Nonallopatric and parallel origin of local reproductive barriers between two snail ecotypes

Abstract

Theory suggests that speciation is possible without physical isolation of populations (hereafter, nonallopatric speciation), but recent nonallopatric models need the support of irrefutable empirical examples. We collected snails (Littorina saxatilis) from three areas on the NW coast of Spain to investigate the population genetic structure of two ecotypes. Earlier studies suggest that these ecotypes may represent incipient species: a large, thick-shelled 'RB' ecotype living among the barnacles in the upper intertidal zone and a small, thin-shelled 'SU' ecotype living among the mussels in the lower intertidal zone only 10-30 m away. The two ecotypes overlap and hybridize in a midshore zone only 1-3 m wide. Three different types of molecular markers [allozymes, mitochondrial DNA (mtDNA) and microsatellites] consistently indicated partial reproductive isolation between the RB and the SU ecotypes at a particular site. However, each ecotype was related more closely to the other ecotype from the same site than to the same ecotype from another site further along the Galician coast (25-77 km away). These findings supported earlier results based solely on allozyme variation and we could now reject the possibility that selection produced these patterns. The patterns of genetic variation supported a nonallopatric model in which the ecotypes are formed independently at each site by parallel evolution and where the reproductive barriers are a byproduct of divergent selection for body size. We argue that neither our laboratory hybridization experiments nor our molecular data are compatible with a model based on allopatric ecotype formation, secondary overlap and introgression.

Intron sequences of arginine kinase in an intertidal snail suggest an ecotype-specific selective sweep and a gene duplication

“…(1) The mutation responsible for the local adaptation could be due to parallel evolution in the strict sense; that is, independent mutations controlling the locally adapted traits could have arisen and been driven to fixation in different geographic locations (Rolan-Alvarez et al, 2004;Panova et al, 2006;Quesada et al, 2007;Galindo et al, 2009). (2) The ecotypes could initially have evolved allopatrically and the current sympatric or parapatric distribution could be the result of secondary contact and introgression (Wilding et al, 2001).…”

Adaptation to a Steep Environmental Gradient and an Associated Barrier to Gene Exchange in Littorina Saxatilis

“…Schilthuizen (2000) suggested that ecotones may be "speciation-prone" -that adaptation to habitat across a pronounced environmental gradient may lead to the evolution of assortative mating, and to parapatric speciation. We consider it premature to claim the Littorina saxatilis clines described here, or in Galicia (Rolán-Alvarez et al 2004) as examples of 'incipient' non-allopatric speciation for several reasons. Our data are consistent with models of introgression following secondary contact.…”

“…On the coast of Galicia, Spain, L. saxatilis is described as being in a state of incipient speciation (Rolán-Alvarez et al 2004), which, it is argued, is proceeding independently on several shores -thus leading the authors to refer to parallel instances of sympatric speciation. In Galicia, the morphotypes look quite unlike H and M, or E and S. The upper shore form (RB, ridged and banded) (Johannesson et al 1993) is a relatively large animal with a sculptured shell, both features which assist in resisting crab predation (Johannesson and Tatarenkov 1997).…”

Insights into the role of differential gene expression on the ecological adaptation of the snail Littorina saxatilis

“…Therefore, here we will use the cDNA-AFLP technique and qPCR to compare the expression profiles between two ecotypes of Littorina saxatilis involved in an incomplete sympatric ecological speciation process [43-45], in order to provide insights into the role of differential gene expression on ecological adaptation.…”