Genetic divergence, reproductive isolation and the early stages of speciation

The process of speciation is the splitting of single populations into two or more distinct, reproductively isolated taxa. Common modes of speciation are sympatric, allopatric and parapatric speciation, with speciation in allopatry being the most frequently documented mode to date. In allopatric speciation, geographical barriers physically separate populations, allowing these now isolated groups to evolve reproductive barriers, i.e. barriers to
successful reproduction, which can take the form of premating, postmating prezygotic or postzygotic barriers. Species level phylogenies derived from molecular data may provide an indirect record of speciation events, and can, when combined with morphological traits, be used to investigate at what stage in the speciation process (e.g. early speciation, recent speciation, reversed speciation) taxa currently are. In this thesis, I used a range of
molecular methods and morphological analysis to investigate different stages in the speciation process. More specifically, I investigated four different species/species complexes exhibiting varying degrees of genetic and morphological divergence in order to investigate where in the speciation process taxa are and to discuss the evolutionary processes involved in the speciation events. First, the phylogeographic pattern of the common redstart (Phoenicurus phoenicurus) was described and the level of genetic divergence quantified. In this system, high divergence within the mitochondrial DNA (5% K2P distance, COI) combined with low morphological divergence appears to reflect reversed speciation. Second, I found a similar pattern of high genetic divergence (1.5-4.1% K2P distance, COI) in the autumnal moth (Epirrita autumnata), for which low morphological divergences have previously been found. Moreover, an association between the moths’ mtDNA divergence and infection by different Wolbachia strains was found, and I suggest that this association
maintains the mitochondrial variation. In contrast to these two studies, the bluethroat (Luscinia svecica) subspecies complex was characterized by exhibiting low genetic divergence (mean genetic distance 0.7%, K2P distance, COI) and high morphological differences and, as such, appears to exhibit signs of early speciation. Importantly, these contrasting patterns may be explained by differences in both ecology and sexual selection pressures experienced by each of the species/populations, with the bluethroats being subject to strong diversifying sexual selection for male primary and secondary sexual characters. A third goal of this thesis was to investigate whether sperm characters and genetic markers evolve at different speeds. In the bluethroat subspecies complex, where mitochondrial divergence was low, I found evidence of rapid evolution of sperm morphology, suggesting that rapid evolution of gametes may be an important factor involved in the early stages of speciation. Finally, I studied the black-and-white Ficedula flycatchers, a group of species suggested to have undergone recent speciation, in order to investigate variation in the rate of evolution between the Z chromosome (i.e. sex chromosome) and the autosomes. In this system, I found contrasting patterns in the evolution of the Z chromosome versus the autosomes. Specifically, my results revealed increased divergence and reduced variation on the Z chromosome compared to the autosomes, a finding that is best explained by the faster-Z hypothesis. As the Z chromosome has been linked to sexually selected traits in the Ficedula flycatchers, I suggest the contrasting pattern of evolution on the Z vs. autosome may have implications for the process of speciation processes in these species. In conclusion, my thesis highlights the utility of combining patterns of genetic and phenotypic divergence to identify at what stage of the speciation process taxa occur and how variation in evolutionary rates between traits can contribute to our understanding of the speciation process