Island-hopping silvereyes and a resolution to 'the paradox of the great speciators'

The 'paradox of the great speciators'1is a classic puzzle in evolutionary biology 2. Great speciators show a high degree of interisland geographic variation, defined by their number of subspecies and allospecies. Their very existence presents an evolutionary puzzle because excellent dispersal ability is required to explain their wide distribution, while their high degree of differentiation suggests limits to their dispersal ability3-7. Post-colonisation changes in dispersal propensity are often invoked to resolve the paradox1,2; however, the underlying mechanism for this putative process has not been identified. Genome-wide studies in natural populations provide an excellent approach to studying the evolutionary processes underlying divergence events, by enabling fine-scale detection of microevolutionary change, such as genetic fingerprints of selection or gene flow, that can be informative in deciphering the evolutionary history of diversifications8.Empirical evidence in birds shows that genetic changes can result in migratory populations becoming year-round residents and such changes may also explain rapid evolutionary shifts from highly dispersive to sedentary forms, thereby providing a mechanistic explanation for the 'paradox of the great speciators'9-12. In addition, it has recently been suggested that non-random mating with respect to personality type may be an important feature that accelerates divergence in colonised populations13. If individuals of similar dispersal propensities tend to mate more often and have higher fitness when colonising, this might promote divergence and lead to reproductive isolation.One of the most diverse passerine families is Zosteropidae, with more than 120 species from 12 genera, of which the white-eyes (genus Zosterops) comprise one of the fastest diversifying vertebrate clades, and it is deemed one of the 'great speciators'2. White-eyes are among the largest avian genera, with about 80 described species found. Within the white-eyes, one species, the silvereye (Z. lateralis) provides an ideal model to examine both the genomic variation associated with dispersal propensity and the timescale of any changes that occur post-colonisation. This is because silvereyes vary in dispersal propensity 14; at one extreme, some populations exhibit partial migration, others are dispersive in the sense of having high levels of outgoing gene flow, and others exist as isolated, sedentary populations15-17. In addition, the colonisation history of island silvereye populations is well characterised, providing a timescale from hundreds to hundreds of thousands of years to calibrate genomic and phenotypic change14,17-19.I propose to study South Pacific Zosteropsspecies and populations to examine genomic divergence and dispersal propensity with an aim to explain the mechanisms underlying the switch from highly dispersive to sedentary taxa, the timescales over which suchswitches occur, and ultimately reconcile the apparently paradoxical features of great speciators.