10,000 years later: body shape and evolution in threespine stickleback

Abstract

Descent with modification (Darwin, 1859) overwhelmingly occurs through the process of natural selection on genetically variable traits. Following deglaciation in the Pleistocene, morphologically conservative marine stickleback (Gasterosteus aculeatus) from two distinct mitochondrial DNA lineages colonized freshwater habitats on the Haida Gwaii archipelago. These freshwater populations have radiated in response to a diverse selective landscape on the archipelago and exhibit morphological diversity that equals or exceeds the known range for the species in the circumboreal distribution. I investigated the body shape of 3808 stickleback from 125 isolated populations from Haida Gwaii using geometric morphometrics. Relative warp and discriminant function analysis were used to quantify lateral shape differences based on partial warp scores. which were generated from twelve homologous landmarks digitally placed on each specimen's image. The possibility of ontogenetic shifts and sexual dimorphism of body shape were examined for each population on the archipelago. Stickleback body-shape changes during ontogeny were highly variable, and cannot be predicted by the volume and water clarity of the habitat. I found a slight sexual dimorphism in adult body shape, the magnitude of which could not be predicted by habitat volume and clarity. A number of comparisons were made to elucidate the possible causes for selection for divergence of adult body shape among Haida Gwaii populations. Body shape of parapatric lake-river stickleback populations differed significantly in concordance with hydrodynamic principles. Comparing the body shape of Haida Gwaii populations to the shape of sympatric benthic-limnetic species pairs from southwestern British Columbia. I found that benthic and limnetic body-shape ecotypes differ by up to 56% of the total variation among Haida Gwaii populations. Tests for phenotypic plasticity of body shape were conducted with two morphologically distinct stickleback populations that had been transplanted into two separate experimental ponds that were the ecological opposites of the respective source lakes. I found evidence for some phenotypic plasticity in body shape; the difference between each source and experimental population was approximately 11% of the total variation in body shape among populations throughout the archipelago. Throughout the islands adult body shape and size can be predicted by both abiotic and biotic factors of the habitat. Populations with derived shape (CV1+), including thicker peduncles, posteriad and closely spaced dorsal spines, anteriad pelvis, short dorsal and anal fins, and smaller body size occur in small, shallow, stained ponds, and populations with less derived shape (CVI-). with smaller narrow peduncles. anteriad and widely spaced dorsal spines. posteriad pelvis. longer dorsal and anal fins, and larger size occur in large, deep. clear lakes. There were large-bodied populations with derived shape (CV2-). including smaller heads and shallower elongate bodies in open water habitats of low productivity, and populations with smaller size and less derived shape (CV2±), with larger heads and deeper bodies, in higher productivity, structurally complex habitats. Populations with robust defensive adaptations have less derived shape (CV1-) and larger size, in response to salmonid predation, while populations with weak defences had derived shape (CV 1+), in response to bird/invertebrate predators. The ecomorphological relationships were consistent between mitochondrial lineages and replicated in each geographical region on the archipelago among geographically distant populations, suggesting the parallel evolution of body shape governed by the hydrodynamic constraints of each habitat. Although initially colonized by ancestors with conserved morphology, the stickleback populations on Haida Gwaii exhibit body shapes suited to the hydrodynamic landscape of the habitat, demonstrating the predictability of natural selection in adaptive radiations.