Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake–stream divergence in parapatricSwiss stickleback

Abstract

The relative importance of ecological selection and geographical isolation in promoting and constraining genetic and phenotypic differentiation among populations is not always obvious. Interacting with divergent selection, restricted opportunity for gene flow may in some cases be as much a cause as a consequence of adaptation, with the latter being a hallmark of ecological speciation. Ecological speciation is well studied in parts of the native range of the three-spined stickleback. Here, we study this process in a recently invaded part of its range. Switzerland was colonized within the past 140 years from at least three different colonization events involving different stickleback lineages. They now occupy diverse habitats, ranging from small streams to the pelagic zone of large lakes. We use replicated systems of parapatric lake and stream populations, some of which trace their origins to different invasive lineages, to ask (i) whether phenotypic divergence occurred among populations inhabiting distinct habitats, (ii) whether trajectories of phenotypic divergence follow predictable parallel patterns and (iii) whether gene flow constrains divergent adaptation or vice versa. We find consistent phenotypic divergence between populations occupying distinct habitats. This involves parallel evolution in several traits with known ecological relevance in independent evolutionary lineages. Adaptive divergence supersedes homogenizing gene flow even at a small spatial scale. We find evidence that adaptive phenotypic divergence places constraints on gene flow over and above that imposed by geographical distance, signalling the early onset of ecological speciation.

Hybrid ‘superswarm’ leads to rapid divergence and establishment of populations during a biological invasion

“…We also found no relationship between genetic differentiation and geographical distance either in combination with the hybrid scenario or by itself. Contrary to previous work performed within Swiss lake systems (Lucek et al 2013), the pattern of genetic population divergence observed here is not likely driven by habitat dependent selection because, although genetically differentiated, many populations occupy similar (e.g., GIP-MOE, both stream habitats), or even the same, habitats (e.g., both RHO-and NEU-like individuals recovered from STS, ALL, GLA, GUP, YVB and YVM). Thus, although parallel habitat based divergence seems evident at a finer, more lake-specific level (Lucek et al 2013), the nature of genetic boundaries between the geographically more inclusive genetic populations identified in the present work is less obvious.…”

“…The approach we used to infer population structure differs from many previous population based stickleback studies, some performed in these systems (Reusch et al 2001;Mäkinen et al 2006;Lucek et al 2010;Lucek et al 2013;Lucek et al 2014a;Lucek et al 2014b). Rather than assigning population status to different sampling sites by default, we used an approach based on individual admixture proportions.…”

“…This could result in Wahlund effects within populations or in signs of recombination or epistatic linkage among loci (Slatkin 2008;Excoffier & Lischer 2010) Constance region (Berner et al 2010;Moser et al 2012;Lucek et al 2013;Lucek et al 2014b) and between Constance region stickleback and those in the upper Rhine (i.e., GIP; Lucek et al …”

“…Following several introductions and the channelization of Swiss waterways (Heller 1870;Fatio 1882;Bertin 1925), stickleback underwent a range expansion and now occupy a wide range of different habitats throughout the country (Berner et al 2010;Lucek et al 2010;Lucek et al 2013;Lucek et al 2014b). The Swiss midlands are characterized by many large lakes linked by a vast network of streams and canals allowing gene flow among different lake systems, which enables adaptation to distinct habitats (e.g., shallow rivers and streams versus deep large lakes; Berner et al 2010;Lucek et al 2010;Lucek et al 2013;Lucek et al 2014b). A mitochondrial DNA survey of samples collected across the country revealed the colonization of Switzerland by three distant genetic stickleback lineages (five mtDNA haplotypes) from different parts of Europe (Lucek et al 2010).…”

Trait dimensionality explains widespread variation in local adaptation

“…Understanding local adaptation is a central goal of evolutionary ecology because of its important role in diversification, conservation and epidemiology [1][2][3][4]. Consequently, a large body of theory has been developed to predict the conditions under which local adaptation is expected to most readily evolve.…”