Contemporary ecotypic divergence during a recent range expansion was facilitated by adaptive introgression

Abstract

Although rapid phenotypic evolution during range expansion associated with colonization of contrasting habitats has been documented in several taxa, the evolutionary mechanisms that underlie such phenotypic divergence have less often been investigated. A strong candidate for rapid ecotype formation within an invaded range is the three-spine stickleback in the Lake Geneva region of central Europe. Since its introduction only about 140 years ago, it has undergone a significant expansion of its range and its niche, now forming phenotypically differentiated parapatric ecotypes that occupy either the pelagic zone of the large lake or small inlet streams, respectively. By comparing museum collections from different times with contemporary population samples, we here reconstruct the evolution of parapatric phenotypic divergence through time. Using genetic data from modern samples, we infer the underlying invasion history. We find that parapatric habitat-dependent phenotypic divergence between the lake and stream was already present in the first half of the twentieth century, but the magnitude of differentiation increased through time, particularly in antipredator defence traits. This suggests that divergent selection between the habitats occurred and was stable through much of the time since colonization. Recently, increased phenotypic differentiation in antipredator defence traits likely results from habitat-dependent selection on alleles that arrived through introgression from a distantly related lineage from outside the Lake Geneva region. This illustrates how hybridization can quickly promote phenotypic divergence in a system where adaptation from standing genetic variation was constrained.

Cryptic invasion drives phenotypic changes in central European threespine stickleback

“…The data overlaps with the following studies a Lucek et al (2010) b Lucek et al (2014a) c Lucek and Seehausen (2015) d Lucek et al (2014b) Conserv Genet (2016) 17:993-999 997…”

“…Introgression at a phenotype-linked marker may nevertheless occur if the phenotype experiences positive selection (Rieseberg 2011). This has been suggested to be the case for Eda in some stickleback populations within their invaded range in Switzerland (Lucek et al 2014a). Indeed, lateral plate number and Eda itself can be under selection (Barrett 2010;Leinonen et al 2011;Zeller et al 2012).…”

Hybridization as a facilitator of species range expansion

“…In some cases, the spatio-temporal dynamics of a range expansion can provide evidence of whether hybridization contributes to range expansion (sensu [53,80]). Specifically, if a range expansion can be observed directly by comparing contemporary populations to historical populations (e.g.…”

“…Specifically, if a range expansion can be observed directly by comparing contemporary populations to historical populations (e.g. using museum specimens), then it could be possible to observe evolutionary shifts in: key functional traits (or their proxies) that confer adaptation; underlying genetic markers linked to those traits and frequency and biogeographic patterns of hybridization that are concordant with a range expansion (sensu [53,80]). As the impacts of invasive species and global change become more evident, such data might be obtainable [81,82].…”

Does eutrophication-driven evolution change aquatic ecosystems?

“…For example, invasive species that established themselves during eutrophication may continue to retain a foothold for some time after nutrient recovery, affecting the functioning of the ecosystem. To make it more complicated, these invasive species may themselves have evolved in response to the changes in the environment they invaded [42].…”