The genomic basis of parallel ecological speciation

Abstract

Ecological speciation, the origin of new species via divergent natural selection, is one of the most fundamental and unresolved processes in evolution. Although the evidence for adaptation of organisms to their environment is abundant, the role of ecological selection in mediating species formation remains controversial. This knowledge-gap arises in part from a scarcity of experimental evidence linking environmental selection to the creation of reproductive barriers that ultimately lead to species formation. An experimental framework to investigate ecological speciation consists in studying the genetic architecture of adaptive traits and reproductive isolation in interbreeding populations adapted to contrasting environments. In my thesis I explored the genomics of ecological speciation in plants using the Senecio lautus species complex, a diverse group of plants that have adapted to a broad array of environment across Australia. It has been suggested that local adaptation to different environments will lead to genetic divergence and speciation only if genomic regions controlling adaptive traits are not exchanged between organisms adapted to different niches. This will happen if adaptive genes also mediate reproductive isolation, thus making migration between environments difficult, or leading to poor survival of recombinants. This model of ecological speciation creates testable predictions on the genomic architecture of adaptation: Firstly, genomic divergence between incipient species is expected to be heterogeneous, where a few genomic regions display outlier differentiation. Secondly one expects divergent regions to contain genes affecting fitness in natural environments. Thirdly, these “genomic islands of speciation” will also contain loci controlling adaptive traits and reproduction. In my thesis I tested these predictions using divergent populations of plants from the S. lautus species complex. I used a combination of genomic and ecological approaches to: (i) Describe patterns of genomic differentiation between natural populations across Australia and made inferences about the forces that generated these patterns. Specifically, I tested the repeated and independent evolution of forms to coastal environments and analyzed whether genomic divergence was more heterogeneous between parapatric than allopatric populations. (ii) Demonstrate experimentally that divergent genomic regions contain genes controlling differential survivorship between environments. (iii) Detect QTLs associated to environmentally selected traits and associate their location to genomic regions of high differentiation between parapatric populations. In combination, these experiments were used to test the role of ecology in creating and maintaining the reproductive barriers that ultimately lead to plant speciation. A phylogenomic study of a continental collection of S. lautus populations showed that these plants have a monophyletic origin and evolved rapidly colonizing a broad array of environments. Importantly, populations adapted to adjacent but contrasting coastal environments, appeared as sister groups in phylogenetic analyses of thousands of loci, which suggests that these environments have been colonized repeatedly, and possibly in the presence of gene flow. To explore this hypothesis in further detail I analysed genetic differentiation between the genomes of populations. Our results revealed that genomic divergence was less heterogeneous between allopatric than parapatric populations, where a few genomic regions showed high differentiation while the rest of the genome was very similar. Additionally, genomic differentiation between some of these adjacent populations was related the magnitude of the differences between the environments that they inhabit, suggesting that divergence between them occurred in the face of gene flow. I investigated the evolutionary role of highly differentiated genomic regions through a combination of techniques that allowed us to connect genotype, phenotype and fitness. Firstly, I showed that these regions are enriched in coding mutations and associations to environmental variables, which suggest that they contain functionally important genes. However, patterns of divergence varied considerably across natural populations indicating that genomic divergence followed complex and divergent trajectories. Interestingly, functional analyses of divergent genes suggest that natural selection could have targeted different genes participating in the similar processes. By mapping loci involved in the control of fitness and convergent morphological traits across replicate populations I was able to demonstrate that divergent genomic regions contain adaptive and reproductive genes. Additionally I showed that genomic regions involved in adaptive trade-offs, have diverged repeatedly between environments, which supports their importance in mediating parapatric divergence. Overall my results provide genomic and functional evidence for a model of ecological speciation where natural selection creates divergence between the genomes of locally adapted organisms. These results also show that natural selection can have a complex genetic basis but create predictable patterns, especially at higher scales of biological organization.