On Speciation in Birds – Genomic Signatures across Space and Time

Sammanfattning: The process of speciation is a cornerstone in evolutionary biology. In Darwin’s On the Origin of Species, he described how he imagined that a new species would evolve to fill an empty niche. This focus on ecology shifted with Mayr towards the importance of isolation, and for many decades the geographic modes of speciation were debated. Speciation in sympatry, i.e. without any isolation between the diverging lineages, was controversial. Can speciation proceed in the face of gene flow, and if so, at what frequency? Lately, the perspective has shifted from the dichotomy of allopatry (i.e. non-overlapping distributions) and sympatry, in favour of investigating the processes involved in speciation, and acknowledging the role of ecology. In this thesis, I explore some of these aspects by studying several different groups of birds, some of which are distributed over three continents, and others that are confined to tiny, isolated, oceanic islands. Birds are highly mobile by nature, and in the absence of geographical barriers, a species is not likely to diverge without isolation, unless there is strong disruptive selection that can counteract the homogenizing effect of gene flow between incipient lineages. For this purpose, studying birds that are isolated on islands is particularly useful. I studied an interesting radiation of finches on Tristan da Cunha, which colonized the islands about four million years ago, but seemingly radiated into one pair of small-billed feeding generalists and large-billed feeding specialists in each of two islands, only a few hundred thousand years ago. I employed an array of genomic tools and uncovered the genetic target of natural selection on bill morphology. Interestingly, one of the two chromosomal regions with a large effect on bill morphology associated differently to small-billed and large-billed birds on the different islands. This supports the scenario that a small-billed ancestor colonized the two islands, and that the lineages then diverged in primary sympatry, in parallel processes on the two islands. This is not known to have happened in any other of the ten thousand species of birds described. Another case of speciation in sympatry, with selection overcoming gene flow, is the Gulf of Guinea seedeaters. Here, two separate colonizations from the same mainland source population led to secondary introgressive hybridization on São Tomé about a million years ago. My results suggest that this was followed by strong, asymmetric, ecological character displacement rendering one of the species an island giant that was previously not even recognized as a seedeater. Morphology was traditionally used as the basis for taxonomic classification, but my work has demonstrated that this is problematic for two opposite reasons. (1) The phenotypic differentiation is not proportional to genetic differentiation or time since divergence. This is illustrated by the relative similarity between blue tit populations on the Canary Islands, which have been isolated for several million years, and by the recent divergence between seedeaters on São Tomé and finches on Tristan da Cunha. On the other hand, (2) convergent evolution made two different Calandrella lark species, which are not each other’s closest relative, look so similar that they have hitherto been treated as the same species.