Trait evolution linked to climatic shifts contributes to adaptive divergence in an alpine carnation (Dianthus sylvestris)

Populations expanding to new habitats may encounter novel selection regimes which can lead to ecotype formation. In the Alps, elevation corresponds to steep ecological gradients, along which ecotype formation has occurred in many species. The majority of alpine plant species are perennial and little is known about how selection acts across different stages of their life-cycles and how fitness trade-offs shape adaptive processes in perennials. We investigated how selection at opposite ends of elevational gradients has driven ecotype formation in Dianthus sylvestris, a perennial herb that expanded its ecological niche to low elevation habitats after the Last Glacial Maximum. Through a multi-year reciprocal transplant experiment including parental populations and recombinant crosses we assessed fitness under natural conditions and dissect how adaptation is mediated by different fitness components with inherent trade-offs, and pinpoint the contribution of growth and reproductive traits to this process. We show that the evolution of local adaptation proceeded by selection acting primarily through reproduction and survival at low and high elevation, respectively. At low elevation the primary contribution to adaptation was third year reproduction, concomitant with a left skewed age distribution. At high elevation the contribution to adaptation and the age distribution were more dispersed across the life cycle. We found that large, early flowering plants have a consistent fitness advantage. This was mediated by direct selection favoring large size through reproductive output at low elevation, and early flowering through the probability to produce seeds at high elevation. Our results indicate that the selection regime imposed by the warm low elevation habitat led to the evolution of an ecotype exhibiting a life-history strategy characterized by high investment in rapid growth and early reproduction. In contrast, the high elevation strategy favors high investment in self-maintenance. Our results suggest that weakening of a key fitness trade-off associated with resource allocation contributed to the evolution of distinct ecotypes in this perennial plant species.