On Being and Becoming Female and Male
On Being and Becoming Female and Male
A Sex-Neutral Evolutionary Perspective
Abstract and Keywords
This chapter introduces a new way to think about the evolution of behavioral sex differences, one that contrasts with the classical evolutionary view. The classical scenario—sex as destiny—holds that key sex differences in behavior are fixed traits of an individual, because innate sex “roles” that evolved in concert with morphology and genes are “the blueprints” for expressed behavior. Mating theory (Gowaty & Hubbell, 2009) shows that such genetically deterministic behavior is often maladaptive, meaning that individuals with fixed behavior are most likely selected against. In this new theory, whenever environments vary, the most evolutionarily successful individuals will be those who are flexible in their behavior. On this view, individuals’ behavior—regardless of membership in a genetically defined or anatomically defined sex category—is always “becoming,” sometimes behaving in ways we consider “female typical” and sometimes in ways we consider “male typical.” Thinking this way provides a new lens through which to view linkages between research in biology and in psychology.
This chapter introduces a new way to think about the evolution of behavioral sex differences, one that contrasts with the classical evolutionary view. The classical scenario—sex as destiny—holds that key sex differences in behavior are fixed (invariant) traits of an individual, because innate sex “roles” evolved in concert with morphology and genes are “the blueprints” for expressed behavior. In a recently developed evolutionary theory (mating theory; Gowaty & Hubbell, 2009), such genetically deterministic behavior is very often maladaptive, selecting against individuals with fixed gendered behavior. From this new perspective, “sex is destiny” is a myth. The conclusion from this updated theory is that whenever environments vary, the most evolutionarily successful individuals will be flexible in their behavior. This new way of thinking prioritizes the ecological constraints and opportunities that individuals experience throughout their lifetimes. On this view, individuals—regardless of membership in a genetically defined or anatomically defined sex category—are (p.78) always “becoming,” sometimes behaving in ways we consider “female typical” and sometimes in ways we consider “male typical.” Thinking this way shifts the study of the evolution of behavioral sex differences, providing a new lens through which to view linkages between research in biology and in psychology.
In this chapter, you will learn about the structure of the classical evolutionary argument for fixed sex differences and the structure of the new evolutionary argument for individuals who constantly evaluate and flexibly respond to the circumstances they experience. You will learn some history and vocabulary associated with evolutionary reasoning. You will learn about the logic of and evidence bearing on the classical and new theories. The chapter is meant to pique your interest and enhance your ability to engage critically with the sweep of evolutionary logic and with the science of the evolutionary origins of sex differences in behavior.
The title of this chapter announces its conclusion: Being gendered is a lifelong process of becoming. Adaptive individuals can be flexible through a lifetime. Being female or male is not necessarily or always or even commonly a static aspect of being, not a binary “trait” fixed at birth. Behaving in ways typical of females or males, or typical of both, or typical of neither, expresses a developmental (ontogenetic) process of continually becoming: Ecological and social contexts continually affect development—from cradle to grave. Accordingly, individuals may be far more flexible in their adaptive behavioral and physiological expression—their gendered behavior and physiology—than many biologists have assumed or predicted.
Few ideas provoke as much ire, frustration, and outright derision as do the classical views of the evolutionary origins of sex differences in behavior, but the irritation is not the point of this chapter. Understanding is. To that end, the chapter reviews the following key concepts:
■ the nature of selection hypotheses and the relationship of selection to evolution;
■ the ways in which information transfers between generations—that is, how heredity can work;
■ the classical evolutionary view of sex differences in behavior, and its flaws;
■ and a theorem (the switch point theorem) for the origins of sex differences in behavior that is fully evolutionary while being also fully sociological (embedded in social circumstances) and fully psychological (dependent on sensitivities to stimuli and cognition), yielding a view of behavior as environmentally contingent, individually based (rather than determined by morphology or sex), and flexible.
Herein a distinction is made between proximate and ultimate causes. These terms refer to different kinds of questions that one can ask about the same phenotypic traits. When evolutionary biologists talk about how a phenomenon develops and expresses, they are referring to proximate causes; when they talk about why it exists, they are referring to ultimate causes.
Some Things About Some Males and Females Are Different
The arguments in this chapter do not take exception to what is commonly observed: The sharing of gametes—sperm and eggs—is an essential element of reproduction in species that only reproduce sexually (as opposed to only reproducing asexually). Humans, up to this time at least, reproduce “sexually” in the sense that to produce offspring to whom they are genetically related, “two must tangle”—that is, share their gametes—to create a zygote, which is the first stage in the developmental process of becoming a human. Human individuals are “diploid,” meaning that each of us had an egg-producing parent and a sperm-producing parent. Both parents are necessary because in the particular domain of creating a new human being, there is a great difference in what people can do: Only people bearing XY (p.80) sex chromosomes (“genetic males”) can produce sperm (though some do not), and only people bearing XX sex chromosomes (“genetic females”) can produce ova and gestate a baby (though some do not), and internal gestation remains necessary for a human to be born. However, a female gender identity (e.g., as a woman, mujer, nǚrén, etc.) is not necessary to bear a child: Transgender female-to-male persons have given birth. Constraints on lactation are slightly less dramatic: Lactation is common after parturition among genetic females, and genetic male humans can—with new reproductive technologies—be hormonally induced to lactate. After all, a universal of human morphology is that people have breasts. The potential for genetic males to lactate just is not expressed in usual circumstances.
Some other changes are less likely. For instance, a transgender male-to-female person could only give birth with extraordinary medical interventions. Mechanisms of physiology that tend to differ between genetic females and males are mutable via hormone injections or pills. Morphology is mutable but with even more invasive interventions such as castration or plastic surgery. These kinds of intervention notwithstanding, it is unlikely that a transgender male-to-female person will ever easily produce ova or that a transgender female-to-male person will produce sperm. In any scenario, either will likely remain exceedingly rare.
Despite these impediments to complete flexibility in every aspect of sex, our discussion so far makes the point that even most of what seem to be the most fundamental or “essential” traits of maleness and femaleness coexist within an individual and can change during an individual’s lifetime in our species and in many others (Crews, 2012; Fausto-Sterling, 2012; Morris, Jordan, & Breedlove, 2004; Roughgarden, 2013).
There also are aspects of being female and male that are totally, unabashedly flexible, particularly in the domain of behavior. Ovulating and ejaculating sperm are hormonally organized and constrained in remarkable ways; they are the exception rather than the rule. Consider a few of the myriad motor acts (i.e., behavior) of which humans are capable: walking, talking, playing soccer, teaching, reading, dancing, tending crops, shooting a gun, playing mahjong, speaking multiple languages, negotiating treaties, arguing a case as a barrister, caring for a sick child, or being (p.81) Prime Minister of Pakistan. It is difficult to imagine a behavioral skill that cannot be improved with training for any person no matter what her/his/their genetic sex is or what sex was assigned at birth. This sensitivity to opportunity and experience speaks to our abilities to be flexible individuals capable of extreme changes in a single lifetime. Yet many behavioral options are closed for some because of what feminists have identified as a prejudice, a perception bias, called “the double standard.” Critics rightly have argued that many behavioral sex differences, rather than being rooted in genetically deterministic, fixed limitations, are rooted in the psychology and sociology of gender prejudice (Fausto-Sterling, 2000, 2012).
The next section concerns how evolutionary biologists think about causes and elements in the theory of evolution by natural selection. Then we tackle a classical evolutionary hypothesis that transformed the double standard into a scientific claim of evolved, immutable, sex differences in behavior. Finally, a mathematical equation—the switch point theorem— derived from formal mating theory is described; it says that individual behavioral flexibility is crucial for individuals’ evolutionary success and, as such, provides an alternative to the classical theory.
A Primer on Thinking Like an Evolutionary Biologist
The Nature of Selection Hypotheses
Artificial selection (Darwin, 1859) is a sorting process analogous to the sorting processes that you are familiar with if you are interested, for instance, in the origin of dog breeds. An example is dog breeders who increase the likelihood of producing puppies with certain traits when they control who mates with whom. If the breeders pick parents whose tail is congenitally crooked, the likelihood that their puppies will have a crooked tail increases. This process is known as selective breeding (Darwin, 1859), and it is a type of selection that depends on the action of humans. Another example is agriculturalists who use selective breeding to enhance the qualities of crop plants or livestock. Humans have been practicing selective breeding for over 10,000 years. Selective breeding works so well so (p.82) often because it is a rule of nature that “offspring resemble their parents.” Darwin used the term “artificial” as a contrast with “natural” selection, but perhaps “human facilitated selection” is an even better term. Humans, after all, are part of nature, not separated from it, and all selection is selection, whether people do it to dogs or slave-making ants (e.g. Polyergus lucidus) do it to other species of ants.
In natural selection, in contrast, no person acts. Natural selection just happens, and it has been happening since the dawn of life on Earth. Charles Darwin’s (1859) genius was to realize how the process of natural selection occurs. He figured out that (1) as long as the individuals in a population (of members of the same species) of any living things varied in heritable traits, and (2) as long as environments—either social or ecological—impacted (3) the survival or reproductive success of individuals in the population because of their heritable trait variants, then natural selection will occur. Therefore, whenever we encounter hypotheses of natural selection, we must think about these three important things:
■ First, do individuals in a population vary in heritable traits?
■ Second, do social or ecological circumstances affect individuals because of their traits?
■ Third, do individuals with some traits have longer life spans or more surviving offspring than other individuals because of their heritable trait variants?
If we are able to show these three things, as well as a positive correlation between the similarities of children to their parents, we can conclude that natural selection has occurred and that evolution—a change in trait frequencies between generations—has occurred.
To make the above description general and to demonstrate the utility and flexibility of selection hypotheses, we can characterize the assumptions of selection hypotheses in another, more general, way (Gowaty, 2011, 2014). The first assumption is about the level at which selection operates. You may: focus on individuals in populations (individual selection); narrow your attention to genes in related individuals (kin selection); or widen (p.83) your attention to groups within populations (group selection). With your choice, you are characterizing the units of organization at which the heritable variation resides and which may be sorted by selection. The second assumption concerns the mechanisms by which selection among the units occurs. For natural selection, any one of thousands of features of the social and ecological circumstances in which individuals live may favor or disfavor some individuals because of their trait variants. The third assumption specifies the components of fitness on which selection acts. Individuals are favored or disfavored only on the basis of their fitness; moreover, “fitness is relative,” meaning that raw survival or raw numbers of offspring do not indicate one’s fitness because fitness is always relative to others in the population. Components of fitness can be characterized in coarse or fine terms: Staying alive is a key fitness measure. Number of mates is another component of fitness. Other components of fitness also fall in the category of “reproductive success,” which investigators estimate using a variety of measures such as the number of eggs laid or fertilized, of offspring born, or of offspring that survive to reproductive age, or the percentage of eggs surviving to adulthood (a measure of parents’ likelihood of having grandchildren). Having high fitness means having longer lives or more offspring than others in the population.
Sexual Selection Is a Kind of Natural Selection
Under the broad heading of natural selection, the concept of sexual selection (Darwin, 1859, 1871) focuses on processes through which individuals in sexually reproducing species have differential access to mates (egg producers for sperm producers, and sperm producers for egg producers). In this context, “female” refers to egg producers and “male” refers to sperm producers. Sexual selection is a concept that many evolutionary biologists think explains sex differences in behavior. Now you will learn to cast your own sexual selection hypotheses. You need to assert the three assumptions (Gowaty, 2011, 2014): one about the level of selection, one about the mechanism(s) by which the trait variants in the level of selection are favored or disfavored (i.e., selected, sorted), and another about the components of fitness through which the mechanisms of selection operate. In (p.84) sexual selection, the level of selection is within-sex within a population, that is, among males in a population or among females in a population. The mechanisms are limited to intersexual interactions (between different-sex individuals) or to intrasexual interactions (between same-sex individuals). Usually the selective forces are via “mate preferences” that individuals have for different-sex individuals or competitive interactions that occur between same-sex rivals. So mate preferences indicate affiliative interactions that can produce a selection pressure that sorts among same-sex individuals on the basis of their behavior toward potential mates. Male-male or female-female competitive interactions like fights are agonistic interactions, and these too can produce selection pressures among males when males fight over access to mates or otherwise compete or among females when females fight over access to mates or otherwise compete.
Two things should be apparent: First, the selection in sexual selection happens within a sex. That is, selection sorts same-sex individuals on the basis of trait variants. Second, the mechanisms that exert selective pressure are social interactions either of mate choice (between different-sex individuals) or of competitive interactions (between same-sex individuals). That means that sexual selection happens only within a population of interacting individuals, not between individuals in different populations. With respect to fitness components, biologists thinking about sexual selection usually posit that the mechanisms act on within-sex trait variants via the effects of mate choice or same-sex competition on variation in number of mates or the quality of mates that individuals of the sex under selection have. Those thinking about sexual selection then posit that individuals in the sex under selection have a greater number of mates or better quality mates (Altmann, 1997), either of which may increase individual reproductive success.
Keep in mind that both sexes can be under sexual selection at the same time. Just because one sex is experiencing selection does not mean the individuals in the other sex could not also be under sexual selection, too. For example, an important component of sexual selection relative to mate choice is that the interaction between different-sex individuals has potential fitness effects on both of them. Most evolutionary biologists have been (p.85) interested in what happens with male-male sexual selection vis-à-vis the relative fitness of males (Arnold, 1994; Bateman, 1948). They have paid far less attention to female-female sexual selection vis-à-vis the relative fitness of females. The mechanism of mate choice is actually about sexual selection among the females in a population as well as selection among the males in a population. You should practice making simultaneous arguments about females and males who interact and how those interactions could affect sexual selection among females and among males; you also should practice looking for such arguments wherever you read claims about sexual selection in the literature.
Sexual Conflict Is Sexual Selection Acting Jointly on Two Sexes
Sexual conflict is a theoretically difficult topic in modern evolutionary biology. Sexual conflict occurs when the fitness interests of the sexes conflict (Gowaty, 2018b). Take, for example, sexual assault in which a man attempts to kiss a woman or grope her genitals, or even copulate with her against her will. The calculation of who is a winner and a loser in evolutionary terms is challenging for more than one reason. To start, dealing with this issue demands of us the ability and willingness to distinguish our consideration of whether an assaultive interaction confers any within-sex fitness advantage or disadvantage (“winning” and “losing” as formal evolutionary terms) from our consideration of the psychological, moral, and legal dimensions of behavior—dimensions that can lead to quite different connotations of “winning” and “losing.” We don’t need a neat resolution among those meanings. We do benefit from understanding how the meanings shift depending on their conceptual context.
Assuming we come to grips with what winning and losing mean in the context of evolutionary theory, we can turn to how sexual conflict is about sexual selection within each sex (Gowaty, 2010)—specifically, the within-sex variation in fitness that occurs when one woman is raped and one man is the rapist. The questions that sexual selection raises are as follows: (1) Is the rapist a winner among other males in a population (e.g., has more offspring, lives longer), including those who do and do not rape? (2) Is the (p.86) raped woman a loser (e.g., has fewer offspring, shorter lifetime) among other females in a population, including those who are sexually assaulted and those who are not?
These, of course, are much harder questions to answer than the psychological, moral, and legal questions we usually ask. I bring up these questions in sexual selection to make two points. One is the fact that what happens in our legal system may be a poor guide to answering questions of how behavior affects fitness (a relative measure of reproductive success or survival that varies between 0 and 1). The second is that in either mate choice or sexual conflict, there are two questions: One is about female fitness relative to other females in the population, and one is about male fitness relative to other males in the population. Both of these questions fall under sexual selection.
Mechanisms of Inheritance
Evolution by natural selection and sexual selection occurs whenever the trait variants sorted by selection are heritable. Offspring inherit the traits of their parents via several mechanisms (Jablonka, Lamb, & Zeligowski, 2014). We sometimes call these mechanisms of inheritance mechanisms of information transfer between generations. Genes are perhaps most familiar. Genes are functional base-pair sequences within DNA inherited from our genetic parents. It turns out that there are other important ways for us to inherit traits from our parents. Epigenetic processes—chemical modifications to alleles on chromosomes—affect “gene regulation,” which means that just because we have a gene does not mean that it expresses. Epigenetic effects determine whether a gene is “turned on”—actively expressing—or “turned off,” as though it were not there. Importantly, epigenetic modifications are common throughout the life span of humans and other animals, and are environmentally induced (e.g., through “maternal effects,” through teaching and learning, and through stress or diet or even air pollution; Salk & Hyde, 2012; Schagdarsurengin & Steger, 2016), and in some cases are heritable. Developmental variation, including many of the changes experienced during puberty, is the result of epigenetic changes in our DNA: Ecological forces induce many of these epigenetic effects.
(p.87) Mechanisms of heredity also exist above the cellular level. Behavior is another mechanism of information transfer between and within generations—and therefore is a mechanism of heredity. You no doubt gained new skill traits by mimicking your elders, or watching others, or being trained to play a musical instrument. Another mechanism of heredity—of information transfer between and within generations—is associated with our symbolic communications, such as oral and written histories. In other words, many mechanisms of information transfer between generations can produce “heritable traits” on which natural selection can occur to produce evolutionary change—differential trait frequencies between generations. If traits are not somehow heritable, selection will not produce evolution or, as Darwin called it, “descent with modification.”
Proximate and Ultimate Causes
For generations, biologists spoke at cross-purposes, often confusing themselves and each other, and sometimes fighting over “the cause” of this or that trait. Along the way, consensus arose so that biologists realized that how and why questions are different, complementary questions about biological phenomena. Proximate causes are those that answer the “how” questions, providing the mechanistic ways that traits work. So, for example, a gene that influences trait expression is a partial answer to how the trait expresses. Hormones that at puberty cause breast development, for example, are proximate explanations for how breasts change during the teen years, how breasts change during pregnancy and lactation, and how breast tissue and breast shape change with menopause. The hormonal variation that occurs over a lifetime gives us an answer to the mechanistic question of how breasts change. Ultimate causes are those that answer the “why” questions about the function of a trait, which is usually a guess about the benefit of traits arising by natural selection. A trait may arise by chance, for example. Or processes of selection producing adaptive advantage or disadvantage may answer the why question of the cause of a trait.
Excellent resources for further understanding of the mutable proximate causes of gendered behavior—that is, the mechanistic bases of how sex differences and similarities arise—are the works of Anne Fausto-Sterling (2000, 2012) (p.88) and Melissa Hines’s Brain Gender (2005; see also Chapter 11). This chapter concerns the ultimate causes and the functional significance of traits. The goal is to explore the why questions of the evolutionary origins of behavioral sex differences and similarities. I first delve into classical sociobiological explanations for sex differences in behavior, and then I contrast those classical ideas and their predictions with ideas and predictions from the switch point theorem (Gowaty & Hubbell, 2009, 2010, 2012, 2013).
The Classical Sociobiological Argument for the Origins of Sex Differences in Behavior
The classical argument centers on morphological differences between the sexes that some believe to be essential sex differences (but probably are not; Gorelick, Carpinone, & Derraugh, 2016). The argument has the form “Sex differences predict sex differences.” This argument is correlational and inductive—that is, the argument does not have the strong form of hypothetico-deduction, in which an hypothesis depends entirely on its assumptions. In other words the assumptions of a hypothetico-deductive hypothesis form the hypothesis.
The classic argument starts with the idea that genetic females and males have different costs of reproduction (COR), which results in selection for differential reproductive decision making and associated behaviors in females and males. There are two related ideas. The first idea is the evolution of gamete size asymmetries, that is, anisogamy (Parker, Baker, & Smith, 1972). Anisogamy refers to the differences between ova and sperm in morphological size and motility, the evolution of which set the stage for the evolution of sex differences in being choosy or indiscriminate about mating. In most sexual organisms, sperm are very small compared to ova, suggesting that more parental resources are needed to produce one egg compared to one sperm. The argument from anisogamy is that females produced relatively large, immobile ova, whereas males produced many (p.89) small, mobile sperm. The ova, it was said, emphasized the accumulation of resources that would later be the source of nutrients for any developing zygote. The small, agile sperm, it was said, emphasized sperm-sperm rivalry over access to the resource-rich ova.
The originators of the anisogamy argument proved mathematically that the differences in gamete size and morphology could indeed lead to disruptive selection on gamete sizes. The authors then made another, less formal ad hoc inference and said that these gamete differences—differences associated with the roles of ova-providing resources and of sperm competing over access to the resource-accruing ova—produced selection favoring “choosy” behavior in the ova-producing sex (females) and “indiscriminate” behavior in the sperm-producing sex (males). And thus, some say, choosy females and indiscriminate males have existed ever since. The selection idea justifying choosy females and indiscriminate males was a correlational add-on to the original mathematically deduced anisogamy argument for the evolution of morphological differences in gamete sizes. In other words, the association of choosy and indiscriminate mating behavior with gamete size was not part of the mathematical argument that described how disruptive selection on gamete sizes would come about. It was a qualitative ad hoc statement.
The second COR idea—parental investment (Trivers, 1972)—came from observations of mammals like us. When a female copulates, she risks having to gestate a fetus for some time (in humans about 9 months), and then she begins lactation and nursing of slowly developing (altricial) babies. Even after lactation has ended, mammal mothers often must care for offspring for years. In contrast, when a male copulates, he risks the energetic costs of producing sperm, getting a female to allow copulation, and ejaculating sperm—a relatively small cost compared to females. These sex differences in COR became the justification for two companion ideas: Sexual selection among females, who have “more to lose” from a copulation than males typically do, will favor females who are choosy, coy, and relatively chaste in their mating behavior. In contrast, sexual selection among males, who have less to lose from choosing poor-quality mates than females typically do, will favor males who are indiscriminate, competitive, and profligate in their mating behavior.
(p.90) Like most natural selection arguments, both COR ideas have three assumptions: First, they assume that within populations, there was between-individual variation in heritable traits—say, in this case, behavioral tendencies to be choosy or indiscriminate about mating. Second, they assume that differences between individuals in the cost of reproduction had fitness consequences—specifically, that choosy males were selected against because less choosy males had more mates, or indiscriminate females were selected against because they mated with males with whom they were unlikely to produce high-quality offspring. In this hypothetical example of selection in action, the males most likely to produce the most offspring were those who were indiscriminate and mated with as many females as possible, and the females who were most likely to produce the highest quality offspring—the ones most likely to survive and have offspring who then also had offspring—were those that were choosy. In that regard, the flow of assumptions and their predictions seem to make good evolutionary sense. But it makes good evolutionary sense only if we can in real time see the work of selection. In fact, in most cases it is very hard to see selection in action even in naturalistic field observations and in laboratory experiments unless an observer can demonstrate the veracity of all three assumptions.
These ideas make so much sense to some readers that they suspect that past selection associated with anisogamy and parental investment honed and mostly eliminated the original within-sex variation in choosy and indiscriminate behavior. Such readers “believe” that almost invariably males are indiscriminate and females choosy. For them, the ideas are proof enough. But that is not how science works. Put aside—for the moment—the problem that these two ideas seem like a good excuse for the double standard, something that may say quite a lot about why these ideas blossomed after 1950 (see Gowaty, 2018). Science demands sound evidence. In the case of selection arguments, one must try to demonstrate all three links in the syllogism of selection. Without that, one only has correlation, and as you know, correlation is not causation. And, as you will shortly see, there are alternative hypotheses that we must consider in any quest to understand sex differences and similarities in behavior.
(p.91) The linchpin in the classical argument about the origin of sex differences in reproductive behavior was a mid-20th-century paper by Angus J. Bateman (1948), who reported a huge experiment using 65 different small populations of fruit flies (Drosophila melanogaster). Bateman predicted that in these small populations, males would have more variation in their numbers of mates than females and that males with more mates would have more offspring; as a consequence, the number of offspring would be more variable among males than among females. This pattern would imply that evolutionary potential was greater in males than in females. Finally, he also predicted that the overall number of offspring would depend more on number of mates for males than for females.
Robert Trivers (1972), the originator of the parental investment idea, made Bateman’s 1948 paper—and “Bateman’s principles”—famous. And many modern investigators claim that their data are consistent with Bateman’s principles. For them, sex differences in the dependence of reproductive success on numbers of mates explain why males act as randy, indiscriminate cads and females as coy, choosy “gold diggers.” They are persuaded that the answer to our gendered mate choices resides entirely with Bateman-like sex differences in variability in fitness, with females being more similar to each other in reproductive success than are males. That belief, coupled with the evolutionary tenet of selection acting on heritable variability, leads to the conclusion that males continue to evolve far more than do females. Males, then it is said, are more powerful in evolution than females, according to this line of reasoning.
Fitness variation does generally seem to be greater in males than in females, and greater variation in number of offspring does appear to be associated with greater variation in number of mates for males than for females. The veracity of these results in terms of the classical model depends, however, on whether its assumptions are met in studies of sex differences in the dependence of number of offspring on number of mates. What if female-female sexual selection is not over number of mates, but quality of mates? If that were so, the appropriate analysis is not of sex differences in the association of number of mates with reproductive success. The appropriate analysis requires investigation, for each (p.92) sex separately, of the relevant fitness components—that is, components of fitness in females hypothetically associated with the mechanisms of sexual selection among females, and the components of fitness in males hypothetically associated with mechanisms of sexual selection among males. Note that these suggested analyses are arguments that are different from the classical arguments about the relative COR for females as compared to males.
As far as I know, no one has done those analyses. Moreover, Bateman’s paper is riddled with inferential and statistical errors (Snyder & Gowaty, 2007), as well as fatal methodological and logical flaws (Gowaty, Kim, & Anderson, 2012, 2013). Most of these serious errors have gone unrecognized by generations of professors and graduate students (see Gowaty, 2018). Fortunately, in recent years investigators found Bateman’s original lab notebooks containing his raw data, which are now available for appropriate analysis. The title of the forthcoming paper (Hoquet et al., in preparation) says it all—“Bateman’s data are inconsistent with Bateman’s principles.” The persistence of Bateman’s principles despite mistakes and flaws in the original paper speaks to the psychological and sociological credulity of some modern students of sex differences in behavior (Gowaty, 2018).
What is needed, then, are carefully constructed observations and experiments to find out whether females are always choosy and males are always indiscriminate. Do the data of nature match the predictions of anisogamy and parental investment theories? As a scientist studying the origins of sex differences in behavior, my job has been to find out how the data do or do not match the predictions of theory. I have spent years studying, in female and male subjects, whether females are more likely to be choosy and males are more likely to be indiscriminate. My studies in several species of fruit flies and in mice have shown that females are often as indiscriminate as males and males are often as choosy as females (Anderson, Kim, & Gowaty, 2007; Drickamer, Gowaty, & Wagner, 2003; Gowaty, Drickamer, & Schmid-Holmes, 2003; Gowaty, Kim, Rawlings, & Anderson, 2010; Gowaty, Steinichen, & Anderson, 2002, 2003; Moore, Gowaty, & Moore, 2003).
(p.93) Flexible Individual Behavior Is an Alternative Hypothesis to the Classical Model for the Origins of Sex Differences in Behavior
In the opening to this chapter, I announced:
Being gendered is a life-long process of becoming . . . Behaving in ways typical of females or males, or typical of both, or typical of neither, expresses a developmental (ontogenetic) process of continually becoming.
This claim comes from The Theory of Mating (Gowaty & Hubbell, 2009, and in progress), a series of formal deductive analytical models that demonstrate mathematically that individual flexibility will more reliably enhance fitness in an enormous range of environments compared to fixed (invariant) sex-specific patterns of reproductive decision making. The mathematical model derived from mating theory described here is the switch point theorem (SPT).
Figure 4.1 depicts a scenario for the evolution of individuals who can modify their behavior in response to changes in key parameters of the environment (Gowaty & Hubbell, 2009, 2010, 2012, 2013). In this scenario, changes in an individual’s physical and social circumstances can induce in real time—not over generations—changes in the individual’s behavior, specifically reproductive decision making. The key selection idea is this: Given variable life-history contexts, selection favors individuals who can and do change the way they behave to achieve a better fit to their changing circumstances. Darwin himself likely would have approved of the SPT, which proves mathematically that in most situations, a fixed mating strategy—whether choosy or indiscriminate—would be selected against. That is, individuals who did not change their behavior as their ecological situations changed would have left fewer descendants than those that can and do change. The SPT starts with individuals, not members of a sex category, and the inducing variables in the SPT act on individuals—as though blind to their sexes—and, in that sense, the SPT is sex neutral.
The SPT posits that chance (stochastic) events in individual life histories that affect individuals’ encounters with potential mates or the likelihood of their continued survival (for instance, potential mates that an individual randomly bumps into or events that alter the odds of the individual’s survival), as well as evolved capacities of individuals (p.95) to be sensitive to their own life-history circumstances, contribute to an individual’s likelihood of behaving in a choosy or indiscriminate way at any particular point in time. An important parameter in SPT is the w-distribution, which we assume individuals learn about during development before they are receptive to mating. The w-distribution is the distribution of fitness values in a population of mating or potentially mating individuals. The w-distribution is a theoretical construct; it is based on a matrix (a grid of columns and rows that define cells) that, although impossible to measure in any real-world situation, is assumed to have measureable empirical effects and in that sense is testable. The cells in the matrix contain the fitness values for every female mated to every male and every male mated to every female. Note that because females vary, their achieved fitness with males will vary and vice versa. The w-distribution is a useful metric, and if we imagine that individuals in a population know something about the w-distribution, their reproductive decisions will be enhanced. For example, imagine that the w-distribution is highly right skewed (values clumped close to 1), meaning that no matter with whom a female or male mates, she/he will reap high fitness. In such a circumstance, there would be little margin in waiting for a better mate, that is in acting choosy. Instead, individuals may mate on encounter, as though indiscriminate. On the other hand, if the w-distribution is flat, meaning that there is very large variation in the likely fitness conferred by any mating, individuals who “wait for a better mate”—acting as if choosy—are likely to gain greater fitness rewards.
Here’s how to think about what the SPT theorem does: First, imagine that before there was natural selection to accept or reject potential mates, there was stochastic (chance) variation in encounters with potential mates (e) and with decision makers’ likelihood of survival (s). Express survival and encounters as probabilities. Second, imagine that an individual’s encounter probability and survival probability influence the expected mean lifetime number of mates (a measure of reproductive success for an individual) and the variance in lifetime number of mates (a measure of the variation in reproductive success among individuals in a population). Both of these measures are important for evolutionary inferences. Third, (p.96) imagine that in a population of n potential mates of varying quality, there are up to n different fitness qualities among the potential mates (<n in a more homogeneous population). Fourth, make the reasonable informal assumption that mate assessment is self-referential, meaning that individuals may take their own variation into account when ranking potential mates in a population, while also using information that they learned during development about themselves. Fifth, hypothesize that individuals update their information as e, s, n, and w-distribution change in real time, to predict adaptive acceptance and rejection of potential mates. The SPT says that individuals who are flexible—sometimes waiting to mate (as if “choosy”) and sometimes mating on encounter (as if “indiscriminate”) thereby maximize their instantaneous contributions to lifetime fitness.
The predictions of the SPT are quantitative. You are invited to consider the nuances later. In the meantime, it is useful for you to know that one’s expected lifetime number of mates will be higher in general when long-term survival is likely (high s) rather than unlikely (low s). Similarly, individuals with higher encounter rates, e, will have a higher expected lifetime number of mates than when e is low. If you understand something about how probability works, you are ahead of the game in the SPT. For instance, a high chance of rain might be announced on the evening news—and yet it doesn’t necessarily rain. So even when one has a high s or a high e, one could—by chance—die tomorrow or never encounter another potential mate.
The probabilities of s and e also affect the movement of the switch point along the axis of all potential mates ranked for fitness quality (i.e., along the x-axis in the right-hand graph in Figure 4.1, with the best potential mate—#1—on the left end, at the origin of the axis). Higher s and e mean in general that the switch point will be toward the left. That is, with good prospects for a long life and plenty of mate encounters, the individual should hold out for high-quality mates; accept few, reject many. If these probabilities decline, the switch point will move toward the right, meaning that more potential mates fall into the acceptable category; fewer would be rejected. The distribution of fitness also affects the switch point: If the w-distribution is skewed toward high-quality mates, most potential mates (p.97) will be acceptable, no matter what an individual’s s or e is. Under such circumstances, most potential mates will boost lifetime fitness, so the mating decision rule would be to mate on encounter, as though “indiscriminate.”
Something important you might notice when comparing the classical model to the SPT concerns the legacy of selection in past generations. In the classical model, selection in past generations favored different traits in females and males, and those traits were assumed to manifest in the behavior of contemporary individuals. In the SPT, selection in past generations favored flexible individuals who were sensitive to environmental changes and modified their behavior in response to those changes. The SPT predicts that flexibility is adaptive and the rules of the SPT show why flexibility is adaptive in almost all demographic circumstances, so that differences in the behavior of contemporary individuals reflect differences in their ecological and social circumstances.
Although both classical theory and the SPT are about Darwinian selection, the SPT does things that classical theory could never do. Among the absolute, can’t-get-around-it essentials of mating are that to mate you must be alive and you must encounter a potential mate. The SPT starts with the absolute essentials and expresses those essentials as stochastic (chance) probabilities. It assumes further that chance effects on life span and mate encounters are certainties, and these probabilities have huge effects on an individual’s expected mean lifetime mating success and reproductive decision making. The SPT models the real world better than the classical model does, because the SPT assumes that individuals live in variable environments, and that the “best fit” individuals will be ones who evaluate their circumstances (perhaps unconsciously) and change their behavior (again, perhaps unconsciously) to fit their particular and unique circumstances.
The value of the SPT does not depend on it being complete and true. However, it is a theorem, and it is a mathematically proven theorem, and that is meaningful. Like all mathematically proven theorems, it cannot be rejected. It might not work in some systems, which is different from a rejection of the theory. For example, Newtonian mechanics do not work (p.98) in some non-Earth bound systems, but do work reliably on Earth. Thus, the questions you should ask about the SPT include whether its assumptions are met in systems of mating decisions in the real world. It is hard to argue with its essentials: One must be alive to mate and one must encounter potential mates. As students of psychology, you can imagine the kinds of observations or experiments that would enable you to test the reliability of its predictions.
The matrix on which the w-distribution is based represents what we assume individuals “know” about the likely fitness benefits of a particular reproductive decision—either to wait to mate or mate on encounter. The assumption about the w-distribution is the most vulnerable in the theory because we know so little about the mechanistic basis of evaluating potential mates, not to mention that there are fewer than 10 measured w-distributions from either captive or wild populations. We—the scientific community—know almost nothing about the w-distributions of populations, although because they have been described in field and lab populations, w-distributions can be empirically measured.
Humans have long known that outbreeding produces the healthiest offspring. Known as “hybrid vigor” in old literature, today we talk about potential genetic parents’ complementarity with respect to genes that code for certain proteins related to immune function, and we hypothesize that the more variable is the parental dyad (more complementary to each other having different immune coding genes), the healthier their offspring will be. Because healthy offspring are more likely to live long and prosper, parents who produce them will likely have future descendants and high lineage success.
Evolutionary Origins of Gendered Behavior and the Potential for Interdisciplinary Inquiry
According to the SPT, there is nothing so like a female as a male and nothing so like a male as a female. Whether it is a genetic female or a (p.99) genetic male, a fruit fly with, for instance, dim prospects for surviving and encountering a mate will mate relatively indiscriminately, whereas a fly with better prospects for future survival and encounters with potential mates will be relatively choosy. Most (not all) psychologists are interested in humans. Does the SPT apply to people? Homo sapiens evolved and are evolving; humans, like flies, are animals. So, in theory, human behavior is amenable to evolutionary analysis. In deciding for yourself the relevance of the SPT to people, it will be helpful to remember that in the SPT, environment is broadly defined as encompassing physical (e.g., climate, topography, availability of fresh water, etc.) and social (e.g., population density, friendship networks, cultural norms, etc.) circumstances. In the SPT, culture is not “outside” of nature or an “alternative” to “biology.” It follows from the SPT that, for instance, the double standard, which creates different developmental contexts for children assigned to different sex categories, is likely to generate “sex differences” in mating strategies—for example, if daughters are not allowed the opportunity to meet and greet potential mates as often as sons. It also follows from the SPT that more egalitarian contexts will result in girls/women and boys/men inhabiting more similar environments and therefore behaving more similarly.
From the SPT come insights remarkably consistent with the ideas of theorists in sociology and psychology who argue against sex/gender invariants, such as “boys will be boys.” Consistent with the SPT, some theorists in psychology and sociology argue that culturally imposed rules codifying what children are allowed to learn and to do constrain their future development, cutting off opportunities for individuals in any sex category. Also like the SPT, some theorists view gendered behavior as flexible throughout the life span. The new evolutionary theory is not the same as sociological or psychological theories, but it shares with them an emphasis on flexible, contingent behavioral expression. These theories share a view of behavioral sex differences as deriving not from some binary essence passed down across generations but rather from dynamic interplay between flexible individuals and their life circumstances.
Consensus on the flexibility and environmental contingency of expressions of gender creates opportunities for new thinking across (p.100) disciplines. Psychologists know how to study processes important in the SPT, such as monitoring the environment, evaluating potential mates, and transmitting information within and across generations. Sociologists know how to study social institutions, organizations, and movements that comprise important features of individuals’ circumstances. Research combining the expertise of biologists, psychologists, and sociologists will provide robust outcomes in tests of the SPT predictions.
As a biologist, I find it daunting to consider the prospects of getting the kind of evidence for humans that would allow strong causal inferences about evolution. For practical and ethical reasons, researchers working with humans cannot randomly assign babies or adults to experimental populations to see how mate choices or fitness are affected. Also, assessing some constructs—such as number of sexual encounters and differential survival—is tricky in humans. Self-report measures, for instance, are vulnerable to people lying about, forgetting about, or differently defining sexual encounters. How diverse groups of scholars might navigate these challenges to bridge disciplines remains to be seen.
This chapter aimed to help you to understand and think critically about theories and data regarding the evolution of gendered behavior. It hopefully made clear why you should not assume that all contemporary evolutionary theories posit fixed, innate, “hard-wired” sex differences or other reductionist or deterministic accounts of behavior. Nonetheless, as you read the literature, you will likely encounter debates about evolutionary processes and mechanisms, even among scholars who agree that social context shapes behavior. The tools that this chapter has offered may enable you to make sense of those debates by considering the assumptions theorists make, as well as dissecting their arguments and evidence.
Altmann, J. (1997). Mate choice and intrasexual reproductive competition: Contributions to reproduction that go beyond acquiring more mates. In P. A. Gowaty (Ed.), Feminism and evolutionary biology (pp. 320–333). New York, NY: Springer.
Anderson, W. W., Kim, Y. K., & Gowaty, P.A. (2007). Experimental constraints on mate preferences in Drosophila pseudoobscura decrease offspring viability and fitness of mated pairs. Proceedings of the National Academy of Sciences of the United States of America, 104, 4484–4488.
Arnold, S. J. (1994). Bateman principles and the measurement of sexual selection in plants and animals. American Naturalist, 144, S126–S149.
Bateman, A. (1948). lntra-sexual selection in Drosophila. Heredity, 2, 349–368.
Crews, D. (2012). The (bi)sexual brain. EMBO Reports, 13(9), 779–784.
Darwin, C. (1859). The origin of species by means of natural selection. London, UK: John Murray.
Darwin, C. (1871). The descent of man, and selection in relation to sex. London, UK: John Murray.
Drickamer, L. C., Gowaty, P. A., & Wagner, D. M. (2003). Free mutual mate preferences in house mice affect reproductive success and offspring performance. Animal Behaviour, 65, 105–114.
Fausto-Sterling, A. (2000). Sexing the body: Gender politics and the construction of sexuality. New York, NY: Basic Books.
Fausto-Sterling, A. (2012). Sex/gender: Biology in a social world. New York, NY: Routledge.
Gorelick, R., Carpinone, J., & Derraugh, L. J. (2016). No universal differences between female and male eukaryotes: Anisogamy and asymmetrical female meiosis. Biological Journal of the Linnean Society, 120(1), 1–21.
Gowaty, P. A. (2010). Forced or aggressively coerced copulation. In M. Breed & J. Moore (Eds.), Encylopedia of animal behavior (pp. 759–763). Oxford, UK: Academic Press.
Gowaty, P. A. (2011). What is sexual selection and the short herstory of female trait variation. Behavioral Ecology, 22, 1146–1147.
Gowaty, P. A. (2014). Standing on Darwin’s shoulders: The nature of selection hypotheses. In Hoquet T. (Ed.), What’s left of sexual selection? New York, NY: Springer.
Gowaty, P. A. (2018a). Biological essentialism, gender, true belief, confirmation biases, and skepticism. In C. Travis (Ed.), APA handbook of the psychology of women (pp. 145–164). Washington, DC: American Psychological Association.
Gowaty, P. A. (2018b). Sexual conflict theory. In H. Callan (Ed.), International encyclopedia of anthropology (pp. 1–6). New York, NY: John Wiley & Sons.
Gowaty, P. A., Drickamer, L. C., & Schmid-Holmes, S. (2003a). Male house mice produce fewer offspring with lower viability and poorer performance when mated with females they do not prefer. Animal Behaviour, 65, 95–103.
Gowaty, P. A., & Hubbell, S. P. (2009). Reproductive decisions under ecological constraints: It’s about time. Proceedings of the National Academy of Sciences of the United States of America, 106, 10017–10024.
(p.102) Gowaty, P. A, & Hubbell, S. P. (2010). Killing time: A mechanism of sexual selection and sexual conflict. In J. Leonard & A. Cordoba-Aguilar (Eds.), The evolution of primary sexual characters in animals (pp. 79–96). New York, NY: Oxford University Press.
Gowaty, P. A., & Hubbell, S. P. (2012). The evolutionary origins of mating failures and multiple mating. Entomologia Experimentalis et Applicata, 146, 11–25.
Gowaty, P. A, & Hubbell, S. P. (2013). Bayesian animals sense ecological constraints to predict fitness and organize individually flexible reproductive decisions. Behavior and Brain Sciences, 36, 215–216.
Gowaty, P. A., Kim, Y.-K., & Anderson, W. W. (2012). No evidence of sexual selection in a repetition of Bateman’s classical study of Drosophila melanogaster. Proceedings of the National Academy of Sciences of the United States of America, 109, 11740–11745.
Gowaty, P. A., Kim, Y.-K., & Anderson, W. W. (2013). Mendel’s law reveals fatal flaws in Bateman’s 1948 study of mating and fitness. Fly, 7, 28–38.
Gowaty, P. A., Kim, Y. K., Rawlings, J., & Anderson, W. W. (2010). Polyandry increases offspring viability and mother productivity but does not decrease mother survival in Drosophila pseudoobscura. Proceedings of the National Academy of Sciences of the United States of America, 107, 13771–13776.
Gowaty, P. A., Steinichen, R., & Anderson, W. W. (2002). Mutual interest between the sexes and reproductive success in Drosophila pseudoobscura. Evolution, 56, 2537–2540.
Gowaty, P. A., Steinichen, R., & Anderson, W. W. (2003). Indiscriminate females and choosy males: Within- and between-species variation in Drosophila. Evolution, 57, 2037–2045.
Hines, M. (2005). Brain gender. New York, NY: Oxford University Press.
Hoquet, T., W. C. Bridges,P. A. Gowaty (submitted). Bateman’s data are inconsistent with Bateman’s Principles. PeerJ (in review).
Jablonka, E., Lamb, M. J., & Zeligowski, A. (2014). Evolution in four dimensions, revised edition: Genetic, epigenetic, behavioral, and symbolic variation in the history of life. Cambridge, MA: MIT Press.
Moore, A. J., Gowaty, P. A., & Moore, P. J. (2003). Females avoid manipulative males and live longer. Journal of Evolutionary Biology, 16, 523–530.
Morris, J. A., Jordan, C. L., & Breedlove, M. (2004). Sexual differentiation of the vertebrate nervous system. Nature Neuroscience, 7, 1034–1039.
Parker, G. A., Baker, R., & Smith, V. (1972). The origin and evolution of gamete dimorphism and the male-female phenomenon. Journal of Theoretical Biology, 36, 529–553.
Roughgarden, J. (2013). Evolution’s rainbow: Diversity, gender, and sexuality in nature and people. Berkeley: University of California Press.
Salk, R. & Hyde, J. S. (2012). Contemporary genetics for gender researchers: Not your grandma’s genetics anymore. Psychology of Women Quarterly, 36, 395–410.
Schagdarsurengin, U., & Steger, K. (2016). Epigenetics in male reproduction: Effect of paternal diet on sperm quality and offspring health. Nature Reviews Urology, 13, 584–595.
Snyder, B. F., & Gowaty, P. A. (2007). A reappraisal of Bateman’s classical study of intrasexual selection. Evolution, 61, 2457–2468.
Trivers, R. (1972). Parental investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man (pp. 139–179). Chicago, IL: Aldine Press.