Repeated and predictable patterns of ecotypic differentiation during a biological invasion: lake-stream divergence in parapatric Swiss stickleback

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 ecologi-
cal 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 differ-
ent 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 trajec-
tories 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 eco-
logical 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.