The genetic and ecological basis of diversification

Abstract

Adaptive radiation is a fundamental driver in the creation of biodiversity, but the processes underlying radiations across broad spatial scales need to be further explored. Organisms that colonize a heterogeneous landscape can occupy a mosaic of environments, exposing them to complex patterns of genetic drift, natural selection and gene flow creating adaptive divergence at different levels of biological organization. Strong differences in natural selection and reduced migration between populations favours the evolution of ecotypes, which can provide the basis for species diversification when reproductive isolation arises between contrasting ecotypes. Identifying how ecological divergence can lead to the evolution of different forms of reproductive isolation and promote species diversification can reveal how adaptive radiation proceeds. Empirical studies linking patterns of adaptive divergence with phenotypic diversification, and the underlying genetic basis, are rare across expansive landscapes. As a consequence, there exists a gap in our understanding of how diversification proceeds during adaptive radiation across heterogeneous landscapes. Research for my dissertation used a combination of extensive reciprocal transplant experiments, field sampling, common garden experiments and quantitative genetic crossing designs to investigate how the ecotypic diversification of an Australian native wildflower species complex, Senecio lautus, has occurred across a heterogeneous landscape. I focussed on four contrasting ecotypes that occupy coastal sand dunes, rocky headlands, dry sclerophyll woodland and moist tableland rainforest. Multiple populations per ecotype, and their hybrids were reciprocally transplanted into the four environments to identify patterns of adaptation both within and between ecotypes. Each population was phenotyped in the glasshouse and environmental variables were recorded in the field to associated phenotype, environment and fitness across a heterogeneous landscape. Crossing designs and extensive phenotyping in glasshouse experiments were used to estimate the additive genetic variance underlying morphological traits and identify whether genetic correlations have constrained adaptation. Finally, artificial hybridization was used to identify whether genetic incompatibilities have created intrinsic reproductive isolation. My results showed that strong patterns of local adaptation were present between ecotypes, but weaker patterns within ecotypes. Populations exhibited trade-offs in performance when planted into foreign environments, which emerged as ontogeny progressed and natural selection acted against foreign populations. The environment played an important role in determining patterns of adaptation, with ecotypes derived from more disparate environments performing more poorly. Suites of phenotypic traits were associated with fitness and exhibited trade-offs between contrasting environments. As a consequence of adaptive divergence, multivariate phenotypic divergence has occurred along two major axes of differentiation, created by differences in plant shape/size in one direction and leaf shape in the opposite direction. Similarly, divergence in genetic variance occurred in plant size/shape traits and aligned with the divergence in phenotypic mean. Finally, given dramatic phenotypic diversification and strong patterns of adaptation, hybridization showed that negative epistasis created genetic incompatibilities in the F2, but not F3 generation and suggests that intrinsic reproductive isolation is progressing, but lags behind ecological divergence. Overall, ecotypic diversification in S. lautus was likely driven by spatial variation in natural selection creating divergence in suites of phenotypic traits and underlying genetic variance. Local adaptation between contrasting environments was associated with performance trade-offs between environments, which may reduce gene flow and maintain ecotypic divergence. Changes in additive genetic variance underlying phenotypic traits suggests that adaptation has either occurred in the direction of greatest genetic variance, or selection on high standing genetic variation has favoured strong genetic correlations and collapsed genetic variance into a smaller number of dimensions. Finally, genetic incompatibilities appeared to be in the early stages of arising, suggesting that ecotypes are moving towards irreversible speciation during adaptive radiation across a heterogeneous landscape.