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Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Infanticide as Sexual Conflict: Coevolution of Male Strategies and Female Counterstrategies Ryne A. Palombit Department of Anthropology, Center for Human Evolutionary Studies, Rutgers University, New Brunswick, New Jersey 08901 Correspondence: [email protected] One of the earliest recognized forms of sexual conflict was infanticide by males, which imposes serious costs on female reproductive success. Here I review two bodies of evidence addressing coevolved strategies of males and females. The original sexual selection hy- pothesis arguing that infanticide improves male mating success by accelerating the return of females to fertilizable condition has been generally supported in some taxa—notably, some primates, carnivores, rodents, and cetaceans—but not in other taxa. One result of recent research has been to implicate other selective benefits of infanticide by males in various taxa from insects to birds to mammals, such as acquisition of breeding status or improvement of the female breeding condition. In some cases, however, the adaptive sig- nificance of male infanticide remains obscure. The second body of data I review is arguably the most important result of recent research: clarifying the possible female counterstrategies to infanticide. These potential counterstrategies span diverse biological systems, ranging from sexual behavior (e.g., polyandrous mating), to physiology (e.g., the Bruce effect), to individual behavior (e.g., maternal aggression), to social strategies (e.g., association with coalitionary defenders of either sex). Although much remains to be studied, these current data provide compelling evidence of sexually antagonistic coevolution surrounding the phenomenon of infanticide. t its most elemental level, infanticide is the and Hausfater 1984, p. xv). These definitions Akilling of a newborn individual by a conspe- highlight the heterogeneous and variable nature cific. With the growing appreciation of its bio- of the phenomenon, which can be perpetrated logical significance, however, infanticide came by either sex, by parents or other kin, by indi- to be defined more broadly as any “behavior viduals unrelated to the victim, in a wide variety that makes a direct and significant contribution of social and mating systems, under a range of to the immediate death of an embryo or newly seasonal or aseasonal breeding regimes, and hatched or born member of the performer’s across diverse taxa straddling vertebrates and own species” (Mock 1984, p. 4) or “any form invertebrates. of lethal curtailment of parental investment in One adaptive form of infanticide—the kill- offspring brought about by conspecifics” (Hrdy ing of infants by unrelated males—is arguably Editors: William R. Rice and Sergey Gavrilets Additional Perspectives on The Genetics and Biology of Sexual Conflict available at www.cshperspectives.org Copyright # 2015 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a017640 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a017640 1 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press R.A. Palombit the archetype of sexual conflict. In 450 BCE, animals as well as additional data from pri- Herodotus not only documented the behavior mates. among Egyptian cats, but explained it as a male “trick” to obtain sexual access to females other- Sexual Selection Hypothesis wise preoccupied with maternal duties (Delibes et al. 2012). Among the myriad ideas inaugurat- Although male infanticide clearly has no uni- ing sociobiology in the 1970s, the hypothesis tary explanation, the biological relevance of in- that infanticide is a male strategy that improves trasexual selection in males makes the sexual reproductive success at the expense of female selection hypothesis a good starting point for fitness (Hrdy 1974) constituted one of the first discussion. As originally formulated for langurs demonstrations of the “battle of the sexes” the- (Semnopithecus entellus), Hrdy’s (1974, 1977) ory developed by Williams (1966) and Trivers argument is that the killing of an infant pre- (1972). Partly because of the controversy sur- maturely ends lactational amenorrhea (the ces- rounding the appearance of this hypothesis sation of ovulatory cycles during nursing) in (Rees 2009), however, subsequent research fo- its mother, thereby significantly advancing the cused more on male strategy than on the other time when she is available for subsequent fer- party in this sexual dialectic, the female. Thus, tilization by the perpetrator. The potential ben- field and laboratory research has helped to es- efit of this strategy to male fitness will depend tablish its many forms and conditional occur- on many variables, but salient among them is rence, describe its distribution across taxa, and the degree to which sexual access to fecund fe- clarify its adaptive significance, but it is only males is limited by two factors: male–male relatively recently that female counterstrategies competition and the reproductive life history have become the subjects of rigorous study, even of females. though their potential importance was grasped The latter of these factors provides a useful early on (Hrdy 1979). context for analyzing the problem of male in- In this article, I review selected aspects of fanticide. The L/G ratio, which compares the this body of data and analysis. My focus is durations of lactation and gestation, summariz- on nonparental male infanticide targeting de- es the potential value (to males) and vulnera- pendent young—in mammals, nursing individ- bility (to females) of infanticide in mammals. uals—as opposed to older, weaned offspring, When lactation greatly exceeds gestation, post- the killing of which is variably rendered “juve- partum mating and early pregnancy impose nilicide,” “pedicide,” or “filicide” (e.g., Agora- potentially prohibitive costs on females in the moorthy and Mohnot 1988; Palombit 2014, in form of simultaneous support of two sets of press). offspring differing in ages, requirements, and competitive capacities (van Schaik 2000b). The adaptive solution to this female problem is lactational amenorrhea, which, however, gen- THE SEXUAL CONFLICT OF INFANTICIDE: erates the reproductive problem for males that MALE STRATEGIES infanticide can solve. Plainly expressed: An in- Several functional hypotheses have been pro- fant is a “perfect contraceptive,” and infanticide posed to explain male infanticide. Foremost simply serves to remove this effect (Altmann among them historically is the sexual selection et al. 1978, p. 1029). hypothesis. I consider this hypothesis first, with The taxonomic distribution of sexually se- special, although not exclusive, taxonomic fo- lected infanticide across mammals is not fully cus on the group of animals that originally gen- resolved, but current reports of infanticide erated the hypothesis—the primates. I then whose patterning is consistent with this hy- move on to several alternative hypotheses for pothesis are predictably concentrated among male infanticide, the discussion of which will taxa with relatively long L/G ratios— namely, incorporate consideration of data from other primates, fissiped carnivores, and odontocete 2 Cite this article as Cold Spring Harb Perspect Biol 2015;7:a017640 Downloaded from http://cshperspectives.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Infanticide as Sexual Conflict whales (Fig. 1) (van Schaik 2000b). Several ca- Schaik and Janson 2000; Ebensperger and veats warrant mention. First, this result does Blumstein 2007; Palombit 2012), but some not mean that male infanticide is uniformly general patterns can be highlighted. The largest expressed within these taxa; on the contrary, body of data supporting this hypothesis has there is often considerable variation over time come from study of the nonhuman primates. and across populations (see below). Second, it is In the last 25 years, the number of species in also not the case that male infanticide is un- which infanticide had been observed directly reported in other taxa with lower L/Gratios, or inferred from substantive indirect evidence but in those cases the sexually selected mecha- in the wild has risen from a dozen (Hiraiwa- nism has been less implicated than alternative Hasegawa 1988) to 54, including 84 distinct hypotheses (see below). Finally, L/G ratios are populations distributed across nine of the 14 important, but other factors mayexplain the rar- families of strepsirrhines, monkeys, and apes ity of infanticide in some mammals, for exam- (updated from Palombit 2012). ple, ecologically determined sexual segregation, The circumstances surrounding infanticide (KunzandEbensperger1999),caching ofinfants in primates are typically (although not invari- as an antipredator strategy (Schu¨lke 2005), need ably) consistent with the sexual selection hy- for hibernation (Thalmann 2001), or even phy- pothesis: (1) replacement of a male occupying logenetic inertia (Ebensperger 2001). the position of sole or dominant breeder in the It is not possible here to review comprehen- group by a male who is unlikely to have sired the sively the empirical tests of the sexual selec- infants he subsequently attacks; (2) resumption tion hypothesis (see Hausfater and Hrdy 1984; of ovulatory cycling by the mother; and (3) Parmigiani et al. 1994; Connor et al. 2000;

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