Classical biologists defined the sexes in terms of differences in gamete (the reproductive cells) sizes, with females having large, relatively immobile, nutrient-rich eggs and males having motile small sperm. This definition describes an essential sex difference in humans and most other sexual organisms. However, even this criterion for maleness in non-human organisms is no longer universal: in some Drosophila species (fruit flies), males have giant sperm, in which a single sperm is as large as a single egg, blurring the classical defming characteristic of the sexes. Thus, the relative size of the reproductive cells defines the sex male in relation to the sexfemale for most biologists to this day.
Classical biologists, including Darwin (1871), defined male behaviour in contrast to female behaviour. Gene-centric sociobiologists (Wilson 1975) took off from there and posited that genes determined fundamental sex differences; that ancient selection pressures favoured these genes for sex-differentiated behaviour; and that these genetically determined traits are invariant (fixed) within sex (so that differences between the sexes are strict). Evolutionary psychologists, who took inspiration from the gene-centrist sociobiologists (Buss 1989) argue that genes determine that men are competitive, indiscriminate and profligate in their mating psychology and females are ‘coy’, discriminating, and passive. They argue that genes favouring these sex-differentiated psychologies accumulated because of the environments experienced by our Pleistocene ancestors, ‘the environment of evolutionary adaptiveness’. Thus, they say, the ancient environments of human ancestors favoured genes that determine sex-differentiated reproductive psychology and behaviour, some of which is now associated with ‘masculinity’ in human societies.
Contemporary with the gene-centrists of the last thirty years were other sociobiologists interested in the origins and maintenance of flexible traits due to developmental plasticity. Their view of how phenotypes arise is considerably more sophisticated than the ideas of the gene-centrist evolutionary psychologists. The ideas of sociobiologists interested in developmental plasticity are based on genes and environmental effects—inextricably intertwined through development. While their ideas have been around for as long as those of gene-centrists, it is only recently that ideas about adaptive, induced, developmentally flexible sex-associated traits are coming into their own (e.g. West-Eberhard 2003). These socio-biologists hypothesise that environmental and social variation coupled with mechanisms of developmental plasticity induce masculinity (and femininity). Thus, these sociobiologists hypothesise that ‘masculinity’—behavioural and psychological traits that are stereotypically associated with men—is context specific, induced and flexible, rather than invariantly determined by genes.
An early selection argument about the origins of sex differences is from anisogamy (Parker et al. 1972). This idea provides a selection scenario for the evolution of two sexes; i.e. it explains how two gamete sizes (anisogamy) may have evolved from an ancestral population of gametes of the same size (isogamy). The anisogamy hypothesis says that disruptive selection on gametes with a normal size distribution favoured large gametes (eggs) that emphasised accumulation of resources and smaller, more mobile gametes (sperm) able to successfully compete over access to the larger, resource-rich eggs. In this scenario, what is emphasised is that the energetic cost of producing an egg is larger than the energetic cost of a sperm, a differential that results in selection with different effects on the behaviour of egg-bearers and spermbearers. Evolutionary biologists (Williams 1966) argued that these cost differentials would favour the evolution of choosy eggbearers but competitive and indiscriminate sperm-bearers. Thus, anisogamy theory says that profligate, competitive males and choosy females arose early in the history of sexually reproducing organisms. ‘Masculinity’ in this context refers to males that compete among themselves for access to females or resources (a surrogate variable that increases the access of males to females) and to males that mate profligately as opportunities arise, in contrast to females that are ‘coy’ and discriminating about those with whom they mate.
In mammals, including humans, sex differences in investment continue after insemination and fertilisation. In contrast to the huge energetic burden of reproduction in female mammals, the cost of reproduction for most male mammals is small, being the cost of spermatogenesis and insemination (Williams 1966). Because of pregnancy and lactation, mothers invest heavily in offspring up through the end of weaning, and, in many cases, as in humans, throughout an extended period of continued offspring dependence. Many, but not all, sociobiologists emphasise the notion that ancestral human mothers, unlike females in most other mammals including most other primates species, were universally less capable of raising their offspring without the help and support of fathers or others. They argue that women are dependent on men and paternal investment for successful reproduction. Parental investment theory (Trivers 1972) says that in species with substantial paternal postzygotic offspring care, selection will have favoured competitive and promiscuous but simultaneously choosy and caring males. As applied to humans, Trivers’s parental investment argument added considerable subtlety to sociobiological discussion of sex essentialisms. Trivers argued that in socially monogamous organisms, selection would favour genes in males for cooperation with one female in raising their offspring, as well as genes for competing over access to females and for seeking copulations with as many other females as possible, most of whom he would not collaborate with in offspring care. Applied to humans, this means that masculine men are competitive and choosy over whom they marry, if not with whom they copulate. Note that this idea assumes that the selective value of male parental care arises because of the neediness of mothers that only fathers can fill. If this assumption is false, another explanation is required for the evolution of male post-zygotic parental care and for the behavioural traits associated with masculinity that supposedly depend on a species-specific requirement of paternal care. With other explanations, changes in sociobiological concepts of masculinity have followed.
Evolutionary psychologists seized on the parental investment hypothesis to characterise human bonding and mating behaviour as short and long term. For long-term mateships, they argue that men prefer young women with ‘high reproductive value’, a stringent criterion that is relaxed for short-term mateships. Reproductive value is a concept associated with demographic analyses of fitness (survival and reproductive success). Reproductive value is a relative term referring to the age-specific likelihood of future reproduction given parameters of average age of first reproduction and age-specific mortality rate. In populations that are increasing, younger breeding individuals have higher reproductive value than older individuals. In declining populations, reproductive value of older individuals is often equal to that of younger individuals. They melded this view with classic socio-biological ones of selection acting on our ancient ancestors, so they assumed that human females are universally dependent on male help in raising offspring: thus, double-standard views of sex differences (dependent, choosy females and profligate, competitive but paternally helpful males) determined by genes gained primacy in sociobiology. Masculinity in this context suggests that men are competitively dominant to one another and compete among themselves for access to resources, because of women’s dependence on men for resources essential for reproduction.
Masculinity also refers to the dominance of men over women, which sociobiologists explain as arising primarily as a by-product of male—male combat, which is thought to favour genes for large males. In as much as size is a determinant of dominance, men thus can physically dominate women.
Criticism of the narrow characterisation of sex differences and their phenotypic origins that define ‘men and masculinities’ began in 1875, three years after Darwin’s (1871) volume, and has continued ever since. Yet few are aware of this long history of criticism, perhaps because mainstream sociobiological ideas fit intuitive expectations of what makes men masculine and women feminine. Modern criticisms focus on the facts from experimental tests. Observations often fail to fit the predictions of universally indiscriminate males. Observations of competitive females are common. The best-known experimental tests used species with male-biased parental investment, in which females were predicted to be the competitive, profligate sex and the males the choosy sex. Results indicated less sex differentiation than predicted, in that both sexes are competitive and both sexes choosy. In fact, in broad-scale testing of nonhuman species, males are often as choosy as females, and females are often as indiscriminate as males.
Thus, these tests, which investigators usually cite as consistent with parental investment theory, because of so-called ‘reversed sex roles’, suggest that sex differentiation is not as invariant as once thought. Such experiments challenge the idea that sex differences are fixed genetically. Under observational controls that levelled the ecological playing fields of females and males, sex differences in behaviour associated with ‘masculinity’ and ‘femininity’ often disappear, raising questions anew about the origins of sex differences in behaviour. Rather than being genetically determined, it appears as though ‘sex typical’ pre-mating behaviour may be similar in males and females, when environmental variation is controlled. In the face of these data, one must wonder if masculinity is induced by the environments males typically experience. If masculinity is environmentally contingent in nonhumans, it is likely that similar processes also account for masculinity in humans.
Roughgarden’s recent critique of sexual selection theory, Evolution’s Kainbow (2004), focuses also on biologists’ often narrow characterisation of male and female. She argues that within each sex there are many genders and that theories that emphasise gender binaries, rather than gender continua, obscure the underlying variation in male-associated and female-associated traits.
An alternative to sexual selection is a new predictive theory of environmentally induced variation in choosy and indiscriminate behaviour (Gowaty and Hubbell 2005). The theory is symmetric in that the inducing factors work the same way in males and females; what determines differences in individual behaviour is variation in the environments they experience. According to this theory, if there is gender-associated variation in the inducing factors, gender-associated variation in choosy versus indiscriminate behaviour will occur. What makes the sexes different or similar in this theory is variation in the inducing factors. The inducing factors are completely specified by two things: first, cues to the amount of time an individual has left for mating during a season and over a lifetime; and second, the fitness variation that would result from mating with alternative potential mates. The hypothesis assumes that all individuals, irrespective of sex, were fixed genetically through very ancient selection to express flexible and adaptive behaviour—specifically tuned to the real-time environments that individuals inhabit. The model predicts quantitatively when females will express competitive, indiscriminate mating behaviour (usually associated with males) and when males will express choosy, ‘coy’ mating behaviour (usually associated with females). The new hypothesis calls for re-evaluation of sex differences under strong experimental controls that level the ecological playing fields of males and females, i.e. under experimental conditions that would inform the mechanisms determining phenotypes.
Sociobiological ideas about masculinity include gene-centric hypotheses, such as those of the evolutionary psychologists, that predict stereotypically masculine behaviour, as well as environmentally contingent, induced, developmentally flexible and adaptive hypotheses that predict considerable within-population variation in male-typical (masculine) behaviour. Modern sociobiology thus accommodates more than one idea about the determination of sex roles, including masculinity. Yet most sociobiological hypotheses predict that masculinity is associated with fitness, either in ancestral environments, as claimed by gene-centric evolutionary psychologists, or in current environments, as claimed by those interested in genes and environments, inextricably entwined during development.
References and further reading
Buss, D.M. (1989) ‘Sex differences in human mate preferences’, Behavioml and Brain Sciences, 12:1–14.
Darwin, C. (1871) The Descent of Man and Selection in Relation to Sex, London: John Murray.
Gowaty, P.A. and Hubbell, S.P. (2005) ‘Chance, time allocation, and the evolution of adaptively flexible sex roles’, Journal of Integrative and Comparative Biology, 45 (5):931–44.
Parker, G.A., Baker, R.R. and Smith, V.G.F. (1972) ‘The origin and evolution of gamete dimorphism and the male—female phenomenon’, Journal of Theoretical Biology, 36:529–53.
Roughgarden, J. (2004) Evolution’s Rainbow, Berkeley, CA: University of California Press.
Trivers, R.L. (1972) ‘Parental investment and sexual selection’, in B.Campbell (ed.) Sexual Selection and the Descent ofMan, Chicago, IL: Aldine, pp. 136–79.
West-Eberhard, M.J. (2003) Developmental Plasticity and Evolution, New York: Oxford University Press.
Williams, G.C. (1966) Adaptation and Natural Selection, Princeton, NJ: Princeton University Press.
Wilson, E.O. (1975) Sodobiology, Cambridge, MA: Harvard University Press.
