Chapter 5
Female Reproductive Strategies in Non-human Species
Copyright © 2002 Michael E. Mills
There is a fundamental set of reproductive problems faced by females. Different ecologies and social systems modify the particular manifestations of these problems. But the fundamental problems associated with survival and reproduction are often similar for females across most species. If female animals could talk, one might imagine that you would hear them express many analogous concerns, hopes, and desires that now can be articulated only by human females.
If you had a female body, what kind of problems would you have to overcome to successfully reproduce? How would you choose the best mate? How would you discern when it is the right time to mate, and when it is not? Here we will explore some general strategies that females across many species have used to solve these problems.
R vs. K reproductive Strategies
Organisms are presented with two mutually exclusive reproductive options: (a) have a great number of offspring but provide very little, or no, parental care, protection and feeding, or (b) have a few offspring but provide a great deal of parental care.
Because of the low parental effort that characterizes the first option, it is associated with high offspring mortality (perhaps 95% or more of the offspring do not survive to reproductive age). The second option, because of increased parental care, has much lower offspring mortality. Organisms that produce a large number of offspring with little parental care and high mortality are called “r-strategists”; those that invest heavily in a few offspring with low mortality are called “K-strategists.” Human females are extremely K-selected organisms; you would find it difficult to find better mothers anywhere on earth.
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The female elephant seal is K-selected. She invests her time and energy feeding and caring for her otherwise helpless baby. |
How did mammals, and in particular human females, evolve to be such extreme K-strategists? Below is a simplified evolutionary timeline.
Major stages of evolution leading to the human K-strategists:
- Asexual cloners (r-strategists, no parental care).
- Sexual reproducer r-strategists. For example, fish deposit eggs in very large numbers, and generally offer no, or little, parental care. Female fish can lay a huge number of eggs because they use external fertilization.
- Reptiles evolved on land, and thus their eggs (ovum) evolved hard shells to avoid being dried up. Eggs also had to have enough protoplasm to support the developing zygote, and therefore, were larger. Larger eggs meant that fewer of them could be produced (compared to fish).
- The hard exterior shell of eggs prevented sperm penetration, so fertilization had to be done internally before the development of the hard sheet. This further limited the number of offspring a female could produce.
- Internal fertilization offered the possibility of completely internal gestation and live births. Egg-shells were thus no longer required. However given a long gestation period, and physical size constraints, the upper limit of the number of offspring mother could produce in her lifetime was now limited to under a hundred (and for most mammalian species, under 10 or 20). This is a radical shift from the thousands, or tens of thousands, of eggs that a female fish could produce.
- Social mammals that cooperate in hunting and defense require the development of social intelligence. Behavior in such situations must be more context-dependent, and thus learning is important. Genetic constraints on behavior no longer “wire in” instinctual, inflexible behavior, but rather produce an array of behavioral emotional, and cognitive predispositions to assess social and environmental variables and respond appropriately to them. Learning requires a period of instruction, provided by parents and the social group in social mammals. This further increased the degree of parental investment required for each offspring.
The human mother is the ultimate K-strategist – no other organism invests 14-18 years of intense effort to fledge her offspring.
COURTSHIP AND EPIGAMIC SELECTION
Given the minimum possible investment that a sexually reproducing female mammal makes, e.g. months of internal gestation, lactation and perhaps years of intense care of her offspring, it is in the best interest of the female to choose her mate wisely. As we shall see in the next chapter, in some species females have little choice. In species in which females do have a choice of potential mates, such as peahens, selection of a suitable mate is accomplished through courtship, elaborate and distinctive behaviors designed to attract and evaluate potential mates. Most vertebrates engage in some sort of courtship ritual, generally with the male as the “advertiser” and the female as the discriminating shopper (Barash 1982). As females engage in epigamic selection by picking and choosing mates that possess traits that they consider attractive, such as bright colors, long tails, (or any characteristic that is not necessary for survival), they are unwittingly controlling the process of sexual dimorphism.
WHY IT IS IMPORTANT FOR A FEMALE TO CHOOSE THE “RIGHT” MALE
Female choice in selecting a mate occurs most often when the males of a species are not too aggressive and restrain from forcing a female into a sexual relationship. The other condition under which female mate selection is most salient occurs when males exhibit secondary sexual characteristics, varying from one species to the next, such as vibrant colors, decorative plumage, and behavioral courtship displays.
An example of female mating selection is seen in the sage grouse. Males aggregate in mating circles, called leks, where they display for females. A female then chooses one male from all of the contestants present with whom to mate. Of all of the males performing at a lek, it is common for a few males to receive all of the females’ attention (Dugatkin & Godin, 1998).
However, females also must select a mate when all of her choices are not presented during one occasion. This task requires cognitive skills to remember the characteristics of the males she has seen. In the three-spined sticklebacks, for example, a female will decide whether to mate with a suitor, comparing his coloring to the previously encountered males. Here a female will show an interest in a male whose red nuptial coloring was brighter than his predecessor’s. Consistent with the selection for bright coloring in the three-spined sticklebacks and in female guppies, most females of varying species choose male traits that attract and stimulate their senses. For example, a green tree frog female will choose a male that calls the loudest and most regularly (Dugatkin & Godin, 1998).
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Seen here is a courtship display of the brightly colored Drake. Notice the head-up, tail-up posture. |
Why are females so selective in choosing mates? It may be as simple a matter as brighter mates are easier to find; however, the answer to this question may be somewhat more complex. Females who choose mates that will increase their reproductive success -- the likelihood of their offspring’s survival -- will be favored by natural selection. A mate choice may help to determine access to resources, such as food and habitat, as well as help to decrease predators or parasites.
If we compare the consequences of a poor mating selection for a female and a male we can see the evolutionary significance of female choice. Let’s say that a female ignores the advertisements of males and chooses her mate randomly. Since males can vary in terms of “status,” the female has the chance to choose poorly. For example, if she randomly chooses a low status male her reproductive possibilities are limited. Her random choice of a low status male makes her unavailable for mating with other, higher status superior males. She will invest much in this offspring for it to survive. If this randomly chosen low status male suffers a genetic defect, the offspring may also suffer the same fate.
The consequence that the male suffers from a bad mating does not compare to the loss that the female endures. The low status male invests a short period of time during copulation and a negligible and easily replaced amount of sperm. There is no wasted energy or time squandered in nurturing an unsuccessful offspring. Nor is he limited by this poor mating, since he can immediately move on to additional mating possibilities with additional females.
FEMALE PROBLEM: ASSESSING HEALTH, GENES, AND BEHAVIOR OF SUITORS
POTENTIAL SOLUTIONS
LOOKING FOR GOOD GENES
Experiments have shown that females do in fact choose males based on good genes (Moller & Alatalo, 1999). Females have evolved to be attracted to signs that indicate genetic fitness. Signals of genetic fitness advertise the males’ ability to survive and reproduce. Since a female’s interest are in nurturing offspring that will survive and reproduce, she will likely look for signals of genetic fitness in her mates. Signs of good genes include observable cues of physical and behavioral qualities. Females rely on observable signs of preferential physical qualities such as size, strength, age, health, vigor, and agility. True indicators of good genes are energetically costly to produce and maintain, and thus are only demonstrated by the most viable males (Dugatkin & Godin, 1998). Behavioral signs of genetic fitness include behaviors that provide a female with the opportunity to assess what the male and his genes have to offer her offspring.
For instance, a larger, older, healthy male who successfully defends his territory will likely be more attractive to a female than will a smaller, younger male who has not had the opportunity, or does not possess the ability, to prove himself or his good genes. A female orangutan may be receptive to a large, territorial male while disinterested in a small, transient sub-adult (Dixson, 1998).
When a
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Examples of female mate choice. |
LOOKING FOR SIGNS OF GOOD HEALTH
Females will typically be sensitive to signals that indicate good health. Males that are perceived to be sick or injured are more likely to be rejected as suitors. Health of a potential mate is important because many diseases are communicable. In order for a female to survive, reproduce, and invest in viable offspring successfully, she must live long enough to do so. Thus, female attraction to an unhealthy, possibly diseased male has been selected against. Females must also be sensitive to cues of good health in a potential mate since those qualities will likely be inherited by her offspring (Thornhill & Gangestad, 1993; Tooby, 1982). If the male’s illness or disease is genetic, her offspring will likely inherit a predisposition to the father’s condition, risking death or infertility, or consideration as unattractive by potential mates should the offspring reach reproductive age.
For a male to grow to a significant size, and cultivate and maintain his physical attractiveness, he must have enough resources (such as energy and health) to do so. A male who fails to grow as large as his counterparts, or who cannot maintain his physical appearance, is displaying to females that he does not have resources to spare. These observable cues to health and fitness can be thought of as “honest advertising” (e.g. Johnstone, 1995; Kodric-Brown & Brown, 1984) or “honest signaling” (e.g. Owens & Short, 1995; Vijugrein, 1997).
Since females use these “honest” physical cues of male quality to choose their mate(s), many species have been selected for their external physical features. The males of these species have evolved coloring, size, and other physical attributes to advertise their fitness to potential mates. For example, it is impossible for a male peacock to fake a large, colorful, albeit practically useless tail. If you compare a male mallard duck’s coloring to that of the female, you will find that the male mallard is brightly colored, which is an attractant to the female duck who is comparatively dull in coloring (Ligon, Thornhill, Zuk & Johnson, 1990).
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Female preference for large–tailed guppies. |
LOOKING FOR GOOD BEHAVIOR
Female animals will typically use the behavioral signals of a male for further evaluation of the quality of his genes. Behavioral exhibitions, such as the aerial displays during the courtship of many eagles and falcons, allow the male to display his physical competence as a mate. By exchanging objects in mid air, the male is able to show his speed and coordination, which are valuable qualities to possess if her mate is to provide food for their young (Barash, 1982). In the case of many songbirds, the female is sensitive to the size of a male’s song repertoire and to the size of his territory (Bensch & von Schantz, 1996; Searcy & Andersson, 1986). These acrobatic stunts and energy consuming displays are difficult to fake for a sickly or injured animal. Ill birds do not have the energy to spare on such consuming exhibitions, and thus selection favors the physical prowess that good health and behavior allow (Clayton, 1990).
GETTING MALES TO COMPETE (AND CHOOSING THE WINNER)
Rose Females may judge which male has the best quality genes by actually inciting competition among the males and then mating with the male who wins. Presumably, the healthiest male with the best genes will win a given conflict, and the female can use this information to her reproductive advantage (Barash, 1982). By choosing the winner, she is maximizing the chances that her offspring will be either well protected, or will inherit some of the dominant male’s qualities, or both.
Mealey has a great cartoon of dominant elephant seals on pg. 147. We should either reproduce it or steal it.
Inciting male competition is common among many species. A female elephant seal will produce loud vocalizations when mounted by a male (especially a subordinate male), which causes other males to battle for the opportunity to mate with her. A dominant male will likely win the ensuing fight, and will then enjoy the spoils of the battle by mounting the female himself. Female mountain sheep will run from a suitor, thus attracting other males who then compete. She will likely then mate with the winner (Barash, 1982).
By competing for the opportunity to mate, the males are in a sense doing the female’s work for her. She does not have to judge the males on different qualities; she merely has to choose the winner!
FINDING HIGH STATUS MALES ATTRACTIVE
Female animals will typically prefer to mate with a high status male. High status can come in the form or combination of dominance, ornamentation, size, age, territory size, health, vigor, previous reproductive success, etc.
A male that has survived the potential challenges that life offers - such as disease, attacks, food shortages, etc. and subsequently holds a position of high status, will likely be more attractive to a choosy female. Having survived to hold an honored position is a possible indicator of having an adaptive genotype, exactly the qualities for which a choosy female searches.
A female may mate with subordinate males during non-fertile phases of the ovarian cycle and reserve the peak of copulation for the most dominant male.
LOOK FOR MALES THAT OTHER FEMALES FIND ATTRACTIVE (“SEXY SON HYPOTHESIS”)
As noted by Dawkins (1976), it may be in a female’s interest to mate with a male for no other reason than other females find him attractive. If the “attractant” that this particular male has is heritable (e.g., such as his brightly colored tail, etc.) her sons are likely to inherit it. Females would thus be attracted to her sons and would likely end up with many grandchildren. This, of course, is an example of “runaway sexual selection.”
Females may imitate other females in their mate selection for several reasons. Young females often copy the mate choice of older females, perhaps due to their experience. By relying on the judgment and choices of other females, a female is able to save time and energy in assessing the quality of a potential mate (Dugatkin & Godin, 1998) With the saved time, she may invest her time elsewhere, such as in foraging, predator avoidance, etc.
AVOID INCESTUOUS MATINGS
One specific type of mating that a female might need to escape is an incestuous one. The increase in homozygosity that results from inbreeding can have deleterious genetic consequences for the offspring of such matings (e.g. Ralls, Brugger & Ballou, 1979). Since a female's reproductive potential is less than that of a male's, the costs (in terms of long-term reproductive success) will tend to be greater for a female than for a male who engages in such matings. This selection differential suggests that females may be more likely than males to avoid incestuous matings.
Incest avoidance can be achieved by a variety of behavioral and physiological means. Across species we see a wide variety of effective mechanisms (Bateson, 1983). For example, in many rodents (e.g. prairie dogs; Hoogland, 1982) and primates (e.g. chimpanzees: Pusey, Williams & Goodall, 1997, Japanese macaques: Enomoto, 1974; olive baboons: Packer, 1979), we see single-sex out-migration: as individuals of one or the other sex reach sexual maturity, they leave their natal group, so that the mating group consists of related males and immigrant females (patrilineal species) or vice versa (matrilineal species).
People are more generally familiar with this pattern in lions, where sisters and their daughters form the core of the pride, while males wander in ones or twos (Packer & Pusey, 1987). In some birds and mammals, incest is avoided by parental suppression of the sexual behavior of cohabiting offspring until both sexes of offspring disperse ( Koenig & Pitelka, 1979.)
Another potential technique for avoiding incestuous matings involves the major histocompatability complex (MHC), which plays an important role in the immune system in fighting infections. As seen in laboratory conditions, it is believed that it may be possible for animals to show a mate preference for individuals with a different MHC phenotype than themselves, thus, selecting mates with an unrelated immune system. This strategy may be a method of avoiding mating with potential relatives (Dixson, 1998; Potts et al, 1991). In addition, the MHC may be responsible for variability in secondary sexual characteristics. In other words, the MHC may produce certain types of secondary sex traits that are attractive only if the male is unrelated (Dixson, 1998).
FEMALE PROBLEM ATTRACTING THE BEST POSSIBLE MALE
Obviously, to reproduce successfully, a female has to attract a sexual partner, but the consequences of anisogamy--that males are more mobile, have a higher sex drive, and seek multiple partners--means that this is a fairly easy task. This circumstance allows females an element of choosiness when it comes to purely sexual partnering.
In most species, females are only receptive to sexual advances when they are fertile, i.e., during a "breeding season" or, in the case of non-seasonal breeders, as related to her own biorhythms. To be the target of a sexual advance, then, a female must signal that she is in breeding condition. Examples of physical signals of breeding readiness include the estrous swellings of the genitalia of many primates (e.g. Altmann, Hausfater & Altmann, 1988; Hrdy & Whitten, 1987) and the release of sex pheromones by other mammals, reptiles and insects (e.g. Crews, 1992, Thornhill & Alcock, 1983). In some species of amphibians and fishes, the key physical indicator might be as simple and direct as the bloated outline of the body when it is full of eggs (e.g. Rowland, 1994). These signals of breeding readiness can attract many males simultaneously-- just think of the randy males that arrive on the scene when a neighborhood cat or bitch is “in heat.”
Behavioral signals of breeding readiness may complement or highlight a physical signal: for example, a female baboon or chimpanzee might approach a male and turn her swollen genitals toward him in an obvious sexual invitation, and a fish bloated with eggs might take turns visiting the territories of several prospective fathers, posturing to display her fertile state. Sometimes just the physical presence of a female in the right place at the right time might indicate her readiness to breed: seals, whales, or migratory birds, for example, may announce their breeding readiness simply by their arrival at a traditional breeding site.
In general, females apportion more of their reproductive effort into parenting effort, and less into mating effort, compared to males (Low, 1998; Queller, 1997). As a result, they do not have to do much more than signal sexual readiness in order to capture the sexual interest of males. In most species the more difficult task for a female is to choose well from amongst the males that are available.
Compared to seeking short-term sexual access, when it comes to seeking long-term partners who will invest parentally, males are not so eagerly available. Thus, in species that tend toward social monogamy, females must compete for the most desirable mates. Females may compete, through displays and sexual attractiveness, as mentioned above, for access to males. High-ranking females usually have greater choice of mating partner. Females must compete even more in polygynous species where the males’ testes are small in relation to their body weights, and sperm is a “limited resource” (Dixson, 1998; Harcourt et al, 1981; Small, 1988).
Although females do occasionally duke it out over males (Gwynne, 1991; Slagsvold & Lifjeld, 1994), such intrasexual combat is energetically expensive and diminishes the energy reserves that are necessary for gamete production and, in mammals, subsequent gestation and lactation. Female mate competition, instead, generally takes place in the less expensive realm of intersexual competition (Campbell, 1995). To this end, females send physical and behavioral signals to potential mates, allowing an element of male choosiness to come into play. What signals do these choosy males find attractive in potential long-term mates?
Not surprisingly, one of the key attributes that males find attractive in a potential female partner is physical health--and for the same reasons that females find physical health to be attractive in males: there is less chance of acquiring a communicable disease from a healthy partner, and health is an indicator of underlying genotypic and immune system quality. Furthermore, since gamete production is so much more costly in females than in males, health is related to fertility in females much more than it is in males. This additional element means that the health indicators of a potential long-term mate carry even more information about females than they do about males, and they are, therefore, especially important to males seeking long-term partners (Monaghan, Metcalfe & Houston, 1996).
Females seeking long-term mates should, then, be expected to display signals related to health and fertility. These will differ for different species, of course, but include, as for males, the apparent absence of parasites and lesions, quality maintenance of external features, and overall size and robustness.
When males are assessing females as potential long-term partners, another factor that comes into play is sexual fidelity. As described in Chapter 4, most males, unlike females, have to deal with uncertainty of paternity and the risk of being cuckolded. Males should therefore seek indicators of female sexual fidelity, and females, in order to attract and retain a long-term partner, should display them.
The fact that males are sensitive to possible indicators of infidelity means that females should hide any indication of sexual interest in, or sexual advertising toward, other males. Any extra-mateship sexual liasons are likely to be engaged in while the partner is out of sight. Davies (1992) and Gowaty (1997) describe how female dunnocks and bluebirds (respectively) engage in extra-pair sex only when their behavior is hidden by bushes or by other obstacles, or when their partner is off foraging.
If a female has aged to the point wherein she is about to leave her “reproductive window” (e.g., her reproductive value is diminishing), males, particularly those in monogamous species, will be increasingly likely to reject her as a potential mate. Anything she can do to retain the appearance that she has higher reproductive value than in fact she does will likely work to her advantage in securing a mate.
The species that perhaps best exemplifies this is the human female (e.g., cosmetic surgery and products designed to make a woman look younger). The females of other species do not have these specific options. However, it is likely, at least in a few species, behavioral and other mechanisms evolved that were designed to deceive males about reproductive value.
FEMALE PROBLEM DIVERTING MALE AGGRESSION
FROM MEALEY
Perhaps one of the most important reasons why a female might establish an ongoing consortship with one male is for protection from other males (Smuts, 1992,1995,1996; Smuts & Smuts 1993). Forced copulations and other forms of sexual harassment are not infrequent in non-human animals; they have been documented in insects, birds, and mammals, including primates (Barash, 1977; Clutton-Brock & Parker, 1995; Crawford & Galdikas, 1986; Emlen & Wrege, 1986; Palmer, 1989; Smuts, 1996). Females draw on a variety of tactics to avoid harassing males, including hiding, running away, fighting back, and forming all-female coalitions (Mesnick, 1997; Smuts, 1996), but for species with significant sexual dimorphism in size, or species in which females are always subordinate to males, the best protection against a harassing male may be the presence of another male.
Sexual harassment has significant negative consequences for females even when it does not end in coerced sex (e.g. Byers, Moodie & Hall, 1994; Mesnick, 1997; Stockley, 1997); it can increase stress and interfere with normal activities, reducing health, fitness and longevity. A solitary bee female, observed while attempting to visit flowers and provision nest cells, was approached by a male for copulation more than once during every 3-second interval (Stone, 1995). These females responded to male harassment by flying away and altering their foraging behaviors which affected their ability to forage (Stone, 1995). Some forms of harassment may culminate in injury or death. Stress from harassment may also cause resorption or abortion of a gestating fetus or brood.
POTENTIAL SOLUTIONS
REDUCE AGGRESSIVE SIGNALS / DISPLAY RECEPTIVITY AND/OR VULNERABILITY
Since most male mammals are larger and more aggressive than the females, most females will not physically challenge a male. To do so would put the female at risk of injury or death. Males respond aggressively to physical challenges or signals offered by other males of the same species. The female inability to display male signals (bright colors, large antlers, etc…) is valuable in this capacity. In many species, a male can switch from aggression to mating behavior simply through the identification of the sex (female) of the approaching animal. In general, a male will not attack an individual of the same species who displays a willingness to copulate. In many species, a female can stop a male from attacking by presenting her rump. This strategy has even been adopted by subordinate males, who use it to ward off attack from males of the same species.
WHY IT IS IMPORTANT FOR A FEMALE TO GET A MALE TO INVEST IN HER OFFSPRING
A female needs male investment in her offspring for access to food, resources, and protection. As previously mentioned, a female must select a mate wisely and possibly compete for a long-term mate who will provide the resources necessary for the survival of her offspring.
FEMALE PROBLEM SECURING MALE INVESTMENT IN OFFSPRING
Remember that females are the sex that invests more heavily in the production of gametes (eggs). This investment is energetically expensive. The more offspring a female attempts to rear, the more energy she must commit to egg production as well as to any subsequent parental care. A female will, thus, benefit by seeking a mate who can contribute resources other than just sperm toward the production and rearing of multiple offspring (Gowaty, 1992). In many insects and spiders, males contribute by provisioning the female with food in the form of a "nuptial gift" which the female consumes during mating (Simmons & Parker, 1989; Thornhill & Alcock, 1983; see Chapter 6). But females of species whose young require significant post-natal investment from both parents may require more than a single gift as evidence of resource commitment (Smith, 1980).
POTENTIAL SOLUTIONS
FIND RESOURCE RICH MALES ATTRACTIVE
In addition to good genes and good behavior, a potential mate could also provide resources. The actual feeding of the female by the male that is often a part of these ritual interactions serves as a kind of parental investment: by offering food to the female, the male helps her to increase her energy levels and her capacity to lay eggs (Nisbet, 1977). His willingness to offer food also serves as a cue that he will be a good provisioner of their future offspring
FIND POTENTIALLY GOOD FATHER BEHAVIOR ATTRACTIVE
Symons (1979) notes that one criterion females should use to evaluate males is whether their behavior indicates that they would likely be good fathers. In addition to ability and willingness to provide food, females may also assess potential partners by other forms of commitment, such as contributing to nest-building (e.g. Collias & Collias, 1984) or ability and willingness to defend a nest and, later, offspring, against predators and neighboring conspecifics (e.g. Curio & Onnebrink, 1995; Yasukawa, Knight & Knight Skagen, 1987).
Once the health and fertility of a long-term partner have been established, reproductive success may then be dependent upon effective parenting skills. In species with long lives and for whom parental experience is particularly important, individuals should seek mates who have already demonstrated successful parenting skills (e.g. Altmann, 1997; Ollason & Dunnet, 1988). In some cases prior parenting success may be known as, say, with regard to last season's partner or last season's neighbor; in many birds, pairs that were successful on one breeding attempt are likely to re-mate in a subsequent season (Choudhoury, 1995). Because of the long period of dependency of offspring on parents, humans are something of an exception to this pattern: people generally seek partners who are likely to have good parenting and nurturing skills, but who do not already have dependent children.
In species that suffer from high adult mortality, females prefer to mate with younger males. However, some species are the opposite and experience high juvenile mortality and low adult mortality. Therefore, older males in these species have shown success in surviving a high-mortality period and are desirable to females (Gee, 2000). Another main reason these older males are attractive to females is that they guard nests more protectively and for longer periods of time than younger males, thus increasing the reproductive success for females choosing older mates (Gee, 2000).
ENFORCE A LONG COURTSHIP BEFORE COPULATION
Particularly in monogamous species, a long courtship period can be used as a “test” of male sincerity and future commitment. A philandering male will typically not tolerate a long wait before copulation. Often, the longer the courtship lasts, the better the test.
For instance, olive baboons have been seen to form long-term associations between a female and a fully adult male who is a long term resident of the troop (Dixson, 1998; Smuts, 1985). These relationships include grooming, huddling, and spending time with one another. The males may even befriend the offspring of these females, who may or may not be their own. These friendships may benefit males in the long-run by giving them the opportunity to mate with the female during her next period of sexual swelling (Dixson, 1998; Smuts, 1985). Future DNA studies will determine if a correlation exists between these long-term associations and the likelihood of a male fathering the offspring of his long-term female companion.
SOLICIT GIFTS
By virtue of committing his time to extended courtship interactions with a single female, a male is precluded from investing mating effort in other females and becomes committed to one partner as the likely sole (or at least, major) route for his successful reproduction. A male's ongoing presence and participation in these rituals thus, serves as a cue to the female that he is not already mated and is not investing in another mate and her offspring.
As noted above, a male’s willingness to offer food also serves as a cue that he will be a good provisioner of their future offspring. In addition to ability and willingness to provide food, females may also assess potential partners by other forms of commitment, such as contributing to nest-building (e.g. Collias & Collias, 1984) or ability and willingness to defend a nest and, later, offspring, against predators and neighboring conspecifics (e.g. Curio & Onnebrink, 1995; Yasukawa, Knight & Knight, Skagen, 1987).
SNEAKY SOLUTION CUCKOLDRY
For many years it was believed that the greater reproductive potential and consequent greater sex drive of males as compared to females meant that virtually all extra-pair sexual initiatives were made by males (e.g. Ford, 1983). We now know this to be false (e.g. Gowaty, 1995,1997; Moller, 1992; Stamps, 1997; Wrangham, 1997).
A female may solicit “extra-pair copulations” (EPCs) from multiple partners for a variety of reasons (Hrdy, 1997): she may be seeking "good genes" for her offspring by finding a sexual partner who is of better quality than her mate (e.g. Moller, 1992); she may be seeking multiple fathers for her offspring, so as to maximize their genetic diversity (e.g. Moller & Birkhead, 1992); she may be seeking parental investment for her offspring from more than just one partner (e.g. Davies, 1992); she may be trying to acquire a new partner after she has lost her own (e.g. Gjershaug, Jarvi, & Roskaft, 1989); or she may be seeking protection of her offspring by confusing parentage and, thus, inhibiting aggression from non-paternal males (e.g. Hrdy, 1979,1981; Palombit, Seyfarth, & Cheney; 1997).
Because birds are more likely than mammals to be socially monogamous, most studies of EPCs are in birds rather than mammals. Humans, however, are unusual mammals and, in terms of mating system, we tend to be more like most birds: that is, like most bird species, most human populations consist of nuclear families consisting of a cohabiting male and female with their joint offspring. Many of the reasons why a female bird might seek EPCs are likely to hold for human females as well.
SNEAKY SOLUTION: CONFUSING PATERNITY AMONG SEVERAL MALES
Another strategy is to mate with all the males in a particular (relatively small) social group (e.g., a troupe of monkeys). A female chimpanzee may receive as many as 135 ejaculations from most of the males in her community before conceiving (Dixson, 1998; Hasegawa and Hiraiwa Hasegawa, 1990, Goodall, 1986). Sara Hrdy has noted that by so thoroughly confusing the issue of paternity, a female may obtain protection and resources from several males (since one or more of her offspring might be genetically his). In addition, males of the troupe would be less likely to kill or injure her offspring. A decrease in infanticide would support the paternity-confusion tactic displayed by females of varying primate species (Dixson, 1998).
Females may also mate with multiple partners to ensure sperm competition and the success of the most viable sperm. Offspring will carry the traits of the most successful male with whom copulation is successful; therefore, females may compete with other females for access to multiple males (Dixson, 1998).
COMPETING WITH OTHER FEMALES
As noted above, FROM MEALEY
while males may be less choosy than females in terms of being less likely to reject a sexual offer, they certainly have reasons to be choosy about whom they pursue (Altmann, 1997). This is particularly true for sexual partners who are also parental partners -- partners in whom they invest and in whose offspring they may invest in the future. Females differ in their likelihood of conceiving and, in the case of viviparous species, in their ability to carry offspring to term. They also differ in health, parenting skills, the level of paternity confidence they offer, and their needs for, and ability to obtain, important resources. To the extent that these differences make males choosy about their partners, females may have to compete with one another (Hooks & Green, 1993). Females may also have to compete directly amongst themselves for feeding or breeding territories (Clark, 1978; Dublin, 1983; Silk, 1983; Sterck, Watts & van Schaik, 1997; Wasser, 1983).
One form of female competition is specifically sexual: females may attempt to use sex to woo a particular male away from his current partner. Gjershaug et al. (1989) describe the tactics of 20 female pied flycatchers after their mates were experimentally removed from the couples' territories. Six of the experimentally "widowed" females proceeded to solicit sex from neighboring males, despite the fact that they were no longer fertile and that non-fertile copulations are otherwise not known to occur in this species. One of these six "widows" was able to get the neighboring male to remain with her and help take care of her offspring. This tactic may be restricted to situations in which males are in relatively short supply. Alternatively, it may be a tactic used by already-mated females to try to obtain a "better" partner.
Perhaps the most common form of competition among females is direct harassment. In primates, Hrdy (1981) and Smuts (1987a) have described the physical harassment of subordinate females by higher-ranking females -- harassment that appears to be aimed at preventing the subordinate females from acquiring resources (Slagsvold & Lifjeld, 1994). Physical harassment is even used as a tactic to interrupt the matings of subordinate females. By interrupting the mating attempts of less-dominant females, dominant females may be able to prevent extended consortship between a couple, thereby reducing the paternity confidence of the male(s) involved, making him (them) less likely to devote further attention or effort toward the subordinate female and her future offspring (and, therefore, more toward herself, the dominant female and her offspring). Females harassing one another during copulations were observed within the Hanuman langur (Dixson, 1998; Sommer, 1989). Since these females also compete for resources such as food, it is believed the harassment during copulation is to prevent the copulating female from reproducing and adding competition for resources with the addition of offspring (Dixson, 1998; Sommer, 1989).
Harassment may also reduce the likelihood that the harassed female conceives or is able to raise viable offspring (Fedigan, 1997). The ultimate result is that there are fewer resource competitors for the harasser and her own offspring. In what is probably the most extreme case of harassment so far documented, a high-ranking mother-daughter pair of chimpanzees was observed to harass new mothers of their own troop to the point of virtual exhaustion. The marauding team is known to have killed and, together, consumed, several of the infants, and they are suspected in the sudden disappearance of several more (Pusey et al., 1997). Whether this behavior represents an aberrant, pathological case or is an example of an uncommonly seen, but evolved adaptive strategy, is unknown.
Females may also compete with other females solely by their status in the social hierarchy. Low social rank, subjection to aggression, or the stress of social isolation has been seen to affect the menstrual cycle duration within female baboons (Dixson, 1998). These subordinate female baboons and mandrills face a longer period of infertility during their menstrual cycles, characterized by no swelling of the hind-quarters (Dixson, 1998). In rhesus monkeys, both dominant and subordinate females reproduce; however, dominant females that begin to reproduce at an early age generally produce offspring earlier during the birthing season (Dixson, 1998; Drickamer, 1974). The dominant females also produce more offspring in their lifetimes that the subordinate females.
INVESTING IN HER OWN OFFSPRING (FEMALE MATERNITY SECURITY)
FEMALE PROBLEM CHOOSING THE BEST TIME FOR PREGNANCY
FROM MEALEY
For some species, when to reproduce is not even a question: they have a single chance in a single window of time. Other, longer-lived species semelparous species- may have an option of when to reproduce, and may face that decision several times. The key factor in making such a decision is this: will delaying reproduction increase the potential for reproduction later? The decision rule says: if not, then reproduce now.
POTENTIAL SOLUTIONS
DO NOT GET PREGNANT DURING HARD TIMES
Females should have been selected to attempt to avoid getting pregnant during difficult times (e.g., famine, social conflict, etc.) Indeed, female reproductive output is decreased as a function of stress (either by failure to ovulate and/or miscarriage).
Life is always uncertain, so in one sense, fast and early reproduction is the best strategy to ensure that multiple copies of one's genes make it into future generations (Low, 1998). Indeed, this is one component of the reproductive strategy of r-selected species. On the other hand, successful reproduction always entails a certain minimum effort, below which, no effort is better than a wasted effort. Thus, if energy resources are at a minimum and there is an option to delay, a delay might be the best course of action (Ono, 1997).
Which option is best depends on the chances of successful reproduction at the moment and the chances of surviving the delay and actually being in better circumstances at a later date (Reiter, 1997). Furthermore, because egg-laying and pregnancy are energy-draining, an early reproductive effort may reduce energy levels or otherwise impede a later reproductive effort; thus, the potential costs of reproduction now versus reproduction later must be considered (Altmann, Altmann & Hausfater, 1978; Clutton-Brock, 1991; Hill, 1993; Wasser & Barash, 1983). All the while, a potential mother must weigh all these factors based on the probability that she will not even survive long enough to reproduce again.
All this gets pretty complicated, and clearly no individual of any species actually calculates such odds directly. Over evolutionary time, however, certain statistical odds prevailed under certain combinations of maternal age, health, and environmental circumstances, giving each individual a statistical probable future reproduction or "reproductive value" (Pianka, 1978). The physiology and psychology of females of different species have evolved so that their reproductive "choices" are based on these prevailing reproductive values. The variables that will, thus, influence any particular female's reproductive "choices" include her age and health, as well as any environmental factors that can serve as a proxy predictor of her future condition (Clutton-Brock, 1991; Fairbanks, 1996; Wasser & Barash, 1983).
SPACE PREGNANCIES
Females should attempt to space pregnancies at appropriate intervals, given the availability of resources in the environment, to maximize her reproductive success. Oftentimes, certain seasons provide the best environment and most abundant resources that will maximize reproductive success and ensure the survival of offspring. During a four-year study of desert bighorn sheep, births occurred during seven months out of the year (Rubin et al, 2000). However, 87% of the young were born during the months of February to April, with the largest concentration of births being in March at 55% (Rubin et al, 2000). This study suggests the environment during the spring in the
FEMALE PROBLEM INVESTING IN THEIR OFFSPRING
POTENTIAL SOLUTIONS
WEANING & ALLOCATING RESOURCES AMONG OFFSPRING
Evolutionary theory suggests that resources should be allocated to offspring as a function of their reproductive potential (e.g., offspring with greater potential getting more resources during harsh times).
FROM MEALEY
Finally, individual mothers also have some choice as to how to allocate their parenting efforts. As a result, the quality, quantity and duration of post-natal parental care is not just something that varies across species; it can also vary facultatively within species, and even within an individual mother over time or in relation to different offspring (Clutton-Brock, 1991; Fairbanks, 1996; Hauser & Fairbanks, 1988; Nicolson, 1987).
Conflict will occur between caretakers and offspring of any species in which there is extended post-natal care. Perhaps the most common and obvious form of parent-offspring conflict manifests as fledging or weaning, but infanticide, neglect, and favoritism can also be viewed as the end result of parental investment decisions.