Admixture between old lineages facilitated contemporary ecological speciation in Lake Constance stickleback

Abstract

Ecological speciation can sometimes rapidly generate reproductively isolated populations coexisting in sympatry, but the origin of genetic variation permitting this is rarely known. We previously explored the genomics of very recent ecological speciation into lake and stream ecotypes in stickleback from Lake Constance. Here, we reconstruct the origin of alleles underlying ecological speciation by combining demographic modelling on genome-wide single nucleotide polymorphisms, phenotypic data and mitochondrial sequence data in the wider European biogeographical context. We find that parallel differentiation between lake and stream ecotypes across replicate lake-stream ecotones resulted from recent secondary contact and admixture between old East and West European lineages. Unexpectedly, West European alleles that introgressed across the hybrid zone at the western end of the lake, were recruited to genomic islands of differentiation between ecotypes at the eastern end of the lake. Our results highlight an overlooked outcome of secondary contact: ecological speciation facilitated by admixture variation.

Phenotypic and genotypic parallel evolution in parapatric ecotypes ofSenecio

“…To characterize the extent of phenotypic and genotypic parallelism within a system, it is necessary to rigorously demonstrate that populations adapting to similar environments (collectively referred to as an ecotype) have arisen multiple times independently. We refer the reader to our previous analyses of parallel evolution in Senecio lautus (Roda et al, 2013b;James et al, 2020) and to systems such as the marine snail, Littorina saxatilis (Quesada et al, 2007;Johannesson et al, 2010;Bierne et al, 2013;Butlin et al, 2014;Pérez-Pereira et al, 2017), and the threespine stickleback, Gasterosteus aculeatus (Colosimo et al, 2005;Chan et al, 2010;Dean et al, 2019;Marques et al, 2019) where one can find some of the strongest evidence for the independent origin of populations, and to the increasing number of potential cases of parallel evolution in plants (Foster et al, 2007;Ostevik et al, 2012;Trucchi et al, 2017;Cai et al, 2019;Konečná et al, 2019;Knotek et al, 2020).…”

Threespine Stickleback in Lake Constance: The Ecology and Genomic Substrate of a Recent Invasion

“…Such comparisons must be made with caution however, as marine populations are also diverging, and can be grouped into several genetically distinct clusters as well (DeFaveri et al, 2012;deFaveri and Merilä, 2014;Fang et al, 2018Fang et al, , 2020aMorris et al, 2018). Furthermore, geographically adjacent marine and freshwater populations and species do not necessarily share the same common ancestor (Dean et al, 2019;Marques et al, 2019a). Within freshwater, ecotypic diversification occurs frequently along a lake-stream axis of divergence and rarely along a benthic-limnetic axis within lakes, where the latter has been found exclusively in coastal sectors of British Columbia, Canada (Bentzen and McPhail, 1984;Schluter and McPhail, 1992;Foster and Bell, 1994;McPhail, 1994;McKinnon and Rundle, 2002;Gow et al, 2008;Willacker et al, 2010;Østbye et al, 2016).…”

Population structure limits parallel evolution

“…The lack of SGV to fuel local adaptation can be mitigated by introgression between divergent clades as this can substantially increase the genetic variation in the affected populations (Anderson 1949;Arnold 1997;Marques et al 2019). This appears to be the case for the Baltic Sea nine-spined stickleback populations which have experienced introgression from divergent western European populations (Feng et al 2020;Shikano et al 2010b;Teacher et al 2011); a comparison of admixed and non-admixed populations revealed the former to have significantly higher heterozygosity than the latter.…”

“…In the case of the threespined stickleback "species pairs", speciation seems to progress rapidly towards completion, but full reproductive isolation is not usually reached (McKinnon & Rundle 2002). In fact, whenever the ecological conditions that drove the evolution of reproductive isolation in the first place cease to exist, hybridization and reverse speciation is known to occur (Marques et al 2019;Rudman & Schluter 2016). Hence, this suggests that strong genetic incompatibilities have not had time to evolve.…”