CHAPTER 3 - EVOLUTION OF SEX AND SEX DIFFERENCES

Opening comments

I. Natural selection

A. Directional selection

B. Stabilizing selection

C. Disruptive selection

II. Evolution of sex

A. Asexual versus sexual reproduction

1. Costs

a. Energetic

b. Genetic

2. Benefits

a. Diversity

b. Red Queen

3. Best of both worlds

4. r- versus K-selection

B. Why two sexes?

1. Anisogamy

a. Its evolution

b. Its consequences

i. Mating strategies

ii. Parental investment

iii. Sexual selection

C. Sex Determination and Sex Ratio

1. Sex determination mechanisms

a. Genetic

b. Environmental

2. Sex ratio

a. Fisher's sex allocation model

b. Trivers-Willard sex ratio manipulation model

III. Parenting strategies

A. Infanticide

B. Parental favoritism and sibling rivalry

C. Parent-offspring conflict

D. Helping/Inclusive Fitness

IV. Evolutionarily stable strategies

A. Maintenance of diversity

B. Facultative mechanisms

V. Illustration: Homosexuality

A. Kin selection

B. Parental manipulation

C. Sibling rivalry

D. Pleiotropy

E. By-product

VI. Caveats on adaptationism

A. Biological determinism

B. Naturalistic fallacy

C. Scientific reductionism

D. "Just-So stories"

Closing comments

CHAPTER 3 - EVOLUTION OF SEX AND SEX DIFFERENCES

Chapter 2 addressed the proximate factors underlying sexual differentiation within the context of an individual's development or ontogeny. This chapter will address the ultimate factors underlying the development of sex differences in the context of evolutionary history or phylogeny. We will explore how and why there got to be two sexes in the first place, then why the existence of two physical sexes virtually ensures the existence of two psychological sexes.

Natural Selection

From one perspective, the ultimate answer to the existence of practically everything boils down to the concept of selection: the differential survival (and sometimes reproduction) of some entities and attributes as compared to others (Dawkins,1976). While countless objects and processes (even ideas) made an appearance for at least some period of time during the existence of the universe, those that still exist today are those that have either managed to survive or managed to get copied before being destroyed.

Artifical selection is the term used to describe the process whereby humans purposefully select which objects, processes, or attributes of things survive and get copied. This concept can be applied to inanimate objects like books, recipes, tools or art styles, as well as to living things. The practise of artificially selecting plants and animals has been around for millenia. Long before people understood anything about the concept of genetics, they understood something about heredity-- that is, the fact that offspring resemble their parents more than can be explained by chance-- and they used this knowledge in agriculture and animal husbandry to selectively breed particular individuals so as to select chosen attributes into (and out of) future generations. It is through such artificial selection that today we have so many breeds and varieties of domesticated animals and plants.

In his revolutionary book "On the Origin of Species" (1859), Charles Darwin used the idea of artifical selection as an analogy to describe the process of "natural selection". According to Darwin's model, in the absence of human intervention, nature selects which individuals will survive and reproduce, and it is those individuals who will pass on their traits and attributes to the next generation. The next generation then, will be slightly different from its predecessor; by virtue of inheriting the attributes of their parents, its members will be, on average, more like the selected individuals than those not selected. This process of population change is the idea behind the phrase "evolution by natural selection".

Working backward from this premise, Darwin realized that the traits and attributes expressed by organisms alive today must have been handed down over the generations from individuals which nature had selected to become successful parents. Traits and attributes that we see in animals and plants surviving today, therefore, must be traits and attributes that, in the past, had "adaptive value": they somehow increased the probability that the individuals expressing them were among the few that nature had selected-- the few who were successful at surviving and reproducing in the face of adversity.

Forces of nature which result in selection are called "selection pressures". These can be categorized into three major types based on their outcome.

In directional selection, only individuals with certain unusual features are successfully able to reproduce, resulting in the exaggeration of those features in subsequent generations. Imagine, for example, the effect of artificial selection over many generations for bigger and bigger udders in dairy cows, or increasing sweetness of corn. On another scale, many species of large mammal have gone extinct because of human hunting, resulting in a smaller average size for mammals today than at the time humans first appeared about five million years ago. As an example of natural selection that is directional, recall that mostly small, nocturnal creatures survived the asteroid collision that wiped out the large, diurnal dinosaurs-- or imagine the coevolutionary directional selection of cats which evolve sharper hearing in response to mice which evolve to be quieter and quieter (in response to cats which evolve sharper hearing in response to mice which evolve to be quieter and quieter in response to...). In sum, directional selection is differential survival and reproduction that results in a change in the average, or mean, expression of a trait over time. (See Figure 3.1)

Insert Figure 3.1 approx here

Stabilizing selection is neither so intuitive nor so noticeable. Rather than resulting in a change in the mean expression of a trait over time, it results in the constant, stable, expression of a trait, by favoring only those individuals or species which are statistically average. Imagine, for example, that birds with long slender bills are unable to crack hard seeds; on the other hand, thick-billed birds are unable to reach into crevices and other tight places where small seeds may be blown out of reach. When large, hard seeds are most abundant, there will be directional selection for thick-billed birds, but when small wind-blown seeds are abundant there will be selection for slender-billed birds. Furthermore, when neither type of seed is abundant and birds must be able to eat both types in order to survive, only birds with a medium-sized bill will survive. Thus, either rapid reversals of directional selection, or sustained periods of selection for the average, will lead, over time, to stabilization of the mean expression of a trait.

* (See Figure 3.2)

Insert Figure 3.2 approx here

The third type of selection, disruptive selection, might be thought of as the opposite of stabilizing selection: rather than enhanced survival and reproduction of the average, there is enhanced survival and reproduction of the extremes at the expense of the average. (See Figure 3.3). It is disruptive selection in its various forms that underlies both the divergence of species and the divergence of different morphs, or forms, within a species. The two sexes are an example of the latter.

Insert Figure 3.3 approx here

Evolution of sex

Before we ask why there are two sexes, we have to ask why there is sex at all. Some species get along just fine without sex and have managed to survive and reproduce effectively and efficiently for eons; we call them asexual, and they reproduce in a variety of ways, such as splitting, budding, sending out runners or laying fertile eggs. In each case, the offspring is genetically identical to its (single) parent; indeed, in some cases it is impossible to distinguish which is "offspring" and which is "parent".

Given that such techniques work so well for so many species, it was for a long time, a curiosity why any species bothered with sex at all (Maynard Smith, 1978a; Daly & Wilson 1978/83). Sex is, in fact, quite costly. First there are the "energetic costs" of sex: energy must be devoted to producing specialized hormones and physical and neural structures; energy must be devoted to finding and recognizing an appropriate mate; and energy must be devoted to attracting, courting, or sometimes, fighting for or with, a potential mate. Then there are the added risks that searching, courting and fighting entail-- such as being noticed by a predator, caught in unfamiliar territory, or contracting a debilitating, perhaps deadly, sexually-transmitted disease. Most costly of all are the "genetic costs". That is, in each act of sexual reproduction, each parent transmits only one-half of its genes to its offspring, so, in order to reproduce itself, each parent must have two surviving offspring. So, even assuming, temporarily, that the energy costs were the same, if one individual could manage to clone itself while another had to reproduce itself sexually, the asexual individual could leave twice as many copies of its genes in the next generation. That is about as strong a selection pressure as can be imagined, and it is in favor of asexuality. So why sex?

The benefits of reproducing sexually are two-fold, and both relate to the fundamental nature of the sex act: exchange and mix of genes. Through the process of genetic recombination (with the rare exception of polyembryony; Thornhill & Alcock, 1983), every individual will be genetically unique. This means that new combinations of traits are constantly being tested by natural selection, and adaptive change can occur at a fairly rapid rate. In asexual species, evolution is limited by the rate of mutation, so that if and when there is a dramatic or rapid change in the environment, asexual organisms may not be able to evolve rapidly enough to accomodate the change. According to this argument, selection favoring sexual species results from the fact that species that cannot change rapidly are the most likely to go extinct (Hurst & Peck, 1996; Maynard Smith, 1978a).

The second argument, sometimes called the Red Queen model (Ebert & Hamilton, 1996; Ridley, 1993; after van Valen, 1973), focuses on the role of a subset of rapidly changing selection pressures, specifically, those provided by host-parasite coevolution (Hamilton, 1980; Tooby, 1982). As in the cat-and-mouse example demonstrating directional selection, it is often the case that important selection pressures derive from other organisms sharing the same environment. Selection pressures may come from predators or prey (as in the cat/mouse example), or from other species competing for the same resources, or, perhaps most importantly, from parasites. Parasites tend to be smaller than their hosts, and to have a shorter life span and a much faster generation time. This means that if both parasites and hosts were restricted to asexual reproduction, parasites could evolve faster than their host species, essentially winning the "coevolutionary arms race" (Alexander, 1987) between them. Sexual reproduction, by creating many new genetic combinations at rates much faster than mutation alone could muster, allows host species to remain "in the race". (Herein lies the analogy to the Red Queen in Alice in Wonderland, who had to keep running just to keep in the same place). It also means that even if a parasite happens to devastate a certain portion of a population that has a certain genetic combination, there are plenty of other individuals with different genotypes who will remain unaffected. Over long periods of time, the likelihood that any particular clonal line will remain immune to parasites becomes negligible, whereas the likelihood that a sexual line will produce at least a few immune individuals each generation, is markedly greater.

Species which reproduce sexually are, therefore, "hedging their bets" and "playing it safe", whereas species which reproduce asexually are staking literally everything on one, hopefully near-perfect, clonal type. We should therefore, expect to find sexual species in rapidly changing environments and in coevolutionary arms races with parasites; asexual species should be found to have more stable environments, fewer parasites, and/or faster life cycles.

An interesting "test" of this model is provided by species which have "the best of both worlds": species which can reproduce sexually or asexually, depending on the circumstances (Daly & Wilson, 1978/83; Thornhill & Alcock, 1983). There are, from a proximate perspective, at least two ways this can happen. In some species each individual has a facultative sexual/asexual option; that is, a particular individual may reproduce sexually or asexually depending on certain relevant environmental parameters. Many common houseplants, for example, will send out asexual reproductive shoots and runners as long as they are kept in the same place and tended regularly; move them or repot them, however, and they opt for sexual reproduction and produce flowers! In other species, sexual or asexual reproduction may be obligate at a certain point in the life history cycle; certain individuals reproduce asexually (at one point in the life cycle), and others reproduce sexually (at another point in the life cycle). These species, many of them parasites themselves, tend to reproduce asexually when in the body of their host (a constant, unchanging environment in which there is no need to "hedge bets") and to reproduce sexually just before or just after being released into a new environment (e.g. through defecation or the death of the host). Non-parasitic but small, fast-breeding aphids reproduce asexually through the long summer days, but as the days shorten and winter approaches, "hedge their bets" and turn to the more costly, but less risky, sexual reproduction (Thornhill & Alcock, 1983).

Obviously, not all species which have evolved sex have retained the ability to reproduce asexually when desirable. Although some once-sexual species have reverted to being asexual (a topic which will be more fully addressed in Chapter 7), most sexual species remain obligately sexual (a paradox that still requires some resolution; Hurst & Peck, 1996). There is however, a way that even obligate sexually reproducing species vary from one another in terms of their proclivity to take reproductive risks or "hedge their bets".

At one end of a continuum is the strategy of having large numbers of offspring, each genetically different, as a way of "hedging bets" in new and changing environments. Most of the offspring are likely to be maladapted and to die without reproducing themselves, but as long as a few are well-matched to the selection pressures they face, their parents will be able to successfully transmit their genes to subsequent generations. At the other end of the continuum is the strategy of having a small number of offspring that are very likely well-suited to their environment. As long as most of these offspring are well-suited, most will survive, so parents need only produce a few offspring to ensure that their genes make it into the next generation. Species which have evolved obligate sexual reproduction but which tend to be in dynamic, rapidly changing environments or which move frequently from one environment to another, are more likely to use the former strategy; they are called r-selected species (with reference to the variable r for the "intrinsic rate of increase" in mathematical models of reproductively unconstrained populations). Obligate sexual species which are in more stable, but perhaps more competitive environments are more likely to use the latter strategy; they are called K-selected species (with reference to the variable K, in the same equation, for a habitat's "carrying capacity"; MacArthur & Wilson, 1967; Pianka, 1970).

In a way, the end result of K-selection is somewhat akin to a return to asexual reproduction: individuals cannot expect to beat the odds with low numbers of offspring unless they are very well adapted to the environment. This means that for K-selected species, like asexual species, if the environment does change rapidly, they may not be able to reproduce fast enough or produce enough diversity of genotypes to keep up with the change. If you take note of which species appear on lists of endangered and threatened species around the world, you will notice that most are species which are particularly tuned to life in a particular environment-- an environment that is now changing rapidly due to human habitat modification and destruction-- and they just can't keep up. On the other hand, "pest" species, which seem to manage to show up everywhere we don't want them, tend to be species that thrive in new environments and which adapt quickly to change.

Why TWO sexes?

There is no particular reason that there have to be two sexes in order for sexual reproduction to occur. In fact, among some algae, bacteria and slime molds, any individual can mate (exchange and mix genes) with any other individual of a different mating type (e.g. A can mate with B or C, B can mate with A or C, and C can mate with A or B; Hurst, 1991). Note the use of the term "mating type" however, rather than "sex". In these organisms there is nothing other than genes that identify a particular mating type, and it is not, therefore, possible to compare types across different species.

The term "sex" however, does refer to a set of identifiable features that are common to two distinct mating types found in most sexually reproducing species. Specifically, those individuals we label "female" are individuals that produce relatively large, nutrient-rich, immobile gametes (sex cells); males are those individuals that produce relatively small, nutrient-poor, mobile gametes. This set of correlated features distinguishing two sexes in most sexually reproducing species is technically termed anisogamy (literally: "not-same-gametes"). While a single plant or animal may produce both types of gametes (a hermaphrodite), we never find individuals that produce gametes that mix features of male and female or that have in-between features; this is because anisogamy (and all its consequences) is a product of disruptive selection (Parker, Baker, & Smith, 1972).

Recall that in disruptive selection, there is selection for both extremes of a continuum concurrent with selection against the average. Now imagine a sexually reproducing species in which all individuals can mate with all others: some individuals make large nutrient-rich gametes, some make small nutrient-poor gametes, some make in-between gametes and some make a mix of gametes. Individuals which make small nutrient-poor gametes can make many more of them than can individuals which devote significant energy toward producing larger, nutrient-rich gametes, so individuals which produce nutrient-poor gametes have a selection advantage by being able to mate many more times; this leads to an initial increase in such types over the generations.

On the other hand, the nutrient-poor zygotes that result from the joining of two nutrient-poor gametes may not have much of a chance at survival. So while "proto-males" are mating more often than "proto-females", the zygotes which come from such couplings are not surviving very well. In a population that has many proto-males, each rare proto-female thus becomes one of the few individuals whose offspring actually survive; this provides the counter-selection pressure for producing larger, nutrient-rich gametes.

Zygotes of individuals which produce in-between gametes do not gain the survival advantage that accrues to zygotes from nutrient-rich gametes, and even if such individuals always manage to find a rare proto-female to mate with, they cannot mate as many times as a proto-male. Thus, we have selection for both proto-males and proto-females as compared to average types. (See Figure 3.4)

Insert Figure 3.4 approx here

Once proto-sexes have started to diverge in terms of gamete production, anisogamy itself creates new selection pressures that lead to further differentiation of the two proto-sexes into full-fledged morphs or types. This is largely a result of the fact that proto-males have a much greater reproductive potential than proto-females.

Specifically, because proto-males can produce so many gametes, their reproductive success is largely constrained by their ability to find proto-female mating partners. This is not the case for proto-females, whose reproductive success is not so much related to their ability to find multiple partners as to their physiological ability to produce high-quality gametes. The existence of anisogamy thus results in selection pressures for proto-males to be mobile and to seek as many proto-female mating partners as possible, and for proto-females to conserve energy and invest it in their (smaller numbers of) gametes.

In this way, anisogamy creates selection pressures for proto-males and proto-females to further diverge in the amount of energy that they devote toward different components of their reproductive effort (Kodric-Brown & Brown, 1987). Proto-females, being committed to devoting large amounts of energy to the production of a relatively small number of gametes and zygotes, must, like K-selected species, ensure that their relatively few offspring have fairly low levels of mortality. Proto-males, on the other hand, like r-selected species, are committed to devoting relatively small amounts of energy to the production of large numbers of gametes and zygotes, and need not ensure the survival of more than just a few of those offspring in order to get their genes represented in the next generation. In technical terms, we say that one of the results of anisogamy is that females devote more of their total reproductive effort to parental effort (Queller, 1997), while males devote more of their total reproductive effort to mating effort (Hawkes, Rogers & Charnov, 1995).

Once two sexes are established, males and females will continue to exert coevolutionary selection pressures on one another, leading to changes in gene frequencies over time. This process of coevolutionary change between the sexes of a single species is a form of natural selection called sexual selection. Like other instances of natural selection, sexual selection can be directional, stabilizing or disruptive; the difference is that with sexual selection, the pressures can be different for the two sexes, with the end result being sexual dimorphism of both body and behavior.

Sexual dimorphism of body and behavior is, of course, what this book is all about. Evolutionary psychologists expect that psychological sex differences, like physical differences, are to a large extent a product of sexual selection. Perhaps you are already beginning to see some parallels between the behaviors and attributes of our hypothetical proto-males and females and the behaviors and attributes of real, human males and females. As mentioned in Chapter 2, males have, on average, a greater sex drive than females and, as it turns out, they also have a greater desire for a greater number of sexual partners. (This phenomenon, called the "Coolidge Effect", will be described in Chapter 4). Even sex differences in cognitive skills (e.g. spatial orientation) and personality (e.g. aggression and nurturance) can be at least partly explained as a result of ongoing disruptive selection for two different mating types.

At this point you might also be asking yourself how the differences between the sexes are maintained across generations, given that in every generation the whole point of sexual reproduction is to mix and recombine genes. Why isn't each offspring of a male-female pair something of an average between the two? The answer, if you refer back to Chapter 2, is that indeed, all genes, including those coding for, and regulating, both male and female attributes, are found in all individuals. Each parent does pass on genes for both male and female attributes to every one of his or her offspring, but which of those genes get activated during a particular individual's development is based on a sequence of specific, proximate triggers. Sexual selection cannot and does not lead to genetic differences between the two sexes; rather, it leads to differential expression of genes shared by both sexes- i.e. sex-limitation.

As described in Chapter 2, sex-limited traits can be either dichotomous or continuous. Because most of the traits psychologists are interested in are continuous, most of the sex differences we will be examining in the rest of this book will exhibit large average differences, but also large overlap between the sexes. Before we move on however, let's take one more look at the evolution of sex per se.

Sex Determination and Sex Ratio

In humans and other mammals, recall, the first proximate trigger in sexual development is the TDF supergene. TDF triggers genes for the development of testes, which, in turn, produce testosterone, which activates genes for development of additional male features; in absence of TDF, genes for ovaries and other female features are activated. Since TDF is typically present on the Y- but not the X-chromosome, and since each offspring has a 50-50 chance of inheriting a Y- or an X-chromosome from his or her father, it would seem obvious that the ratio of males to females would always, for simple statistical reasons, be very close to 1.00. This is not the case, however.

First of all, while TDF is an example of a genetic mechanism or "switch" for sex determination, not all sex determination mechanisms are genetic (Bull, 1980,1983; Charnov & Bull, 1977; Mittwoch, 1996). In some species, including a variety of fish, reptiles and amphibians, the ambient temperature during a critical period of embryo development is what determines the sex of the hatchling, and, as will be discussed in Chapter 7, individuals of some species have their sex "determined" by social, rather than physical factors (e.g. Lutnesky, 1994; Warner, 1988).

More importantly, regardless of what it is that triggers sexual differentiation, just because there are two possible outcomes does not mean that both outcomes have to occur with equal frequency. (Just think about eye color or right- and left-handedness.) Indeed, when it comes to sex determination, it is often the case that the two outcomes are not equally frequent; many species are female-biased (Hamilton, 1967).

Remember, in sexually reproducing species, males have a virtually unlimited reproductive potential, but it is the nutrient-rich gamete of the female that ensures the viability of a zygote. This means that, theoretically, a single male could sire an entire generation of offspring by mating with each female in a population. In a population of 100 consisting of 99 females and 1 male, each generational event could produce 99 offspring (at one per female); on the other hand, a population of 100 consisting of 50 males and 50 females would produce, in the same generation time, only 50 offspring. The first population should overwhelm the second very rapidly, and in so doing, should spread genes for producing large numbers of females. This is indeed what we find in some species (Hamilton, 1967)-- but not most.

Since large numbers of males are, in theory, unnecessary, why is it that so many species bother to produce so many? Why aren't all species female-biased? The first, and still major, explanation underlying the (in retrospect, surprisingly common) 50-50 sex ratio typical of so many species, came from population geneticist R.A. Fisher (see Charnov, 1982; Karlin & Lessard, 1986; and Maynard Smith, 1978a). Fisher realized that in a hypothetical population like the one described above, with 99 females and one male, selection would typically be acting on parents to produce more males. Since the single male of our hypothetical population would be father of all the offspring, it is his genes that would be preferentially transmitted into the next generation. Any female parent that could produce a second male in this mostly-female population, would, through her prolific son, get her genes preferentially into the third generation. Thus, there would be selection on females to produce sons, and any female that was successful would get her own genes- including the ones for producing sons- reappearing in future generations.

Selection on females to produce sons will persist as long as the average male has more offspring than the average female; this point is reached when the population sex ratio is at 50-50. Even if it happens that a single male sires all the offspring in a population and all other males die without issue, when the sex ratio is 1.00, the average reproductive success of males will equal the average reproductive success of females; mathematically, this is the key.

There are some systematic and predictable deviations from the 50-50 sex ratio, however. Fisher's equations actually demonstrate that parents will put 50% of their parental effort into the production of each sex. To the extent that offspring of one sex may require more parental effort than offspring of the other sex, the actual sex ratio at the time of cessation of parental reproductive effort will favor the less expensive sex in direct proportion to its lesser cost (Bodmer & Edwards, 1960). Further, the differential survival of the two sexes before parental effort is complete will also influence the final sex ratio (Maynard Smith, 1980).

In humans, in whom parental effort doesn't cease until offspring are of reproductive age themselves, the sex ratio in young adulthood (what we call the tertiary sex ratio) is about 1.00. But this is not a necessary outcome, and the full explanation for it is still unclear (Smith, 1993).

We do know that the human sex ratio at birth (the secondary sex ratio) is about 1.05 (it varies slightly at different times and places; Guttentag & Secord, 1983; Mackey, 1993), and although we don't know by how much so, we know that the sex ratio at the time of conception (the primary sex ratio) is even greater. The tertiary sex ratio reaches approximately 1.00 because males die at greater rates than females both during pregnancy and during post-natal, pre-reproductive years (Hazzard, 1994; Kellokumpu-Lehtinen & Pelliniemi, 1984; McMillen, 1979; Smart, Fraser, Roberts, Clancy & Cripps, 1982). Of course, males continue to die at higher rates at all ages, so beyond adolescence the sex ratio drops to well below 1.00 (Gosden, 1996; Hazzard, 1994).

The reproductive costs to human mothers of rearing sons versus daughters are not all known (Smith, 1993). But the fact that the sex ratio at conception is not 50-50-- despite a genetic sex determination mechanism which is transmitted through the males' gametes at the rate of 50-50-- is evidence for past selection on human females to manipulate the sex ratio.

The idea that mothers may have even greater control over the sex of their offspring than predicted by Fisher's sex allocation model was put forward by Trivers & Willard in 1973. These authors suggested that females have been selected not only to produce, on average, the optimum ratio of male and female offspring, but to do so by facultatively controlling the sex ratio of each litter or, in the case of single births, the sex of each individual offspring.

According to Fisher's model, from a mother's perspective, ALL ELSE EQUAL, the value of producing a male or a female offspring is equal when the average reproductive sucess of males in the population equals the average reproductive success of females. However, it is not the case that all else is always equal. Since the reproductive potential of an individual male is much greater than the reproductive potential of an individual female, the variability of reproductive success is always greater for males. Following this reasoning, if a mother can predict that a particular offspring is more likely to realize its reproductive potential than a randomly chosen individual in the same population, she should "try" to have a son--- because a successful son will likely be much more successful than a successful daughter. If, on the other hand, a mother can predict that a particular offspring is less likely to realize its reproductive potential than a randomly chosen individual in the same population, she should "try" to have a daughter--- because even a relatively unsuccessful daughter is more likely to at least have some offspring, than is an unsuccessful son. In sum, the reproductive value of a son versus a daughter, while equal on average, is not equal in all circumstances, and to the extent that a female can accurately assess the relevant circumstances, she should control the sex of her offspring.

The so-called "Trivers-Willard model" has now been tested in a variety of species including humans. On the whole, data support the model: mothers who are dominant over their peers, who are in better health than their peers, or who have greater access to resources than their peers, tend to give birth to more males than would be expected by chance, and vice versa (e.g. Boesch, 1997; Clutton-Brock, Albon & Guinness 1981,1984; Gaulin & Robbins, 1991; Gomendio, Clutton-Brock, Albon, Guiness & Simpson, 1990; Grant, 1990,1994; James, 1985a,1987; Mealey & Mackey, 1990; Meilke, Tilford, & Vessey, 1984; but see Hiraiwa-Hasegawa, 1993). How they manage to do so is not yet clear, but proximate mechanisms could entail selective ovulation or selective yolking of eggs (in birds; Oddie, 1998), and hormonal manipulation of the chemical constituents of vaginal secretions or manipulation of uterine or placental physiology (in mammals; Baker & Bellis, 1995; Grant, 1996; James 1986,1992; Krackow, 1995; Martin, 1994,1995; Meilke et al, 1984). Post-natal discrimination, neglect and infanticide have also been documented as a means of manipulating offspring sex ratios to promote a mother's probable reproductive success (Baker & Bellis, 1995; Cockburn, 1994; Cronk, 1991a; Dickemann, 1979,1981; Dickman, 1988; Hrdy, 1990; Krackow, 1995; McClure, 1981; Voland, 1984).

Parenting strategies

What?! Mothers may neglect or kill their offspring as a means of promoting their own reproductive success? How could killing one's offspring increase one's genetic representation in future generations? It doesn't make sense. True, at first. But then again the whole idea of sexual as opposed to asexual reproduction doesn't make sense either, until one realizes the kinds of selection pressures and constraints that each individual is up against.

Potential parents have a limit on their energy and access to resources, and most of it must go into somatic effort (Cichon, 1997; Cronk, 1991b), i.e., maintaining their own life systems; only what is left over can be devoted to reproductive effort*. In any species which requires post-natal care, a parent that devoted all of its energy into reproductive effort and none into somatic effort would leave behind a set of starving orphans; this pattern of energy allocation would quickly be selected out of future generations (Deerenberg, Arpanius, Daan & Bos, 1997).

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Some animals and plants do, in the final stage of their life, put all of their effort into reproduction. This pattern is called semelparity. It is most commonly exemplified by salmon who, upon returning to their natal stream after two to four years of maturation in the ocean, stop eating and put no further energy into maintaining body tissues or warding off disease. As they swim back to the shallows to breed, they become fungus-infested and finally reach their spawning grounds with skin and muscle tissue literally hanging off their bones. All available energy is devoted to one final act of reproduction-- and then they die.

Mammals, on the other hand (with the exception of the Australian marsupial Antechinus; Lazenby-Cohen & Cockburn, 1988; Lee & Cockburn, 1985), and other species which are iteroparous (repeat breeders) must devote a significant portion of their energy resources to self-maintenance- not only so that they can care for their current offspring but so that they can survive the ordeal to breed again! If the extra energy that it takes to rear one added offspring in a current brood is likely to deplete parental resources to the point of preventing further reproduction, then it is in the parent's reproductive interests to terminate investment in that offspring.

In what Mock & Forbes (1995) refer to as "parental optimism", many species initially invest in more offspring than can possibly survive (see also Moller, 1997; Schwabl, Mock & Gieg, 1997; Kozlowski & Stearns, 1989). For example, in marsupial mammals, young are born in what is virtually an embryonic state; they must crawl to a teat and attach there full-time in order to complete development in the mother's pouch. If a mother produces more embryos than she has teats, the last few to emerge simply die (Lee & Cockburn, 1985). The mother has not lost much at this stage since her offspring are so undeveloped, and she could not possibly provide enough milk for all of them to reach full growth. But, if a mother is in good condition and can survive the maximum parental effort of a complete litter, she should begin a few more embryos than necessary, just in case-- another form of "bet-hedging". Many bird species follow a similar pattern, laying more eggs than they can rear (Aparicio, 1997; Faaborg & Chaplin, 1988; Schwabl et al, 1997). Because birds are not dependent on lactation to nourish their young this strategy is a gamble: it might be the case that in a particular season they can raise one or two more offspring than normal, because it is a particularly good year with lots of food available.

For both mammalian and avian mothers, the best strategy is to start a few extra embryos if the mother is in good condition herself; if all goes well, she will be able to raise a maximum-sized brood. But for both mammalian and avian mothers, if more offspring are born (or hatched) than she can rear in that season, it is better to stop investing in one or a few very young infants than to try, unsuccessfully, to invest equally in all with the result that all die. Various forms of maternal "disinvestment", infanticide and infant neglect appear across a large variety species, but generally only at very early stages of offspring development (Clutton-Brock, 1991; Hausfater & Hrdy, 1984; Moller, 1997; O'Conner, 1978; Wasser & Barash, 1983).

Mothers (and in some cases fathers) must rely on environmental cues to determine whether conditions are sufficient to raise all of their young or not. Some of these cues involve the relative presence or absence of food sources; others involve the condition of the young themselves (Kozlowski & Stearns, 1989; Mock & Forbes, 1995). When pressed, parents will selectively devote parental effort toward those young which seem to have the best prospects- i.e., the oldest, the largest, the healthiest and, in some cases, offspring of a particular sex (Hausfater & Hrdy, 1984; Hrdy, 1979; Moller, 1997; Schwabl et al, 1997). Energy devoted to young which are unlikely to survive and thrive is energy that could have been allocated to more promising offspring or saved for future reproductive effort. This seemingly "cold-hearted" approach to parenting, while distasteful and difficult to "appreciate", makes perfect sense from an evolutionary perspective: sometimes it does "make sense" to abandon, neglect, or even overtly kill, one's own offspring (Daly & Wilson, 1984).

Even after the decision has been made to attempt to rear a particular offspring, discriminatory parental solicitude (Daly & Wilson, 1988,1995) may appear in other forms. For example, parents may favor one offspring over another (see Figure 3.5), or may tolerate expressions of sibling rivalry that have significant costs to one of the siblings (Mock, 1984; Schwabl et al, 1997). Sometimes, as in the case of certain human forms of parental investment, favoritism is obvious and calculated (e.g. selective endowment of dowries, inheritance, or schooling opportunites; Dickemann, 1993; Hartung, 1982; Hrdy, 1990); in other cases it may be more subtle (Sulloway, 1996; Zervas & Sherman, 1994). One of the most interesting areas of current research in human parent-offspring relations is the extent to which various cues of an offspring's potential reproductive value might influence parenting strategy (Daly & Wilson, 1984; Hill & Ball, 1996; Mann, 1992); likewise, as will be seen shortly (and in later Chapters), cues from parents to offspring may, in turn, have significant effects on the offspring's reproductive potential and choice of reproductive strategies (Stamps, 1991).

Insert Figure 3.5 approx here

(Photo of woman with twins)

As just demonstrated, the reproductive interests of a parent are not always identical to the reproductive interests of its offspring. Trivers modelled this phenomenon in another classic paper: "Parent-offspring conflict" (1974). Trivers showed that parents should terminate parental investment in a particular offspring whenever the costs (in terms of the parent's future reproduction) are more than the benefits (in terms of increased survivorship of the current offspring). From the offspring's perspective, on the other hand, as long as it is not yet ready to reproduce on its own it should continue to seek further parental investment, because its own interests always outweigh its interest in future siblings. This model was first used to understand the conflict between mothers and offspring during the process of weaning (Lee, 1996). It also predicts that very old mothers who have no future reproductive potential may not wean their last offspring until they are literally physically incapable of providing further nourishment (see Clutton-Brock, 1984 for discussion and Goodall, 1988 for an eloquent and touching example). In this regard, the last reproductive effort of an iteroparous organism may get treated as if the only reproductive effort of a semelparous species.

Further modeling has demonstrated that in cases of parent-offspring conflict it is the parents' interest that is most favored by natural selection (Alexander, 1974). This can lead, in some circumstances, to a phenomenon called parental manipulation. Parental manipulation describes the situation in which the reproductive potential of one or more offspring is actively compromised by the parent so that the parent can increase its own reproductive potential or that of another of its (more favored) offspring. In the extreme, parental manipulation can involve the uterine cannibalisation of some offspring by others (e.g. Dominey & Blumer, 1984); uterine resorption of one of a pair of twin embryos is not uncommon in humans (Corney, Seedburgh, Thompson, Campbell, MacGillivray & Timlin, 1981). In less extreme cases parental manipulation involves not the death of an offspring, but the reduction of its reproductive opportunities. An example that is seen in many species involves the "recruitment" of offspring from one breeding episode to be "helpers-at the nest" during a subsequent breeding episode (Brown, 1978; Emlen, 1978). The net result of this phenomenon is an increase in the reproductive output of parents but a detriment of the reproduction of the helping offspring.

Not all cases of cooperative breeding are a result of parental manipulation, however (Snowdon, 1995). In cases when the older offspring, for one of a variety of reasons, does not have opportunity to breed anyway, helping its parents is a reasonable alternative investment of its parenting effort: the older offspring is helping to raise siblings that are as related to it as its own offspring would be. Without knowing what the breeding opportunities are, it is not possible to distinguish parental manipulation from what Dawkins (1980) calls "making the best of a bad job".

Indeed, it may be the case in some situations that it is best for an individual to help its parents and other kin even when it does have its own breeding opportunity. Behaviors are selected into subsequent generations based on increased representation of the genes that increase the behavior, regardless of who those genes came from. If an individual can increase the prevalence of genes for helping, it does not matter if it does so via having its own offspring- which are likely to carry those genes- or by helping to raise offspring of other individuals (generally speaking, its relatives) who also are likely to carry those same genes. This is referred to as the principle of inclusive fitness (Hamilton 1964a,1964b,1972,1975) and is perhaps the most important concept in modern evolutionary studies of behavior.

Evolutionarily stable strategies

Perhaps the second most important concept in modern evolutionary studies of behavior is the idea of evolutionarily stable strategies or ESSs (Parker, 1984). The concept of ESSs was developed in mathematical game theory rather than evolutionary biology, but it has adapted well (pun intended).

Game theorists model situations that are similar to games in that it is the interaction of various "strategies" used by two or more "players" which determines the final outcome of a "contest". Different combinations of strategies can be "played out" on computers over many many trials in order to see which strategies work best under which conditions (where the different conditions have to do with what strategies other players are playing). An evolutionarily stable strategy is a strategy which, when "played" in repeated "contests" over the long-term, cannot be "beaten" by any other strategy that might be introduced.

Game theory can be used to model the potential value of various strategies in real games (such as poker or tic-tac-toe), "war games", "business wars", or interpersonal interactions such as "political battles" or "the battle between the sexes". It has also been used to model the interactions between two or more parties in coevolutionary relationships such as those of predator and prey, proto-male and proto-female, or host and pathogen (see Pool, 1995). Fisher's model of sex allocation is perhaps the earliest example of game theory applied to evolution: once sex has evolved, the best "strategy" of a mother is to expend half of her parental effort toward male offspring and half toward female offspring; when all mothers are playing that same strategy, no mother can do better by trying something different; the 50:50 allocation of parental energy to the two sexes is thus, an ESS of parenting strategy.

Game theory as applied to evolutionary theory was taken up in earnest by John Maynard Smith and colleagues, who used it to model the evolution of sex and sex ratio (e.g. Maynard Smith, 1978a,1980) as well as to model behavioral contests between individuals (e.g. Maynard Smith,1974,1978b; Maynard Smith & Price, 1973). The latter studies showed that ESSs could be mixed, as well as fixed. That is, the most stable strategy over time might involve a combination of different strategies played by different "players" or chosen on different "turns". (From hereon plays made on individual turns will be referred to as "tactics" so as to reserve the term "strategies" for reference to long-term styles of play.)

Game theory models demonstrate that in many types of "contests", versatility -even unpredictability- can be more advantageous than the use of any particular fixed strategy. As Alexander (1986) writes: "It would be the worst of all strategies to enter the competition and cooperativeness of social life, in which others are prepared to alter their responses, with only preprogrammed behaviors" (p. 171). Because they show how mixed strategies may be evolutionarily stable in the long-term, game theory models can help us to understand the ultimate reasons behind the selection for, and maintenance of, genetic diversity and behavioral flexibility.

Mixed ESSs can theoretically be maintained in at least five ways (after Buss, 1991 and Mealey, 1995):

-- (1) Different individuals could use different strategies in that each individual always plays the same tactic, but because of genetic differences, different individuals must obligately use different tactics. An example might be the fact that people are born with different physiology and personality types; as a result of these inborn differences, people are somewhat different from one another other, but each person is fairly consistent and predictable over time;

-- (2) All individuals might use the same genetically-programmed mix of tactics, playing various tactics in a set proportion, but randomly and unpredictably. An example might be that each of us will engage in either "fight" or "flight" in response to danger, but which one happens when may be unpredictable;

-- (3) All individuals might use a mix of environmentally-contingent, facultative tactics. That is, every individual might use each available tactic, but use them flexibly, adaptively, and predictably according to circumstances-- as is the case for the use of reproductive tactics in species which are facultatively sexual or asexual;

-- (4) Each individual might use a single strategy to which he or she was obligately constrained by development, or "canalized" (Gottlieb, 1991) during a critical period. One example is sexual differentiation itself; other possible examples will appear at several points later in the book;

-- (5) Some individual differences in strategy might result from a classic gene-environment interaction. That is, individuals of one genotype might develop in one way in response to certain environmental conditions, while individuals of other genotypes develop in a different way in response to those same conditions, resulting in an ESS in which all individuals use tactics in an environmentally-contingent manner, but different individuals use different patterns of tactics. As an example, muscular children might win fights more often than skinny children; muscular children therefore may learn that aggression "pays" and they will use it in the future, whereas skinny children learn that aggression "doesn't pay" and they will learn to use other tactics. Other possible examples of this, too, will appear at several points later in the text.

While game theory can be used to model these kinds of dynamic, it cannot tell us what is happening in any particular real-life situation-- our current understanding of genetics and development is simply too rudimentary. At the moment we have only a basic understanding of ESSs of type (1)- in terms of elementary genetics, and type (3)- in terms of the basic "laws" of behavior studied by psychologists; ESSs of type (2) seem not to be very adaptive or very common, and while types (4) and (5) are probably very common, they are too complicated for us to unravel as of yet.

Some of the most interesting research in behavior genetics and developmental psychology is moving in this direction under the rubric of the study of "life history strategies" (Chisholm, 1993; Daly & Wilson, 1978/1983; Fleagle, 1993; Mealey, 1999; Moffitt, Caspi, Belsky & Silva, 1992; Morbeck et al, 1997; Scarr, 1992), but most of the scenarios that will be raised in this text are examples of ESSs of type (4) or (5) and, at this point, remain fairly theoretical. Wherever possible we will try to integrate proximate and ultimate explanations of sex differences (as well as within-sex individual differences); keep in mind however, that the connections between proximate and ultimate generally remain to be worked out.

The next section provides an illustration of the attempt to integrate proximate and evolutionary models. The concepts presented in this chapter are used to provide an ultimate explanation for a behavior that, in Chapter 2, was discussed from a proximate perspective: homosexuality.

Illustration: Homosexuality

If the only criterion for natural selection were the maximization of an individual's offspring, then homosexuality clearly should have been selected out of the population: as mentioned in Chapter 2, although many homosexuals are not exclusively homosexual and some have children, their average number of children is less than that of heterosexuals. Despite this fact, homosexuality as both a behavior and an orientation is more common than can be explained by genetic mutation, leading several people to postulate that through human evolutionary history, it must have been an alternative, adaptive, life history strategy (Dickemann, 1993; Dizinno, 1983; Dragoin, 1997; Kirsch & Weinrich, 1991; Mealey, 1993; Roes, 1993; Ruse, 1982; Salais & Fischer, 1995; Weinrich, 1984).

One possible adaptive scenario is the kin selection model of homosexuality. According to this model, homosexuals (at least, in the past), diverted their energy and resources away from the rearing of their own children, but redirected it toward helping their brothers, sisters, parents, nieces, and nephews. By helping their kin to survive and reproduce, the helper's extended family would be larger than if each individual had tried to rear offspring on their own, and since each of their relatives shares some of their genes, helpers would be passing on their genes not through their own children, but through the children of relatives. In this way, the genes for homosexuality would be maintained in the population through the increased reproduction of the relatives of non-reproductive helpers.

Possible evidence for this model comes from the role of the Native American berdache (Dragoin, 1997; Forgey, 1975; Greenberg, 1986; Williams, 1986). The berdache is a role reserved for chosen individuals who, early in life, display cross-gender attributes. In some societies the berdache was given high status and served as the tribe's medicine man (or woman) or as a mediator of disputes. While not necessarily homosexual, a berdache might, via the high status of the position, increase the wealth and health of his or her extended family, and through kin selection, pass on the genes for cross-gendered behavior (Callendar & Kochems, 1986; Weinrich, 1987). Other similarly prestigious roles for cross-gendered or otherwise non-reproductive individuals might have been more common in our evolutionary history than they are today. Weinrich (1995) and Dragoin (1997) have suggested that the differing occupational and interest profiles of homosexuals compared to heterosexuals might be a remnant clue of that other time.

Trivers (1985) dismisses this type of model by pointing out that while it might offer an adaptive explanation for asexual orientation, it cannot explain same-sex orientation, as the investment devoted to same-sex relationships would detract from potential investment in kin. Roes (1993), however, notes that in other group-living primates, male-male alliances allow individuals to increase their social status, power, and access to resources; factoring in the increased resources perquisite to higher status could easily skew the cost:benefit calculations of asexuality/homosexuality toward pairing. Hewitt (1995) documents that in the U.S., homosexual males have on average, higher status jobs and higher incomes that heterosexual males.

A second possible scenario is the parental manipulation model of homosexuality. According to this model, certain offspring may be recruited by their parents to be non-reproductive helpers, even though it is not in the offspring's best interest. (Remember, Alexander showed that in parent-offspring conflicts, selection favors the parents over the offspring.)

In highly stratified cultures, parental investment, including financial inheritance and social status (e.g. title), is often passed almost in its entirety to the child with the greatest reproductive value-- generally the oldest male (Dickemann, 1993; Hartung, 1982). Younger sons, who, in such cultures would be unable to attract wives, may become superfluous in terms of their parents' reproductive potential; historically, many were sent to live as wards of the church or to become "expendable" soldiers and mercenaries (Dickemann, 1993). This pattern of parental favoritism is compatible with the otherwise unexplained fact mentioned in Chapter 2, that homosexual orientation is more frequently found in later-born individuals from families that already have large sibships. (Remember that in other animals younger offspring of large sibships may be "sacrificed" by the parents in order to provide greater support to the older sibs.)

Parental behavior is certainly different toward early-born versus later-born children, with significant sex-related interactions (Sulloway, 1996). Such differences might be designed by evolutionary selection pressures to subtly manipulate offspring based on their differential reproductive value. Interestingly, this model has a parallel in the psychodynamic model of homosexuality in that homosexual men, more often than heterosexual men, report having a domineering mother and a cold, distant father. Research suggests that these parental attitudes are consequent to, rather than causes of, the early appearance of cross-gender behaviors in their sons (e.g. Bell, Weinberg & Hammersmith, 1981; Freund & Blanchard, 1983; Sipova & Brzek, 1983). This is just what we would expect if parents were responding to cues related to the reproductive potential of individual offspring.

A variant of the parental manipulation model involves sibling rivalry: older siblings may manipulate the younger in order to reduce mate competition. In this scenario, younger boys in a family might respond to dominance cues from their older brothers and subconsciously undervalue their own reproductive value. By channeling their sex drive into relationships which do not require parental investment, younger sibs are not only diverted from competition with older sibs, but their parental effort can be diverted to care of kin, i.e., the offspring of their older siblings. Evidence for the sibling rivalry model comes from reports by Blanchard & Bogaert (1997 and references therein) that male homosexuality is concentrated not just in later-borns of large sibships, but specifically in later-born males belonging to sibships of mostly boys.

Note that in the latter two models- the parental manipulation model and the sibling rivalry model- those individuals who take the non-reproductive role are those with the least (perceived) reproductive potential. Because males have a greater variance in reproductive success than females, we know that a randomly chosen male is less likely to successfully realize his reproductive potential than is a randomly chosen female; we thus would expect that, to the extent that individuals can monitor their own reproductive value and compare it to that of others, more males than females would be in the position of having to "make the best of a bad job" and opt for alternative life history strategies involving non-reproductive roles. Thus, another otherwise unexplained fact from Chapter 2- the fact that cross-culturally, homosexuality is more common in males than females- might be explained as one of the ultimate consequences of anisogamy. Likewise, the fact that male homosexuality is more common in societies that practise polygyny (the system in which some men have multiple wives, leaving some men unmarried and unmarriageable), also suggests that the higher reproductive variance and therefore, mating competition of males might explain the higher rates of male, as compared to female, homosexuality (Dizinno, 1983).

A fourth adaptive scenario of homosexuality has been proposed that can also account for this robust sex difference. This model is quite different from those above, however, which rely on the concept of reproductive value. Instead, the relevant concept for this model is genetic pleiotropy. Pleiotropy refers to the fact that any particular gene may have multiple effects-- a situation which is likely to be the case for most genes, although it is not commonly discussed or mathematically modelled. Sometimes the multiple effects of a gene appear simultaneously in an individual, in which case its net effect is what is relevant for selection. There is also the possibility however, that a gene may have different effects at different periods of development (e.g. Williams, 1957), or have different effects under different conditions-- such as the different hormonal conditions typical of males and females (Charnov, 1979).

Turner (1995a) suggests the possibility that while a particular gene or gene complex may increase the likelihood of homosexuality in males and therefore, on average, reduce the reproductive success of males who carry it, the same gene might increase the reproduction of those males' sisters. Recent data from Turner (1995b) and from Hamer et al (1993) suggesting that genes on the X chromosome might play a role in the development of male sexual orientation fit well with this model, in that girls, having two X chromosomes, would be twice as likely as their brothers to inherit such genes. Selection for the gene would thus be stronger than selection against the gene, maintaining it in the population. (In an interesting and somewhat ironic twist given the current strength of the Red Queen explanation for the evolution of sex, Turner postulates that the evolutionary advantage that females might have obtained from this gene complex is genetic resistance to the smallpox virus.)

A fifth proposed evolutionary explanation for homosexuality suggests that it is not adaptive at all, but is maintained in the population as a by-product of selection for maleness (Gallup & Suarez, 1983). According to this model, the directional selection pressures on males which are consequent to anisogamy (selection for high sex drive, desire for a large number of partners, and low investment in parenting effort as compared to mating effort), will inevitably result in a small percentage of individuals who exhibit these characteristics to the extreme. Some sort of counter-selection must be acting however, and in this case it might be the unacceptability of such extremity to potential female partners. The result is stabilizing selection, with asexual males at one (selected against) extreme and highly sexually active homosexual males at the other (selected against) extreme.

As you see, using evolutionary theory to devise ultimate explanations of current traits and behaviors does not lead to one obvious and correct answer: it may be that any one of these explanations of the maintenance of homosexuality is correct, or that all are correct, or that none are correct; the hard part is setting up opposing models to test the different possibilities. Evolutionary theory is no different from any other theory in this regard, and tests of the concepts you have read about in this chapter could fill several libraries.

Those libraries, however, would be full of studies of other animals. If you wish to study the human animal, direct experimentation is often impractical or unethical. Those of us who want to apply evolutionary theory to Homo sapiens must, therefore, rely on comparative animal studies, cross-cultural studies, developmental studies, and "experiments of nature" (just as we did in Chapter 2 when we addressed proximate explanations). This multidisciplinary "methodological triangulation" is the best approach to the study of complex phenomena when direct experimentation is not possible (Holcomb, 1995; Mealey, 1994a,b). Still, because we can never "prove" any particular historical or ultimate explanation of anything (Mealey, 1994c), many people criticize the ultimate approach when applied to humans. We will end this chapter with a discussion of those criticisms.

Caveats on adaptationism

We opened this chapter with the claim that, at least from one perspective, the ultimate answer to the existence of practically everything boils down to the concept of selection. This perspective, called the "adaptationist approach" (e.g. Cosmides & Tooby, 1997), is not, however, the only perspective, and it has been criticized on many grounds- including political, philosophical, methodological and empirical (see Buss & Malamuth , 1996; Gowaty, 1997; Rose & Lauder, 1996; Ruse, 1987). One recent (and excellent) critique begins: "Adaptation is no longer something that can be safely assumed by evolutionary or other biologists. Indeed, the more one examines the concept, the more it comes to resemble a newly landed fish: slippery, slimy, obstreperous, but glittering with potential" (Rose & Lauder, 1996, p9). To close this chapter we will address the shortcomings of "the adaptationist programme"- as it has come to be called by its detractors (Gould & Lewontin, 1979; see also Brown, 1983 and Mealey, 1994d).

The major political criticism of the adaptationist approach was briefly addressed in Chapter 1 but will be discussed once again here. Specifically, the argument is that the adaptationist programme supports the notion of biological determinism, i.e., the idea that "biology is destiny". (See Mealey, 1994e and the final chapter of this book for a more detailed discussion of biological determinism and gender inequality).

In the extreme, of course, biological determinism is true: none of us will turn into chickens when we hit 40. But as a political critique, the more serious implications are that 1) the adaptationist programme ignores environmental contributions to individual development and behavior, and that 2) it assumes that what is "biological" cannot be changed.

On the one hand, adaptationist, ultimate explanations do ignore environmental contributions to individual development and behavior, as their traditional focus is not on the individual and the ontogenetic, but on the historical and the phylogenetic; the role of the environment in the development of individuals tends to fall in the domain of proximate, rather than ultimate explanations (Cosmides & Tooby, 1997; Mealey, 1999). On the other hand, adaptationism does not ignore the role of the environment in history and phylogeny; indeed the entire idea of evolution by natural selection is based on the existence of environmental pressures.

The "environment" in which humans evolved includes abiotic selection forces (such as constraints of physics on the body) and biotic selection forces (such as pressure from parasites). The latter include coevolutionary pressures between-species (as from parasites) and coevolutionary pressures within-species (as from the opposite sex). This book, written by two adaptationists, is chock full of examples of the role of the environment in the evolution of behavior-- examples such as have already been presented in the explanations for the initial evolution of sex and sex differences. Adaptationists do not ignore the environment.

It is also not the case that what has evolved is just a collection of inflexible, obligate, strictly canalized strategies that do not respond to environmental input. Recalling the discussion of ESSs, only ESS types (1) and (2) describe anything like strict "biological determinism"; ESS types (3), (4) and (5) all describe situations in which evolved adaptations support the ability of the organism to respond to the environment within its own lifetime. This book will, too, be full of examples of such facultative responses to the environment. IF we, as individuals or as a society, decide we want to change something about human behavior (and note the "big if"), it is more likely that we will be able to do so by changing the human environment-- as we do when we give antibiotics or hormone replacement therapy, when we teach our children (things for their benefit or our own), and when we build prisons, televisions and computers-- than by artificial selection or genetic engineering. Adaptationists do not assume that behavior cannot be changed by environmental input (see also Waage & Gowaty, 1997).

The BIG IF of the preceeding paragraph brings us to the major philosphical critique of the adaptationist programme: the claim that adaptationists commit the naturalistic fallacy by assuming that what is the result of selection is what ought to be, and that therefore, even if we can change something, we shouldn't. Once again, there is a simple retort to this criticism, in that it should be fairly obvious to most people (once they stop to think, which, unfortunately, they don't always do), that just because something is "natural" doesn't mean it is good. Pestilence and parasites are natural but we don't typically think of them as "good" and we certainly try to intervene in their path; food and drink may be natural and "good" in moderation, but deaths from alcohol and from diabetes, heart attack, and other obesity-related diseases show that there can be "too much of a good thing". As you may have anticipated from hints in Chapter 2, we will be arguing that rape is natural in that it is a consequence of selection; but by no means will we argue that it cannot or should not be eradicated.

If you have the time and inclination to read a bit further on this issue, we have provided a scheme for classifying "natural" traits, events and behaviors into different categories using an evolutionary perspective. (See Box 3.1.) You might find this scheme to be a useful heuristic or point for discussion. As you will see, while it says something about ethics, it cannot tell us what we "should" do.

BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX BOX

Nature and Normality: An Evolutionary Perspective

Chapter 2 presented five common approaches to distinguishing between normality and abnormality; these were: the statistical definition, the medical model, social prescriptions, cultural value, clinical (psychological) normalcy, and legal norms. Each of these approaches has its worth, but each also has severe limitations-- and they certainly do not all lead to the same "answer" (their various categorizations of homosexuality providing a good example).

When we have to decide what criteria to use in decisions about whether to try to promote, prevent or intervene in the development of various traits, events or outcomes, our lack of a singular definition of "normality" proves a major stumbling block. While evolutionary philosophy cannot provide an algorithm for ethical decision-making, it can provide an additional perspective. Here is one (adapted from Mealey, 1997; see other similar schemes in Crawford, 1998 and Nesse, 1991).

--------------------------------

Using a perspective akin to the evolutionary medicine model of Nesse and Williams (1991,1994), consider that in a multi-party interaction- be it a host-parasite interaction, two humans interacting with one another, or one human interacting within a social network- what is adaptive for one party may not be adaptive for another. What is "functional" or what is "normal" or what is a "desirable outcome" is relative to the perspective taken by the different parties in the interaction. This perspective leads to three possible categorizations of various "natural" processes or outcomes.

First are the true pathologies. These are processes or outcomes that are dysfunctional from the perspective of an individual person who is directly affected by a non-human force or event. True pathologies would include, for example, effects of toxins, infectious disease, and injury. Events and processes in this category are likely to reduce a person's fitness, but lowered fitness per se cannot be used as a criterion for identifying them. Some supposed medical and psychiatric "disorders" may actually have an unknown adaptive function and/or be the best available option of a set of alternative strategies- what Dawkins (1980) calls "making the best of a bad job". True pathologies can only be recognized as such in that they elicit a combative (healing) response from the individual. Toxins, infectious disease and injury for example, all elicit complex, coordinated, obviously evolved, adaptive responses from the affected person. These responses are proof of selection pressures in the past, demonstrating that the insult has a history of causing harm. Generally we have no ethical dilemma in deciding whether to try to prevent, or intervene in, cases of true pathology; rather, the dilemmas that arise are more likely to involve practical questions such as how to allocate scarce resources.

Modern pathologies, like true pathologies, are dysfunctional from the perspective of an individual person who is affected. Also like true pathologies, they are likely, on average, to lead to a reduction in fitness. Modern pathologies can be discriminated from true pathologies in that there is no identifiable coordinated counter-response from the affected individual-- indeed, the source of the "problem" may seem to be internal. Modern pathologies may have a complicated genesis that consists of a variety of coordinated changes in the state of the organism, but these coordinated changes reduce, rather than enhance, adaptive function. This set of circumstances would suggest that an evolved mechanism has been triggered, but that its deployment is no longer appropriate in the modern human environment: Modern pathologies are likely to represent adaptations gone awry. Examples may include diabetes, myopia, anorexia, breast cancer, and endogenous depression. (See Anderson, Crawford, Nadeau & Lindberg, 1992; Crawford, 1995; Eaton, Pike, Short, Lee, Trussel, Hatcher, Wood, Worthman, Blurton Jones, Konner, Hill, Bailey & Hurtado, 1994; Lappe, 1994; Nesse & Williams, 1994; Price, Sloman, Gardner, Gilbert & Rohde, 1994; Surbey, 1987; and Wallman, 1994 for possible proximate explanations of these mechanisms-gone-awry.)

In the case of modern pathologies we are confronted with an ethical dilemma in that the afflictions of some individuals are, in essence, costs of "social progress". As with illnesses that are due to pollutants that never before existed in our evolutionary history (asbestos, radioactive waste), prevention of such pathologies may require that we, as a society, give up some modern conveniences and innovations (both technological and sociological-- see e.g. Crawford, 1995); there are likely to be significant disagreements amongst people on this point.

Third are the ethical pathologies. Ethical pathologies are traits or behaviors that may be functional and adaptive for one individual in a social interaction, but which have dysfunctional, maladaptive consequences for one or more other participants in the interaction. Ethical pathologies would include rape, theft, adultery, and warfare. Such traits or behaviors presumably, on average, increase one party's fitness to the detriment of another. Ethical pathologies can be identified by finding complex, coevolved, complementary response sets amongst the different parties to the interaction. Various deception strategies, for example, will be countered by deception-detection strategies (Alexander, 1987; Cosmides, 1989; Mealey, Daood & Krage, 1996); rape attempts will be countered by rape-avoidance strategies (Malamuth, 1996; Smuts, 1996; Thornhill, 1996; Thornhill & Thornhill, 1992); theft will be countered by protective measures (Cohen & Machalek, 1988; Machalek & Cohen, 1991; Vila, 1997; Vila & Cohen, 1993).

Since ethical pathologies may involve large numbers of interactors, we can expect to see complex social strategies evolve out of this type of "arms race". Government and various service providers (counselors, lawyers, and consumer activists) can, from this perspective, be seen as part of the "extended phenotype" (Dawkins, 1982) that individuals, acting as potential victims, have evolved in order to counteract the strategies of the potential perpetrators and social parasites among us.

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While evolutionary philosophy cannot tell us how to act in any given ethical dilemma, it can certainly be used to model and predict how the various participants of a dispute will behave (e.g. Beckstrom, 1993). If there is a conflict over the distribution of resources to those afflicted by various true pathologies, for example, we can expect disputants to favor their kin and their allies over strangers or potential competitors. In the context of modern pathologies we should expect that the beneficiaries of technology will argue for "progress" while the afflicted argue for a halt. In the case of the more complicated ethical pathologies, we are all potentially the cheaters and the cheated, but not necessarily with the same likelihood. Evolutionary analyses of rape and other crimes, for example, can help to identify the most likely perpetrators and the most likely victims, providing suggestions for means of prevention and remediation (e.g. Mealey, 1995; Quinsey, & LaLumiere, 1995).

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The third type of criticism aimed at the adaptationist programme has to do with scientific assumptions and methods. Specifically, adaptationism has been labelled as a form of scientific reductionism. Reductionism involves the attempt to understand things by literally or metaphorically breaking them down into their component parts and studying the parts. This approach is obviously integral to scientific method (Mayr, 1983), and is particularly integral to understanding things at a proximate level. Reductionism is not the only approach to science, however, and the criticism aimed at adaptationism is that the adaptationist programme (as in research program or agenda) ignores the other approach: holism.

Holism, or system theory, takes the view that an entitity is "greater than the sum of its parts", so to understand it, you must study what it is and what it does, not what it is made of. One of the main concepts of system theory is the "emergent property". Emergent properties are properties of a system that cannot be explained solely by an understanding of the constituent parts or units that make up the system. As examples, the properties of water cannot be predicted or explained simply by understanding hydrogen and oxygen, the properties of life cannot be predicted or explained simply by understanding the molecules that make up an organism, and the properties of consciousness cannot be predicted or explained simply by understanding the components of the brain (although to say "simply" in this context is rather ludicrous at this stage in our understanding of the brain).

Is it true then, that adaptationism, being reductionist, cannot explain any of these "emergent" phenomena? Well, no and yes. Reductionism can be framed in three ways. (The following is modified significantly from Ayala, 1985). The first version asks whether natural laws that operate on entities at one level are still manifest when those entities are organized into complex, hierarchical systems. The answer to this question is 'yes': the laws of physics and chemistry continue to operate on the molecules that make up living organisms, and the laws that operate on living organisms continue to operate when those organisms form social or ecological groups (etc.). The second version asks whether laws operating at lower levels are sufficient to account for processes that happen at higher levels. Again, the answer to this question is also 'yes': even though we may not yet completely understand how, the laws of physics and chemistry and the processes of natural selection are the basis of the hierarchical, complex systems that we see today, and there is no need to postulate other, non-physical processes. The third version asks: can we explain the existence and operation of higher level systems solely by understanding the laws and processes that operate on the lower levels? Here the answer is 'no'. Physical laws can accomodate infinitely many more entities than currently exist, and natural selection, being neither purposeful nor directed can have a variety of end results. Whatever exists today must be compatible with natural selection, but is not predictable from it. Without an asteroid collision at the end of what is now called the Cretaceous period, for example, humans (and many other species) would not exist; without plate tectonics, the world might have no marsupial mammals--- or might have only marsupial mammals--- or might have no mammals at all (etc.). There are an infinite number of possible worlds that are compatible with the laws of physics and with selection; there is also quite a bit of diversity around today. To be able to understand the development and maintenance of particular systems, one must know their particular history.

Ernst Mayr, one of the most important figures in twentieth century biology, agrees that: "biological systems store historically acquired information. (On this point) we cannot reduce biological phenomena and processes to purely physical ones" (1985, p 54). Quoting another key figure in twentieth century biology, George Gaylord Simpson, Mayr emphasizes: "Living things have been affected for... billions of years by historical processes... The results of those processes are systems different in kind from any non-living systems and almost incomparably more complicated... (but t)hey are not for that reason any less material or less physical in nature" (pp 54-55).

So, while human brains, human bodies, human social systems, and the coevolutionary systems in which humans interact with other humans and other species can be accounted for by the processes of natural selection, because we do not know the actual history of the evolution of our species, we cannot be assured of completely understanding our own complexity. In theory, if we could know our entire history, including our interactions with all of the abiotic and biotic elements of our environment, we would have all the information needed to completely understand our selves. But we cannot. No such enterprise can ever be complete.

In its third incarnation, then, (and the third incarnation only), the criticism that adaptationism is reductionist is a legitimate one. But this fact should not dissuade us from trying to postulate and test ultimate, evolutionary explanations of behavior: understanding the principles of evolution can help us to devise new hypotheses and to rule out postulated explanations that are not compatible with natural selection (and there are many in the social sciences! See Cosmides, Tooby & Barkow, 1992; Tooby & Cosmides, 1992). The value of this particular criticism is not that (as is sometimes intended) it squelches the generation and testing of adaptationist hypotheses, but that it calls to our attention the fact that just because we happen to have a possible explanation does not mean that it is necessarily the correct one. (This point was already illustrated when discussing the various evolutionary explanations of homosexuality.) This caveat about scientific method and assumptions leads us to the fourth and final criticism of the adaptationist program.

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The Spandrels of San Marco and the Panglossian Paradigm:

A Critique of the Adaptationist Programme

An adaptationist programme has dominated evolutionary thought in England and the United States during the past 40 years. It is based on faith in the power of natural selection as an optimizing agent. It proceeds by breaking an organism into unitary 'traits' and proposing an adaptive story for each considered separately. Trade offs among competing selective demands exert the only brake upon perfection; non-optimality is thereby rendered as a result of adaptation as well. We criticize this approach and attempt to reassert a competing notion (long popular in continental Europe) that organisms must be analyzed as integrated wholes, with Bauplane so constrained by phylogenetic heritage, pathways of development and general architecture that the constraints themselves become more interesting and more important in delimiting pathways of change than the selective force that may mediate change when it occurs. We fault the adaptationist pe for its failure to distinguish current utility from reasons of origin (male tyrannosaurs may have used their diminutive front legs to titillate female partners, but this will not explain why they got so small); for its unwillingness to consider alternatives to adaptive stories; for its reliance upon plausibility alone as a criterion for accepting speculative tales; and for its failure to consider adequately such competing themes as random fixation of alleles, production of non-adaptive structures by developmental correlation with selected features (allometry, pleiotropy, material compensation, mechanically forced correlation), and the separability of adaptation and selection, multiple adaptive peaks, and current utility as an epiphenomenon of non-adaptive structures. We support Darwin's own pluralistic approach to identifying the agents of evolutionary change.

-- S.J. Gould & R.C. Lewontin

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Box 3.2 reprints the abstract of a paper which heartily, almost blood-thirstily, takes the adaptationist approach to task. As you can see, reductionism is only one of many criticisms leveled at adaptationist, selectionist thinking.

This classic paper was published in the Proceedings of the Royal Academy of London (Series B) by Stephen Jay Gould and Richard C. Lewontin in 1979. Both men have been out-spoken and frequent critics of adaptationism in general, and of sociobiology and evolutionary psychology in particular. Might we just say at the start, that despite our disregard for some of the statements penned by these two prolific authors, every criticism in this paragraph was true at the time it was written and every criticism remains true today. We recommend that you read the paper in its entirety. (See also Gould, 1982.)

The adaptationist programme has been extremely successful (Mayr, 1983). Much can be learned through reductionist science and through the methodological triangulation mentioned earlier in this chapter. But science typically proceeds by small research projects which, one by one, add bricks to our edifice of knowledge; as a result, what projects get done depends to a large extent on what other people are doing (Kuhn, 1962). Despite the successes of the adaptationist programme, Gould and Lewontin are quite just in pointing out that with such an intense focus on selection, many of the interesting historical dimensions of evolution have been relatively ignored. While it is absolutely true that the current (or past) existence of any particular trait or entity is (or was) a "result of" natural selection, natural selection has to have something to act upon. Genes, traits, and species cannot be selected in or out unless they first appear. That is, natural selection can only operate on the relative adaptive value of extant, competing entities, and Gould and Lewontin are correct to point out that the roles of history, chance, and constraint in the generation and availability of biological diversity have been relatively overlooked. (Then again, as Mayr notes, adaptationists like himself had already made these points before Gould and Lewontin did.)

Among the many historical effects that Gould and Lewontin mentioned in their critique is one we would like to draw particular attention to: the concept of "spandrels". Like the architectural spandrels of adjacent archways, some features of biological structures, too, may be neutral in terms of their adaptive value; they may be correlated by-products of something else. Some evolutionary philosophers and theorists (e.g. Dennett, 1995) would suggest that this could be true only for trivial features, but in this quite heated debate (see e.g. Alcock, 1997 and Gould, 1997a&b) we choose to remain neutral (pun, once again, intended). As Carl Sagan often said about the possible existence of God: "the data just aren't in".

Finally, it is still the case now, as it was when Gould and Lewontin first wrote their critique, that much of evolutionary theory as applied to humans is just "story telling". (Often such stories are referred to as "Just-So stories" after Rudyard Kipling's famous children's stories such as "How the Elephant Got its Trunk".) We do not want to discourage story telling. Indeed, another most important figure of twentieth century biology- W.D. Hamilton, whose name has popped up so many times already in this chapter- has been known to encourage "Just-So story-telling" as a means of brainstorming creative ideas. It is new creative ideas after all, that allow a few individuals to break off from standard science and introduce the kind of revolutions in thought that Gould and Lewontin might like to see.

The problem with story-telling is not in the stories or in the telling; it is in the fact that some people just stop there, without testing their ideas against any other stories (models), or even, sometimes, against a null hypothesis! This kind of story-telling is, if not dangerous, a waste of time and ink. We hope that we have sufficiently documented most of what we report in this book; but when you come across what you perceive as story-telling (which should happen if you are paying attention and are a critical thinker!), we hope you will take the story for what it is worth- as an example of evolutionist thinking- and realize that there may be other plausible stories that no one happens to have yet considered.

Closing comments

This has been a long chapter, but it has provided you with most of the concepts that you will need to follow the adaptationist "stories" that follow. The remaining chapter of this introductory section, Chapter 4, will now summarize these concepts with specific reference to sex differences.