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

Abstract

Distinct ecotypes of the snail Littorina saxatilis, each linked to a specific shore microhabitat, form a mosaic-like pattern with narrow hybrid zones in between, over which gene flow is 10 -30% of within-ecotype gene flow. Multi-locus comparisons cluster populations by geographic affinity independent of ecotype, while loci under selection group populations by ecotype. The repeated occurrence of partially reproductively isolated ecotypes and the conflicting patterns in neutral and selected genes can either be explained by separation in allopatry followed by secondary overlap and extensive introgression that homogenizes neutral differences evolved under allopatry, or by repeated evolution in parapatry, or in sympatry, with the same ecotypes appearing in each local site. Data from Spain, the UK and Sweden give stronger support for a non-allopatric model of ecotype formation than for an allopatric model. Several different non-allopatric mechanisms can, however, explain the repeated evolution of the ecotypes: (i) parallel evolution by new mutations in different populations; (ii) evolution from standing genetic variation; and (iii) evolution in concert with rapid spread of new positive mutations among populations inhabiting similar environments. These models make different predictions that can be tested using comprehensive phylogenetic information combined with candidate loci sequencing.

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

“…One potential origin of such variation, as suggested in this study and in Johannesson et al (2010), is ecotype evolution in concert, that is, new positively selected alleles directly sweep to high frequency in a specific habitat (ecotype) over large parts of a species' distribution. This explanation is similar to the 'transporter mechanism', as suggested by Schluter and Conte (2009), in which selection in one habitat repeatedly acts on standing genetic variation that is maintained in another habitat by export of alleles adaptive to the first habitat from elsewhere in the range.…”

“…(4) Locally adapted characters could have evolved in a concerted fashion; that is, the alleles responsible for trait differences have each arisen once and thereafter they have spread by spatial selective sweeps to similar microhabitats in other locations. This idea assumes that gene flow among ecotypes is high enough to allow the spread of advantageous alleles at a rate that at least overrides the rate by which these alleles would have arisen by repeated new mutations in each local site (for a similar mechanism explaining the collective evolution of species, see Rieseberg and Burke, 2001;Morjan and Rieseberg, 2004;Johannesson et al, 2010).…”

“…Ecotype-specific selective sweep Four alternative (not mutually exclusive) genetic mechanisms have been suggested for the repeated evolution of phenotypic traits ('parallel evolution') in pairs of contrasting ecotypes (see Johannesson et al, 2010). (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).…”

“…The genetic mechanisms behind this process are in many cases unclear but possible scenarios (reviewed in Johannesson et al, 2010) include: (1) parallel evolution, that is, the independent evolution of homologous loci that fulfil the same function in two or more lineages (Wood et al, 2005), (2) secondary contact after an initial allopatric divergence (Wilding et al, 2001), (3) evolution from standing genetic variation (Campbell and Bernatchez, 2004;Schluter et al, 2004;Barrett and Schluter, 2008) and (4) evolution in concert where positively selected alleles, directly after their appearance, spread among demographically independent populations by migration (Rieseberg and Burke, 2001;Morjan and Rieseberg, 2004;Johannesson et al, 2010). Distinguishing between these scenarios is possible but requires the detailed and joint analyses of both neutral and selected loci (Johannesson et al, 2010). An increasingly popular approach to identify loci under selection is to look for outliers in genome scans (see Nosil et al, 2009 for a review).…”

Seascape genetics of Indo-Pacific reef organisms: methodologies and case studies for an emerging discipline

“…On a small spatial scale (tens of meters), several recent studies have highlighted strong genetic discontinuities between adjacent populations segregating by intertidal height (periwinkles: Johannesson et al 2010) or by depth (gorgonians: Mokhtar--Jamai et al 2010 andPrada et al 2008; bird's nest coral: Bongaerts et al 2010). In addition to the caveats about correlation mentioned above, even if genotype--by--environment fitness differences can be demonstrated (as in Bongaerts et al 2011), it will be important to consider whether endogenous reproductive incompatibilities also maintain genetic divergence, with multiple loci segregating with environmental features indicative of such a situation.…”