Genetic Connectivity of a Coral Reef Ecosystem Predator: The Population Genetic Structure and Evolutionary History of the Caribbean Reef Shark (Carcharhinus perezi)

Aim The Caribbean reef shark (Carcharhinus perezi) is one of few extant reef sharks inhabiting the Atlantic Ocean. Its variability in movements across habitat types suggests the possibility of a complex genetic population structure. Here, we use mitochondrial and nuclear DNA to investigate the genetic connectivity of the Caribbean reef shark across contemporary and evolutionary time-scales and relate our findings to the ecology of this understudied species. Location Tropical western Atlantic and Caribbean. Methods Samples were obtained from 216 individuals from six western Atlantic and Caribbean locations. Individuals were genotyped at seven nuclear microsatellite DNA loci and sequenced at two mitochondrial (control region [CR]; NADH dehydrogenase subunit 4 [ND4]) and one nuclear locus (lactate dehydrogenase [LDH]). Analyses to resolve the population genetic structure and evolutionary history of this species were adopted. Results Sequencing of the CR (1,068 bp, n = 216), ND4 (741 bp, n = 213) and LDH (258 bp, n = 165) loci, resolved 11, 8 and 13 unique haplotypes (or alleles), respectively. Overall, Caribbean reef sharks showed low levels of genetic diversity and most marker sets identified strong genetic differences (FSTand ΦST) between sharks sampled in Brazil versus all other locations (msat FST \u3e 0.017; CR-ND4 ΦST \u3e 0.013). Mitochondrial DNA showed evidence of increased genetic partitioning among western North Atlantic sampling sites, although widespread haplotype sharing (~85%–92%) and a shallow population history were found. Main Conclusions Findings of genetic differentiation are concordant with previous movement studies showing residency and/or site-fidelity to specific locations by individuals. However, similar to other reef shark studies, we found that the level of genetic connectivity among populations was context dependent—i.e., sharks occupying isolated habitats showed greater genetic differentiation compared with those sharks occupying semi-isolated or continuous reef habitats. Furthermore, low genetic diversity and a shallow mitochondrial population history were found, suggesting historical demographic fluctuations, including population collapse and more recent expansions

Phylogenomics of the genus Tursiops and closely related Delphininae reveals extensive reticulation among lineages and provides inference about eco-evolutionary drivers

Phylogeographic inference has provided extensive insight into the relative roles of geographical isolation and ecological processes during evolutionary radiations. However, the importance of cross-lineage admixture in facilitating adaptive radiations is increasingly being recognised, and suggested as a main cause of phylogenetic uncertainty. In this study, we used a double digest RADseq protocol to provide a high resolution (∼ 4 Million bp) nuclear phylogeny of the Delphininae. Phylogenetic resolution of this group has been especially intractable, likely because it has experienced a recent species radiation. We carried out cross-lineage reticulation analyses, and tested for several sources of potential bias in determining phylogenies from genome sampling data. We assessed the divergence time and historical demography of T. truncatus and T. aduncus by sequencing the T. aduncus genome and comparing it with the T. truncatus reference genome. Our results suggest monophyly for the genus Tursiops, with the recently proposed T. australis species falling within the T. aduncus lineage. We also show the presence of extensive cross-lineage gene flow between pelagic and European coastal ecotypes of T. truncatus, as well as in the early stages of diversification between spotted (Stenella frontalis; Stenella attenuata), spinner (Stenella longirostris), striped (Stenella coeruleoalba), common (Delphinus delphis), and Fraser’s (Lagenodelphis hosei) dolphins. Our study suggests that cross-lineage gene flow in this group has been more extensive and complex than previously thought. In the context of biogeography and local habitat dependence, these results improve our understanding of the evolutionary processes determining the history of this lineage

Use of Photo-Identification and Mark-Recapture Methodology to Assess Basking Shark (Cetorhinus maximus) Populations.

Following centuries of exploitation, basking sharks (Cetorhinus maximus) are considered by IUCN as Endangered in the Northeast Atlantic, where they have now been substantially protected for over two decades. However, the present size of this population remains unknown. We investigated the use of photo-identification of individuals' dorsal fins, combined with mark-recapture methodology, to investigate the size of populations of basking shark within the west coast of Scotland. From a total of 921 encounters photographed between 2004 and 2011, 710 sharks were found to be individually identifiable based on dorsal fin damage and natural features. Of these, only 41 individuals were re-sighted, most commonly both within days of, and close to the site of, the initial encounter. A smaller number were re-sighted after longer periods of up to two years. A comparison of the distinguishing features of individuals on first recording and subsequent re-sighting showed that in almost all cases these features remained little changed, suggesting the low re-sighting rate was not due to a loss of distinguishing features. Because of the low number of re-sighting we were not able to produce reliable estimates for the long-term regional population. However, for one 50 km diameter study area between the islands of Mull, Coll and Tiree, we were able to generate closed-population estimates for 6-9 day periods in 2010 of 985 (95% CI = 494-1683), and in 2011 of 201 (95% CI = 143-340). For the same 2011 period an open-population model generated a similar estimate of 213 (95% CI = 111-317). Otherwise the low rate and temporal patterning of re-sightings support the view that such local basking shark populations are temporary, dynamic groupings of individuals drawn from a much larger regional population than previously supposed. The study demonstrated the feasibility and limitations of photo-identification as a non-invasive technique for identifying individual basking sharks

Transatlantic migration and deep mid-ocean diving by basking shark

Despite being the second largest fish, basking sharks (Cetorhinus maximus) have been assumed to remain in discrete populations. Their known distribution encompasses temperate continental shelf areas, yet until now there has been no evidence for migration across oceans or between hemispheres. Here we present results on the tracks and behaviour of two basking sharks tagged off the British Isles, one of which released its tag off Newfoundland, Canada. During the shark's transit of the North Atlantic, she travelled a horizontal distance of 9589 km and reached a record depth of 1264 m. This result provides the first evidence for a link between European and American populations and indicates that basking sharks make use of deep-water habitats beyond the shelf edge

Sample basking shark dorsal fin photograph and sketched cartoon.

<p>The figure illustrates how a dorsal fin photograph is used to generate a cartoon (sketch diagram) to aid recording and cataloguing of distinctive features for individual identification.</p

Comparison of abundance estimates obtained during peak periods in 2010 and 2011 for Inner Hebrides study area.

<p>The columns relate to the outputs of the open- and closed-population models indicated; the error bars represent 95% Confidence Intervals.</p

Results of boat-based surveys of basking sharks in the two study areas.

<p>Results of boat-based surveys of basking sharks in the two study areas.</p

Re-sightings of basking sharks across years.

<p>Re-sightings of basking sharks across years.</p

Variants of the Jolly-Seber model used in population estimations.

<p>Variants of the Jolly-Seber model used in population estimations.</p

Sample photographs of fins assigned to each distinctiveness grade.

<p>A1—very conspicuous marks or injuries, likely to be recognisable in the very long term (a badly damaged fin apex), A2—clear marks or injuries, likely recognisable across year (a smaller injury to the fin apex), B1 -surface features or patterns such as lamprey scars and mottling—likely recognisable during a season (a conspicuous lamprey scar), B2—less permanent surface features, such as copepods, likely recognisable only in the short-term (note the clusters of copepods to the rear of the fin), and C—no readily evident distinguishing marks or features (although some marking and crenulation is still visible around the lower rear margin). Image D shows the situation in which quality images were typically obtained, with a surface feeding shark approaching close to a stationary boat.</p