Philopatry drives genetic differentiation in an island archipelago: comparative population genetics of Galapagos Nazca boobies (Sula granti) and great frigatebirds (Fregata minor)

Abstract

Seabirds are considered highly mobile, able to fly great distances with few apparent barriers to dispersal. However, it is often the case that seabird populations exhibit strong population genetic structure despite their potential vagility. Here we show that Galapagos Nazca booby (Sula granti) populations are substantially differentiated, even within the small geographic scale of this archipelago. On the other hand, Galapagos great frigatebird (Fregata minor) populations do not show any genetic structure. We characterized the genetic differentiation by sampling five colonies of both species in the Galapagos archipelago and analyzing eight microsatellite loci and three mitochondrial genes. Using an F-statistic approach on the multilocus data, we found significant differentiation between nearly all island pairs of Nazca booby populations and a Bayesian clustering analysis provided support for three distinct genetic clusters. Mitochondrial DNA showed less differentiation of Nazca booby colonies; only Nazca boobies from the island of Darwin were significantly differentiated from individuals throughout the rest of the archipelago. Great frigatebird populations showed little to no evidence for genetic differentiation at the same scale. Only two island pairs (Darwin - Wolf, N. Seymour - Wolf) were significantly differentiated using the multilocus data, and only two island pairs had statistically significant φ(ST) values (N. Seymour - Darwin, N. Seymour - Wolf) according to the mitochondrial data. There was no significant pattern of isolation by distance for either species calculated using both markers. Seven of the ten Nazca booby migration rates calculated between island pairs were in the south or southeast to north or northwest direction. The population differentiation found among Galapagos Nazca booby colonies, but not great frigatebird colonies, is most likely due to differences in natal and breeding philopatry.

Keywords: Galapagos; natal philopatry; population genetics; seabird.

Figure 1

Map of the Galapagos Islands with sampled islands labeled. Numbers next to arrows are pair-wise F_ST values calculated for colonies of Nazca boobies (Sula granti) using eight microsatellite loci. Arrows show directional migration (rates calculated in BayesAss). Thick arrows indicate higher migration rates (0.18–0.29) while thinner arrows represent lower migration rates (0.01–0.06). Lines with no arrowheads have directional migration rates <0.01. Bidirectional migration rates >0.01 are indicated by lines with arrowheads on both ends.

Figure 2

Haplotype network for Nazca boobies (Sula granti) (A) and great frigatebirds (Fregata minor) (B) based on three mitochondrial genes. Circles are proportional to the number of individuals that share the haplotypes and the colors correspond to different islands. Black = Darwin, blue = Wolf, green = Genovesa, red = Española, purple = San Cristobal (Nazca booby only), yellow = N. Seymour (great frigatebird only).

Figure 3

(A) Posterior probability of assignment for 133 Nazca boobies (Sula granti) to three genetic clusters based on a Bayesian analysis run in STRUCTURE (using Locprior) of variation at eight microsatellite loci. Individuals are grouped by population and the different genetic clusters are indicated by the different colors. Every vertical bar corresponds to an individual bird and the section of each bar represented by a color is equal to the number of times (calculated as a proportion of the total STRUCTURE runs) that individual was assigned to each genetic cluster. (B) Posterior probability of assignment for 114 great frigatebirds (Fregata minor) showing no population differentiation using the Locprior setting in STRUCTURE. While k = 3 is shown here for comparison with the results from the Nazca booby, no structure was found from k = 2 to k = 8; one genetic cluster was most likely in all cases.