DNA from historical and trophy samples provides insights into white shark population origins and genetic diversity

Abstract

Characterizing genetic variation by retrospective genotyping of trophy or historical artifacts from endangered species is an important conservation tool. Loss of genetic diversity in top predators such as the white shark Carcharodon carcharias remains an issue, exacerbated in this species by declining, sometimes isolated philopatric populations. We successfully sequenced mitochondrial DNA (mtDNA) D-loop from osteodentine of contemporary South African white shark teeth (from 3 jaws), and from 34 to 129 yr old dried cartilage and skin samples from 1 Pacific Ocean and 5 Mediterranean sharks. Osteodentine-derived sequences from South African fish matched those derived from an individual's finclips, but were generally of poorer quality than those from skin and cartilage of historical samples. Three haplotypes were identified from historical Mediterranean samples (n = 5); 2 individuals had unique sequences and 3 shared the contemporary Mediterranean haplotype. Placement of previously undescribed mtDNA haplotypes from historical material within both the Mediterranean and Pacific clades fits with the accepted intraspecific phylogeny derived from contemporary material, verifying our approaches. The utility of our methodology is in its provision of additional genetic resources from osteodentine (for species lacking tooth pulp) and cartilage of rare and endangered species held in often uncurated, contemporary and historical dry collections. Such material can usefully supplement estimates of connectivity, population history, and stock viability. We confirm the depauperate haplotype diversity of historical Mediterranean sharks, consistent with founding by a small number of Pacific colonizers. The consequent lack of diversity suggests serious challenges for the maintenance of this top predator and the Mediterranean ecosystem.

The importance of considering genetic diversity in shark and ray conservation policies

“…However, there are currently a few examples of the use of aDNA for shark species. Gubili et al (2015) sequenced a small fragment (135-228 bp) of mtDNA (D-loop) from 34-to 129-yearold dried cartilage and skin samples from six Carcharodon carcharias individuals and found greater genetic diversity (number of haplotypes and nucleotide and haplotype diversity) in the historical samples than in contemporary samples found in the Mediterranean Sea. Moreover, Li et al (2015) used the complete mitochondrial genome of aDNA to infer the phylogeny and gene flow of endangered river sharks (Glyphis spp., Carcharhinidae).…”

Extracting DNA from ‘jaws’: high yield and quality from archived tiger shark (Galeocerdo cuvier) skeletal material

“…They were able to amplify and sequence a large (700 bp) mitochondrial DNA segment from 44% (15) of the historical samples. Recently, Gubili et al (2015) extracted DNA from 34-to 129-year-old samples of fins and cartilage from six white sharks for subsequent successful analysis of small (135-228 bp) mtDNA sequences. Thus, both studies were primarily focused on demonstrating the applicability of archived shark samples for PCR amplification of mtDNA segments.…”

Pliocene colonization of the Mediterranean by Great White Shark inferred from fossil records, historical jaws, phylogeographic and divergence time analyses

“…Efforts have been made in the past to resolve the phylogenetic relationships of the Mediterranean GWS population using mitochondrial DNA (mtDNA) sequences (Gubili et al, , ). Using up to five specimens from the Mediterranean, Gubili et al (, ) concluded that the population is more closely related to populations in the Pacific Ocean (Australia, New Zealand and North‐eastern Pacific) than to those from the western Indian Ocean (South Africa) and north‐western Atlantic Ocean (Florida).…”

“…Efforts have been made in the past to resolve the phylogenetic relationships of the Mediterranean GWS population using mitochondrial DNA (mtDNA) sequences (Gubili et al, , ). Using up to five specimens from the Mediterranean, Gubili et al (, ) concluded that the population is more closely related to populations in the Pacific Ocean (Australia, New Zealand and North‐eastern Pacific) than to those from the western Indian Ocean (South Africa) and north‐western Atlantic Ocean (Florida). Based on a nucleotide substitution rate between the two major lineages (North‐eastern Pacific vs. North‐West Atlantic and Eastern Indian) calibrated by the formation of the Isthmus of Panama (3.5 Ma) and the Sunda‐Sahul Shelves (5 Ma), respectively, Gubili et al () suggested that Mediterranean GWS are descendants of a few disoriented individuals who immigrated from Australia/New Zealand during the Pleistocene (348–565 ka) by an antipodean route along the western coast of Africa.…”

“…Based on a nucleotide substitution rate between the two major lineages (North‐eastern Pacific vs. North‐West Atlantic and Eastern Indian) calibrated by the formation of the Isthmus of Panama (3.5 Ma) and the Sunda‐Sahul Shelves (5 Ma), respectively, Gubili et al () suggested that Mediterranean GWS are descendants of a few disoriented individuals who immigrated from Australia/New Zealand during the Pleistocene (348–565 ka) by an antipodean route along the western coast of Africa. A scenario of multiple relatively recent colonization events was also considered, based on the haplotype relationships that were generated using a few historical and contemporary Mediterranean specimens (Gubili et al, ).…”