Adaptive Divergence and the Balance Between Selection and Gene Flow: Lake and Stream Stickleback in the Misty System

Abstract

Abstract. We investigated the interplay between natural selection and gene flow in the adaptive divergence of threespine stickleback (Gasterosteus aculeatus) that reside parapatrically in lakes and streams. Within the Misty Lake system (Vancouver Island, British Columbia), stickleback from the inlet stream (flowing into the lake) have fewer gill rakers and deeper bodies than stickleback from the lake-differences thought to facilitate foraging (benthic macroinvertebrates in the stream vs. zooplankton in the open water of the lake). Common-garden experiments demonstrated that these differences have a genetic basis. Reciprocal transplant enclosure experiments showed that lake and inlet stickleback grow best in their home environments (although differences were subtle and often not significant). Release-recapture experiments in the inlet showed that lake fish are less well-suited than inlet fish for life in the stream (higher mortality or emigration in lake fish). Morphological divergence in the wild and under common rearing was greater between the lake and the inlet than between the lake and the outlet. Genetic divergence (mitochondrial DNA and microsatellites) was greatest between the lake and the upper inlet (1.8 km upstream from the lake), intermediate between the lake and the lower inlet (0.9 km upstream), and least between the lake and the outlet stream (1.2 km downstream). Relative levels of gene flow estimated from genetic data showed the inverse pattern. The negative association between morphological divergence and gene flow is consistent with the expectation that gene flow can constrain adaptation. Estimated absolute levels of gene flow also implied a constraint on adaptation in the outlet but not the inlet. Our results suggest that natural selection promotes the adaptive divergence of lake and stream stickleback, but that the magnitude of divergence can be constrained by gene flow.

Fine-scale local adaptation in an invasive freshwater fish has evolved in contemporary time

“…Indeed, similar environments often yield more similar patterns of ecological selection [3]. This pattern is consistent with other taxa where the degree of adaptive divergence scales with differences in ecological conditions and strength of divergent selection [51,52]. An additional (but not mutually exclusive) explanation is that the homogenizing effect of gene flow between the Rennies and Waterford locations may result in similar survival responses to similar conditions.…”

Shared and unique morphological responses of stream fishes to anthropogenic habitat alteration

“…Within basins, any known physical barrier that would hinder gene flow was not present between reservoir and stream populations. High rates of gene flow between reservoir and stream habitats should degrade morphological differences between habitats, if selective pressures are not strong enough to maintain trait divergences [21,47]. The relatively high morphological divergence here suggests either plasticity plays a large component in phenotypic variation or gene flow is not high enough to degrade differences in body shape between habitat types.…”

“…Indeed, intraspecific body shape variation investigated in reservoirs and nearby streams corroborated this pattern [13,14]. Yet, these relationships are not ubiquitous as some fishes can exhibit the opposite pattern: more streamlined body shapes in lentic (natural lakes) habitats compared with streams [21][22][23]. Therefore, species' ecologies and their evolutionary histories will likely regulate how traits respond to selective pressures.…”

Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions

“…It may be that differences in predation regimes [18,26], or other biological and physical factors beyond the benthic -limnetic ecological contrast typically invoked [22,23], are required to drive divergence to the level observed in these Haida Gwaii populations. Or perhaps, the particular haplotypes under selection are restricted to this geographical area.…”