Metapopulation connectivity retains genetic diversity following a historical bottleneck in a federally endangered seabird

Abstract

Abstract Despite intensive management since the 1970s, recovery of the endangered northwestern Atlantic population of the Roseate Tern (Sterna dougallii dougallii) has not offset low productivity from a female-biased sex ratio, low adult survival, and habitat constriction. Now, >90% of individuals breed at three sites within 200 km from Long Island, NY, to Buzzards Bay, MA (warm-water subregion). To characterize the impact of historical bottlenecks, metapopulation structure, and demographic fluctuations on genetic variation, Roseate Terns from the warm-water (1870s, 1970s, 1997, 2016) and cold-water (Nova Scotia, Canada; 2018) subregions were genotyped at 8–16 microsatellites and 2–3 mitochondrial regions. Diversity declined in the warm-water subregion from the 1870s (expected heterozygosity [HE] = 0.44, allelic richness [AR] = 2.86) and 1970s (HE = 0.53, AR = 3.25) to 1997 (HE = 0.38, AR = 2.58). Genetic signatures of bottlenecks persisted in 1997 (P = <0.001–0.003) and 2016 (P = <0.001–0.005), but an increase in variation occurred by 2016 (HE = 0.50, AR = 2.85). Weak structure was detected between contemporary warm- and cold-water subregions (θ = 0.06) and within the warm-water subregion (θ = 0.04). Both demographic (3,439–3,821) and genetic (3,040) estimates suggested effective population size (Ne) stability over the last 100 years, despite large fluctuations in census size (4,000–8,662). Results suggest that 50 years of management (restoring habitat, preventing gull encroachment, controlling predators) at colony sites supported a small, stable Ne and maintained a hierarchical metapopulation that allowed gene flow to redistribute genetic variation throughout the northwest Atlantic. The metapopulation remains highly vulnerable to stochastic events but harbors resiliency and redundancy through gene flow and a stable Ne. For long-term persistence from a genetic perspective, managers must maintain the major source colonies, increase the availability of high-quality peripheral breeding sites, and protect concentrated nonbreeding sites that facilitate gene flow.