Pronounced phenotypic differentiation in a wide-dispersing marine snail in response to contrasting selection pressures at a local scale

Abstract

Heterogeneous environments pose a particular challenge for organisms because the same phenotype is unlikely to perform best regardless of the variety of encountered stressors. To understand how species meet this challenge, we investigated the extent to which contrasting environmental pressures induced ecological and phenotypic responses in a natural population of a wide-dispersing marine snail at a small spatial scale. We analyzed several traits of Heleobia australis (Rissooidea: Cochliopidae) collected from heterogeneous, but highly connected, habitats from the intertidal area of the Bahia Blanca estuary, Argentina. We also conducted molecular analyses by amplifying the COI gene in individuals sampled from each habitat. We found that sympatric subpopulations of H. australis exhibited a strong phenotypic divergence in shell characters and body weight in response to thermal, saline, and dehydration stress, crab predation risk, and parasitic castrators. 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 divergence in penis size in snails collected from each habitat and raised in common garden laboratory conditions. The molecular analyses confirmed that the individuals studied constituted a single species despite the strong phenotypic differences among subpopulations. The small-scale phenotypic differentiation suggests that H. australis experienced a fine-grained environment where conditions imposed by different sources of stress favored the expression of beneficial traits. We discuss the role of plasticity in shaping adaptive phenotypic responses that increase the likelihood of persistence of subpopulations facing environmental stress conditions.