence that nearly match levels of distance driven isolation provide evidence against ongoing gene flow between ecotypes eroding historical patterns of divergence.…”

“…Our phylogenetic and genetic differentiation analyses of neutral loci suggest a large degree of genetic independence of ecotypes in each site. Repeated observation of mitochondrial phylogenies that cluster by sampling site rather than ecotype, including between southern sites (Quesada et al, 2007;Tirado et al, 2016), and support for independent ecotype origin between northern and southern sites using demographic modeling , together provide strong evidence for local emergence of ecotype pairs.…”

“…Samples were obtained from three sites across the known distribution of crab and wave L. saxatilis ecotypes in NW Spain, depicted in Figure a: Silleiro (Long – 8.90°, Lat 42.13°), Corrubedo (Long – 9.10°, Lat 42.60°), and Burela (Long – 7.36°, Lat 43.67°). These three sites allow comparison of population genetic structure and genomic divergence between ecotypes from two separate postglacial colonizations, as recent evidence suggests Burela and Silleiro have been colonized from distinct northern and southern refugia (Butlin et al., ; Tirado, Saura, Rolán‐Alvarez, & Quesada, ).…”

Population genomics of parallel evolution in gene expression and gene sequence during ecological adaptation

“…Here we combine genome-wide evolutionary analyses of coding sequences and gene expression data using microarrays for investigating the molecular basis of adaptive divergence, employing L. saxatilis ecotypes from NW Spain as a model system. In this region, a large “crab ecotype” and a smaller “wave ecotype” have evolved repeatedly in response to crab predation and wave exposure respectively 33 , 35 , 40 , 55 . The recent origin of these ecotypes (<10,000 years) 35 is expected to be associated with high levels of shared genetic constraints and standing variation that would facilitate a rapid and more pervasive repeated evolution.…”