Insurgencies against misogyny (including rape, aggression violence against girls and women, sexual coercion, sexual harassment, or pay discrimination) seem greater today than at any time in my life. The revolts remind me of a dramatic image, on a cover of Science of two Hanuman langur females charging at an adult male who had an infant in his clutches. The collaborative ferocity of the females captured the backstory: the male had seized the infant from its mother and wounded it, an attempted “sexually selected infanticide”. The two females retrieved the infant, and one of the females continued to harass the would-be killer as the other female returned the infant to its mother. The revolts reminded me of bonobos too, the make-love-not-war chimpanzees in which females are dominant to males, and female-female friendships seem to trump all. “Sisterhood” is powerful in non-humans just as it was in 1960s and 1970s feminism.
To understand the evolutionary implications of female pushback against male control requires more attention to the evolutionary sources of insurgencies. Why do females act as though their own control of reproductive decisions is important? What selection pressures favor the agency and power of females?
The compensation hypothesis provides answers to these questions and its main points are captured here:
1. The most crucial component of reproductive success is having children who survive to have their own children, a reproductive success component called “offspring viability.”
2. Mating preferences – liking one potential mate but not another – predict the health of future offspring.
3. Within populations the ecological and social environments in which females live vary, and females vary intrinsically as well.
4. Extrinsic circumstances and intrinsic traits affect the abilities of females to remain in control of their reproductive decisions.
5. Females with greater control of the reproductive decisions about with whom they mate have healthier, longer-lived offspring than females who have less control. 
6. Females without or with little control of their reproductive decisions attempt to compensate – try to match the success of females with more control – by laying more eggs or giving birth to more offspring than females with greater reproductive control, and compensating females thereby often incur significant costs to their own survival.
The last two of these assumptions confuse those who fail to appreciate that mothers may be competing to produce not just a lot of eggs or pups, but healthy offspring: To win or place or stay even with un-constrained females – those who got to mate with their most preferred partners — constrained females compensate by laying more eggs or giving birth to more young, on the “hope” that some of her offspring – assumed to be less healthy than the offspring of unconstrained females – also enter their own breeding cohort. Having even one grandchild keeps a lineage alive.
What these two assumptions indicate is that sometimes females with less control must give birth to more offspring to guarantee than any of her offspring make it into their own breeding cohort. It means that in a comparison of reproductive success among females that the best predictor of lineage success is the health of a female’s kids, i.e., the number of her eggs or pups that grow up and breed. In other words, the best measure of reproductive success is having offspring that have offspring.
Given the compensation hypothesis, it is possible to make some predictions about the dynamics of different social systems, that is, if one also takes into account what might happen not just to female fitness, but also to male-male competitive dynamics when females are in control of their own reproductive decisions. Yes, these ideas put females in the center, and the news is not all bad for males either. The transmogrified compensation hypothesis, which we can now call the “female control hypothesis” (FCH), makes two additional assumptions that the CH did not make:
1. When females have the least control of their own reproduction, many males also have little control of their own reproductive decision-making.
2. The more control individual females have over their own reproductive decisions, the more individual males have control over theirs.
These two additional assumptions allow for more predictions: Not only does it predict the Familiar idea that compared to females with little or no fecundity – laying fewer eggs or giving birth to fewer young that are healthier, live longer, and are more likely to produce grand-offspring. But, importantly, it also says that when females have more control of reproduction, the variance in male mating success is reduced, making more males into winners, reducing the number of “loser males” who have little or no sexual access to females. In human sociological terms the hypothesis predicts variation in the magnitude of population-wide birth rates, the health of children, and the reproductive fates of men. The explicit – and testable — assumptions of the female control hypothesis are in Figure 2.
Figure 1. The assumptions of the compensation hypothesis are that a preferred mate is one with whom a chooser would have highly viable (healthy) offspring (1st panel). Constrained females are those unable to mate with the males they uniquely prefer, and it is constrained females that give birth to more offspring or lay more eggs than females mated with males they do uniquely prefer (2rd panel), which sometimes results in constrained females producing as many offspring as unconstrained females, i.e., those able to mate with the males they preferred. Costs to constrained females that compensate by increasing fecundity result in shorter lifespans for constrained females that compensate compared to constrained females that do not compensate.
Given its assumptions, the female control hypothesis (Figure 2) predicts qualitatively the lifespan of females, the number of eggs or pups that females produce, the viability of their offspring, and the variance among males in their reproductive success. The FCH also makes predictions about the nature of coalitions (not discussed here) among individuals against the forces that limit females’ reproductive control.
Figure 3. The Female Control Hypothesis assumes that female control of reproductive decisions is the key variable influencing the fitness of females, their mates, and their offspring.
In the graphs, the components of fitness are general indicating the application of the FCH to non-human and humans. The societal correlates of female reproductive autonomy are indicated as low in tribal-despotic societies but much higher in democratic, equalitarian, and open societies.
Understanding the pathways to the FCH and its predictions about fitness outcomes for females, males and offspring, might require a bit of history about the nature of sexual power dynamics.
Almost half a century ago, when the middle class in the United States was still going strong, Gordon Orians hypothesized that polygyny – in which a male simultaneously lives with and mates with more than one female – occurs because of the settling decisions of females when they were seeking nesting territories usually in the early spring, a birdy idea later applied to humansOrians’ polygyny threshold hypothesis (PTH) (Figure 3) was in keeping with Darwin’s that it’s the females who choose mates not the other way around, but Orians’ theory importantly did not promulgate Darwin’s notion of coy and passive females. Rather, the females Orians imagined were in control of their own social behavior and the reproductive success variation of males. The PTH assumed that females were entirely in charge of where they settled and with whom they would mate – in other words there was little scope for sexual conflict.
The idea also assumed that male parental care always enhanced female reproductive success (in birds males often feed nestlings). When a female opted to mate with an already-mated male, she made him polygynous, and increased his likely number of offspring compared to a male with only one mate. However, these king-maker females also risked having to work harder to raise their offspring, because the now-polygynous male would be splitting his parenting between the offspring of two females, or worse, only providing care for the offspring of the first female who settled. Orians assumed then that a female settling with an already mated male lowered her own reproductive success compared to monogamously mated females in the same kind of habitat (e.g., habitats with similar number of insects for feeding nestlings), an assumption that silently embodied the idea that all females were intrinsically alike in their parenting competencies.
But Orians’ theory also provided an out for females in the form of variation in habitat quality meaning that some breeding places were better than others because there were better food availability, for example. If there was ecologically significant habitat variation, the cost of polygyny for a female who settled with an already-mated male could be offset if the territory was a superior one: the reproductive success of a female mating with an already-mated male in fact could be equal or even greater than the fitness of monogamously mated females on an inferior territory. In other words, the PTH says that females can trade off male help in raising offspring with habitat quality, and this predicted a new thing: induced, flexible (contingent) behavior of females in response to male mating status and his territory quality.
Figure 3. (copied from (Orians 1969)). The elegance of the polygyny threshold hypothesis is captured in the graph illustrating the main assumptions of the PTH. The vertical or y-axis is female fitness in terms of reproductive success predicted by the interaction of the variation in the horizontal, or x-axis parameter of “environmental quality” with the amount of help a female was likely to get if she joined an unmated male (indicated by the top curve) compared to if she joined an already mated male (the bottom curve). The PTH assumed that male help always enhanced female fitness as indicated by the relationship of the two curves on the graph. It also assumed that environmental quality was a forcing function such that better habitats predicted higher fitness. The polygyny threshold line – indicated by the dashed line marked “2” shows the difference in habitat quality needed to make up the fitness loss to a female who mates with an already mated male rather than an unmated male.
When I was a young scientist, Orians’ approach provided me with a vivid lesson in the power of deduction. His idea encouraged me to test its assumptions and predictions and it captivated me so that I modified the model to account for the evolution of helping systems. Like Orians’ model, my extended x-axis was environmental quality, which included poorer and poorer quality habitats. That is, both the PTH and my new extension assumed that habitats could be the constraint that favored the evolution of social polyandry (a female simultaneously consorting with two males – all on the same territory). The y-axis again was fitness, but this time, it was for a threesome. The logic works to explain the evolution of some types of helping too. At the time, all sorts of alternatives were afoot to explain helping behavior, most centered on kin-selection. However, both the models of Fig. 2 & 3 emphasized that environmental contingency could result in induced flexible behavior of both sexes to produce some of the variations of social groups common in nature.
Despite what the PTH said to me, others interpreted the PTH more broadly, inserting assumptions that felt much like the social fabric of its time, namely that female fitness was really determined by a male’s help and his territorial resources (in bird world, “his wealth”), setting the stage for backlash selective scenarios of female dependency, male control of social organization and individual behavior that, in the 1970s, became the rule under sociobiology. In contrast to Orians’ notion that females were in control of their own survival probabilities and their own reproductive success, Bob Trivers argued that male-male competitive contests resulted in extra-pair paternity in which a male mated monogamously (with one female) but sought copulations with other females socially paired with other males. Trivers’ idea predicted that monogamously mated males would contribute care to the offspring of their territorial mate, but simultaneously seek copulations with other females whom he would not help raise the offspring. Trivers’ idea following on Darwin’s said that male-driven sexual conflict – uncertain paternity – is the center piece of the dynamics of sex. Trivers emphasized the assumption that the number of offspring a female had was unaffected by the number of mates she had, but that male reproductive success was limited only by the number of females he uniquely mated, both ideas modern data challenge. He emphasized too the risk to females of males withdrawing parental care if their paternity certainty was questionable.
Darwin’s and Trivers ideas assumed female dependency on males, which as a young scientist I saw as a type of propaganda, not consistent with the bellicose female bluebirds I was watching, or the curious cases of most female mammals who had it all and did it all (finding the nesting spot, gestating the fetuses, nursing the pups, and nudging them to independence). Orians’ idea at least had female agency front and center, with the dependency of females on males being associated with the fact that migrating male birds arrived first on breeding grounds, so that males, when they could, “brokered female access” to nesting opportunities.
Female dependency wasn’t universal no matter what Darwin said in 1871 or Trivers in 1972.
Unlike mammals, bird males can do many of the parenting activities that females do. Male birds often build nests; in some species, males incubate, and in a large majority of passerines males feed nestlings, thus the competencies of female birds were just not as clear to observers as say, the parenting competency of female mice. A field experiment showed that the fitness of “socially monogamous” female eastern bluebirds did not depend on male help. Controversial at first, that study was followed by many others (see reviews in (Gowaty 1999, Gowaty 2006), showing that the fitness benefits of male help in raising offspring was environmentally contingent, so that females often were able to raise their offspring alone without decrements in their numbers of surviving and returning offspring.
Post Trivers, molecular genetic characterization of parentage revealed in the majority of tested socially monogamous birds (see review, (Gowaty 2006) extra-pair paternity (EPP), which happens when a socially monogamous female mates with her cohabitor, but also with other males, so that in single broods there are multiple sires. At first, investigators claimed that EPP was best explained as a result of males forcing copulation on faithfully monogamous, passive females, a form of male-male competitive behavior. That possibility rang suspicious to those of us aware of what really happens when passerines have sex. For sperm to be successfully transferred requires as much female agency as male in that both sexes must evert the second compartments of their cloacae through their vents to the air for the tissues to touch in the pair’s cloacal kiss. Male aggression against females in passerines often looks like doggy-style doing it, in that a male may stand on a female’s back and bite her neck or otherwise rough her up. But discerning whether bird doggy-style is an efficient transfer of sperm or something else entirely is in most instances a matter of the observers’ imaginations, as the real sex acts of half the birds in the world, the cloacal kisses, are almost instantaneous (e.g. in bluebirds about 4 seconds), and extremely difficult to see, particularly in wild-living birds. The female-active postures of cloacal kisses are quite different from the receptive posture of doggy-style in most mammals or the missionary-style of many people: The mechanics of passerine copulation guarantee females’ agency in the sex act. And, some birds do it in flight, on the wing! And, in most bird species, female can just fly away, so that forced copulation is additionally unlikely.
As more scientists studied avian mating behavior from a female-centric perspective, the debate swiveled back to Orians-like assumptions that females had profound influence on social organizations. Radio-telemetered female subjects (Neudorf, Stutchbury et al. 1997, Pitcher and Stutchbury 2000, Woolfenden, Stutchbury et al. 2005, Chiver, Stutchbury et al. 2008, Evans, Stutchbury et al. 2008) left their home territories to seek copulations with other males; and molecular genetics studies confirmed that female-solicited extra-pair mating resulted in extrapair offspring, again revealing the lie of female coyness and passivity.
The most informative example of the evolutionary agency of females came from an experiment investigating “sexually antagonistic co-evolution”. Here the assumptions are that females and males inevitably share many genes, some of which are fitness enhancing in one sex, but fitness depressing in the other. The force of sexually antagonistic coevolution – an evolutionary sea-saw – might most often produce dynamic equipoise in the power of one sex to manipulate and control the other. Rice wondered what would happen if he produced a dramatic power asymmetry with males having greater power than females. He used captive flies from the species Drosophila melanogaster, and he loaded the dice on behalf of males by allowing the males to continue to evolve while arresting female evolution. Arresting female evolution meant that Rice only allowed males in the “evolving hyper males” population to mate with females from a static population started at the same time as the “evolving hyper males” population. He then used artificial selection to reinforce the usual absence of recombination in male Drosophila. After 41 generations and two replicates, there was substantial evidence of male adaptation to the females in the non-manipulated static population.
In each generation Rice kept females who evolved with hyper-males from contributing to the next generation: using two large populations, he was able to allow the evolving hyper males less and less selective push-back from females, because, instead of being allowed to mate with coevolving females, the males only mated with females from the static population. By allowing males to evolve without the force of antagonistic selection on females, females died faster probably because of the increased toxicity of male seminal fluid, which had increased the rate at which males were able to overcome the tendencies of females to delay remating.
Hyper-males apparently were able to overcome female control of reproductive decisions. But, what we do not know from Rice’s experiment was how healthy were the offspring of hyper males with source population females as mates. Did these offspring, like their mothers, die like flies too? Were populations that evolved hyper males on the road to extinction from disease and pestilence?
What we do know is that the shrewd experimentalist created a female fly’s dystopia. And, by doing so, he implied that through evolutionary time sexually antagonistic coevolution should be a draw, a sea-saw of regularly fluctuating sexual power dynamics.
Rice explained the results of his experiment in terms of genes beneficial in one sex, but deleterious in the other, thereby producing a never-ending struggle of genes in sexually antagonistic coevolution: a perpetual war between the sexes that would be due to sexually antagonistic selective pressures.
But, is there more to this story still?
Is there a way out of this war?
What if, over evolutionary time, the interests of the sexes are more congruent than antagonistic?
Are sexually harmonious selection pressures for healthy offspring strong enough to overcome sexual antagonism?
What if females’ control of their own reproductive decisions is a more important selective force than male-male competition?
What if the most important selection pressure on individuals is the health of their offspring?
Can our germs be the leveler of sexual power asymmetries?
Many of the answers to these last questions are not known yet, but little doubt remains that the health – the viability – of offspring is important: mate preferences, not just of females, but also for males in flies, mice, and fish, and probably people and ducks too predict offspring viability. Choosers constrained to breed with the ones they did not like had less healthy offspring. Flies, cockroaches, fish, ducks, and mice represent a lot of taxonomic diversity, so it would be little surprise if a similar (illegal, immoral) experiment on people produced similar results.
Having healthy offspring who survive long enough to enter their generation’s breeding cohort to successfully produce offspring may be the brass-ring of evolutionary lineage success.
That is the conclusion from the evolutionary biologists who think about the sway of evolutionary potential of our pathogens and parasites. Our germs have vastly faster generation times than we do, meaning that over evolutionary time, it is likely that the germs win. Thus, it is said that our germs favored the evolution of sex in the first place.
Could it be that it is our germs that also favor sexual equalitarianism, equal partners in search of healthy descendants?
Of course, the proof is in the pudding of tests of the assumptions of the FCH.
Can another clever experimentalist create a female utopia, in which most females have social and ecological control of their reproduction?
Postscript: Savvy readers will know that my inspiration comes from the troubles of our times. My simultaneous engagement with science and current social rumblings is not unique: We should suspect, as science historians do (e.g., see (Desmond and Moore 2009) that current political discourse profoundly affects scientists’ thinking about behavior evolution and just might produce (biased) commitments to the concepts of male dominance, female competence, male coercive sexuality, female vulnerabilities or lack thereof and so on. Reading Desmond and Moore made me think that Darwin’s torments and his long path to publication were symptomatic of his efforts to disabuse himself of his own good ideas. Darwin’s anguish reminded me of the best short-hand definition of science I know said by Richard Feynman, “Science is a way of trying not to fool yourself. The first principle is that you must not fool yourself, and you are the easiest person to fool”. Unconscious – and perhaps conscious – misogyny has produced facile, intuitive theory, while modern feminist and scientific consciousness made vigilance against bias in observations and experiments a necessity.
We, humans around the world, are in a cultural moment of sexual conflict, not unlike that terrible and righteously ferocious “cultural moment” of langur females. Reporting of feminist insurgencies is surging perhaps because of reporting bias (more of us care about and buy newspapers that report it or click on web sites that do). I prefer to think that female push-back is truly increasing, as more and more people lobby for women’s education, as more women (and men) learn about birth control methods, as more and more resist female genital mutilation, as we work to defend abortion rights, as we seek new memes to allow more even playing fields (like California’s new rule that “yes means yes”), as we feminists find thousands of ways to resist and forge opportunities for the expansion of women’s rights.
One of my hopes is that scientific study of the phylogenetic, ecological and social contingencies that produce the variation in the evolutionary power of non-human females will give us keys to understanding how this particular human cultural moment has drifted so far from the sexual equalitarianism our germs seemed to have promised us.
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