Semelparity: the great parental sacrifice

By Tamara Claire Fernandez

Being a parent is not easy, but being a semelparous parent is deadly. In contrast to iteroparity with its multiple reproductive cycles, semelparity is a reproductive strategy where species have a single reproductive cycle ending in death (Young, 2010). Also known as ‘suicide reproduction’, this approach is employed by several animal species including insects, arachnids, fish and some peculiar insectivorous marsupials. Despite the obvious sacrifices involved, semelparity has evolved and persisted in these animals due to its high pay-off in terms of offspring numbers and survival. The question ecologists have grappled with is: in what scenarios would a one-off reproduction event confer greater fecundity to individuals than multiple reproductive cycles?

It is believed that many animal species which undergo this extreme reproductive event often have lower mortality rates as juveniles than as adults (Young, 2010). This theory has origins in the 1970s, where ecologists classified species into r- or k-strategists. While k-strategist populations have a “high carrying capacity (K) which is achieved by slow development, a large body size, delayed reproduction, iteroparity, and a long lifespan”, r-strategist populations have high intrinsic growth rates (r), where individuals undergo “rapid development, a small body size, early reproduction, semelparity, and a short lifespan” (Jeschke et al., 2019). The fast life history of r-strategists makes semelparity a viable option, as reproductively mature adults are uncertain of their survival for future rounds of reproduction. This gives rise to an “all-or-nothing” mentality, where adults would rather expend all their energy for a chance at producing offspring, than die without doing so. A notable study of 52 species by Fisher et al. (2013) found that as insectivorous marsupials moved to habitats of higher latitudes, prey abundance becomes more seasonal. This in turn motivated females to shorten annual breeding seasons to ensure that peak prey abundance coincides with maternal weaning, forcing males to compete ferociously for a chance to mate. Combined with the uncertainty of each male’s survival to the next year, this explains the emergence of lethal male reproductive competition (Fisher et al., 2013). Though one cannot know for certain if semelparity arose from rapid juvenile development, short species lifespans and seasonal environmental conditions, these are probable factors in the evolution of such an extreme reproductive strategy. 

A key benefit of being semelparous is the sheer quantity of offspring that can be generated when all of an organism’s resources are focused on reproduction. To illustrate, semelparous species like the American eel (Anguilla rostrata) can lay up to 8.5 million eggs in one go (Wenner & Musick, 1975), while parasitic insects of the order Strepsiptera produce up to 750,000 larvae each (Kathirithamby, 2009). Without a need to hold back on reserves for future survival, parents are willing to become oocyte factories to optimise offspring numbers and survival. 

Besides egg and sperm production, some parents go the extra step to spend their final days protecting their young from predation. After a more than 3000 km journey to spawning grounds (Eiler et al., 2014), exhausted Chinook Salmon (Oncorhynchus tshawytscha) mothers still muster the energy to guard their spawning “nests” in hopes of increasing the odds of their young’s survival (Connor et al., 2018). Even more extreme is the practice of matriphagy, where mothers are eaten by their offspring. For instance, the crab spider (Australomisidia ergandros) is consumed by her offspring from the inside out until only its exoskeleton remains, providing food and nourishment to its young (Evans et al., 1995). An additional perk of matriphagy in this brutal species is that it reduces sibling cannibalism, therefore increasing offspring survival (Evans et al., 1995). Interestingly, matriphagy also serves as a checkpoint for semelparity. Specifically, some species along the semelparous-iteroparous spectrum like the Black lace-weaver spider (Amaurobius ferox) produce a second clutch of eggs if matriphagy does not occur (Kim & Horel, 2010). This ensures that the mother only dies for a worthy cause – in this case, that her offspring are guaranteed to be well-nourished and likely to survive to adulthood. These efforts all add up to maximise fitness, explaining the existence and success of semelparous species.

Though matriphagy paints semelparous mothers as the losers in this reproductive game, there are female-specific advantages as well. As an example, the Dusky Antechinus (Antechinus swainsonii) has a three-week long mating marathon which leaves males lifeless (Fisher & Blomberg, 2011). During the mating season, males enter a crazed state with high corticosteroid (stress hormone) levels but low concentrations of glucocorticoid-binding protein, leading to extreme stress arising from a lack of negative feedback (Boonstra, 2005). This leads to immunosuppression (Harshman & Zera, 2007) which, when combined with extreme exertion, fat loss, and muscle loss, often culminates in death (Handwerk, 2013). Meanwhile, despite being left alone with the lactation and childcare, females benefit immensely through promiscuous mating with several males and letting the best sperm win. This allows them to rear the fittest possible offspring, as only males with the best endurance, largest testes and optimal sperm quality get to father their young (Handwerk, 2013). In addition, this has wider benefits for the population as a whole, as in such a frenzy, there is no time to carefully select a partner. Such random mating in panmictic populations maximises genetic diversity faster than in monandrous ones (Beveridge & Simmons, 2006).

Parenthood is not for the faint-hearted, and that is certainly the case for the semelparous. However, these species often have the best shot at reproduction using this “live fast, die young” strategy. The theories surrounding why and how fatal reproduction occurs are still a work in progress, but it is clearly working for some species. To further understand the evolution and fitness benefits of semelparity, long-term life history studies are required. In particular, it could be useful to study anomalous semelparous species who do not fit the description of an r-strategist, yet adopt this plan of action anyway.

References:

Beveridge, M. & Simmons, L.W. (2006) Panmixia: an example from Dawson’s burrowing bee (Amegilla dawsoni) (Hymenoptera: Anthophorini). Molecular Ecology. 15 (4), 951–957. Available from: doi:10.1111/j.1365-294x.2006.02846.x

Boonstra, R. (2005) Equipped for Life: The Adaptive Role of the Stress Axis in Male Mammals. Journal of Mammalogy. 86 (2), 236–247. Available from: https://www.jstor.org/stable/4094341?seq=1 [Accessed: 27th October 2020].

Connor, W.P., Tiffan, K.F., Chandler, J.A., Rondorf, D.W., Arnsberg, B.D. & Anderson, K.C. (2018) Upstream Migration and Spawning Success of Chinook Salmon in a Highly Developed, Seasonally Warm River System. Reviews in Fisheries Science & Aquaculture. 27 (1), 1–50. Available from: doi:10.1080/23308249.2018.1477736

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Fisher, D.O., Dickman, C.R., Jones, M.E. & Blomberg, S.P. (2013) Sperm competition drives the evolution of suicidal reproduction in mammals. Proceedings of the National Academy of Sciences. 110 (44), 17910–17914. Available from: doi:10.1073/pnas.1310691110

Handwerk, B. (8 October 2013) Why Some Animals Mate Themselves to Death. National Geographic. Available from: https://www.nationalgeographic.com/news/2013/10/131007-marsupials-mammals-sex-mating-science-animals/ [Accessed: 27th October 2020].

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Kim, K.-W. & Horel, A. (2010) Matriphagy in the Spider Amaurobius ferox (Araneidae, Amaurobiidae): an Example of Mother-Offspring Interactions. Ethology. 104 (12), 1021–1037. Available from: doi:10.1111/j.1439-0310.1998.tb00050.x

Wenner, C.A. & Musick, J.A. (1975). Food habits and seasonal abundance of the American eel, Anguilla rostrata, from the lower Chesapeake Bay. Chesapeake Science. 16, 62–66. Available from: https://link.springer.com/article/10.2307%2F1351085#citeas [Accessed: 27th October 2020].

Young, T. P. (2010) Semelparity and Iteroparity. Nature Education Knowledge. 3 (10), 2. Available from: https://www.nature.com/scitable/knowledge/library/semelparity-and-iteroparity-13260334/ [Accessed: 26 October 2020].

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