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

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.

Standing genetic variation andde novomutations underlie parallel evolution of island bird phenotypes

“…PC2 explained 6.8% of the variance and separated the two main archipelagos within SM: New Caledonia and Vanuatu. This population structure aligns with previous analyses using fewer individuals (Estandía et al 2023). We visualised further substructure within the SM and ANZO clusters (Fig.…”

“…This pattern held even within popula- tions, indicating no bias due to population structure. Variation could be maintained across the archipelagos if different degrees of size are favoured in different populations connected by gene flow as seen across Southern Melanesian silvereye populations (Clegg and Phillimore 2010;Estandía et al 2023). While larger size of island silvereyes appears generally to be favoured, other species, and indeed other Zosterops white-eye species that co-occur, could impose local constraints on size.…”

“…To test whether de novo mutations or ancestral standing genetic variation led to similar phenotypes, we did a Genomewide Association Study (GWAS) under the idea that if the associated variants are common to all populations then they are likely due to standing genetic variation but if they are present in a specific population or specific lineage, they may represent de novo mutations that have accumulated since the lineage split. This framework assumes no potential gene flow among colonisations, which is supported by genome-wide data (Estandía et al 2023).…”

“…1). The populations arising from these independent colonisations are genetically isolated from the original mainland source and other colonisations, though gene flow occurs among Southern Melanesian islands and among recently colonised populations (Estandía et al 2023). The combination of independent and known colonisation sequences, along with broadly repeated shifts in body and bill size in similar ecological contexts provides an excellent system to explore the genetic mechanisms of parallel evolution.…”

Islands promote diversification within the silvereye clade: a phylogenomic analysis of a great speciator

“…Under the ‘taxon cycle’ framework—the idea that speciation on islands proceeds through phases of range expansion and contraction (Wilson, 1961) —a great speciator has undergone the first two phases of a cycle: an initial expansion followed by a reduction in dispersive behaviour that promotes population differentiation and sub-speciation. This pattern can be seen in multiple south-west Pacific birds, including kingfishers (Andersen et al, 2018; DeRaad et al, 2023; O’Connell et al, 2019), corvids (Pepke et al, 2019) and passerines (Estandía, Sendell-Price, Oatley, et al, 2023; Klicka et al, 2023; Pedersen et al, 2018).…”