Published 2021
INTRODUCTION
Conspecific non-parental infanticide by males (henceforth, just ‘infanticide’) was a crucial finding in culling the notion that ‘animals behave for the good of the species’ and suggested instead that animal behaviour has evolved in ways which maximise their individual reproductive success (Sapolsky, 2017). This type of infanticide has been observed across a wide range of the animal kingdom and is most commonly documented among the mammalian orders Euarchonta, Rodentia and Carnivora (Breedveld, Folkertsma & Eccard, 2019). Sexual selection is widely accepted as the main driver for its evolution (Ebensperger, 1998) where intra-sexual competition between males for reproductive investment by females can mean killing the offspring of a competing male is advantageous (Hrdy, 1979). In intra-sexual competition, males committing infanticide would be more reproductively successful than males who don’t making infanticide an adaptive behavioural trait which has the potential to have increased in frequency over evolutionary time (Sapolsky, 2017). Where perpetrators consume their victims under resource limited conditions, infanticide can be a mechanism to obtain food (the predation hypothesis) (Ebensperger, 1998) leopards may gave an insight here (Balme & Hunter, 2013). The circumstances of infanticide by pinnipeds is consistent with the argument that infanticide is a maladaptive behaviour (Harano & Kutsukake, 2017), occurring accidentally as a bi-product of aggressive male behaviour (the social pathology hypothesis) (Hrdy, 1979). The social pathology hypothesis is often resorted to when circumstances surrounding infanticide are ambiguous but the evolutionary basis of the behaviour here can be open to argument (Ren et al., 2011). It is also likely that none of the hypotheses for the evolution of infanticide are mutually exclusive (Knörnschild et al., 2011).
THE SEXUAL SELECTION HYPOTHESIS
The Sexual Selection Hypothesis is often considered as the evolutionary basis of infanticide when cases meet the necessary assumptions (Harano & Kutsukake, 2018). These assumptions are firstly, the victim of the infanticide should not be related to the perpetrating male; secondly, the removal of the infant victim should allow the perpetrating male to mate with the mother of said victim; and thirdly, the subsequent mating typically occurs due to the infanticide shortening the inter-birth interval of the victim’s mother (Hrdy, 1979). From these assumptions, it can be concluded that infanticide is an adaptive behaviour because the removal of infants can bring nursing females back into oestrus and allows the perpetrator more time to successfully mate with the females, increasing their own reproductive success and reducing that of their competitors (Sapolsky, 2017). For example, the sexual selection hypothesis is well established in lions (Panthera leo) where repeated cases of infanticide fulfil all of the assumptions to consider sexual selection (Packer & Pusey, 1983). The first cases of infanticide to be documented were in old world monkeys (genus Semnopithecus) (Sugiyama, 1965) and many observations of the behaviour in old world monkeys have since supported the sexual selection hypothesis (Kavana, Erinjery & Singh, 2014). Particularly, in Presbytis entellus, unequivocal DNA evidence has been used to confirm non-relatedness between perpetrators and infanticide victims as well as relatedness between perpetrators and subsequent offspring (Borries et al., 1999). More recently, in wild groups of Trachypithecus leucocephalus, cases strongly suggest that the intent of infanticide by males is to reduce the inter-birth interval of females (Yin et al., 2013).
Social Pathology vs Sexual Selection in Rhinopithecus spp.
On the contrary, some old world monkey species e.g. Rhinopithecus spp. have exhibited cases of infanticide which are ambiguous in support of the sexual selection hypothesis and are instead documented in favour of the social pathology hypothesis (Ren et al., 2011; Yao et al., 2016). The social pathology hypothesis states that infanticide is a maladaptive behaviour resulting from unnatural living conditions inducing high levels of male aggression (Borries et al., 1999). Cases of infanticide in this case may be accidental (Ebensperger, 1998). For example, two incidents of infanticide in Rhinopithecus spp. are ascribed to accident during episodes of male aggression in populations residing in Chinese nature reserves (Ren et al., 2011; Yao et al., 2016). Additionally, it was found that new males established themselves in breeding groups without committing infanticide (Ren et al., 2011) and this is not consistent with the predictions of sexual selection hypothesis (Hrdy, 1979). However, it can be argued that the sexual selection hypothesis for the evolution of infanticide in Rhinopithecus spp. is possible due to the following.
To start with, the first accidental infanticide documented in Rhinopithecus bieti (Ren et al., 2011) could be argued to meet the assumptions to consider sexual selection by Hrdy (1979); the threatening behaviour of the male was towards the non-related infant of a lactating mother, who was previously avoiding him, ultimately resulting in the death of the infant. The infanticide also resulted in the reproductive success of the perpetrating male by means of shortening the inter-birth interval of the victim’s mother, who mated with the male shortly after the infanticide. The second case in Rhinopithecus roxellana (Yao et al., 2016) did not meet the assumptions to consider sexual selection as the preparator did not benefit reproductively from the infanticide. However, the same perpetrator committed a second infanticide seven months later which met the necessary assumptions. There have also been two other cases of infanticide by R. roxellana which fulfil the assumptions to consider the sexual selection hypothesis (Yao et al., 2016).
The lack of infanticide by males in newly establishing breeding groups (Ren et al., 2011) may also be explained by the use of female strategies to avoid infanticide such as voluntary abortion or pseudo oestrus (Hrdy, 1979). One female voluntarily aborted seemingly due to the instability of a male in the breeding group and females have been observed performing sexual behaviours while lactating (Ren et al., 2011). Furthermore, despite R. roxellana being a seasonal breeder, the average inter-birth interval of females is 18-21months (Qi, Li & Ji, 2008; Bao-Ping et al., 2003) and can still be reduced by killing dependant infants (Yao et al., 2016). This means biologically, infanticide can be beneficial in Rhinopithecus spp. which would not be consistent with non-adaptive explanations.
The Rhinopithecus genus is in close relation to Semnopithecus, Presbytis and Trachypithecus (Wang, Zang & Yu, 2013), all of which are documented with significant evidence for the sexual selection hypothesis as explained previously. The identification of independent evolutionary changes by use of phylogenies here may be useful in better understanding the evolution of infanticide amongst Rhinopithecus spp. in relation to the related genus’ (Davies, Krebbs & West, 2011). The Rhinopithecus genus could highlight an area where more research is needed in order to better gage the evolution of infanticide in old world monkeys. It also supports the notion that the hypotheses for the evolution of infanticide may not be mutually exclusive, as suggested by Knornschild et al. (2011).
The Sexual Selection and Predation Hypotheses in Leopards
Leopards (Panthera pardus) are another species which provide evidence that the hypotheses for the evolution of infanticide are not mutually exclusive. Many cases of infanticide by leopards fulfil the assumptions of the sexual selection hypothesis (Harano & Kutsukake, 2018; Balme et al., 2012; Balme & Hunter, 2013). However the repeated occurrence of cannibalism (De Luca & Mpunga, 2018; Henschel, Abernethy & White, 2005) and specifically perpetrators consuming infanticide victims (Balme & Hunter, 2013), means there could also be support for the predation hypothesis, as perpetrators are gaining a nutritional benefit (Hrdy, 1979). It has been suggested that this nutritional benefit is only an addition to the reproductive advantages of committing infanticide in leopards and is unlikely to be the main driver for its evolution (Balme & Hunter, 2013). Equally, the fact that there are both nutritional and reproductive benefits to infanticide in leopards could explain the evolution of its common occurrence, which is more so than any other mammalian carnivore (Balme & Hunter, 2013) and accounting for the majority of cub mortalities (Balme et al., 2012).
CONCLUSION
The sexual selection hypothesis is most widely supported for the evolution of conspecific non-parental infanticide by males in number of taxa including carnivores and primates, specifically in lions, leopards and old world monkeys. Amongst these orders, there are groups in which infanticide does not convincingly support the sexual selection hypothesis such as the Rhinopithecus genus where the social pathology hypothesis is referred to instead. These cases demonstrate how the evolutionary origin of infanticide can be open to argument and highlight an area in which more research could give a better insight into how infanticide evolved in relative taxonomic groups. They also introduce the idea that the proposed hypotheses may not be mutually exclusive in explaining the evolution of infanticide. This is further evident in leopards where there is evidence for both the sexual selection hypothesis and the predation hypothesis. Though sexual selection is likely to be the main drive, the additional benefit from consuming infanticide victims may have contributed to the extant in which infanticide occurs and hence, exerted its evolution in leopards. The debate over the evolution of conspecific non-parental infanticide reflects the difficulty in finding and interpreting undeniable evidence which can explain how animal behaviours may have evolved in light of proposed theories.
REFERENCES
Balme, G.A, Batchelor, A., Britz, N., Seymour, G, Grover, M, Hes, L., Macdonald, D.W. and Hunter, L.T.B, 2012. Reproductive success of female leopards Panthera pardus: the importance of top-down processes. Mammal Review, [e-journal] 43(3), pp.221-237. http://dx.doi.org/10.1111/j.1365-2907.2012.00219.x
Balme, G.A. and Hunter, L.T.B, 2013. Why leopards commit infanticide. Animal Behaviour, [e-journal] 8(4), pp.791-799. http://dx.doi.org/10.1016/j.anbehav.2013.07.019.
Borries, C., 1977. Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis entellus) in Ramnagar (South Nepal). Behavioral Ecology and Sociobiology, [e-journal] 41(3), pp.139-150. http://dx.doi.org/10.1007/s002650050373
Borries, C., Launhardt, K., Epplen, C., Epplen, J.T. and Winkler, P., 1999. DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys. Series B: Biological Sciences (Proceedings on the Royal Society of London), [e-journal] 266(1422), pp.901-904. http://dx.doi.org/10.1098/rspb.1999.0721.
Breedveld, C.L., Folkertsma, R. and Eccard, J.A., 2019. Rodent mothers increase vigilance behaviour when facing infanticide risk. Scientific Reports (Nature Publisher Group), [e-journal] 9, pp.1-10. http://dx.doi.org/10.1038/s41598-019-48459-9.
Davies, N.B., Krebs, J.R. and West S.A., 2011. An Introduction to Behavioural Ecology (4th edition). Oxford: Wiley-Blackwell.
De Luca, D. and Mpunga, N.E., 2018. Leopard abundance, distribution and food habits in the Mt. Rungwe-Kitulo landsape, Southern Tanzania. African Journal of Ecology, [e-journal] 56(2), pp.358-367. http://dx.doi.org/10.1111/aje.12464.
Harano, T. and Kutsukake, N., 2018. The evolution of male infanticide in relation to sexual selection in mammalian carnivores. Evolutionary Ecology, [e-journal] 32(1), pp.1-8. http://dx.doi.org/10.1007/s10682-017-9925-0.
Henschel, P., Abernethy, K.A. and White, L.J.T., 2005. Leopard food habits in the Lopé National Park, Gabon, Central Africa. African Journal of Ecology, [e-journal] 43(1), pp.21-28. http://dx.doi.org/10.1111/j.1365-2028.2004.00518.x.
Hrdy, S.B., 1979. Infanticide Among Animals: A Review, Classification, and Examination of the Implications for the Reproductive Strategies of Females. Ethology and Sociobiology, [e-journal] 1(1), pp.13-40. http://dx.doi.org/10.1016/0162-3095(79)90004-9.
Kavana, T.S, Erinjery, J.J. and Signh, M., 2014. Male Takeover and Infanticide in Nilgiri Langurs Semnopithecus johnii in the Western Ghats, India. Folia Primatological, [e-journal] 85(3), pp.164-177. http://dx.doi.org/10.1159/000362546.
Knörnschild, M., Ueberschaer, K., Helbig, M. and Kalko, E.K.V., 2011. Sexually Selected Infanticide in a Polygynous Bat. PLoS One, [e-journal] 6(9): e25001. http://dx.doi.org/10.1371/journal.pome.0025001.
Packer, C. and Pusey, A.E., 1983. Adaptions of female lions to infanticide by incoming males. The American Naturalist, 121(5), pp.716-728.
Qi, X., Li, B. and Ji, W., 2008. Reproductive Parameters of Wild Female Rhinopithecus roxellana. America Journal of Primatology, [e-journal] 70(4), pp.311-319. http://dx.doi.org/10.1002/ajp.20480.
Ren, B., Li, D., He, X., Qui, J. and Li, M., 2011. Female Resistance to Invading Males Increases Infanticide in Langurs. PLoS ONE, [e-journal] 6(4): e18971. http://dx.doi.org/10.1371/journal.pone.0018971.
Sapolsky, R., 2017. Behave: The Biology of Humans at Out Best and Worst. London: Penguin Random House.
Sugiyama, Y., 1965. On the social change of hanuman langurs (Presbytis entellus) in their natural condition. Primates, [e-journal] 6(3-4), pp.381-418. http://dx.doi.org/10.1007/BF01730356.
Wang, X., Zhang, Y. & Yu, Li., 2013. Summary of phylogeny in subfamily Colobinae (Primate: Cercopithecidae). Chinese Science Bulletin, [e-journal] 58(18), pp.2097-2103. http://dx.doi.org/10.1007/s11434-012-5624-y.
Yao, H., Yu, H., Yang, B., Yang, W., Xu, H., Grueter, C.C., Li, M. and Xiang, Z., 2016. Male Infanticide in the Golden Snub-Nosed Monkey (Rhinopithecus roxellana), a Seasonally Breeding Primate. International Journal of Primatology, 37(2), pp.175-184. http://dx.doi.org/ 10.1007/s10764-016-9892-2.
Yin, L., Jin, T., Watanabe, K, Qin, D., Wang, D. and Pan, W., 2013. Male attacks on infants and infant death during male takeovers in wild white-headed langurs (Trachypithecus leucocephalus). Intergrative Zoology, [e-journal] 8(4), pp.367-377. http://dx.doi.org/10.1111/1749-4877.12022.