Replicated evolutionary inhibition of a complex ancestral behaviour in an adaptive radiation

Adaptive radiations often exhibit high levels of phenotypic replication, a phenomenon that can be explained by selection on standing variation in repeatedly divergent environments or by the influence of ancestral plasticity on selection in divergent environments. Here, we offer the first evidence that plastic loss of expression of a complex display in a novel environment, followed by selection against expression, could lead to replicated evolutionary inhibition of the phenotype. In both ancestral (oceanic) and benthic (freshwater) populations of the threespine stickleback fish, cannibalism is common and males defending nests respond to approaching groups with a complex diversionary display. This display is not exhibited by males in allopatric, limnetic (freshwater) populations from which cannibalistic groups are absent. Laboratory-reared males from three limnetic populations exhibit a reduced tendency to respond to cannibalistic foraging groups relative to laboratory-reared ancestral and benthic males, but still are capable of producing a similar array of forms of the display despite many generations of disuse. Thus, replication in adaptive radiations can reflect reduced expression of an ancestral trait followed by evolutionary inhibition while the population retains the capacity to express the trait under extreme ancestral conditions.