Something that has long-baffled scientists about sharks, is how incredibly diverse their reproductive strategies are. Some sharks lay eggs... others give birth to live young... some do something in between. Some sharks have huge litters, some only one pup and others are literally pregnant all of their adult life! Even close relatives can have completely different ways of breeding. And at the centre is an on-going debate about what came first.. Did the first sharks lay eggs or have live births? Which evolved earliest? And why is each shark so different?
There are a myriad of different ways that sharks reproduce and for many species and there are not really two species that breed exactly the same way. This has allowed sharks to evolve into many different evolutionary niches and to breed successfully in many different situations. Rather than different categories, there is more of a continuum of different ways that sharks reproduce and every species is unique. Yet there are some broad terms we can use to describe the different methods:
Oviparity
ōvum (Latin) "egg" + perə (Proto-European) "to bring forth"
Oviparity involves a female shark laying fertile eggs after she has mated with a male. The eggs then develop, before young sharks hatch out. Around 40% of sharks are oviparous. They are mostly small, "benthic" species (that live on or near to the ocean floor), like catsharks, skates, all bullhead sharks and some carpet sharks (Abel & Grubbs, 2020; Ebert et al, 2021; Katona et al, 2023).
The benefits are that this type of reproduction is not too costly to the mother - she does not need to invest a lot of time or energy. These sharks can often breed more regularly compared to live-bearing species (Parsons et al, 2008; Abel & Grubbs, 2020; Ebert et al, 2021).
On the other hand, this means that she also cannot protect the young from predators and mortality rates can be very high. This is especially true in sharks that breed by "immediate oviparity"; where the female only gestates eggs for a short period of time before laying them. Slightly less so in sharks with "delayed oviparity"; where gestation periods are longer and female investment is higher (Parsons et al, 2008; Abel & Grubbs, 2020; Ebert et al, 2021).
Many scientists believe that egg-laying was the ancestral reproductive method for sharks; that is to say it evolved first and then other methods appeared later in evolutionary history (Musick & Ellis 2005; Abel & Grubbs, 2020; Katona et al, 2023).
Ovoviviparity
Also known as "aplacental viviparity" or "yolk sac viviparity"
ōvum "egg" + vividus "to live" (Latin) + perə (Proto-European) "to bring forth"
Between egg-laying and live young, there are sharks which do a bit of both; hatching eggs internally to then give birth to live young. Around 40% of sharks are ovoviviparous, including dogfish, angel, frilled, gulper, sleeper and cow sharks, and also torpedo rays, guitarfish and wedgefish (Parsons et al, 2008; Abel & Grubbs, 2020; Ebert et al, 2021).
In ovoviviparous reproduction, the egg hatches internally and then the young are nourished in different ways, depending on the species. In some sharks, the embryos simply continue to absorb yolk. This is known as "lecithotrophy" (Greek - lecithin "the fat found in egg yolk" + trophos "feeder") (Parsons et al, 2008; Abel & Grubbs, 2020; Ebert et al, 2021).
For some species the cost to the mother is higher. In great white sharks (Carcharodon carcharias) and their relatives for instance, the mother keeps producing eggs throughout the whole pregnancy, which the developing embryos eat! This is known as "oophagy" (Greek - oon "egg" + phagos "to eat"). It requires energy from the mother to feed the young in this way (Parsons et al, 2008; Abel & Grubbs, 2020; Ebert et al, 2021).
The sandtiger shark (Carcharias taurus) goes one step further and after the young have chomped their way through the other eggs, they move on to eat their live brothers and sisters for nourishment! This is known as "intrauterine cannibalism" (to learn more, you can check out Shark Tartare) (Abel & Grubbs, 2020; Ebert et al, 2021).
In other species the cost to the mother is even higher. For example, smoothhounds (Family Triakidae) and dogfish like the Greenland shark (Somniosus microcephalus), feed their young by secreting a protein- and fat-rich fluid from the lining of the uteri. The pups can absorb this nutritious liquid through their gills or their mouths to help them grow. This is known as "histotrophy" (Greek - histo "body tissue" + phagos "to eat") (Parsons et al, 2008; Abel & Grubbs, 2020; Ebert et al, 2021).
Tiger sharks (Galeocerdo cuvier) boast a completely unique strategy. After the yolk has been depleted, the embryos switch to feeding on a nutritious fluid that is held within intrauterine sacs. This is known as embryotrophy and cannot be found in any other species of shark. But it’s very productive. A female can produce a litter ranging from 45 to 60 pups from one pregnancy and each pup will see as much as a 1000% weight gain throughout the pregnancy. This is one of the highest increases of body mass for a developing embryo found in any species of shark (Castro et al, 2016).
The benefit of ovovivipary is that the pups are protected inside the female for a longer period compared to ovipary and the cost to the mother is still relatively low compared to vivipary (Ebert et al, 2021).
Viviparity
Also known as "placental viviparity"
vividus (Latin) "to live" + perə (Proto-European) "to bring forth"
Finally, around 18% of sharks give birth to live young which must be nourished by connection directly to the mother after thay have absorbed their egg yolk. Mostly belonging to the Order Carcharhiniformes (ground sharks), including the bull shark (Carcharius leucas), weasel sharks (Family Hemigalaidae) and the hammerheads (Family Sphyrnidae), but placental viviparity can also be found in the Orectolobiformes (carpet sharks) (Parsons et al, 2008; Ebert et al, 2021).
Live-bearing is especially associated with sharks that live in shallow regions and also those that are found in "pelagic" habitats (far off shore away from land) (Katona et al, 2023).
In these sharks, after the yolk is depleted, the egg case morphs into a "yolk stalk", which glues itself to the uterus wall. Whilst similar, this is not like the ambolical cord in humans, as it does not connect to the mother's blood stream. Instead, the pups are nourished through the a "yolk stalk placenta", hence the name "placental viviparity" (Parsons et al, 2008; Ebert et al, 2021).
Viviparity is very costly to the mother because she has to invest a lot of time and her own energy into nourishing her young as they grow. Some sharks can be pregnant for years and require a long recovery period before they can breed again. On the other hand, the pups are born big and strong, so they have a very high chance of survival, which makes the investment worth it (Ebert et al, 2021).
What Came First?
Scientists always thought that viviparity arose recently in the evolutionary history of sharks. However, some scientists have argued that, in fact, having live young was the ancestral reproductive method for sharks, and egg-laying arose later on. They have suggested that egg-laying evolved recently, as it allowed small-bodied species to produce more young more rapidly, but that subsequently, some larger sharks then reverted back to the ancestral form of live-birth (Abel & Grubbs, 2020; Ebert et al, 2021; Katona et al, 2023).
If we look at the shark family tree (known as a "phylogenetic tree"), we can see that giving birth to live young (via ovoviviparity or true viviparity) is the most dominant method, with 60% of sharks breeding this way (Musick & Ellis 2005; Abel & Grubbs, 2020).
If we are to believe that egg-laying came first, we would expect to see this type of reproduction in the oldest species of sharks. However, this is not the case! the "Hexanchiformes" (six-gills and cow sharks) are thought to be one of the oldest evolutionary lineages of sharks, around for as long as 190 million years, yet they are viviparous. The same pattern can also be found in the phylogenetic tress for rays (aka "Batoids"). Whatsmore, if we consider fossils of ancient species of extinct sharks, we find carpet sharks ("Orectolobiformes") that gave birth to live young! So, this reproductive method has been around for a long time! This suggests that the ancestral form of reproduction was live birth and egg laying came later (Musick & Ellis 2005; Abel & Grubbs, 2020).
On the other hand, there are many scientists that argue that egg-laying came first and birthing live young evolved more recently. They argue that because some of the most ancient known species of sharks, like Cladoselache, were egg-layers, that this is proof that at one time, all sharks and their ancestors were oviparous. Also, as the modern bullhead sharks (Order "Heterodontiformes") are most closely related to the ancient "Hybodont" sharks, which lived around 240 million years ago, and they all lay eggs, many think it is just logical that egg-laying came first (Abel & Grubbs, 2020).
We may never know the answer for sure... But it's a pretty exciting mystery to try to unravel! But one thing is for certain, the myriad of different ways that sharks reproduce is truly amazing!
To learn more about ancient sharks you can check out The Good, The Bad and The Ugly and I Will Survive!
References
Abel DC & Grubbs RD (2020). Shark Biology and Conservation: Essentials for Educators, Students, and Enthusiasts. Johns Hopkins University Press, Canada. IBAN: 9781421438368.
Castro JI, Sato K & Bodine AB (2016). A novel mode of embryonic nutrition in the tiger shark, Galeocerdo cuvier. Marine Biology Research, 12:2, 200-205. Access online.
Ebert DA, Dando M& Fowler S (2021). Sharks of the World: A Complete Guide, Second Edition. Princeton University Press: UK. IBAN: 978-0-691-20599-1.
Katona G, Szabó F, Végvári Z, Székely Jr T, Liker A, Freckleton RP, Vági B & Székely, T. (2023). Evolution of reproductive modes in sharks and rays. Journal of Evolutionary Biology. Access online.
Musick JA & Ellis JK (2005). Reproductive evolution of chondrichthyans. In: Hamlett W (Ed.), Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids, and Chimaeras, 45–79. Science Publishers, Plymouth, UK. Access online.
Nakaya K, White W & Ho H (2020). Discovery of a new mode of oviparous reproduction in sharks and its evolutionary implications. Scientific Reports, 10:1. Access online.
Parsons GR, Hoffmayer ER, Hendon JM, Bet-Sayad WV, Rocha MJ, Arukwe A & Kapoor BG (2008). A review of shark reproductive ecology: life history and evolutionary implications. Fish reproduction, 1, 435-469. Access online.
By Sophie A. Maycock for SharkSpeak
