Rethinking Bateman's Principles: Challenging Persistent Myths of Sexually Reluctant Females and Promiscuous Males.

In 1948, Angus Bateman published a paper on fruit flies that tested Charles Darwin's ideas of sexual selection. Based on this one fruit fly study, Bateman concluded that because males are able to produce millions of small sperm, males are likely to behave promiscuously, mating with as many females as possible. On the other hand, because females produce relatively fewer, larger, and presumably more expensive eggs, females are likely to be very discriminating in selecting only one high-quality sexual partner. He also posited that a male's reproductive success increases linearly with the number of females he is able to mate with, but that a female's reproductive success peaks after she mates with only one male. Consequently, in almost all organisms, sexual selection acts most strongly on males. These ideas became a recurring theme in attempts to explain wide-ranging differences in male and female behavior not only in nonhuman animals but also in humans. As such, Bateman's conclusions and predictions have become axiomatic and, at times, have gone unquestioned even when modern empirical data do not conform to this model. This article reviews the origins and history of these ideas and uses modern data to highlight the current and growing controversy surrounding the validity and general applicability of this paradigm.

Effects of food, proximity, and kinship on social behavior in ringtailed lemurs.

Efforts to understand the variation in primate social systems and their underlying interaction patterns have focused on both intrinsic and extrinsic factors. In the socioecological model, food distribution and abundance have been argued to be the primary influences on the social behavior of primate species. We examined the relationship of food resources and two intrinsic factors-kinship and proximity-with patterns of affiliative and agonistic relationships in two semi-free ranging ringtailed lemur, Lemur catta, social groups (N=14) at The Duke Lemur Center in Durham, NC. In analyzing these three factors concurrently within the same system, we attempt to establish their relative power in explaining the characteristics of social relationships. Patterns of affiliation and high-intensity agonism were best explained by kinship. Proximity also explained affiliation but did not explain agonism, which varied considerably between groups. The influence of food on social interactions was highly variable between the two groups and, therefore, did not convincingly account for the social behavior patterns we observed. Finally, different intensities of agonism have different patterns and should be analyzed individually. The variation between social groups makes it difficult for us to conclude that any one factor is primarily and universally responsible for patterns of social behavior in this species.

Individual discrimination by odors in sibling prairie voles (Microtus ochrogaster).

The habituation-discrimination paradigm has been used widely to demonstrate that animals can detect individually distinctive odors of unfamiliar conspecifics. By using a modification of the habituation-discrimination technique, Todrank et al. (Anim Behav 55:377-386, 1998) found that golden hamsters discriminate between the individual odors of their own familiar brothers but cannot discriminate between the odors of two siblings that are unrelated and unfamiliar to the subject. This suggested that previous evidence showing that animals could discriminate between the odors of individuals actually may have demonstrated the ability to discriminate between genetically unrelated conspecifics (i.e., members of different families). To test this possibility, we conducted habituation-discrimination experiments with prairie voles, Microtus ochrogaster. Voles were tested under three conditions: subject and both targets were unrelated and unfamiliar; subject and both targets were brothers and familiar; subject was unrelated and unfamiliar to targets, but targets were brothers. In all cases, voles discriminated between the two individual odors. Thus, prairie voles can discriminate individual differences between the odors of brothers and they do not have to have previous experience with the conspecifics in order for discrimination to occur. The theoretical importance of these results is discussed.

Olfactory responses of neotropical short-tailed singing mice, Scotinomys teguina, to odors of the mid-ventral sebaceous gland: discrimination of conspecifics, gender, and female reproductive condition.

We examined the olfactory communication of the Neotropical short-tailed singing mouse, Scotinomys teguina, by investigating whether S. teguina responded to odors produced by the mid-ventral sebaceous gland of conspecifics. Females spent significantly more time investigating male odor than an odorless stimulus or a female odor. Males spent significantly more time investigating female odor than an odorless stimulus, but not that of a male odor. This latter result does not seem to be explained by differences in age or sexual experience of test subjects, but may be influenced by reproductive condition of the female odor donor. Male S. teguina spent significantly more time (1) investigating and (2) in total proximity to odors of estrous than non-estrous females. Males spent more time (1) investigating and (2) in total proximity to odors of males than non-estrous females. Finally, given the choice between odor of males vs proestrous females, males showed no preference. Thus, the mid-ventral gland in S. teguina seems to convey information about conspecifics, sex, and female reproductive condition. Male odor, compared with proestrous female odor, is equally interesting to males, suggesting that the gland also plays an important role in male-male communication. Sexual dimorphism in the size of the gland and in the amount of secretion produced by the gland may be related to either male-male competition or female choice.

The Problem with Paradigms: Bateman's Worldview as a Case Study.

Bateman's principles, their corollaries and predictions constitute a paradigm for the study of sexual selection theory, evolution of mating systems, parental investment theory, and sexual dimorphism in male and female behavior. Some aspects of this paradigm have been challenged in recent years, while others have been supported by empirical and theoretical research. We re-examine Bateman's 1948 paper in detail, including some methodological problems. Additionally, we review three areas in which an over-reliance on Bateman's predictions about sexual dynamics hindered our ability to understand the potential importance of certain behaviors: 1) male mate choice and sperm allocation; 2) the role of females in initiating and soliciting extra-pair copulations and fertilizations; and 3) the role of females in lekking systems, in which recent evidence suggests that copulations with multiple males (polyandrous behavior) may be common. We conclude this introduction to the symposium by emphasizing the heuristic value of Bateman's contributions, as well as the problems that arise when Bateman's paradigm is viewed through the lens of modern behavioral ecology and evolutionary theory.

Bateman gradients in field and laboratory studies: a cautionary tale.

Since tools of molecular genetics became readily available, our understanding of bird mating systems has undergone a revolution. The majority of passerine species investigated are socially monogamous, but have been shown to be genetically polygamous. Data sets from natural populations of juncos suggest that multiple mating by females results in a sexual selection gradient as steep for females as for males (a result that does not support Bateman's predictions). However, in males, fitness is enhanced directly through fertilization success with multiple matings; in females fitness benefits may be enhanced immediately through direct access to food, protection against predators, or other resources received from males, or they may be delayed through improvement in offspring quality (e.g., through good genes, or greater genetic compatibility between the female and the extra-pair male). But a steep sexual selection gradient for females can be difficult to interpret. If all females copulate with multiple partners that are equally likely to fertilize eggs, then females that produce larger clutch sizes, for any reason, will appear to have copulated with more males. That is, multiple sires have a higher probability of detection in larger clutches than in smaller ones, giving the impression that females that mate with multiple males increase their reproductive success. Yet, in most studies in which there is a correlation between number of offspring produced by females and number of extra-pair males, causation has not been clearly established and other factors may explain the results. Additional complications in understanding male and female reproductive strategies are: (1) Molecular studies cannot detect extra-pair copulations that did not result in fertilizations; yet if a female acquires food or other resources from extra-pair males, such extra-pair matings may have significant effects on female fitness. Thus, molecular studies provide only a conservative estimate of the number of extra-pair copulations or "mates" that a female has. (2) Clutch size affects the probability that any given male will be successful in fertilizing a female's eggs. Specifically, at any given point, a male's chances of fertilizing at least one egg in the female's clutch will be greater as clutch size increases. We predict that in avian species with small clutch sizes, males may be selected to be choosy and avoid extra-pair copulations, while females should be selected to be less discriminating. Moreover, if extra-pair males provide resources that increase female fitness, the females should seek extra-pair copulations, whether or not the males are likely to fertilize any of her eggs.Laboratory studies with insects have yielded clearer evidence of the causal relationship between multiple mating and increased female fitness. We review studies on a tenebrionid beetle in which female fecundity increases directly with number of mates. In these experiments, the nutritive value of the spermatophores does not fully explain the increase in female reproductive success.