Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

Abstract

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo-Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea-level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial-scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo-Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.

iDNA at Sea: Recovery of Whale Shark (Rhincodon typus) Mitochondrial DNA Sequences from the Whale Shark Copepod (Pandarus rhincodonicus) Confirms Global Population Structure

“…A total of 45 copepods were collected from 31 individual whale sharks sampled in Baa Atoll in the Maldives, at Ningaloo Reef, Western Australia, off Tofu Beach, Mozambique and off the coast of Mahe in the Seychelles as part of an earlier study using approved procedures under the Western Australian Department of Parks and Wildlife (WADPW) and University of Tasmania (UTAS) ethics permits (WADPW: SF009814 and SF009227; UTAS: 2255 and 2307) (Vignaud et al, 2014) (Supplementary Table 1). Copepods were scraped off the edges of the fins or lips using a plastic knife by a snorkeler who swam alongside an unrestrained animal, collected in an aquarium net and brought back to the vessel where they were preserved in 100% ethanol.…”

“…Authenticity of the DNA sequences of the mitochondrial control region of whale sharks were validated by BLAST searches, and sequences were aligned with previously generated sequences (Castro et al, 2007;Vignaud et al, 2014) using MAFFT version 7.310 with the option "-adjustdirection" activated (Yamada et al, 2016). The 5 ′ and 3 ′ ends of the alignment were manually trimmed using MEGA 6 (Tamura et al, 2013) so that each aligned control region had the same flanking sequence (Supplementary Figure 1).…”

“…The mitochondrial control regions of whale sharks generated using iDNA were combined with 613 sequences published by previous studies of whale shark populations (Castro et al, 2007;Ramírez-Macías et al, 2007;Schmidt et al, 2010;Vignaud et al, 2014). Identical iDNA sequences from the same whale shark host were removed prior to genetic analysis, to eliminate the chance of biasing estimates of population genetic differentiation (Supplementary Table 1).…”

“…Haplotype clustering confirmed a 100% sequence match for DNA sequences amplified from copepods collected from the same whale shark host (Supplementary Data 1). An initial alignment of the 31 newly-generated iDNA control region sequences with the 613 sequences provided by previous studies (Castro et al, 2007;Schmidt et al, 2010;Vignaud et al, 2014;Walter and Boxshall, 2017) yielded a 1,910 bp product (Supplementary Data 2). Trimming using 5 ′ -and 3 ′ -ends produced a final alignment length of 750 bp (Supplementary Data 3), from which a total of 163 unique haplotypes were evident (Supplementary Data 4).…”

“…Tagging, genetic and modeling studies suggest that individuals can disperse widely (Sequeira et al, 2013), although there is evidence of isolation between populations in the Indo-Pacific and Atlantic oceans (Vignaud et al, 2014). However, the scale at which population structure can be discerned is dependent on sample sizes, with low numbers reducing analytical power to reject the null hypothesis of a panmictic population (Castro et al, 2007).…”