Genetic homogeneity in the face of morphological heterogeneity in the harbor porpoise from the Black Sea and adjacent waters (Phocoena phocoena relicta)

Absence of genetic differentiation is usually taken as an evidence of panmixia, but can also reflect other situations including even nearly complete demographic independence among large-sized populations. Deciphering which situation applies has major practical implications (e.g., in conservation biology). The endangered harbor porpoises in the Black Sea illustrates well this point. While morphological heterogeneity suggested that population differentiation may exist between individuals from the Black and Azov seas, no genetic study provided conclusive evidence or covered the entire subspecies range. Here, we assessed the genetic structure at ten microsatellite loci and a 3,904 base-pairs mitochondrial fragment in 144 porpoises across the subspecies range (i.e., Aegean, Marmara, Black, and Azov seas). Analyses of the genetic structure including F_ST, Bayesian clustering, and multivariate analyses revealed a nearly complete genetic homogeneity. Power analyses rejected the possibility of underpowered analyses (power to detect F_ST≥0.008 at microsatellite loci). Simulations under various demographic models, evaluating the evolution of F_ST, showed that a time-lag effect between demographic and genetic subdivision is also unlikely. With a realistic effective population size of 1000 individuals, the expected "grey zone" would be at most 20 generations under moderate levels of gene flow (≤10 migrants per generation). After excluding alternative hypotheses, panmixia remains the most likely hypothesis explaining the genetic homogeneity in the Black Sea porpoises. Morphological heterogeneity may thus reflect other processes than population subdivision (e.g., plasticity, selection). This study illustrates how combining empirical and theoretical approaches can contribute to understanding patterns of weak population structure in highly mobile marine species.