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Who's Your Daddy?

One of the most baffling and fascinating things about sharks and rays is how diverse their methods of breeding are. Of the 530+ different sharks that scientists know of, every single species has a unique reproductive strategy... Some lay eggs, some give birth to live young... Some feed their unborn though egg-yolks, others via a placenta and some embryos eat all of their siblings in the womb! Some sharks can even give birth to a litter of pups which has multiple different fathers! So which sharks are capable of this "multiple paternity"? And why do they do it?


Female nurse sharks can give birth to a litter with as many as four different fathers - a phenomenon known as "multiple paternity"or "polyandry" (Image Credit: Jakob Owens / Unsplash)

What is Multiple Paternity?

Multiple paternity, also known as "polyandry", is the phenomenon by which one female can give birth to a litter of several young which have multiple different fathers. This happens when a fertile females mates with multiple males over a short period of time and becomes pregnant by multiple fathers at once. This means that the offspring in the litter are only half siblings. Sometimes they can have two different fathers, or it may even be several! Multiple paternity can be found throughout the animal kingdom - in mice, birds and turtles, to name but a few (Byrne & Avise, 2012).


Sharks do not mate for life like penguins or wolves. The males also do not offer nuptual gifts - such as a nest or food - as is seen in many species. Instead, sharks select a different partner each time they are fertile, the pair separates after copulation and polyandry is very common (Byrne & Avise, 2012).


So why do sharks practice multiple paternity? What's in it for them?


Lemon sharks were the first species of Carcharhinids found to practice multiple paternity, but it is now known to happen in several other species (Image Credit: nicolasvoisin44 / Shutterstock)

Spreading Wild Oats

For the male sharks, the advantages of multiple paternity are obvious. Males want to produce offspring wherever possible, so they are driven to mate with a female even if she has already taken another partner. If there is any chance his efforts will yield results, he will take the opportunity, even if he cannot be certain that the entire litter will be his. As the only investment he has to make is to provide his sperm, it is in his best interest to just go for it with as many females as possible. Men! 😉 (Byrne & Avise, 2012)


For the females though, it is a little more complex... Shark mating is quite violent - with the males biting down on the female's flanks and fins as they copulate (see Fifty Shades of White to learn more). So for the female, fighting off a male, or multiple males, could lead to serious injuries or infections. Therefore, some scientists think that a female will decide to allow multiple males to mate with her because there is greater cost to her to try to refuse them. The advantage to her in this situation is to avoid harm. This is known as the "convenience polyandry theory" (Byrne & Avise, 2012).




However, other experts disagree and think that the female has more agency in her choices than this because females make a much larger investment in their offspring compared to the males. Whilst along with the male the female also doesn't care for the newborn offspring (all baby sharks are left by their parents to fend for themselves!), the female must still invest a large amount of time and resources into growing her embryos. Shark pregnancies can be very long - frilled sharks (Chlamydoselachus anguineus) for example, carry their young for 3.5 years (Byrne & Avise, 2012).

Scientists think that multiple paternity in sandbar sharks occurs because of coercive mating - with females yielding to multiple males to avoid injuries (Image Credit: Benjamin Suter / Unsplash)

Growing embryos is also energetically expensive; rather than using her resources to grow stronger herself, she must divert her resources into nourishing her unborn young. Whilst she is pregnant she is also more vulnerable to predators and is not able to produce offspring with a better male if one happens to come along. Therefore, it is advantageous for a female to ensure she only mates with the best male, who is likely to father the healthiest children, so she can get a decent return on her investment (Byrne & Avise, 2012).


In this case, it stands to reason that polyandry might actually be favourable to female sharks and they may actively choose to mate with several males. This will increase her odds of getting (at least one) genetically good father and reduce the likelihood of she has to carry a brood with dud genes. Multiple fathers also mean that her offspring will be more diverse and that at least some of her litter should be able to survive in their unpredictable, ever-changing environment (Byrne & Avise, 2012).




Which Sharks Have Multiple Baby-Daddies?

Experts have discovered multiple paternity exists in many different species of sharks and it is now thought to be very widespread in the shark family tree. Because polyandry is so prevalent across many different groups of sharks, both closely and distantly related, scientists think that the reasons it has evolved may be different for each unique species (Feldheim et al, 2001; Daly-Engel et al, 2006; Byrne & Avise, 2012; Griffiths et al, 2012).


Whilst not common, multiple paternity does occur in tiger sharks (Image Credit: le bouil baptiste / Shutterstock)

For instance, scientists working in California have found that polyandry is very common in the brown smoothhound (Mustelus henlei). Using genetic methods to determine the relatedness of litters of offspring, they discovered that females averaged 2.3 fathers per litter. The researchers theorised that polyandry might be beneficial to these sharks because it allows the female to reduce the probability of being impregnated by a genetically incompatible male (Byrne & Avise, 2012).


Multiple paternity is rare in leopard sharks because living in all-female groups means they are protected from pushy males trying to coerce them into mating (Image Credit: Barbara Ash / Shutterstock)

In nurse sharks (Ginglymostoma cirratum) from Florida, scientists found some litters had as many as four different fathers! The experts believe that the homing behaviours of this species drove the evolution of polyandry. Even if they migrate far away, nurse sharks will always return back to the same locations on a regular schedule (a phenomenon known as "philopatry"). This means they may commonly mingle with close relatives. Therefore, producing genetically diverse offspring via multiple paternity is vital to avoid "genetic bottlenecks" or "inbreeding" (Saville et al, 2002).


So far multiple paternity is more commonly found in "viviparous" sharks (that carry their embryos to term and give birth to live young), but there are also some examples of "oviparous" (egg-laying) species practicing polyandry. For example, researchers have found that as many as 92% of egg clutches laid by small spotted catsharks (Scyliorhinus canicula) are the result of polyandry. Researchers think that these females submit to multiple matings to avoid injuries from males (Byrne & Avise, 2012; Griffiths et al, 2012).


Multiple paternity is common in sharks that give birth to live young, but is also know to happen in sharks that lay eggs, like the smaller spotter catshark (Image Credit: valda butterworth / Shutterstock)

Founding Fathers

Knowing whether different species of sharks practice multiple paternity is important to understand how rapidly their populations grow - in fact it is of critical importance for conservationists hoping to protect endangered species (Chapman et al, 2004).


For example, scientists have found that bonnethead sharks (Sphyrna tiburo) very rarely breed by polyandry. Over 81% of offspring sampled in a study in Florida had only one father per litter (known as "genetic monogamy").

Low levels of multiple paternity in bonnethead sharks means they could be susceptible to genetic bottlenecks (Image Credit: Idealphotographer / Shutterstock)

The females that did have litters with multiple fathers were relatively larger and had more offspring. This means certain individuals are more "fecund" (aka fertile) than others and have relatively higher value for maintaining genetic diversity in the population. So it may be worth prioritising their protection. It also means that this species may be more susceptible to genetic bottlenecks than others, making them more vulnerable to diseases and shifts in environmental conditions, such as climate change (Chapman et al, 2004).



To learn more, you can check out my other articles about shark reproduction.



References

Byrne RJ & Avise JC (2012). Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species. Marine Biology, 159, 749–756. Access online.


Daly-Engel TS, Grubbs RD, Holland KN, Toonen RJ & Bowen BW (2006). Assessment of multiple paternity in single litters from three species of carcharhinid sharks in Hawaii

Environmental Biology of Fishes, 76, 419–424. Access online.


Feldheim KA, Gruber SH, Ashley MV & McEachran JD (2001). Multiple paternity of a lemon shark litter (Chondrichthyes: Carcharhinidae). Copeia, 3, 781–786. Access online.


Griffiths AM, Jacoby DMP, Casane D, McHugh M, Croft DP, Genner MJ & Sims DW (2012). First analysis of multiple paternity in an oviparous shark, the small-spotted catshark (Scyliorhinus canicula L.). Journal of Heredity, 103:2, 166–173. Access online.


Pirog A, Jaquemet A, Soria M & Magalon H (2015). First evidence of multiple paternity in the bull shark (Carcharhinus leucas). Marine and Freshwater Research. Access online.


Saville KJ, Lindley AM, Maries EG, Carrier JC & Pratt, HL Jr. (2002). Multiple paternity in the nurse shark, Ginglymostoma cirratum. Environmental Biology of Fishes, 63: 347–351. Access online.


Whitney NM, Pratt HL & Carrier JC (2004). Group courtship, mating behaviour and siphon sac function in the whitetip reef shark, Triaenodon obesus. Animal Behaviour, 68, 1435–1442. Access online.




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