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

The “paradox of the great speciators” has puzzled evolutionary biologists for over half a century. A great speciator requires excellent dispersal ability 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. Here, we explore 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. 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 colonised island populations (< 200 years), compared to evolutionarily older populations. Bayesian broken stick regression models supported a reduction in CREB1 length with time since colonisation and decreasing dispersal propensity; and iii) like CREB1, DRD4 showed differences in polymorphisms between recent and old colonisations but a further sample size 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.