Cross ocean-basin population genetic dynamics in a pelagic top predator of high conservation concern, the oceanic whitetip shark, Carcharhinus longimanus

The oceanic whitetip shark, Carcharhinus longimanus, is a Critically Endangered, circumtropical, and highly migratory, pelagic shark. Yet, little information exists on its population genetic dynamics to guide conservation management practice. We present a first worldwide, mitochondrial and nuclear DNA assessment of the population genetic status of this imperiled species based on sequences of the complete mitochondrial control region (n = 173) and partial ND4 gene (n = 172), and genotypes from 12 nuclear microsatellites (n = 164). Statistically significant mitochondrial and nuclear DNA population genetic differentiation was detected across all marker datasets between Western Atlantic and Indo-Pacific oceanic whitetip sharks. Additionally, our data, combined with previously published, partial (701-base pairs) mitochondrial control region sequences from additional locations in the Atlantic and Indian Oceans, confirmed significant matrilineal population structure between the Western and Eastern Atlantic. The combined data also provisionally (i.e., with FST but not ΦST) indicated differentiation between Western North and Central-South Atlantic sharks, pointing to the need for further assessment in this region. Matrilineal differentiation was also detected between Indian and Pacific Ocean sharks via pairwise analyses, albeit with the ND4 gene sequence only (ΦST = 0.051; FST = 0.092). Limited sampling in the Pacific leaves open questions about the connectivity dynamics in this large region. Despite the presence of geographic population genetic structure, the mitochondrial data showed no evidence of across ocean basin phylogeographic lineages. A provisional assessment of mitochondrial and nuclear genetic diversity indicated the oceanic whitetip shark’s status falls in the middle to upper ranges compared to other shark species, potentially lending some optimism for the present adaptability and resiliency of this species if strong conservation measures are effectively implemented.

Methods
Oceanic whitetip shark samples were genotyped at 14 microsatellite loci including three loci from Carcharhinus longimanus (OCS_08, OCS_13, OCS_19) previously described by Mendes et al. (2015) and 11 loci isolated in other shark species that also cross-amplified in C. longimanus [Cl13, Cl15, Cl17 from Carcharhinus leucas (Pirog et al. 2015); Cli107 from Keeney and Heist (2003); Cpe141, Cpe334, Cpe352 from Carcharhinus perezi (Bernard et al. 2017); Pgla-02 from Prionace glauca (Fitzpatrick et al. 2011); Ct06 from Carcharhinus tilstoni (Ovenden et al. 2006); and A2ASY, CY92Z from Prionace glauca (Taguchi et al. 2013)]

Electrophoresis of amplified microsatellite loci was performed on an Applied Biosystems 3130 Genetic Analyzer. Alleles were sized using GeneScan LIZ 600 size standard and scored using the software GeneMapper v.3.7 (Applied Biosystems Inc.).

Bernard AM, Horn RL, Chapman DD, Feldheim KA, Garla RC, Brooks EJ, Gore MA, Shivji MS (2017) Genetic connectivity of a coral reef ecosystem predator: the population genetic structure and evolutionary history of the Caribbean reef shark (Carcharhinus perezi). J Biogeogr 44:2488-2500. https://doi.org/10.1111/jbi.13062

Fitzpatrick S, Shivji MS, Chapman DD, Prodöhl PA (2011) Development and characterization of 10 polymorphic microsatellite loci for the blue shark, Prionace glauca, and their cross shark-species amplification. Conserv Genet Resour 3:523-527. https://doi.org/10.1007/s12686-011-9395-6

Keeney DB, Heist EJ (2003) Characterization of microsatellite loci isolated from the blacktip shark and their utility in requiem and hammerhead sharks. Mol Ecol Notes 3:501-504. https://doi.org/10.1046/j.1471-8286.2003.00492.x

Mendes NJ, Cruz VP, Mendonça FF, Pardo BG, Coelho R, Ashikaga FY, Camargo SM, Martínez P, Oliveira C, Santos MN, Foresti F (2015) Microsatellite loci in the oceanic whitetip shark and cross-species amplification using pyrosequencing technology. Conserv Genet Resour 7:585-589. https://doi.org/10.1007/s12686-015-0435-5

Ovenden JR, Street R, Broderick D (2006) New microsatellite loci for Carcharhinid sharks (Carcharhinus tilstoni and C. sorrah) and their cross-amplification in other shark species. Mol Ecol Notes 6:415-418. https://doi.org/10.1111/j.1471-8286.2005.01254.x

Pirog A, Blaison A, Jaquemet S, Soria M, Magalon H (2015) Isolation and characterization of 20 microsatellite markers from Carcharhinus leucas (bull shark) and cross-amplification in Galeocerdo cuvier (tiger shark), Carcharhinus obscurus (dusky shark), and Carcharhinus plumbeus (sandbar shark). Conserv Genet Resour 7:121-124. https://doi.org/10.1007/s12686-014-0308-3

Taguchi M, Shigenobu Y, Ohkubo M, Yanagimoto T, Sugaya T, Nakamura Y, Saitoh K, Yokawa K (2013) Characterization of 12 polymorphic microsatellite DNA loci in the blue shark, Prionace glauca, isolated by next generation sequencing approach. Conserv Genet Resour 5:117-119. https://doi.org/10.1007/s12686-012-9746-y