Rapid intralacustrine evolution of an invasive pelagic three-spined stickleback (Gasterosteus aculeatus) ecotype in Lake Constance

Abstract

The rapid invasion of the pelagic zone in Lake Constance by three-spined sticklebacks (Gasterosteus aculeatus) since 2012 and their subsequent drastic population growth has had stark ecosystem-wide effects, such as food-web shifts and declines in native biodiversity, including commercially important fish species. Yet, the origin of this invasive pelagic ecotype remains unclear. This study aims to determine if the pelagic ecotype arose in situ from the existing littoral population or following external colonisation, identify potential phenotypic differences between individuals from different habitats, and assess genomic signals of selection. Integrating RAD-sequencing of Lake Constance individuals and whole-genome sequence data for European outgroup populations, this study shows that the pelagic Lake Constance population likely arose recently within the lake from the littoral population, with only weak genome-wide differentiation between individuals from different habitats. This is further supported by minimal differences in meristic and morphometric traits, with shape differences only found between pelagic/inflow sticklebacks and littoral sticklebacks. Using genome scans, we identified multiple outlier loci between littoral and pelagic ecotypes across the genome, potentially suggesting early signs of sympatric speciation despite high connectivity. Furthermore, increased differentiation between pelagic and littoral sticklebacks for body shape-associated loci and the overlap of outlier loci with quantitative trait loci for ecologically relevant traits points toward a driving role of selection in this pelagic invasion. This study provides an important example of rapid ecological diversification from standing genetic variation and a rare case of littoral-pelagic ecotype divergence under high gene flow in a large oligotrophic lake. Ultimately, the results of this study will have major implications for the management of the invasive pelagic ecotype, and the entire stickleback population as a whole.

Escaping malnutrition by shifting habitats: A driver of three‐spined stickleback invasion in Lake Constance

“…However, given that all sticklebacks spawn in the same shallow waters of ULC (Gugele et al, 2020), the mechanism of separation (e.g., mate choice) is not known at this stage. Nevertheless, our results together with the genetic evidence by Dahms et al (2022) point to a rare case of littoral‐pelagic ecotype divergence, with food selectivity as an important factor.…”

“…Therefore, the hypothesis arose that a benthic‐pelagic species pair in ULC with reduced genetic exchange in this system exists (cf. Dahms et al, 2022). Our data support this hypothesis, highlighting differences in the diets and fatty acid profiles of littoral and pelagic groups.…”

“…Genetic studies by Dahms et al (2022) identified multiple outlier loci between littoral and pelagic ecotypes across the genome, which may be early signs of sympatric speciation. Therefore, the hypothesis arose that a benthic‐pelagic species pair in ULC with reduced genetic exchange in this system exists (cf.…”

“…Although the two populations of stickleback remain morphometrically and genetically very similar, and the pelagic type remains associated with the littoral zone for purposes of breeding, they already show early signs of sympatric speciation (Dahms et al, 2022). In May and June they build nests in shallow areas, spawn, and guard their young alongside the littoral type (Gugele et al, 2020), but from July to April they expand into pelagic habitats.…”

Small but voracious: invasive generalist consumes more zooplankton in winter than native planktivore

“…during whitefish larvae stocking (Roch et al 2018). Due to rapid evolution, sticklebacks may now diverge into groups occupying littoral, pelagic or profundal habitats (Hudson et al 2021), albeit, up to now only subtle genetic differences between individuals occupying different habitats were observed (Dahms et al 2022). Our study showed that the pelagic sticklebacks have already specialised in feeding on zooplankton.…”