Candidate gene polymorphisms are linked to dispersive and migratory behaviour: Searching for a mechanism behind the “paradox of the great speciators”

Abstract

Abstract The “paradox of the great speciators” has puzzled evolutionary biologists for over half a century. A great speciator requires excellent dispersal propensity to explain its occurrence on multiple islands, but reduced dispersal ability to explain its high number of subspecies. A rapid reduction in dispersal ability is often invoked to solve this apparent paradox, but a proximate mechanism has not been identified yet. Here, we explored the role of six genes linked to migration and animal personality differences (CREB1, CLOCK, ADCYAP1, NPAS2, DRD4, and SERT) in 20 South Pacific populations of silvereye (Zosterops lateralis) that range from highly sedentary to partially migratory, to determine if genetic variation is associated with dispersal propensity and migration. We detected genetic associations in three of the six genes: (i) in a partial migrant population, migrant individuals had longer microsatellite alleles at the CLOCK gene compared to resident individuals from the same population; (ii) CREB1 displayed longer average microsatellite allele lengths in recently colonized island populations (<200 years), compared to evolutionarily older populations. Bayesian broken stick regression models supported a reduction in CREB1 length with time since colonization; and (iii) like CREB1, DRD4 showed differences in polymorphisms between recent and old colonizations but a larger sample is needed to confirm. ADCYAP1, SERT, and NPAS2 were variable but that variation was not associated with dispersal propensity. The association of genetic variants at three genes with migration and dispersal ability in silvereyes provides the impetus for further exploration of genetic mechanisms underlying dispersal shifts, and the prospect of resolving a long-running evolutionary paradox through a genetic lens. Abstract Great speciators are species present on multiple islands that have many subspecies, many of which are single island endemics. This pattern is paradoxical because to colonize islands a good overwater dispersal ability is required, but divergence often requires limited gene flow, suggesting limits to dispersal. To resolve the ‘paradox of the great speciators’, many authors suggest that strong selection against dispersal ability after island colonization may shift populations to become less dispersive. We tested whether candidate genes for personality traits and migration were associated with population age and dispersal ability in the silvereye, a great speciator from the South Pacific. We found that old populations where individuals have lower dispersal ability had shorter microsatellite alleles at the CREB1 gene. We also found that, in a partial migrant population, migrant individuals had more repeats at CLOCK compared to resident individuals from the same population.