Uncovering the evolution of elevational ecotypes in Alpine carnations

Abstract

Divergent selection pressures imposed by contrasting environmental conditions at opposite ends of environmental gradients can drive the evolution of populations that are adapted to local conditions. Elevational gradients in the Alps coincide with steep climatic gradients where plant populations experience divergent selection within a limited geographic scale. This feature makes alpine plants with a broad elevational range ideal for the study of evolution of local adaptation. In this thesis, we aimed to unravel the evolution of distinct locally adapted ecotypes of alpine carnations (Dianthus spp., Caryophyllaceae) in response to climate driven selection imposed by contrasting elevational habitats. As a study system, we used two perennial systems with an elevational distribution ranging from the colline to alpine belts in central Europe, D. carthusianorum and D. sylvestris. We used populations from low and high elevation growing in long-term reciprocal transplant experiments to study the evolutionary processes underlying ecotype formation by investigating performance across multiple fitness components and life stages of the perennial life cycle. Experiments for D. sylvestris were further combined with phenotypic selection analyses and a genome-wide association study based on a transplant of recombinant F2 crosses, which were used to examine the both contribution of divergent traits to adaptation and the fitness effect of alleles underlying these traits. In chapter I, we first tested for local adaptation in D. carthusianorum by using data on performance in individual fitness components measured over a period of three years in the reciprocal transplant experiment. We found evidence of genotype by environment (GxE) interactions and fitness advantages of the local ecotype, though with extensive variation at different stages of the life cycle. We thus performed a complementary seedling recruitment experiment and integrated fitness over the course of the experiment through matrix population models. Population growth rates showed a strong signal of local adaptation in both elevational environments and further provided evidence of alternate life-history traits as determinants of plant fitness. The low elevation environment caused the local plants to express a faster life cycle characterized by high investment in early reproduction. Contrarily, fitness of the local plants in the high elevation ecotype was driven primarily by survival. The high elevation plants also reproduced more in the foreign environment, which caused them to exceed their physiological limit of resource allocation to reproduction and suffer a cost in terms of reduced post reproductive survival. Chapter I shows how selection imposed at the extremes of an elevational gradient drove ecotype formation in a perennial plant, highlighting the influence of trade-offs and phenotypic plasticity of life history traits as determinants of population performance under different environmental conditions. In chapter II, we explored how selection acting through different fitness components of the perennial life cycle has driven ecotype formation in D. sylvestris, and we dissected the contribution of divergent traits to this process. Populations of D. sylvestris persisted in high elevation refugia during the Last Glacial Maximum and have subsequently colonized low elevation habitats. We combined phenotypic and fitness data collected in a reciprocal transplant experiment over five years with phenotypic selection analyses on F2 crosses to unravel the contributions of adaptive traits to the responses to the contrasting environmental conditions and associated selection regimes. Our results revealed a strong genetic basis for plant size, plant height and flowering time, associated with elevational adaptation. The high elevation environment favored a conservative life history strategy characterized by a long life span and limited investment in reproduction. Consistently, selection acted towards early flowering to ensure completion of the reproductive cycle in the short alpine summer season. In contrast, the warmer low elevation environment favored a life history strategy characterized by high investment in early reproduction at the expense of a shorter life cycle, and thus plants achieving large size and maximized fecundity. Our results show that colonization of the warmer low elevation habitats proceeded through a shift in both phenotypic and life history traits linked to resource allocation in a high-energy environment with a longer reproductive season. In chapter III, we leveraged results from chapter II to uncover the fitness effect of alleles underlying the traits that contributed to the adaptive divergence between the low and high elevation populations of D. sylvestris. We performed genome-wide association analyses and identified a polygenic genetic architecture underlying the studied adaptive traits. We found examples of both antagonistic pleiotropy and conditional neutrality describing the fitness effects of allelic variation at these loci. By dissecting separate fitness components, we revealed that alleles underlying successful reproduction at high elevation had a negative effect on fecundity, while this relationship turned positive at low elevation. These results suggest that the trade-off in resource allocation indicated in chapter II is accompanied by congruent signals at the level of the underlying genetic variants.