“Quite possibly, readers ten years from now may take for granted the occurrence of infanticide in various animal species,” Glenn Hausfater and I rashly conjectured back in 1984, in a preface to the first book on this subject, “and [they] may even be unaware of the controversies and occasionally heated debate that have marked the last decade of research on this topic…”. For biologists, that projection turned out to be more or less accurate. For those with backgrounds in the social sciences, perhaps especially in my own field of anthropology, it was wildly optimistic.

Most animal behaviorists now take for granted that the killing of infants by conspecifics can be found throughout the natural world and that, for many primate species, the arrival in their group of unrelated males represents a threat to infant survival. Many anthropologists, however, remain skeptical of the proposition that a propensity to attack infants born to unfamiliar females evolved in non-human primate males because it increased their chances to breed. This would require accepting that a behavior obviously detrimental to the survival of the group or even the species could evolve in males through Darwinian sexual selection because it provided the killers with a reproductive edge in their competition with rival males.

Introduction

Female competition, especially female reproductive competition, is likely to play an important role in shaping the social systems of all mammals (Altmann 1997; Gowaty 1997b; Hrdy 1981). While this competition can often be subtle, it also can lead to what is perhaps the most extreme form of reproductive competition: infanticide.

The chapters in this volume focus primarily, if not exclusively, on the phenomenon of infanticide by males and how it may be influencing the evolution of social systems. Generally, threats from conspecific males intensify under a specific context: the presence of an unrelated male, often following immigration into an established group (e.g., Hrdy 1974). But females and their young also face threats from conspecific females, including both unfamiliar intruders and fellow group mates. The threat of infanticide by females is likely to be taxonomically more widespread and, for group-living females, potentially a more constant threat than other forms of infanticide.

The purpose of this chapter is to examine the phenomenon of infanticide by females other than the mother (hereafter “infanticide by females”) in a variety of mammalian taxa. How similar is this behavior to infanticide by unrelated males? What makes infants vulnerable to attack from female conspecifics, and what are the contexts in which female attacks on infants occur?

Introduction

Infants have the strongest incentive to avoid infanticide. Paradoxically, they are the least capable of preventing it. Primate infants are particularly vulnerable because they take a long time to develop the physical and cognitive capacity to avoid risk. Yet infants are not utterly helpless in the face of infanticidal threats. Through detection, avoidance and deterrence, infants and their caregivers prevent infanticide. If infanticide is treated as a series of steps preceding lethal injury, one can see several junctures at which animals can act to lower risk (Figure 10.1). Protectors can prevent infanticide at every step. Neonate self-protection is generally limited to the earliest steps in the process. An older infant may have more options.

In this chapter, I explore the behaviors used by primates to prevent infanticide. I begin with protectors and then turn to infant self-protection. In both sections, I search for evidence of specific adaptations to infanticide prevention. The final section specifically addresses infant transport and the coevolution of primate mothers and infants.

Protectors

Primate infants are cared for by a variety of individuals: mothers, fathers, older siblings, more distant kin, as well as some unrelated adults (Hrdy 1976; Nicolson 1987; Whitten 1987; Manson 1999; Paul 1999). Within groups, the sexes usually take different roles in infant protection. A common pattern is for females to perform direct care (e.g., transport, feeding) while males provide indirect care (e.g., guarding).

Introduction

We simultaneously know more about the proximate causes of infanticide in rodents and less about its adaptive consequences and evolution than in any other taxon. Rodents are the largest mammalian order with over 440 genera and 2021 of the 4629 described species (Musser & Carleton 1993; Wilson & Reeder 1993). Infanticide by either or both males and females may be found in 46 species from 22 genera in 3 rodent groups (see below). A number of previous reviews illustrate the detailed understanding of proximate causation, development, and function gained by studying infanticide in rodents (Sherman 1981; Brooks 1984; Elwood & Ostermeyer 1984; Huck 1984; Labov 1984; Svare et al. 1984; vom Saal 1984; Labov et al. 1985; Trulio 1987; Elwood 1992; Elwood & Kennedy 1994; Ebensperger 1998a). In this review, I take a slightly different approach to study the evolution of infanticide in rodents. I first use the taxonomic distribution of infanticide by males and infanticide by females along with available phylogenetic evidence to parsimoniously reconstruct the evolution of infanticide by males, infanticide by females, and a potential female response to infanticide by males – male-induced pregnancy termination (Bruce effects; Bruce 1960). Then, using these evolutionary reconstructions, I test specific functional hypotheses about infanticide.

A thumbnail sketch of infanticide in rodents

Rodents provide some of the richest information about infanticide because studies of the proximate causation of infanticide are integrated with studies designed to document ultimate function.

Introduction

It has often been noted that female primates tend to have extended mating periods in their ovarian cycles, tend to mate polyandrously and also tend to mate during pregnancy (cf. Hrdy 1979; Hrdy & Whitten 1987). Since females in species vulnerable to infanticide show these features to a greater extent, this behavior was interpreted as serving to confuse paternity (cf. van Schaik et al. 1999; van Noordwijk & van Schaik, Chapter 14). The extent to which such mating tactics succeed in confusing paternity depends on the outcome of an “arms race” between males and females concerning the amount of information on paternity available to males. In order to examine more closely the claim that sexual behavior in primates serves at least in part to reduce infanticide risk, we must examine the physiological basis for paternity confusion, as well as for its complement, paternity concentration. Since ovarian cycles vary considerably in detail among taxa (e.g., Short 1984), we limit this examination to primates, the best-known order in this respect. We ask therefore how the ovarian cycles of female primates are organized in relation to the need for strategies to reduce infanticide risk. Two features are examined in particular which we will argue are related to the benefits to females of unpredictability in the timing of ovulation: (1) the large variance in the length of the preovulatory or follicular phase both within and between individuals, and (2) interspecific variation in the mean length of the follicular phase.

Introduction

Sexual selection theory suggests that divergent reproductive interests of the sexes impede the evolution of enduring social bonds between males and females. Males are more likely to increase reproductive success by acquiring multiple mates whereas females enhance fitness more by discriminative choice of individual mate(s) (Darwin 1871; Trivers 1972). Consequently, insofar as postcopulatory bonds limit a male's sexual access to additional fertile females and are irrelevant to antecedent female mate choice, such bonds should be relatively rare. The mostly polygynous mammals, for example, fulfill this expectation: male mating effort generally exceeds paternal effort, and affiliative interactions between the sexes center on the period of copulation or female fertility (Clutton-Brock 1989b).

And yet, males and non-fertile or anestrous females maintain stable relationships with one another in some species. The same theoretical framework that predicts the rarity of persistent heterosexual bonds also highlights a primary context for their evolution: when a male restricts his mating to a single female, a postcopulatory relationship with her is not only less costly to him, but may also offer fitness advantages to both parties. The proposed benefit to the female is the extensive parental care she receives from a male that is now certain of paternity. Thus durable male–female relationships were originally viewed as part of a coevolved suite of behaviors including monogamy, biparental care, and, in gregarious animals, “nuclear families” of parents and offspring (Morris 1967; Wittenberger & Tilson 1980; Gubernick 1994). The primarily monogamous, biparental birds have long served as vivid examples of this system (Lack 1968).

Introduction

Emelina was a great beauty. She was proud, passionate and extremely ambitious. She forced all of the men who asked for her to their knees and only gave herself to the one who had money and power. She had three children. One day a prince galloped into the village on a golden horse. His face had the beauty of a god. He had a generous heart and a noble character. It is said that the man drove the whole village crazy with his magnanimity and that he was able to seduce every woman with a single glance or a simple gesture. He loved women and women loved him. And so Emelina came to know him. He was not just any man, he was a powerful leader and had many men under his command. And he had money. He owned so many sacks of grain that they could have filled the storehouse of the whole village. They met. They made love. They floated in the realm of dreams on the fragile wings of passion. Nevertheless, they were unable to attain perfect happiness because the man was married and polygamous, while Emelina was married and had three children. Their mutual dream was to live together until death parted them, but this dream was unattainable. Emelina compared her husband with her lover. Separating from a husband was simple, but how was she to separate herself from her children? She had to find a way to free herself of them.

Introduction

Sexually selected infanticide is relatively widespread among primates, but has been documented primarily in one-male–multifemale reproductive units, e.g., in guenons (Cercopithecus spp.) (Butynski 1982; Fairgrieve 1995), langurs (Presbytis spp.) (Hrdy 1974; Newton 1988; Sommer 1994), howler monkeys (Alouatta spp.) (Crockett & Sekulic 1984), and mountain gorillas (Gorilla gorilla berengei) (Fossey 1984; Watts 1989). Although male infanticide has been invoked as a selective force in multimale–multifemale groups, such as in macaques (Macaca fascicularis) (van Noordwijk 1985), capuchin monkeys (Cebus olivaceus) (O'Brien 1991), and chimpanzees (Pan troglodytes) (Smuts & Smuts 1993), it has rarely been observed in these species (e.g., Valderrama et al. 1990; Camperio Ciani 1984) or follows patterns partly inconsistent with Hrdy's (1974) sexual selection hypothesis (Hiraiwa-Hasegawa & Hasegawa 1994). Thus current data suggest that the presence of multiple males in a primate group discourages infant-killing by other males.

Relative to one-male groups, the presence of additional, reproductively active males may both dilute the benefits of infanticide and increase its costs. Exploitation of the reproductive opportunity created by infanticide depends upon the perpetrator's ability to monopolize subsequent fertilizations, which is a function of social variables such as the number of males in a group, the intensity of male–male mating competition, and the potential for effective mate guarding.

Introduction

Food acquisition and predator avoidance are two major factors proposed to promote social grouping in animals (Krebs & Davies 1987). In the primate literature, these two factors have been presented as alternative hypotheses (Wrangham 1980; van Schaik 1983). Defense against potential infanticide by new males also favors social grouping in primates: females form permanent associations with protective males, including their dependent infants' fathers (Wrangham 1979; van Schaik & Dunbar 1990; Smuts & Smuts 1993; van Schaik & Kappeler 1993, 1997; Sterck et al., 1997). The present volume originated from the recognition of the importance of infanticide avoidance in shaping primate social organization.

Factors favoring the formation of permanent social groups of females and males are not necessarily the same factors influencing the size of the groups. For example, many believe food competition to be the principal factor limiting primate group size (Janson 1988; van Schaik 1989; Isbell 1991; Janson & Goldsmith 1995). Upper group-size limits may be mediated by the maximum daily travel distance individuals can sustain as they forage in groups (Wrangham et al. 1993). In this chapter, we present evidence from red howler monkeys (Alouatta seniculus) that infanticide, too, may play a role in limiting group size in primates (see also Steenbeek, Chapter 7). When infanticide rates increase with the number of reproductive females, females may opt for dispersal, thus keeping total group size small. We propose that indirect evidence previously suggesting the role of food competition in limiting group size might actually reflect infanticide.

Introduction

Although all female eutherian mammals share the same basic reproductive physiology, they show great variation in their sexual behavior (van Tienhoven 1983; Short 1984; Flowerdew 1987). In some families, especially among primates, females can mate over a period of weeks and may actively pursue polyandrous mating, whereas in others, for example some bovids, females restrict sexual behavior to a single mating with a single male per conception. Likewise, females of some species regularly mate while pregnant, whereas in most others mating stops upon fertilization. Details of the regulation of ovarian cycles also vary greatly. For example, in the ovarian cycles of many carnivores, extensive stimulation by mating is required for ovulation to occur (known as induced ovulation), whereas in many rodents ovulation is spontaneous but mating induces the formation of the corpus luteum; in primates, in contrast, the whole cycle proceeds spontaneously regardless of whether any mating occurs.

Traditionally, such variation in ovarian cycles and sexual behavior has been regarded as a feature that reflected merely evolutionary history rather than current function. Reproduction is critical to fitness, however, and, increasingly, adaptive explanations are sought for these variations in sexual behavior, its regulation and other features of reproduction (e.g., Eberhard 1996). Ever since Hrdy's (1977, 1979) research, it has been argued that some features of sexual behavior are best considered an adaptive counterstrategy to the threat of infanticide by males.

Introduction

Hanuman langurs (Presbytis entellus) have been among the first primate species where infanticide by adult males was observed and reported in the wild (at Dharwar, Sugiyama 1965; at Jodhpur, Mohnot 1971; at Abu, Hrdy 1974). Most cases were reported for hanuman langurs living in one-male groups (e.g., Sugiyama 1965; Mohnot 1971; Hrdy 1974, 1977; Newton 1986; Sommer 1994) and they usually took place after the resident male was replaced by a new immigrant. The occurrence of infanticide in hanuman langur multimale groups was first mentioned in 1980 by Ripley and has recently been documented in detail for a wild population at Ramnagar/Nepal (Borries 1997). Other studies on wild primate multimale groups confirmed that infanticide occurs in multimale groups (e.g., Papio ursinus, Busse & Hamilton 1981, see also Palombit et al. 1997; Alouatta seniculus, Crockett & Sekulic 1984; Macaca fascicularis, de Ruiter et al. 1994).

Generally, it is expected that the risk and frequency of infanticide should be lower in multimale groups as compared with one-male groups (e.g., Hrdy & Hausfater 1984; Leland et al. 1984; Altmann 1990; Newton & Dunbar 1994; Sommer 1994; van Schaik 1996). This is indeed supported by fewer infanticides in multimale groups of mountain gorillas (Robbins 1995), a low prevalence of infanticide in populations of hanuman langurs with a predominating multimale structure (Newton 1988; but see Sterck 1999) and low rates of infanticide in most baboon and macaque species (van Schaik, Chapter 2).

Introduction

Infanticide by males is costly to females and so should select for female counterstrategies (Hrdy 1979; Smuts & Smuts 1993; van Schaik 1996; Ebensperger 1998a). Some of these hypothesized female counterstrategies are social, such as special relationships with “protector” males (Palombit et al. 1997). Female counterstrategies to infanticide may therefore explain important variation in primate social systems, including monogamy (van Schaik & Dunbar 1990), patterns of male–female association (van Schaik & Kappeler 1997) and female coalitions (Treves & Chapman 1996).

Female primates also face ecological pressures that may account for cross-species variation in social systems. For example, predation pressure may select for larger female groups, which then leads to greater withingroup competition for food resources (van Schaik 1989; Sterck et al. 1997). Additionally, predation pressure may select for an increase in the number of males in the group (Hall & DeVore 1965; van Schaik & Hörstermann 1994; Hill & Lee 1998), especially when males are more vigilant than females (van Schaik & van Noordwijk 1989) and when they deliver more effective communal defense (Stanford 1998).

The goal of this chapter is to examine the relative roles of ecology and intersexual conflict in primate social evolution. To achieve this goal we need independent estimates of the relevant ecological and intersexual pressures, but three issues complicate this effort. First, quantification of the relevant factors is difficult. For example, infanticide and predation are rare events, and when they do occur they often happen quickly and out of direct sight.