First-ever chromosome-level genome sequences completed for sharks

The first chromosome level genome sequences for great hammerhead and shortfin mako sharks have shown that both species have experienced major population declines over a 250,000-year history. Low genetic diversity and signs of inbreeding are concerning for Critically Endangered great hammerhead sharks, whose overfished populations have plummeted. With higher levels of genetic diversity, shortfin mako sharks may be more resilient to environmental change; that is, if the current fishing pressure on them is substantially reduced.

With their whole genomes deciphered at high resolution we have a much better window into the evolutionary history of these endangered species."

Mahmood Shivji, Ph.D., Professor at Nova Southeastern University's (NSU) Halmos College of Arts and Sciences and Director of the Save Our Seas Foundation Shark Research Center and NSU's Guy Harvey Research Institute

It's a startling image that describes a milestone in conservation science for sharks. Shivji, Michael Stanhope, Ph.D., from Cornell University's College of Veterinary Medicine and their collaborators have glanced back in history by sequencing to chromosome level the genomes (entire genetic blueprint) of great hammerhead and shortfin mako sharks. Their DNA timeline shows that their populations have declined substantially over 250,000 years. What the scientists have also found is worrying: great hammerhead sharks have low genetic variation, which makes them less resilient to adapting to our rapidly changing world. The species also shows signs of inbreeding, an issue that can lower the ability of its populations to survive.

The shortfin mako shark, however, showed higher diversity and limited inbreeding, a hopeful glint in the gloomy conservation climate. Understanding change over such a large timescale can put into context the current conservation status of these endangered animals. The results can help direct us towards much more nuanced management strategies for sharks.

The research paper, Genomes of Endangered Great Hammerhead and Shortfin Mako Sharks Reveal Historic Population Declines and High Levels of Inbreeding in Great Hammerhead, has been published in iScience:

This research was led by Stanhope and Shivji, with collaborators from Cornell University, NSU, Temple University, Governors State University and the San Diego Zoo Wildlife Alliance.

The scientists acquired and assembled entire genome sequences for great hammerhead and shortfin mako sharks and compared their genomes with genome information available for the whale shark, white shark, brownbanded bamboo shark and cloudy catshark. Their methods read like complex puzzle-building by scientific sleuths: successively assembling from tiny fragments of DNA different sequences like a great patchwork tapestry that details the blueprint of life. Reaching chromosome level represents the latest in high-quality whole genome sequence research - and a tricky feat to achieve for species like sharks that have enormous genomes.

They found that great hammerhead sharks have a high probability of inheriting two copies of the same DNA sequence (homozygosity), including various genes, from their parents.

"To understand why this might be undesirable, you can think about it in terms of disease," said Shivji . "You need two copies of the gene to express certain recessive diseases: one from your mother and one from your father. If you are homozygous for a trait, you have inherited the same gene sequence from both your mother and father, and the trait will be expressed".

In the case of great hammerhead sharks, showing what the scientists dub "high runs of homozygosity" in their genome means that large sections of their genome were homozygous, increasing the chances of expressing undesirable traits. By contrast, if one inherits two different sequence forms (alleles) of a gene from the mother and the father (i.e., heterozygosity), the effects of the recessive allele can be masked by the dominant allele. If an undesirable trait is recessive in this heterozygous state, it will not be expressed. Shortfin mako sharks had lower runs of homozygosity relative to great hammerheads, a genetic windfall that may stand them in better stead to adapt to change.

The application of advancing techniques comes amidst bleak reports for sharks and rays.

"Technical advances in the study of genomes mean that DNA sequencing approaches are much more powerful and efficient now", said Stanhope. "We can apply these new technologies to gain insights about the organism, information that we hope can be leveraged to protect sharks and rays".

While we don't know exactly the effects of inbreeding in sharks, findings from wolves and cheetahs show that problematic traits can creep in over time. The result is often lowered survival of the species.

The picture for great hammerhead sharks - overfished and traded for their fins – is worrying. But without these critical genetic insights, we would be unable to modify how their vulnerable populations are currently managed.

The researchers are cautious about overstating results.

"Genetics has advanced such that chromosomal level genomes are the expectation for a reference quality genome for species however, conservation research presents its own challenges to achieving this consistently and at the resolution expected in other fields," said Shivji. "Obtaining tissue samples from endangered marine vertebrates is a major hurdle. You can assemble the genome with a single tissue sample from a single shark, but the ideal circumstance would be to sequence genomes from multiple individuals from different parts of their ocean range, an ethically difficult and costly endeavor."

Indeed, the researchers state this as a limitation of their current study. The ethical limitations to working with endangered species means that conservation geneticists must balance the latest advances with respect for the fragile populations they study. In addition to revealing the genetic diversity and fragile status of two endangered shark species, the researchers hope that their results will provide what they term reference-quality genomes, from which future foundational science can build to improve what we know about sharks. Certainly, as new possibilities arise, our insights into the blueprint of sharks will help strengthen the way we understand these ecologically important species and conserve their vulnerable populations.

Source:
Journal reference:

Stanhope, M.J., et al. (2022) Genomes of endangered great hammerhead and shortfin mako sharks reveal historic population declines and high levels of inbreeding in great hammerhead. iScience. doi.org/10.1016/j.isci.2022.105815.

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