Environmental stressors induced strong small-scale phenotypic differentiation in a wide-dispersing marine snail

Abstract

Heterogeneous environments pose a particular challenge for organisms because the same phenotype is unlikely to perform best regardless of the types of stress it encounters. The grain size theory predicts that species with high dispersal potential experience a more heterogeneous, fine-grained environment where phenotypic plasticity may evolve to cope with habitat heterogeneity.To understand how species meet this challenge, we investigated the extent to which contrasting selection pressures induced ecological and phenotypic responses in a natural population of a wide-dispersing marine snail.We collected, measured external and internal characters, weighted, and dissected individuals of Heleobia australis (Rissooidea: Cochliopidae) from heterogeneous habitats from the intertidal area of the Bahía Blanca estuary, Argentina. We also conducted molecular analyses by amplifying the COI gene in individuals sampled from each habitat.We found that subpopulations of H. australis, inhabiting close to each other and without physical barriers, exhibited a strong phenotypic differentiation in shell characters and body weight in response to environmental conditions (thermal, saline, and dehydration stress), crab predation, and parasites. We proved that this differentiation occurred even early in life as most of the characters observed in juveniles mirrored those found in adults. We also found a clear variation in penis size in snails collected from each habitat and raised in common garden laboratory conditions. The COI gene analysis confirmed that the individuals studied constituted a single species despite the strong phenotypic difference among subpopulations.The pronounced phenotypic differentiation in H. australis is all the more remarkable because it occurred at a very small geographical scale, which is rarely documented for a wide-dispersing species. Our findings provide a reasonable ground for advocating that H. australis experienced a fine-grained environment and, thus, benefited from the combined effect of directional selection and plasticity to evolve locally adapted phenotypes to contrasting habitat conditions at a local scale.