Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini)

Abstract

Background: The scalloped hammerhead shark, Sphyrna lewini, is a large endangered predator with a circumglobal distribution, observed in the open ocean but linked ontogenetically to coastal embayments for parturition and juvenile development. A previous survey of maternal (mtDNA) markers demonstrated strong genetic partitioning overall (global Φ(ST) = 0.749) and significant population separations across oceans and between discontinuous continental coastlines.

Methodology/principal findings: We surveyed the same global range with increased sample coverage (N = 403) and 13 microsatellite loci to assess the male contribution to dispersal and population structure. Biparentally inherited microsatellites reveal low or absent genetic structure across ocean basins and global genetic differentiation (F(ST) = 0.035) over an order of magnitude lower than the corresponding measures for maternal mtDNA lineages (Φ(ST) = 0.749). Nuclear allelic richness and heterozygosity are high throughout the Indo-Pacific, while genetic structure is low. In contrast, allelic diversity is low while population structure is higher for populations at the ends of the range in the West Atlantic and East Pacific.

Conclusions/significance: These data are consistent with the proposed Indo-Pacific center of origin for S. lewini, and indicate that females are philopatric or adhere to coastal habitats while males facilitate gene flow across oceanic expanses. This study includes the largest sampling effort and the most molecular loci ever used to survey the complete range of a large oceanic predator, and findings emphasize the importance of incorporating mixed-marker analysis into stock assessments of threatened and endangered shark species.

Figure 1. Map showing collection sites.

TEP = Tropical East Pacific, HH = Hawaii, TW = Taiwan, PH = Philippines, EA = East Australia, W = West Australia, SY = Seychelles, SA = South Africa, WAF = West Africa, SC = South Carolina, and GM = Gulf of Mexico. Sample numbers for each site are in parentheses.

Figure 2. Unrooted radial dendrogram of pairwise F _ST genetic distances generated from microsatellite genotypes using TreeFit .

Lengths of braches demonstrate allelic similarities between nodes, each of which represents a separate sampling site. R-square value expresses the proportion of variation in the distance matrix that is explained by the dendrogram. TEP = Tropical East Pacific, HH = Hawaii, TW = Taiwan, PH = Philippines, EA = East Australia, W = West Australia, SY = Seychelles, SA = South Africa, WAF = West Africa, SC = South Carolina, and GM = Gulf of Mexico.

Figure 3. Proportions of population ancestry from each of four multi-locus lineages (C1–C4) defined by Structure .

Pie charts in the top figure indicate the relative proportion of individuals from each sampling site that assign to each lineage, and the bottom figure shows individual genotypic assignments in a conventional bar plot, organized by sampling site. TEP = Tropical East Pacific, HH = Hawaii, TW = Taiwan, PH = Philippines, EA = East Australia, W = West Australia, SY = Seychelles, SA = South Africa, WAF = West Africa, SC = South Carolina, and GM = Gulf of Mexico.