Key points
- White sharks exhibit stark differences between the DNA in their nuclei and the DNA in their mitochondria. Until now, scientists have pointed to the migration patterns of great whites to explain these differences.
- Scientists tested this theory in a new study by analyzing genetic differences between global white shark populations. In doing so, they discovered that great whites were restricted to a single population in the Indo-Pacific Ocean at the end of the last ice age 10,000 years ago and have since expanded to their current global distribution.
- The results also invalidate the migration theory, but an alternative explanation remains elusive.
White sharks (Carcharodon carcharias) almost went bottom-up during the last ice age, when sea levels were much lower than they are today and sharks had to get by with less space. The most recent cold snap ended about 10,000 years ago, and the planet has been gradually warming ever since. As temperatures increased, glaciers melted, and sea levels rose, which was good news for great whites.
Results of a study published in the journal Proceedings of the National Academy of Sciences show that white sharks had been reduced to a single, well-mixed population somewhere in the southern Indo-Pacific Ocean. White sharks began genetically diverging about 7,000 years ago, suggesting that they had broken up into two or more isolated populations by this time.
This is new information but not particularly surprising. There are never many white sharks around even at the best of times, as befits their status at the top of the tapered food chain, where a lack of elbow room limits their numbers. Today, there are three genetically distinct white shark populations: one in the southern hemisphere around Australia and South Africa, one in the northern Atlantic and another in the northern Pacific. Though widespread, the number of white sharks still remains low.
"There are probably about 20,000 individuals globally," said study co-author Gavin Naylor , director of the Florida Program for Shark Research at the Florida Museum of Natural History. "There are more fruit flies in any given city than there are great white sharks in the entire world."
Organisms with small populations can be pushed dangerously close to the edge of extinction when times are tough. Mile-high glaciers extended from the poles and locked away so much water that by 25,000 years ago, sea levels had plunged by about 40 meters (131 feet) , eliminating habitat and restricting great whites to an oceanic corral.
But something happened to great whites during their big comeback that remains as much of a mystery now as it was when it was first discovered more than 20 years ago. The primary motivation for this study was to lay out a definitive explanation, but despite using one of the largest genetic datasets on white sharks ever compiled, things did not go quite according to plan.
"The honest scientific answer is we have no idea," Naylor said.
Female great white sharks wander off for years to feed but come back home to breed
Scientists first got a whiff of something strange in 2001, when a research team published a paper that opened with the line, "… information about … great white sharks has been difficult to acquire, not least because of the rarity and huge size of this fish."
The authors of that study compared genetic samples taken from dozens of sharks in Australia, New Zealand and South Africa. They found that though the DNA produced and stored in the nuclei of their cells were mostly the same between individuals, the mitochondrial DNA of sharks from South Africa were distinctly different from those in Australia and New Zealand.
The seemingly obvious explanation was that great whites tend to stick together and rarely make forays into neighboring groups. Over time, unique genetic mutations would have accumulated in each group, which, if it went on long enough, would result in the formation of new species.
This would explain the observed differences in their mitochondrial DNA but not why the nuclear DNA was virtually identical among all three populations. To account for that, the authors suggested that male sharks traveled vast distances throughout the year, but females either never traveled far, or if they did, they most often came back to the same place during the breeding season, a type of migration pattern called philopatry.
This idea was based on the fact that nuclear and mitochondrial DNA are not inherited in equal proportion in plants and animals. The DNA inside nuclei is passed down by both parents to their offspring, but only one — most often the female — contributes mitochondria to the next generation. This is a holdover from the days when mitochondria were free-living bacteria, before they were unceremoniously engulfed and repurposed by the ancestor of eukaryotes.
This was a good guess and had the added benefit of later turning out to be mostly accurate . Male and female great whites do travel large distances in search of food throughout the year, and females consistently make the return journey before it's time to mate.
Thus, the nuclear DNA of great whites should have less variation, because itinerant males go around mixing things up, while the mitochondrial DNA in different populations should be distinct because philopatric females ensure all the unique differences stay in one place. This has remained the favored explanation for the last two decades, one that seemed to fit like a well-worn glove. Except, no one ever got around to actually putting it on to test its size. This is primarily because the data needed to do so was hard to get for the same reasons mentioned in the touchstone study: There aren't many great white sharks, and when researchers do manage to find one, taking a DNA sample without losing any appendages in the process can be tricky business.
Shark migration cannot explain nuclear and mitochondrial discordance, so what can?
Naylor and his colleagues began collecting the necessary data back in 2012. "I wanted to get a white shark nuclear genome established to explore its molecular properties," he said. "White sharks have some very peculiar attributes, and we had about 40 or 50 samples that I thought we could use to design probes to look at their population structure."
Over the next few years, they also sequenced DNA from about 150 white shark mitochondrial genomes, which are smaller and less expensive to assemble than their nuclear counterparts. The samples came from all over the world, including the Atlantic, Pacific and Indian oceans.
When they compared the two types of DNA, they found the same pattern as the one discovered in 2001. At the population level, white sharks in the North Atlantic rarely mixed with those from the South Atlantic. The same was true of sharks in the Pacific and Indian oceans. At a molecular level, the nuclear DNA among all white sharks remained fairly consistent, while the mitochondrial DNA showed a surprising amount of variation.
The researchers were aware of the philopatric theory and ran a few tests to see if it held up, first by looking specifically at the nuclear DNA. If the act of returning to the same place to mate really were the cause of the strange mitochondrial patterns, some small signal of that should also show up in the nuclear DNA, of which females contribute half to their offspring.
"But that wasn't reflected in the nuclear data at all," Naylor said.
Next, they concocted a sophisticated test for the mitochondrial genomes. To do this, they first had to reconstruct the recent evolutionary history of white sharks, which is how they discovered the single southern population they'd been reduced to during the last ice age.
"They were really few and far between when sea levels were lowest. Then the population increased and moved northward as the ice melted. We suspect they remained in those northern waters because they found a reliable food source," Naylor said. Specifically, they encountered seals, which are a dietary staple among white sharks and one of the main reasons why they have such a strong fidelity to specific locations.
"These white sharks come along, get a nice blubbery sausage. They fatten up, they breed, and then they move off around the ocean."
Knowing when the sharks split up was key, as each group would have begun genetically diverging from each other at this time. All the researchers had to do was determine whether the 10,000 years between now and the last ice age would have been enough time for the mitochondrial DNA to have accumulated the number of differences observed in the data if philopatry was the primary culprit.
They ran a simulation to find the answer, which came back negative. Philopatry is undoubtedly a behavioral pattern among great whites, but it was not responsible for the large mitochondrial schism.
So Naylor and his colleagues went back to the drawing board to figure out what sort of evolutionary force could account for the differences.
"I came up with the idea that sex ratios might be different — that just a few females were contributing to the populations from one generation to the next," Naylor said. This type of reproductive skew can be observed in a variety of organisms, including meerkats, cichlid fish and many types of social insects.
But yet another test showed that reproductive skew did not apply to white sharks.
There is a third, albeit less likely, option the team members said they can't rule out at this stage, namely that natural selection is responsible for the differences. The reason why this is far-fetched has to do with the relative strength of evolutionary forces. Natural selection — the idea that the organisms best suited to leave behind offspring will, in fact, generally be the ones that have the most offspring — is always active, but it has the strongest effect in large populations. Smaller populations, in contrast, are more susceptible to something called genetic drift, in which random traits — even harmful ones — have a much higher chance of being passed down to the next generation.
Florida panthers, for example, are highly endangered, with only a few hundred individuals left in the wild. Most of them have a kink at the end of their tail, likely inherited from a single ancestor. In a large population, subject primarily to natural selection, this trait would have either remained uncommon or disappeared entirely over time. But in a small population, a single cat with a kinked tail can change the world purely by chance through the auspices of genetic drift.
By way of comparison, gravity exerts a force at all scales of matter and energy, but it is by far the weakest of the four fundamental physical forces. At the scale of planets and stars, gravity can hold solar systems and galaxies together, but it has very little influence on the shape or interactions of atoms, which are governed by the three stronger but more localized forces, such as electromagnetism.
According to the study's results, genetic drift cannot explain the differences between mitochondria in great whites. Because it is a completely random process, it cannot selectively target one type of DNA and spare another. If it were the culprit, similar changes would also be evident in the nuclear DNA.
This leaves natural selection as the only other possibility, which seems unlikely because of the small population sizes among white sharks. If it is the causative agent, Naylor said, the selective force "would have to be brutally lethal."
If you collect enough mass in a concentrated space, say on the order of a black hole, the otherwise benign force of gravity becomes powerful enough to devour light.
If natural selection is at play in this case, it would manifest itself in a similarly powerful way. Any deviation from the mitochondrial DNA sequence most common in a given population would likely be fatal, thus ensuring it was not passed on to the next generation.
But this is far from certain, and Naylor has his doubts about the validity of such a conclusion. For now, scientists are left with an open-ended question that can only be resolved with further study.
Additional co-authors of the study are: Romuald Laso-Jadart, Elise Gaya, Pierre Lesturgie and Stefano Mona of the Muséum National d'Histoire Naturelle; Shannon L. Corrigan, Lei Yang and Adrian Lee of the Florida Museum of Natural History; Olivier Fedrigo of the The Rockefeller University; Christopher Lowe and Kady Lyons of California State University Long Beach; Greg Skomal of the University of Massachusetts Dartmouth; Geremy Cliff of the University of KwaZulu-Natal; Mauricio Hoyos Padilla of Pelagios-Kakunjá Marine Conservation; Charlie Huveneers of Flinders University; Keiichi Sato of the Okinawa Churaumi Aquarium; and James Glancy of the British Museum of Natural History.
