Population genetics of Southern Hemisphere tope shark (Galeorhinus galeus): Intercontinental divergence and constrained gene flow at different geographical scales

Abstract

The tope shark (Galeorhinus galeus Linnaeus, 1758) is a temperate, coastal hound shark found in the Atlantic and Indo-Pacific oceans. In this study, the population structure of Galeorhinus galeus was determined across the entire Southern Hemisphere, where the species is heavily targeted by commercial fisheries, as well as locally, along the South African coastline. Analysis was conducted on a total of 185 samples using 19 microsatellite markers and a 671 bp fragment of the NADH dehydrogenase subunit 2 (ND2) gene. Across the Southern Hemisphere, three geographically distinct clades were recovered, including one from South America (Argentina, Chile), one from Africa (all the South African collections) and an Australia-New Zealand clade. Nuclear data revealed significant population subdivisions (FST = 0.192 to 0.376, p<0.05) indicating limited gene flow for tope sharks across ocean basins. Marked population connectivity was however evident across the Indian Ocean based on Bayesian clustering analysis. More locally in South Africa, F-statistics and multivariate analysis supported moderate to high gene flow across the Atlantic/Indian Ocean boundary (FST = 0.035 to 0.044, p<0.05), with exception of samples from Struisbaai and Port Elizabeth which differed significantly from the rest. Discriminant and Bayesian clustering analysis indicated admixture in all sampling populations, decreasing from west to east, corroborating possible restriction to gene flow across regional oceanographic barriers. Mitochondrial sequence data recovered seven haplotypes (h = 0.216, π = 0.001) for South Africa, with one major haplotype shared by 87% of the individuals and at least one private haplotype for each sampling location except Port Elizabeth. As with many other coastal shark species with cosmopolitan distribution, this study confirms the lack of both historical dispersal and inter-oceanic gene flow while also implicating contemporary factors such as oceanic currents and thermal fronts to drive local genetic structure of G. galeus on a smaller spatial scale.

Accounting for kin sampling reveals genetic connectivity in Tasmanian and New Zealand school sharks, Galeorhinus galeus

“…Interestingly, our findings contradict nuclear DNA results from a recent study of Bester‐van der Merwe et al (). Potential sibling‐ or sex‐biased sampling could explain the observed nuclear signal of structure (Allendorf & Phelps, ; Benestan et al, ; Feutry et al, ; Waples, ).…”

“…This is supported by the large dispersal abilities of school sharks (Coutin et al, ; Hurst et al, ; McAllister et al, ; McMillan et al, ; Olsen, ). Genetic diversity was similar between both sampling regions, but lower compared to previous studies (He = 0.5–0.75; Hernández et al, ; Bester‐van der Merwe et al, ; Domingues et al, ). This discrepancy with other studies can be explained by the choice of genetic markers.…”

“…School sharks are known to school by size and sex (Francis, ; Olsen, ). The nine Tasmanian and 20 New Zealand individuals from Bester‐van der Merwe et al () were obtained to identify biased sampling. We were unable to test the sex‐biased sampling hypothesis, because of missing sex information, but we re‐analyzed the 19 microsatellites in COLONY2.…”

“…This study builds on the many telemetry and genetic studies that have investigated movement and connectivity of school sharks within Oceania (Bester‐van der Merwe et al, ; Coutin et al, ; Hernández et al, ; Hurst et al, ; McAllister, Barnett, Lyle, & Semmens, ; McMillan et al, ; Olsen, ; Ward & Gardner, ). Based on current results, the null hypothesis of a single panmictic population cannot be rejected.…”

“…A lack of apparent genetic structure between these Australian and New Zealand sharks has been reported, using allozyme, mitochondrial DNA (mtDNA), and microsatellites (Hernández et al, ; Ward & Gardner, ), thus questioning the existence of impervious reproductive boundaries in this region. However, a more recent study, with the mitochondrial and similar nuclear microsatellite markers, found a clear separation in the microsatellite data between Tasmania and New Zealand (Bester‐van der Merwe et al, ). Single nucleotide polymorphisms (SNPs) have been shown to outperform microsatellites in population discrimination due to their random spread across the genome, lower ascertainment bias, higher accuracy and resolution, reproducibility, and comparability (Andrews, Good, Miller, Luikart, & Hohenlohe, ; Fischer et al, ; Muñoz et al, ; Seeb et al, ).…”