Global population genetic dynamics of a highly migratory, apex predator shark

Mol Ecol. 2016 Nov;25(21):5312-5329. doi: 10.1111/mec.13845. Epub 2016 Oct 18.

Abstract

Knowledge of genetic connectivity dynamics in the world's large-bodied, highly migratory, apex predator sharks across their global ranges is limited. One such species, the tiger shark (Galeocerdo cuvier), occurs worldwide in warm temperate and tropical waters, uses remarkably diverse habitats (nearshore to pelagic) and possesses a generalist diet that can structure marine ecosystems through top-down processes. We investigated the phylogeography and the global population structure of this exploited, phylogenetically enigmatic shark by using 10 nuclear microsatellites (n = 380) and sequences from the mitochondrial control region (CR, n = 340) and cytochrome oxidase I gene (n = 100). All three marker classes showed the genetic differentiation between tiger sharks from the western Atlantic and Indo-Pacific ocean basins (microsatellite FST > 0.129; CR ΦST > 0.497), the presence of North vs. southwestern Atlantic differentiation and the isolation of tiger sharks sampled from Hawaii from other surveyed locations. Furthermore, mitochondrial DNA revealed high levels of intraocean basin matrilineal population structure, suggesting female philopatry and sex-biased gene flow. Coalescent- and genetic distance-based estimates of divergence from CR sequences were largely congruent (dcorr = 0.0015-0.0050), indicating a separation of Indo-Pacific and western Atlantic tiger sharks <1 million years ago. Mitochondrial haplotype relationships suggested that the western South Atlantic Ocean was likely a historical connection for interocean basin linkages via the dispersal around South Africa. Together, the results reveal unexpectedly high levels of population structure in a highly migratory, behaviourally generalist, cosmopolitan ocean predator, calling for management and conservation on smaller-than-anticipated spatial scales.

Keywords: genetic population structure; microsatellite DNA; mitochondrial DNA; phylogeography; tiger shark.

MeSH terms

  • Animals
  • Atlantic Ocean
  • DNA, Mitochondrial / genetics
  • Female
  • Genetics, Population*
  • Haplotypes
  • Hawaii
  • Microsatellite Repeats
  • Pacific Ocean
  • Phylogeography
  • Sharks / genetics*
  • South Africa

Substances

  • DNA, Mitochondrial

Associated data

  • GENBANK/KU847364
  • GENBANK/KU847386
  • Dryad/10.5061/dryad.g41cj