Genomic patterns in the dwarf kingfishers of northern Melanesia reveal a mechanistic framework explaining the paradox of the great speciators

Abstract

The paradox of the great speciators describes a contradictory biogeographic pattern exhibited by numerous avian lineages in Oceania. Specifically, these lineages display broad geographic distributions across the region, implying strong over-water dispersal capabilities; yet, they also display repeated genetic and phenotypic divergence—even between geographically proximate islands—implying poor inter-island dispersal capabilities. One group originally cited as evidence for this paradox is the dwarf kingfishers of the genus Ceyx. Here, using genomic sequencing and comprehensive geographic sampling of the monophyletic Ceyx radiation from northern Melanesia, we find repeated, deep genetic divergence and no evidence for gene flow between lineages found on geographically proximate islands, providing an exceptionally clear example of the paradox of the great speciators. A dated phylogenetic reconstruction suggests a significant burst of diversification occurred rapidly after reaching northern Melanesia, between 3.9 and 2.9 MYA. This pattern supports a shift in net diversification rate, concordant with the expectations of the “colonization cycle” hypothesis, which implies a historical shift in dispersiveness among great speciator lineages during the evolutionary past. Here, we present a formalized framework that explains how repeated founder effects and shifting selection pressures on highly dispersive genotypes are the only ultimate causes needed to generate the paradox of the great speciators. Within this framework, we emphasize that lineage-specific traits and island-specific abiotic factors will result in varying levels of selection pressure against dispersiveness, caused by varying proximate eco-evolutionary mechanisms. Overall, we highlight how understanding patterns of diversification in the Ceyx dwarf kingfishers helped us generate a cohesive framework that provides a rigorous mechanistic explanation for patterns concordant with the paradox of the great speciators and the repeated emergence of geographic radiations in island archipelagoes across the globe.