Do the same genes underlie parallel phenotypic divergence in different Littorina saxatilis populations?

Abstract

Parallel patterns of adaptive divergence and speciation are cited as powerful evidence for the role of selection driving these processes. However, it is often not clear whether parallel phenotypic divergence is underlain by parallel genetic changes. Here, we asked about the genetic basis of parallel divergence in the marine snail Littorina saxatilis, which has repeatedly evolved coexisting ecotypes adapted to either crab predation or wave action. We sequenced the transcriptome of snails of both ecotypes from three distant geographical locations (Spain, Sweden and United Kingdom) and mapped the reads to the L. saxatilis reference genome. We identified genomic regions potentially under divergent selection between ecotypes within each country, using an outlier approach based on FST values calculated per locus. In line with previous studies indicating that gene reuse is generally common, we expected to find extensive sharing of outlier loci due to recent shared ancestry and gene flow between at least two of the locations in our study system. Contrary to our expectations, we found that most outliers were country specific, suggesting that much of the genetic basis of divergence is not shared among locations. However, we did find that more outliers were shared than expected by chance and that differentiation of shared outliers is often generated by the same SNPs. We discuss two mechanisms potentially explaining the limited amount of sharing we observed. First, a polygenic basis of divergent traits might allow for multiple distinct molecular mechanisms generating the same phenotypic patterns. Second, additional, location-specific axes of selection that we did not focus on in this study may produce distinct patterns of genetic divergence within each site.

What can be learnt from a snail?

“…Sequencing was in this study targeting the coding part of the genome (the transcriptome), and the results showed that overall sharing was similar and unexpectedly low (although higher than expected by chance), with most outlier loci being unique to populations from one country (Westram et al. ). Overall, 5–20% of all outlier loci were shared between any two countries and only very few (<6) loci were shared among all three countries, out of a total of ~7000 loci.…”

“…; Westram et al. ). This, perhaps, corroborate the suggestion that the size dimorphism caused by divergent natural selection is after all the most crucial component to the strength of the reproductive barrier.…”

“…If so, this would allow for idiosyncratic patterns of genetic divergence in each local population (Westram et al. ).…”

Heritable gene expression differences between lake and stream stickleback include both parallel and antiparallel components

“…In particular, these studies have usually examined gene expression in wild-caught individuals (see, for example, Galindo et al , 2010; Manousaki et al , 2013; Westram et al , 2014) that will include an unknown combination of plastic and gene sequence effects on gene expression. Plasticity in such situations can either promote or constrain adaptive divergence (Pfennig et al , 2010; Moczek et al , 2011; Fitzpatrick, 2012; Ghalambor et al , 2015; Oke et al , 2016); but, importantly, plastic expression changes are not encoded by sequence changes, and therefore cannot be used to predict evolutionary trajectories.…”

Mild osmotic stress in intertidal gastropods Littorina saxatilis and Littorina obtusata (Mollusca: Caenogastropoda): a proteomic analysis

“…During the last decades, Littorina species have become model organisms for the study of population biology, physiological adaptations, genetics, behavior, and parasitology (Johannesson et al, 1997;Sokolova et al 2000, Sokolova andPörtner 2001a,b;Panova and Johannesson, 2004;Panova et al, 2006;Quesada et al, 2007;Mikhailova et al, 2009;Conde-Padín et al 2009Galindo et al, 2010;Storey et al 2013;Lobov et al, 2015;Rolan-Alvarez et al, 2015;Maltseva et al, 2016;Westram et al, 2014;Ravinet et al, 2016, Granovitch, 2016. Along the North Atlantic shore, Littorina saxatilis (Olivi, 1872) and L. obtusata (Linnaeus, 1758) are most common (Reid, 1996).…”