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

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Understanding the microevolution of the shortfin mako shark

An EU-funded project examined how external pressures impact on the genetic diversity and long-term resilience of the iconic marine predator, the shortfin mako.

Known for its acrobatic hunting abilities and for being the world’s fastest shark, the shortfin mako (Isurus oxyrinchus) can reach top speeds of up to 74 km per hour. While a skilful swimmer, it has not been able to outswim the threat of extinction and is currently listed as an endangered species by the International Union for Conservation of Nature’s red list of threatened species and included in Appendix II of the CITES convention. “Sharks are quite vulnerable to exploitation and climate change. Shortfin mako, in particular, are commercially exploited throughout their distribution range, and in some cases the population appears to be under severe pressure,” explains Romina Henriques, Marie Skłodowska-Curie Actions (MSCA) fellow. Declines in population abundance can impact on genetic diversity levels and therefore the evolutionary potential of a species in the long term. “In the case of shortfin mako, little is known about their genetic history and ecological effects on their population. In the DiMaS project, with the support of the MSCA programme, we set out to understand the long-term changes in the population history of this species,” notes Einar Eg Nielsen, a professor at the Technical University of Denmark.

Looking to the past to understand the future

To achieve this, DiMaS employed a retrospective genomics approach. The team used historical and contemporary jaw, vertebrae and tissue samples to investigate changes in population connectivity, genetic diversity and population size in the last 200 years. “To truly understand the effect that external pressures, such as fishing, have on the evolutionary history of shortfin mako, it is necessary to obtain samples that pre-date the establishment of increased exploitation,” adds Henriques. The oldest sample collected in the project was from 1790 and the most recent from 2018. The researchers employed a target-enriched sequencing approach to minimise possible DNA contamination from other sources. They then generated a panel of molecular markers specific to the Lamniformes (white shark, shortfin mako shark and sandtiger shark) to assess contemporary population structure, as well as historical changes in connectivity patterns, genetic diversity levels and effective population sizes. “We had samples from major regions, including the north-western and north-eastern Atlantic, the Mediterranean Sea, the south-western and south-eastern Atlantic, the south-western and south-eastern Indian Ocean, and the south-western and north-eastern Pacific Ocean,” says Henriques.

Key insights

“Interestingly, our results suggest shifts in historical connectivity among populations of shortfin mako. The levels of gene flow among regions have not remained constant through time,” confirms Henriques. Results also suggest that this species, previously considered as having a single population, might be composed by discrete population units within each basin. However, connectivity remains high. One of the main aspects of DiMaS was to also assess if the reported population declines in shortfin mako were accompanied by declines in genetic diversity. “This was not proved with the data generated. Although this might give us reason to be cautiously optimistic, it might also result from the fact that shortfin mako is a relatively long-lived shark, and thus the pressures on the population have not had enough time to lead to declines in genetic diversity,” reports Henriques. Looking to the future, the population connectivity results can help inform sustainable fishing management policies for shortfin mako, as these generally have a geographical backing. “I believe this is one of the major impacts that DiMaS will have. Now, we will finish some of the data analyses to statistically evaluate changes in population connectivity through time,” concludes Henriques.

Keywords

DiMaS, shortfin mako, genetic diversity, population connectivity, population history, retrospective genomics approach, evolutionary history

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