03/12/2021

It’s Time To Rethink Shark Sex—With Females In Mind

16:42 minutes

two smallish white sharks head to tail, murky under the water
Sand tiger sharks mating at the Georgia Aquarium. Credit: Georgia Aquarium

Sharks, rays, and skates—all fish in the subclass Elasmobranchii—are a beautifully diverse collection of animals. One big way they differ is in how they reproduce. They lay eggs, like traditional fish, and let them mature in a select corner of the ocean. Or, they might let the eggs hatch inside their bodies. But they can also give live birth to pups gestated like mammals: with an umbilical cord and a placenta in a uterus.

It doesn’t end there. These fish, like many other members of the animal kingdom, have two uteruses. Females are capable of reproducing asexually, without help from a male. As genetic sequencing has advanced, researchers have been finding another curious pattern: Many litters of pups will have more than one father, a phenomenon known as multiple paternity.

Evolutionary ecologists seeking to explain why sharks would use this strategy of multiple paternity have hypothesized it’s one of convenience for females. In species with aggressive and competitive mating practices, like many sharks and rays, it’s possible females find it saves them precious resources to acquiesce to multiple males.

But what if there’s something in it for the female, and her likelihood of having successful, biologically fit offspring? That’s the question a team of researchers sought to answer in new research published in Molecular Ecology this month, where they asked what kinds of physiological mechanisms a female shark or ray might use to wield agency in her own reproduction. The researchers also write that a male-dominated field may be more likely to miss a female-driven reproductive strategy, and push for more study of female reproductive biology. 

John Dankosky talks to the lead author on the research, Georgia Aquarium shark biologist Kady Lyons, about the vast wonderland of reproductive strategies in this fish subclass—and what a history of male-centered research may have missed.


Further Reading

  • Read more about reexamining gender biases in mating research in sharks and rays.
  • Check out the full study on an “inconvenient tooth.”

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Segment Guests

Kady Lyons

Kady Lyons is a research scientist at The Georgia Aquarium in Atlanta.

Segment Transcript

JOHN DANKOSKY: This is Science Friday. I’m John Dankosky. Next, we’re going to talk about baby sharks. And as a bonus, we’re not going to play that song for you. But we are going to tell you about some things you might not know about baby sharks and their relatives, baby rays.

First of all, did you know they’re called pups? Yeah, they’re born in litters, just like dogs or cats. Pretty cute, right? And it often takes a long time to grow them. Most female sharks are pregnant for at least a year, though sometimes as long as three years. And yeah, that’s the other thing, many sharks and rays gestate mammal-style, with umbilical cords, placentas, and uteruses. And yes, that’s uteruses plural.

We’re going to spend the next few minutes talking about these and other shark reproduction wonders with my next guest, Dr. Kady Lyons. She’s a research scientist at the Georgia Aquarium in Atlanta, and lead author on new research looking at one very specific reproductive mystery, which we will hear all about. Welcome, Kady, to Science Friday. Thanks so much for being here.

KADY LYONS: Thank you for having me. It’s such a pleasure.

JOHN DANKOSKY: So Kady, to get started, before we get to this new research that you’ve just published, everything I just talked about is pretty cool to think about, but maybe you can start by telling us what else sharks and rays have going on reproductively.

KADY LYONS: Oh my goodness, so many things. So I am going to bias this conversation a little bit towards the gestating animals. So moms are pregnant, just like you would see somebody on the street. We’ll be a little biased against the egg layers, but they’re really cool, too. So we have a range of these reproductive characteristics.

So females can gestate, and just basically lay an egg in their body and not provide any extra nutrition, and we have all the way to the other end of the spectrum, where females will continuously ovulate eggs, and those babies can eat those eggs like you would have eggs for breakfast every morning, all the way to intrauterine cannibalism, where it is a literal Hunger Games inside the female’s body, where siblings eat each other, and the ones who make it are the ones who make it.

JOHN DANKOSKY: So hold it– talk about a little bit more about that. I mean, that sounds both incredibly frightening but also probably efficient, right? If you are eating all your brothers and sisters, you’re probably coming out pretty strong.

KADY LYONS: That’s what we would assume would happen, is those genes from that particular embryo are the ones that are going to make it out into the greater population. So it’s incredibly energetic, of course, for both mom, but it limits the number of offspring that she can produce. So if she’s not going to be able to produce many offspring, that’s going to limit her overall reproductive fitness.

So the whole goal of biology, the meaning of life isn’t 42, it is to pass on your genes. And so if she has less opportunities to do that, that could have some important consequences. So she’s going to want to make sure that those offspring are as fit and ready to go as they can be. There can be up to 300 pups for a mature whale shark, but you can have a single pup, like in a cownose ray. They only have one pup per litter.

JOHN DANKOSKY: As I mentioned early on, two uteruses? Tell us more about that.

KADY LYONS: Yeah, so it’s actually fairly common across the animal world, but they have two, a left and a right. They can have pups in both. There are some species that have a completely vestigial uterus. So they have two, but they only really use one. So they have all kinds of cool things going on.

JOHN DANKOSKY: And some sharks can reproduce asexually, too.

KADY LYONS: That’s right, yeah. So a lot of these things were observed in aquaria, actually, because we’re keeping animals here, and oftentimes, it’s more convenient to have a single-sex group. Females tend to be a little more chill and not as frisky as the males. And what was noticed is that, in a lot of species that lay eggs, that there’s no male in there, and then there’d be these little embryos developing. And like, what’s happening here? So it does seem that there is a whole other complex reproductive mode going on, too, where a female, maybe if she doesn’t have access to that sperm, and she’s like, well, I’ve got to pass my genes on one way or another, so we’re going to find a way to do that.

JOHN DANKOSKY: All right, well let’s get back to something you just said. You talked about the males being frisky. From what we understand, the mating process for sharks and rays is pretty aggressive. Maybe we can just talk about that piece of it first.

KADY LYONS: Yeah, absolutely. So as everyone probably knows, sharks don’t have hands, so manipulating things is going to be a little difficult. But they do have teeth. And those teeth can be very sharp. So you have males that will grasp onto females. So a lot of times when people are observing mating behavior, or not observing it directly, but you can look at those scars on females as a cue of, oh, maybe this is around when mating season is, because we see these open wounds. But in addition, males are known for being fairly aggressive, and to gang up on females in groups. So that can be a little overwhelming, as you might imagine, for a female shark or ray.

JOHN DANKOSKY: All right, so this gets us to your research, which just appeared in the journal Molecular Ecology. There’s this phenomenon, as we talked about, where sharks and rays will have litters, but with multiple sires or fathers. So tell us a little bit more about that, and how this plays into the research that you’re doing.

KADY LYONS: So it’s been going on for decades that people started looking into this. You have a litter of pups, and it’s like, oh, let’s just do some genetic testing. We kept finding that multiple paternity or having multiple fathers in a single litter is actually more of the norm than it is the exception. Some explanations for that, though, tend to be very male-biased.

And that gets back to some of that mating behavior that we talked about, where you have very frisky males that might gang up on females. And so it’s not hard to see why a female might be mated multiple times with different males, and that we can wash our hands of that explanation as, yeah, sure, that makes sense. But for our paper, we wanted to flip the other side of that coin because there is a whole suite of physiological mechanisms that females are going through to actually bring that egg all the way up to a completely developed embryo that is fully functional and ready to go.

JOHN DANKOSKY: You’re looking at this from the female shark’s perspective, whereas most research has looked in the past at male sharks not just being the aggressor, but also as the driver of this multiple paternity.

KADY LYONS: More or less, yeah. There has been some casual nods to females, but because those explanations are a lot harder to empirically demonstrate than the de facto explanation of late is just, oh, well, it’s because it’s convenient for females just to acquiesce and let the males have their way with her. And so we were saying, hold on, she is investing a ton of energy into producing these babies. Why would she not have a stake in that? Why wouldn’t she have a say in who’s going to get to fertilize her eggs?

JOHN DANKOSKY: All right, so what did you find?

KADY LYONS: Some really cool stuff, actually. We set up a few hypotheses, both from the male and female perspective. And essentially, what we demonstrate is that there is an equally plausible explanation that these observances of multiple paternity or having those multiple fathers in a single litter can be by female drivers. And then we go on to talk about all the cool ways that females might potentially be able to do that based on other literature, all the way from fruit flies up to complex mammals like us.

JOHN DANKOSKY: What are some of these cool ways that the female sharks are controlling their own reproduction?

KADY LYONS: These are just hypotheses. So we hypothesize that this might be happening, and very much advocate for a whole other field of research to really look into this to demonstrate that those are happening. But some of those ways can be through sperm storage. So I’m sure some people have heard of sperm competition, where it’s like the fastest swimmer gets to the egg, and everything’s hunky dory for that little sperm. But that all occurs in the female body. And she can actually manipulate those fluids to change the way that that sperm can move. So that’s been demonstrated in other animals. So if she can alter that swimming, she’s going to be able to alter who is going to be able to access her eggs.

Some other things that we hypothesize is that she might be able to regulate when she ovulates. So if she can ovulate over a long period of time, maybe if she mates with another male down the line, then she can replace that other sperm from the first male with sperm from the second male. So again, these are all hypotheses that we propose that people should look into. But they could be plausible explanations.

JOHN DANKOSKY: When you talk about sperm storage, we just talked recently on the program about how bees do this. Queen bees will mate, a lot of times, very early on, and store sperm for sometimes a very long period of time. Is it similar? Do we know how long female sharks store sperm after mating?

KADY LYONS: We’re not sure exactly, except that there are some species where it’s purported to happen for perhaps up to a year. So definitely a huge area of research that would be great. And a lot of that has been hypothesized in species that are more oceanic. So they might not encounter mates very often. So it’s thought, OK, well, maybe she has some mechanisms to store sperm on board for when she needs it. And perhaps she could alter who gets to survive within her body and who doesn’t. We don’t really know, but there’s just a ton of even just basic anatomy that I think hasn’t really been properly addressed and giving females their full due.

JOHN DANKOSKY: And for the species that have placentas, there’s a way to selectively direct resources to different embryos, to essentially say, here’s where we want our body’s resources to go.

KADY LYONS: Oh, that’s so exciting. Yeah, so a lot of research about that has been done in mammals. We actually don’t know a whole lot about that in sharks. And that’s kind of the next paper that I’m hoping to work on, is taking that to the next level to say, OK, is mom able to actually control that? Because when you think about it, mom has little parasites in her body, and those little parasites, those embryos, they’re going to want to maximize their resources, but that isn’t necessarily in the benefit of the female if she’s too weak to reproduce another season. That doesn’t benefit her fitness. So that intrauterine competition between mom and pup I think is going to be fantastic to really dig into further.

JOHN DANKOSKY: Why does it matter so much which parent has agency in reproduction? Why is this so interesting to you?

KADY LYONS: Well, again, I’m a little female-biased, and that’s probably because I would identify as a feminist. So I’m going to bring my own biases to the table. But I think all researchers, whether they know about it or not, are going to have some bias that they come with. But I find this reproductive aspect so interesting because, as humans, we’re rather boring. We have essentially one way that we do it. And sharks and rays have evolved numerous different ways on providing the supplemental nutrition. And so my interest is, well, how, and who does it benefit, and how are they able to do this?

Studying these mating systems is important because males and females have different prerogatives of what is going to increase their fitness. And so for males, it behooves them to mate with as many females as possible. Females, on the other hand, are limited because they have a certain amount of space and a certain amount of resources they can put into the production of young.

So mating with more males, to a certain point, is not going to benefit them because, if they are only going to ovulate five eggs, they’re only going to ovulate five eggs. And so for them, that cost then becomes mating with a low-quality male or a concept called genomic incompatibility. And that basically is where not every sperm is going to be able to fertilize every egg. So for a female, if she is mating with a genetically incompatible male, that actually has a real cost to her because she’s limited in how many young she can produce.

JOHN DANKOSKY: I’m John Dankosky, and this is Science Friday from WNYC Studios. And we’re talking with Dr. Kady Lyons. She’s a research scientist at the Georgia Aquarium in Atlanta. We talked about asexual reproduction before. Would there be reasons, you think, for a female shark to find it advantageous to essentially clone herself, even if she has access to sperm from a male?

KADY LYONS: Yeah. And there’s some new research by one of my colleagues, actually, that’s looking at that. So they artificially inseminated bamboo sharks. And they found that, even when females had access to sperm, some of them still chose– sure, at a lower rate, but asexual reproduction still happened. So we’re not exactly sure why, but it could be maybe a female is able to say that this sperm isn’t compatible with me, and I know I’m compatible with me, so I’m not going to waste my energies. We just don’t know, but that could be a reason.

JOHN DANKOSKY: You’ve said a lot here that these are hypotheses that need to be tested. So what’s missing right now from the research?

KADY LYONS: I think we need to completely delve into female reproductive biology from, like, a mechanistic standpoint. And part of this is just it’s very difficult to study sharks and rays. They’re caught in the wild. You don’t know where they’re going to be. And sometimes they’re hard to keep in human care. So there’s all these things that we really don’t know from a microscopic level. And so I think changing that narrative, and once we can look through that female lens, I really hope that that’s going to open up a lot of research. But we really just need to start using sharks and rays as model species. And that hasn’t really been done a whole lot because of their difficulty in caring for them.

JOHN DANKOSKY: Does it help us understand evolution, in some way?

KADY LYONS: Absolutely. I mean, considering that sharks and rays have been around for millions and millions of years, that’s given plenty of time for different lineages to go their own way and figure out what seems to be working for them. I think that there is going to be a lot of interplay between physiology and ecology. And that would be another exciting avenue to pursue this research, to say, well, when is it advantageous to do this type of reproduction in this particular environment or in this social context? So I think there’s definitely a larger picture that we can look at to start to understand why this particular thing would be beneficial in this particular scenario.

JOHN DANKOSKY: One thing that you have noted in your research and in our conversation here is an awful lot of the theories that we have in ecology have come from male scientists in the past. I guess I’m wondering how much you think about how that has colored the way in which we think about something like shark reproduction.

KADY LYONS: Yeah, and I think that it has, in a way. And part of that has to do with things that get ingrained. So Darwin is the father of evolutionary biology and a lot of modern science. And it’s fantastic, but there was literally hundreds of years where only male voices were being heard, and female voices and females’ perspectives were not.

And so we’re leaving out of these important things that might not occur to men. Everyone’s perspective is going to change the way or alter the way that they look and approach a particular problem. So if we can have a more holistic inclusion, I think that’s going to make for richer science, and that’s going to help us uncover things that maybe we didn’t even think about because it was in the dark, and our spotlight was only on this other corner.

JOHN DANKOSKY: Unfortunately, that’s all the time we have. Thanks so much to my guest, Dr. Kady Lyons, research scientist at the Georgia Aquarium in Atlanta. Thanks so much for joining me today, Kady.

KADY LYONS: Thank you. This has been a delight.

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About Christie Taylor

Christie Taylor is a producer for Science Friday. Her day involves diligent research, too many phone calls for an introvert, and asking scientists if they have any audio of that narwhal heartbeat.

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John Dankosky is a contributing editor with Science Friday, and occasional guest host. He also works with public radio collaboratives, and hosts “Steady Habits”—a podcast of the digital news service, The Connecticut Mirror.

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