Population genomics informs conservation and management of the Galapagos shark (Carcharhinus galapagensis) at local, regional and oceanic scales

Pazmiño Jaramillo, Diana Alexandra (2017) Population genomics informs conservation and management of the Galapagos shark (Carcharhinus galapagensis) at local, regional and oceanic scales. PhD thesis, James Cook University.

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Elasmobranchs (sharks and rays) have increasingly experienced human pressures over recent decades, ranging from overfishing to habitat loss. Addressing these pressures is the main challenge for elasmobranch conservation. Specific life-history traits (including slow growth, late maturation, long gestation periods, and small litters) have resulted in high susceptibility to excessive mortality, and have limited their recovery ability. A better understanding of aspects of their biology, population connectivity, habitat use, adaptation and demographic patterns is an important step towards improved management and conservation of elasmobranchs. Yet there is insufficient information to understand the status of almost 50% of elasmobranch species, according to the IUCN Red List of Threatened species. The advent of Next Generation Sequencing (NGS) technologies has seen a transition from conservation genetics to genomics (from gene to genome scales), which is informing our understanding of species and improving conservation outcomes based on these insights. This technology has provided access to thousands of genome-wide markers, collectively capable of providing reliable inferences about demographic patterns and enabling detection of local adaptation. Developing and applying genomics tools to investigate elasmobranch biology and ecology is therefore an important step towards improving their management and conservation.

This thesis focuses on the Galapagos shark (Carcharhinus galapagensis), a species categorized as "Near Threatened" by the IUCN in 2003, with a circumtropical distribution and a preference for isolated oceanic islands in tropical and warm temperate waters. Importantly, information about population structure and connectivity across most of the species' geographic range is lacking, and current knowledge of habitat use and population structure is limited to specific areas. Hence, C. galapagensis is a good elasmobranch case study to apply comprehensive genomics tools to detect stock structure, inter-population connectivity, intra-population self-replenishment and to estimate effective population sizes. Informed by these measures, population status at different geographic scales can be used to prioritize populations in need of improved management. Galapagos sharks also co-occur with a closely related carcharhinid, Carcharhinus obscurus in parts of their respective distribution ranges. Although the Galapagos shark shows some level of site fidelity, there have been reports of individuals traveling long distances (>2,000 km). Despite their ecological importance in ecosystems as high-level predators, limited genetic and genomic resources are available for Galapagos sharks worldwide. Therefore, the main objective of this thesis was to develop genetic and genomic resources for the Galapagos shark, and to use these to confirm species status, identify inter-specific hybridisation if present and investigate population structure at different geographic scales across the Pacific Ocean, in order to inform and improve conservation efforts of the species at local and regional scales.

By sequencing the mitochondrial control region (947bp in length) and developing thousands of genome-wide Single Nucleotide Polymorphisms (SNPs), I was able to detect population structure at a relatively small geographic scale within the Galápagos Islands (Ecuador). While mitochondrial DNA did not identify structure among these Islands, clustering and network analyses using 8,103 neutral SNPs congruently indicated that two well-differentiated stocks exist in the southern Galápagos Marine Reserve - western (Isabela Island) and eastern (San Cristobal and Santa Cruz Islands). Effective population size (Ne) estimation of both populations was relatively low (approximately 200 for each population), highlighting their vulnerability to harvest (including by-catch) and habitat loss. Regional environmental differences across the archipelago or in their behaviors may underlie the observed population structure, but the extent of the influence of these and other factors are still to be investigated. This is the first effort to include genomic tools to assess genetic structure and connectivity of elasmobranchs within the archipelago. Implications of these findings are important for appropriate management of Galapagos sharks in the Galápagos islands, where previous management plans have based conservation strategies on acoustic and satellite tagging information of other species with different ecological characteristics, such as the scalloped hammerhead shark.

The population structure and connectivity of C. galapagensis across the Pacific Ocean using a combination of mtDNA and nuclear genome-wide SNPs for 229 individuals was also examined. At least two genetically discrete geographic groups were delineated by analysing 7,274 neutral SNPs: an East Tropical Pacific (including samples from Mexico and the Galápagos Islands) and a central-west Pacific group (including samples from Hawaii, New Zealand (the Kermadec Islands), Australia (Elizabeth and Middleton Reefs, Lord Howe and Norfolk islands)), along with a few South African samples from the Indian ocean). Additional population structure was suggested using outlier SNPs, potentially under selective pressure, at the within region level, with four putatively adaptive conservation units identified: the west Pacific (Australia and New Zealand), the central Pacific (Hawaii), Mexico and the east Pacific (Galápagos). The identification of management and adaptive units at various spatial scales is particularly important for overharvested large predatory organisms, often characterized by smaller, localized populations. I highlight the importance of including both regional and global scale assessments, as well as the use of putative adaptive loci to accurately inform conservation at different geographic scales.

Finally, aiming to understand the relationship between Galapagos and dusky (Carcharhinus obscurus) sharks, given the debate in the literature regarding their validity as independent species, this thesis addressed the taxonomic status of the Galapagos shark and investigated possible hybridisation between these two shark species. Appropriate taxonomic identification, as well as a comprehensive understanding of hybridisation (if detected) in ecologically important species like sharks, is an important step towards achieving effective long-term conservation goals. With a single documented case of inter-species hybridisation in sharks to date - between the Australian Carcharhinus tilstoni and common C. limbatus (blacktip shark) - hybridisation amongst sharks remains poorly investigated. Morphological similarities between the Galapagos and dusky sharks have previously resulted in misidentifications in areas where they co-occur, indicating the need for appropriate tools to distinguish these species in the first instance. Although a recent study helped define them as valid independent species, no evidence of ongoing hybridisation was found, probably due to small sample sizes from contact zones. Therefore, I proposed that hybridisation and introgression between Galapagos and dusky sharks be examined by sampling more individuals of both species from contact zones (specifically, along the western Mexican coast in the east Pacific), and by using an approach capable of detecting low levels of admixture, such as SNPs. Using empirical analytical approaches and simulations, I first identified a subset of 1,873 highly informative and reliable discriminatory loci for these two species. These discriminatory SNPs were able to identify the extent and direction of hybridisation and introgression between Galapagos and dusky sharks, indicating the presence of four individuals corresponding to various hybrid generations. Given the morphological similarities between these, and other closely related Carcharhinus species leading to mislabelling/misidentification cases, I emphasise the importance of a robust and broad sampling strategy across the Pacific distribution of both species. Furthermore, I highlight the need for a complete phylogenomic study of the whole genus, together with comprehensive quality assessment and data filtering in order to accurately define species relationships and detect rare hybridisation and introgression cases.

Overall, this thesis presents the most comprehensive set of genomic resources for the Galapagos shark to date and results provide important novel insights into the species conservation genetic status across the Pacific Ocean, as well as within regional and local geographic areas. This will better inform what needs and challenges are faced by Galapagos shark populations and will ultimately help inform improved conservation and management efforts of more shark species as well.

Item ID: 52674
Item Type: Thesis (PhD)
Keywords: DArTSeq SNPs, management units, connectivity, Ne, fisheries, Galapagos, marine protected area
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Pazmiño, Diana A., Maes, Gregory E., Simpfendorfer, Colin A., Salinas-de-León, Pelayo, and van Herwerden, Lynne (2017) Genome-wide SNPs reveal low effective population size within confined management units of the highly vagile Galapagos shark (Carcharhinus galapagensis). Conservation Genetics, 18 (5). pp. 1151-1163.

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Date Deposited: 26 Feb 2018 01:06
FoR Codes: 06 BIOLOGICAL SCIENCES > 0604 Genetics > 060411 Population, Ecological and Evolutionary Genetics @ 80%
07 AGRICULTURAL AND VETERINARY SCIENCES > 0704 Fisheries Sciences > 070402 Aquatic Ecosystem Studies and Stock Assessment @ 20%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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