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Retrospective genomic analyses of shortfin Mako shark (Isurus oxyrinchus) using DNA from archived jaws

Periodic Reporting for period 1 - DiMaS (Retrospective genomic analyses of shortfin Mako shark (Isurus oxyrinchus) using DNA from archived jaws)

Reporting period: 2019-11-15 to 2021-11-14

The project DiMaS focused on evaluating long-term changes in population connectivity and genetic diversity of the endangered shortfin mako shark (Isurus oxyrinchus) throughout its distribution range. Shortfin mako is a migratory top predator, with a world-wide distribution in the tropical and warm-temperate oceans. The species is currently targeted commercially throughout its distribution, both directly and as by-catch from longline fisheries. Intense exploitation coupled with inadequate catch-and-landing statistics, led to a worldwide population decline, with shortifin mako currently listed as Endangered by the IUCN’s Red List of Threatened Species, and included in Appendix II of the CITES convention. In particular, recent declines in abundance have been observed in the Northeast Atlantic where catch rates have declined by 50%, or more, due to 10-fold under-reporting of catches.

Declines in population abundance can have repercussions on genetic diversity levels, and consequently in the long-term evolutionary potential of a species. However, little is known regarding the evolutionary history of shortfin mako, as previous molecular studies have employed a small number of molecular markers and focused on contemporary samples only. Temporal genetic data can, thus, provide information on population range shifts, fluctuations in population size and direct adaptive genetic changes in response to exploitation, allowing inferences to be drawn regarding the evolutionary history of shortfin mako.

In this context, DiMaS employed a retrospective genomics approach making use of historical samples archived in national and regional museums, national fishery institutes and personal collections, as well as contemporary samples obtained from fishery institutes, throughout the species’ distribution range, to investigate if reported declines had impacted its genetic diversity and evolutionary history. Using a novel exome-targeted sequencing approach, genome-wide markers were generated for 471 samples, spanning all oceans and time periods from 1790 – 2018. Our aims were to assess spatio-temporal population sub-structuring, estimate long-term genetic diversity levels and effective population size and understand the most likely mechanisms and processes influencing the evolutionary history of shorting mako through time and space.

Overall, the results generated in DiMaS suggest a complex evolutionary history of this species. Analyses of spatio-temporal patterns of genetic diversity did not reveal significant losses of genetic diversity in line with an increase in exploitation pressures (from 1980 onwards). In addition, weak signals of break in gene flow are reported between individuals caught in the Northwest Atlantic (USA), Southwest Atlantic (Brazil), South Africa, New Zealand and Eastern Pacific (Gulf of California). This differentiation patterns were not constant through time, and point to a complex migratory behaviour. Our findings suggest that gene flow and genetic drift as the most likely micro-evolutionary mechanisms shaping the evolutionary history of shortfin mako, and this project leaves many doors open to understand the complex evolutionary history of this endangered shark.
The sampling effort for DiMaS took place between 2018 and 2019, and targeted 16 Museums, 14 Fishery Institutes, one University and 10 Private Collections, covering the entire distribution range of shortfin mako. In total, we obtained 945 samples spanning three centuries. We then selected the best quality samples (including those with the largest volume of metadata - year of birth, catch location, sex, etc.) to process in the laboratory and generate genomic data from. We employed a bait capture approach, where we designed 20 000 baits (120bp sequences of DNA) to increase the yield of targeted shortfin mako DNA, as historical samples generally have lower DNA concentrations, fragmented DNA and are often contaminated by other sources of exogenous DNA (bacteria, fungi, human, etc.). A total of 471 samples were prepared at DTU Aqua Silkeborg, and sequenced at the genomic facilities of the University of Queensland.

Analyses of the obtained genomic data followed a custom-designed pipeline, and a total of 11 297 linked and 2 900 unlinked molecular markers (Single Nucleotide Polymorphisms - SNPs) were obtained for 330 individuals. These markers were then used to estimate genetic diversity, patterns of population connectivity and assess the evolutionary history of shortfin mako. Analyses were performed for the overall species (all samples) and per collection (regional and temporal). In the latter case, samples were divided into regions and decade of catch, to assess the possibility of shifts in distribution ranges and genetic diversity levels through space and time. Obtained results suggest a complex meta-population structure for shortfin mako with at least five putative populations observed: Northwest Atlantic (USA), Southwest Atlantic (Brazil), South Africa, New Zealand and Eastern Pacific (Gulf of California). No declines of heterozygosity were observed through time, with levels remaining relatively stable from 1790 to 2018.

These results, once peer-reviewed, can greatly aid in the establishment of sustainable management and conservation strategies for shortfin mako throughout its distribution, and will be reported to relevant stakeholders, including the International Council for the Exploration of the Seas Working Group on Elasmobranch Fishes (ICES-WGEF), the Benguela Current Commission, the International Council for the Conservation of Atlantic Tunas (ICCAT) and the Indian Ocean Tuna Commission (IOTC).
From a conservation perspective, migratory marine species such as shortfin mako can occupy both coastal and oceanic environments and are thus subjected to different types of pressures throughout their range (e.g. degradation of nursery, breeding/puping grounds and offshore fishing activities). In addition, they tend to transverse international boundaries making it difficult to establish meaningful conservation plans. Long-lived, late-maturing species such as shortfin mako are of particular conservation concern, as their life history features result in relatively small effective population sizes, low reproductive potential (and thus replenishing capacity) and high natural mortality at early life stages, making them especially vulnerable to anthropogenic pressures. This innate vulnerability is further compounded when the species are targeted by fishing, either directly or as by-catch. Accurate knowledge of population structure is thus fundamental if we are to successfully preserve this iconic species.

The findings of DiMaS revealed previously unknown spatio-temporal population sub-structuring patterns in shortfin mako. Furthermore, our results highlight a dynamic population connectivity through time, but still identified local populations particularly in the northwestern Atlantic, the southwestern Atlantic and the northeastern Pacific. These findings have strong implications for the management of this highly migratory species, and thus may aid in the establishment of more accurate (and country-specific) management plans for this valuable species. Conserving marine biodiversity, and top predators in particular, is crucial to ensure the long-term health of marine ecosystems. Therefore, our findings have the potential to assist in conserving this iconic marine predator.
Shortfin mako shark jaws. Port Elizabeth Museum, South Africa, 2018. Photo by Gary I Stafford