Site‐specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers

Abstract

The evolution of reproductive isolation in the presence of gene flow is supported by theoretical models but rarely by data. Empirical support might be gained from studies of parallel hybrid zones between interbreeding taxa. We analysed gene flow over two hybrid zones separating ecotypes of Littorina saxatilis to test the expectation that neutral genetic markers will show site-specific differences if barriers have evolved in situ. Distinct ecotypes found in contrasting shore habitats are separated by divergent selection and poor dispersal, but hybrid zones appear between them. Swedish islands formed by postglacial uplift 5000 years ago provide opportunities to assess genetic structure in a recently evolved system. Each island houses a discrete population containing subpopulations of different ecotypes. Hybrid zones between ecotypes may be a product of ecological divergence occurring on each island or a consequence of secondary overlap of ecotypes of allopatric origin that have spread among the islands. We used six microsatellite loci to assess gene flow and genetic profiles of hybrid zones on two islands. We found reduced gene flow over both hybrid zones, indicating the presence of local reproductive barriers between ecotypes. Nevertheless, subpopulations of different ecotypes from the same island were genetically more similar to each other than were subpopulations of the same ecotype from different islands. Moreover, neutral genetic traits separating the two ecotypes across hybrid zones were site-specific. This supports a scenario of in situ origin of ecotypes by ecological divergence and nonallopatric evolution of reproductive barriers.

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).…”

Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation

“…A few, probably introduced, populations are present elsewhere (Italy, South Africa, California). The species forms distinct ecotypes in different microhabitats and gene flow between adjacent ecotypes is strongly (although not completely) impeded with the formation of micro-scale hybrid zones (Johannesson et al 1993(Johannesson et al , 1995aRolán-Alvarez et al 1999;Grahame et al 2006;Panova et al 2006). A most important trait is the lack of migratory (pelagic) larvae resulting in restricted dispersal among populations.…”

“…Estimates of gene flow outside and across hybrid zones using genetic markers show that gene flow over hybrid zones is only 10-30%, or sometimes even less, of gene flow over similar distances within continuous populations of the same ecotype (Rolán-Alvarez et al 1996;Grahame et al 2006;Panova et al 2006;Galindo et al 2009). Both extrinsic and intrinsic effects are likely to contribute to the impeded gene flow.…”

“…The evolution of partially reproductively isolated ecotypes in the seashore periwinkle Littorina saxatilis has been suggested as an example of parallel evolution of reproductive isolation/incipient speciation Panova et al 2006;Quesada et al 2007;Schluter 2009) showing circumstantial evidence for strong ecological separation being the main factor behind the evolution of reproductive barriers. Nevertheless, it has been suggested that these barriers may, at least in part, be due to genetic differences accumulated during an earlier period of allopatric separation (Grahame et al 2006;Butlin et al 2008).…”

Phylogeographic analysis reveals a deep lineage split within North Atlantic Littorina saxatilis

“…on the scale of metres) habitatspecific morphological differentiation driven primarily by variation in crab predation and wave exposure [15,17,18]. In each location, pairs of divergent ecotypes display distinct morphologies (E & S, Sweden [19]; RB & SU, Spain [20]; H & M, Britain [21]), partial reduction of gene flow [22][23][24][25] and evidence of reproductive isolation [21,26,27], providing support for multiple independent divergence events and suggesting L. saxatilis as a model of incipient sympatric speciation [17,18,26,28]. Yet, despite its importance as one of the few marine examples of incipient sympatric speciation [29], the necessity of lineage-wide phylogenetic context for model systems of sympatric speciation [30,31] and the established role of historical allopatric divergence in North Atlantic marine species [3,4], little is known about the evolutionary history of L. saxatilis across its trans-Atlantic range.…”