Crossing extreme habitat boundaries: Jack‐of‐all‐trades facilitates invasion but is eroded by adaptation to a master‐of‐one

Abstract The invasion of new environments can be a key instigator of adaptive diversification, but the likelihood of such invasions succeeding can depend on the attributes of would‐be invaders. Chief among these seems to be a generalist or ‘jack‐of‐all‐trades’ phenotype. Yet, despite the obvious link between habitat transitions and adaptation, we know surprisingly little about how phenotypes that might initially allow taxa to transition between habitats subsequently evolve or influence post‐invasion differentiation. We tested how a generalist phenotype of a broad diet and behavioural plasticity in marine blenny fish has facilitated the repeated invasion of extreme environments—particularly land—and how the conditions post‐invasion have impacted that generalist phenotype and associated trophic morphology. Our data show that a wide diet and plasticity in being able to shift between environments freely have been instrumental in the progressive invasion of land by amphibious blennies. Once established, however, terrestrial blennies have experienced strong stabilizing selection for a restricted diet, little to no plasticity and a highly specialized morphology. Instead of promoting diversification, the invasion of land appears to offer only a limited niche for survival, constraining descendent blennies to a specific adaptive phenotype. While our study supports the view that generalism facilitates invasion and that habitat transitions instigate adaptation, it also shows a generalist strategy is not optimal for successful establishment and new environments may offer fewer (not more) opportunities for diversification. This has broad implications for how taxa might be expected to respond or adapt to abrupt environmental change more generally. A free plain language summary can be found within the Supporting Information of this article.