Chapter 7
MATING SYSTEMS
Copyright © 2004, Michael E. Mills
A mating system describes the way in which organisms develop and maintain reproductive partnerships. The type of mating system that evolves (e.g., monogamy, polygyny, polyandry, promiscuity, etc.) in a particular species is determined by several ecological and social variables (Barash, 1982). Here we will attempt to understand why certain variables tend to produce a specific type of mating system.
There are four major classifications of mating systems:
(a) MONOGAMY. A male and female form a durable reproductive partnership. It may last for only one breeding season, or it may last an entire lifetime. Males and females of most monogamous species tend to have little sexual dimorphism (e.g., the males and females are about the same size and morphology).
(b) POLYGYNY. Some males mate with more than one female (other males do not get to mate at all).
(c) POLYANDRY. Some females mate with more than one male.
(d) "PROMISCUITY." Males and females may mate with more than one member of the opposite sex--no long-term bonds are formed.
There are various subcategories of each of these mating systems, some of which some particular species practice more than one, which we will explore below.
We will start with monogamy since it is the mating system with which we are most familiar. Indeed, in most modern human cultures today, mating systems other than monogamy have been made illegal. However, monogamy is surprising rare across species, especially in mammals.
Since there are reproductive rewards for males to attempt to mate polygynously, how did monogamy, choosing and committing to only one mate, develop at all? For males, monogamy represents a compromise – one in which he is obligated to reduce his maximal reproductive rate to the slower rate of a single female. In monogamous mating systems, males and females have identical fitness variances. For example, if the female has a reproductive maximum of eight offspring, then the male’s reproductive maximum is the same (Barash, 1982).
Monogamy tends to evolve when male parently investment is obligatory (i.e., when the young are not likely to survive without him), or when the benefits of the male moving on are too low (i.e., other female mates are hard to find, and the female he is with will be ready to mate again soon) (Owens & Bennett, 1997).
Most bird species are monogamous, for example, because eggs require incubation from two parents, and the young are helpless and unable to locate food on their own at birth. In addition, they have high metabolic rates that require large amounts of food to be acquired by both the mother and father to ensure the young’s survival (Barash, 1982). A male bird with several mates and broods cannot adequately provision them.
This theory helps to explain why monogamy tends to be much less common in mammals as compared to other animals: in mammals, females make a sizable investment in their young through lactation. This might render the father’s contribution less important. When the paternal contribution in raising the young is not as crucial, such as in most mammals, the reproductive consequences to males for desertion are not as high.
However, male contribution of resources is often valuable in mammalian carnivores. The prey caught and killed by a male can be shared with offspring. Also, in marmosets and small
In primates, the meaning of monogamy can be extended to include characteristic social behaviors. Among monogamous primate partners, characteristic behaviors include mate guarding, pair-bonding, and the formation of a family unit (Fuentes, 1999).
Since monogamous mating systems impose parental investment costs on males, males will only mate monogamously if there is a good chance that their offspring are genetically their own – that is, if they have paternity security. This leads to what might be called the “biological marriage contact.” This contract involves an exchange. Males offer parental investment in exchange for female sexual access and sexual fidelity. Females offer their fertility and fidelity in exchange for male parental investment. “Divorce” tends to occur when one partner reneges on his or her part of the “agreement.” Males tend to abandon their partner when she shows evidence of sexuality infidelity; females tend to reject their partner when he fails to invest parentally (or show signs that he can’t, or won’t, invest in the future).
The term “monogamy” is generally thought of as faithfulness, and, in fact, the concepts of monogamy and sexual fidelity are often used interchangeably in language referring to human relationships; in the animal world, however, there are actually two kinds of monogamy, and neither of them necessarily involves sexual fidelity. There is lifetime monogamy, in which animals remain with one partner throughout all breading seasons. There is also serial monogamy, in which animals switch partners with each consecutive season. Both kinds of monogamy involve shared resources, living arrangements, and economic investments.
Even in monogamous mating systems, at times both males and females may stray from their partner sexually. The reproductive benefits to males of additional mating partners are obvious, but what does a female have to gain?
A female may sometime invests in two partnerships, her monogamous relationship and an “extra-pair copulation”, each for different reasons. She may choose one for parental investment and the other for good genes (Birkhead & Moller, 1992). Immunity is also a consideration in such extra-pair copulations: the female will have a better chance of succeeding in raising surviving offspring if those young are parented by different fathers. Having several offspring with differing immunity profiles allows the female to cover the possibility of various parasites and ensure her reproductive success. Studies have shown that within one litter or brood is often evidence of multiple paternity, as shown by DNA fingerprinting (e.g. Hasselquist, Bensch, & Schantz, 1996).
One of the most well-known species in which males end up raising and providing resources for the offspring of other males is the cuckoo. The female cuckoo lays her eggs in other birds’ nests, tricking the nest owner or host into adopting and providing for the offspring. In fact, it is from the name of this species of bird that the term “cuckold” derives; it refers to males who end up raising offspring who were fathered by another male. Males generally try to avoid such an outcome, as it requires a great investment of energy with no reproductive payoff. Frequent female infidelity (aimed at ensuring the female’s own reproductive success) exerts pressure on males to be aggressively vigilant in preventing such an outcome from occurring. As we have seen in earlier chapters, when males (either polygynous or monogamous) have mated, they often demonstrate “mate guarding” behaviors: they may follow their mates and prevent opportunities for the female to mate with other local males (e.g. Birkhead & Moller, 1992). Males of many species even develop anti-sperm apparatus on their sex organs which wipe out sperm from previous inseminations, thereby reducing the chance that recent competitors will successfully impregnate the females with whom they are now mating (Eberhard, 1985; Smith, 1984).
In monogamous systems, sexually dimorphic traits are generally not available to select a mate. In monogamous species, signs of health and good genes are the general criteria for mate selection. Individuals of monogamous species also use another gauge of selecting a mate right for them: in a type of mating selection called positive assortment or assortive mating, individuals generally mate with partners who are similar to themselves, in both physical features and behavioral traits (e.g. Cooke & Davies, 1983).
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Why does assortive mating occur? Several explanations have been offered for this fascinating phenomenon (Burley, 1983). One explanation suggests that since some individuals are obviously fitter and healthier than most, they will be attractive to virtually all of their potential partners, and will be able to select from all of them. Thus the most attractive potential partners will be likely to find each other, while the least attractive suitors will be left with other less attractive individuals as potential partners.
Another explanation is that choosing partners based on similarity to oneself may discourage outbreeding. This would offer the benefits of the kin cooperation of extended families. The optimal level of mating relatedness, it has been suggested, may be that of cousins, who are one-eighths related (Bateson, 1983; Partidge, 1983). Studies have shown that cousins who were previously unknown to each other are more likely to choose each other as a partner than other individuals with whom they are also unacquainted (Bateson, 1982,1983). This startling finding occurs whether the other potential choices are less or more closely related to the chooser. This gives some scientific credence to the idea of “kissing cousins”, suggesting that in monogamous species, cousins are indeed the pairing of choice.
Yet another compatible explanation for assortive mating is that there may be reproductive benefits to two partners who are similar in preferences and lifestyle raising young together. For instance, if a pair of mates have genetic preferences in food which are very different from one another, offspring may inherit only one of the preferences and reject the feedings by the other parent, which would make cooperative rearing difficult. An illustration of a similar phenomenon is that birds with contrasting preferences for nest incubation shift-length will have a difficult time coordinating schedules, and may end up both leaving the nest unattended at times, which could have serious negative consequences for the survival of their young (e.g. Mills, Yarrall, & Mills, 1996). Those animal partnerships, including humans, which have frequent disagreements over raising young and home-making, and (often causally related, as in the previous example) who have offspring that die early in their relationship, are most likely to separate and seek other breeding partners (Choudhury, 1995).
Assortative mating, thus, is generally the rule in monogamous relationships; the one exception to this is the disassociative mating that occurs for the major histocompatibility complex, or MHC (Hedrick, 1994). Reproductive success of both partners will be more likely if each contributes different genetic sequences for various immunities. The importance of selecting a mate with a dissimilar MHC sequence is evident in the fact that mice, for instance, can discern such specific differences (Yamakazi, Boyse, Mike, Thaler, Mathieson, Abbott, Boyse, Zayas, & Thomas, 1976). MHC status seems to be detectable through scent; a potential mate that smells different from oneself, implying the specific genetic dissimilarity of MHC, seems to be preferred (Potts, Manning & Wakeland, 1994).
It follows then, from the discussion above, that both sexes should be choosy in selecting a mate in species in which the investment of both parents is necessary to ensure the survival of young. In these cases, theoretically, both sexes will select mates based on signs of good genes and immunocompetence, but also based on signals that the potential mate of either sex will be committed to the family. Indeed, in species that are monogamous, both males and females are quite selective in choosing a mate, mutually sizing up each other’s displays of devotion to estimate whether the potential mate will remain loyal. In fact, courtship displays of males and females in such species are often nearly indistinguishable. Because sexual selection is does not operate as strongly on males of monogamous species, males and females tend to be monomorphic (similar in body) in species that mate monogamously.
Courtship displays advertise readiness and capability for commitment; such repetitive interchanges are usually lengthy and highly ritualized, often resembling a dance. In such intercommunications, both the male and the female may take turns actively displaying the energy they are willing to devote, as a token of their fidelity. Once mated, the couple may continue to enact these courtship displays; when partners have already mated and still repetitively engage in such courtship dance sequences This is referred to as pair bonding.
Recall from Chapter 5 the curious courtship and pair bonding behavior of courtship feeding. It works like this: usually the male offers the female a piece of food, as a display of his willingness and ability to feed her and her offspring. The female may then return the food back to the male, displaying that she is willing and able to do without food: that she is healthy enough to bear young and is not starving, and that she will be willing to go without for their young as well. Generally this passing of the food back and forth is repeated; usually the female ends up eating the food, as she will need it more to nourish the offspring (Avery, Krebs, & Houston, 1988).
It should be clear from previous chapters that the most widely used mating system in non-human animals is polygyny (from the Latin poly, many; and gyn, female), a system whereby certain males attain more than one female mate, while some males acquire no female mates at all.
Four types of polygyny are distinguished by the particular method used by males to monopolize female mates and to increase their offspring: harem defense, resource defense, scramble competition, and female choice (Andersson, 1994).
In species practicing territory defense, the richness of resources within a territory is not the only criterion a female uses to choose a territory; the number of other females with whom she is to share such resources is also a salient factor. Under certain conditions, it may be more advantageous to be the only mate on a poor territory than to be one among numerous females and offspring sharing a richer territory’s resources. These conditions may occur when a rich territory becomes too crowded to be more attractive than a poorer alternative; the point at which this happens is called the polygyny threshold (Orians 1969, Verner & Willson 1966; see Figure 7.4). Therefore, polygyny is most common in areas where territory quality is highly variable. If there is not a high variance in territory quality, a female will chose to mate with a remaining bachelor rather than become a second mate to a male with a slightly more resourceful territory (Daly & Wilson, 1983). Rather than being a constant, the polygyny threshold varies with population density and competition for resources. For instance, females who settle earlier in a rich territory may keep other females out, or even eject late-settling females, which can cause dramatic shifting of territory boundaries and residence patterns (Slagsvold & Lifjeld 1994).
(Insert polygyny threshold diagram)
A male who mated with fewer females may be more successful than a male who mated with many females if he is able to provide more assistance to his offspring and ensure their survival. In other words, the more likely a large male mammal is to contribute to parental investment of offspring, the more likely monogamy and reduced sexual dimorphism will occur. On the other hand, an extremely polygynous male may be unable to provide parental investment to his offspring (Barash, 1992).
As we know, polygynous relationships are almost always preferred by males of varying species, but why would a female agree to polygyny if she would be most successful with the undivided attention of a bachelor or otherwise uncommited male? First, if a male can contribute nothing to a female other than fertilization of her egg then females would benefit equally by mating with a mated or unmated male (Barash, 1992). Secondly, as previously mentioned, a female, who mates with males that other females desire, is selecting the best possible mate with the healthiest genes which will be passed on to her offspring.
Insert figure: Polygyny threshold model of habitat quality.
The polygyny threshold leads to certain predictions that can be ascertained through female mate selection:
Each of these predictions were confirmed by an experiment in a study of lark buntings. Female territory preference was characterized by the presence of shade in each of the areas. When the researcher experimentally added shade, by attaching plastic rosettes of leaves to alfalfa plants in territories that previously contained no shade, females became attracted to these areas and the males guarding these territories benefited greatly by increased reproductive success (Daly and Wilson, 1983). The females began to choose these areas over other areas and reproduced more successfully.
In harem defense polygyny, dominant males acquire and keep groups of female mates by frequently engaging in acts of aggression toward other males and, less frequently, even toward those females in their group who exhibit signals that they may leave the harem. These battles are usually won by the largest, fittest, and most aggressive males, allowing them to successfully mate. Such intrasexual selection for physical and behavioral traits occurring among males, but not females, of a species, results in significant sexual dimorphism (differences in body type and behavior), whereby the males typically have substantially larger body size than females and, in some species, display more weapon-utilizing behavior (Packer, 1983). The degree of this sexual dimorphism within a species is highly correlated with the ratio of breeding males to breeding females, known as the “operational”, “functional”, or “socionomic” sex ratio, of that species (Weckerly, 1998).
As we have seen in the previous chapter, struggles for dominance between males who want to breed often have their costs and casualties. Within species of large mammals, such as elephant seals and bison, harem masters may lose a large portion of their body weight during mating season, largely due to the energy expended battling other males over potential mates (Reiter, 1997). Wounds of battle are sometimes fatal, especially in species that have evolved the use of weaponry. To counteract this lethality and make such dominance struggles less dangerous, males have evolved two primary protective tactics: to put on a show of fighting rather than actually fighting; and to not fight at all before their prime.
The first strategy ensures that males struggling for breeding dominance will attempt to resolve a struggle by a ritualized contest of behaviors intended to display their superiority in battle, without having to actually engage in the potentially deadly battle itself. These behaviors often involve the males displaying their size and weaponry by pacing parallel to one another, or bellowing, with the winner of the contest producing the loudest vocalization. In such competitions, the smaller, less experienced, or less impressive male will usually concede victory, thus saving himself the fatal cost of actually going through with the battle when the opposing male has displayed that he will probably win. These ritualized display contests are exceedingly efficient at getting the job done of selecting the fittest breeder without loss of future breeders. This is especially advantageous for the potential loser, who gets to live and perhaps have a chance to breed in future years.
The second strategy males use to minimize the cost of battle is also a model of evolutionary efficiency. In many species which exhibit harem defense strategies, young males who are too small and inexperienced to win battles over potential mates, rather than resorting to the massive energy expenditure of building up the bulk of their body size and weaponry, instead show delayed maturation, reaching sexual maturity later than females of the same species. Until they are large enough to be capable of competing successfully with fully grown males, the younger males exhibit a marked delay in production of secondary sex characteristics and sperm. Adolescent males in species which exhibit delayed maturation have evolved to appear more like females than like fully adult males, to avoid competing before their prime with other males. Such younger males may often even act like females as well. By avoiding the expression of signals of dominance or readiness to mate, such feminine behavior deflects the potential threat of being challenged to battle by an older, stronger, and more competitive breeding male (Lyon & Montgomerie 1986). When older and fully engaged in battle, adult males also may behave in a way that shows submission; by using female mimicry, they can avoid injury and end the battle intact.
In species that exhibit harem defense, there is fierce competition among males for the chance to breed. In this system, there is great variance in male reproductive success (Clutton-Brock 1988). Males who have been able to survive long enough to obtain dominance as harem master are often soon replaced within one or two breeding seasons. This high rate of turnover, in a species with what may superficially seem to be an extremely imbalanced sex ratio, ensures that the ratio of mating-eligible males to females will not be so extremely high.
One choice a female in a harem group may make is whether she should stay, or join another harem. Since only the very best males are able to win and maintain harems, it generally is not advantageous for a female to leave her harem and risk the trials of journeying to a new territory to find and join a new group. There are situations, however, when it may become reproductively advantageous to transfer to another group. In species with small harem groups and/or harem masters who maintain superiority for a long time (such as gorillas), a female runs a reproductive risk by staying with the same group she was born into: the possibility that when she reaches reproductive maturity, the harem master may still be one of her close relatives. Mating systems in groups like these often allow female transfer as a way of avoiding inbreeding. Females who try to leave these groups are less likely to be restrained by the dominant male or to suffer retaliation from him for trying to leave than females in larger or more variable harem groups (Clutton-Brock & Parker, 1995). Such female emigration tends to happen at the onset of reproductive maturity, to avoid the danger of infanticide, which can occur if the female transports offspring with her or is pregnant at the time of transferring to another harem.
Areas in which resources are distributed in concentrated patches are tend to produce polygyny since males can monopolize and control access to necessary resources. In resource defense polygyny, boundaried territories are guarded by males against invasion by other male challengers. Females, however, are allowed on the territory only if they become mates of the territory holder. Females are attracted to territories that are sizable and have rich resources; males who are able to defend large territories with quality resources are likely to gain the most matings. A male long-billed marsh wren is able to attract females if he guards a large territory and is able to build numerous nests, demonstrating the abundance of food and resources within his area . By defending his resource-rich land, a male is providing for the success of his offspring.
For example, in the American bird, dickcissel Spiza americanus, males that defended territories with dense vegetation attracted more mates than those males with sparsely vegetated territories due the higher potential for secluded nesting sites within their territory. Female stickleback fish were attracted to males with large territories rather than those with small territories as male sticklebacks will eat the eggs and young of their neighbors. A male who can defend a large territory is probably aggressive enough to ward off predation from other males.
Holding onto a territory may not be as taxing as maintaining a harem against constant challengers, but defending a territory is costly in terms of time; in maintaining large territories, much time is required to patrol their boundaries and guard against intruders. The size and strength of a territory holder may not matter as much as that of a harem master; a territory holder may be large and strong, but an intruder could still slip onto his property through one border while the territory holder is patrolling another border. In harem defense, size and strength are of primary importance, to ward off constant challengers to his mates. In territory defense, however, the assets of agility, vigilance, endurance, and the ability to advertise one’s presence and phenotypic superiority over large areas are much more important (Weckerly, 1998). Intrasexual selection in territory defense species will thus be different than that in harem defense species. Trait selection in territory defense species will be based more on auditory and visual displays than on body size; sex differences will thus be less apparent in body size dimorphism than in advertising displays.
In addition to having this effect on body size of the territory holders, the constraints of territory defense also help define the size of the territories held. Territories that are rich in resources tend to be much smaller than territories which have few resources, because the borders of resource rich territories will be encroached upon by intruders much more frequently. But recall that rich territories tend to attract the most females; thus, a territory owner will not be able defend a territory large and rich enough to support the number of females and offspring that a harem master would be able to support. Species with territory defense polygyny will therefore generally have a less disproportionate socionomic sex ratio (the ratio of breeding males to breeding females) than species with harem defense polygyny; males in such species will still have greater variance in their reproductive success than females.
Males are not the only ones who hold territories; in some species, such as rats, the female is the territory holder while the male is nomadic (Foltz & Schwagmeyer, 1989). In other species, such as tigers, females and males hold separate but overlapping territories that they each defend separately against same-sex intruders (Sunquist, 1981). In some species, such as orangutans, both males and females wander within a range without territories to defend (Rodman & Mitani, 1987). To mate in such species, males have to find and monopolize females who happen to be ready to breed; this is often challenging, because a female may only be sexually receptive for a very short time. In species practicing this system, called scramble competition polygyny, the most successful males will be skilled at detecting females ready to breed; successful males will also be able navigators who can negotiate hazards of strange terrain to reach such females (Schwagmeyer, 1995).
Scramble polygyny results in even less conspicuous sexual dimorphism than resource defense polygyny. In scramble polygyny species, sexual selection tends to be for behavioral instead of physical sex differences (Jacobs, 1994). In such species, males are rewarded for exhibiting risk-taking behaviors, wandering, being flexible in feeding patterns, navigating well, and being good detectives. Behavioral characteristics and skills such as these may be sexually dimorphic to varying degrees. In many rodent species, according to recent studies, sexual differences in spatial skills tend to favor males; how much of this cognitive dimorphism is present in a species is directly related to the species’ degree of polygyny (Gaulin, 1992; Gaulin & Fitzgerald, 1986; Jacobs, 1994).
A form of polygyny in which females choose a mate from many potential suitors competing for her favor is called female choice polygyny. In species with this system of polygyny, females who are ready to breed make direct choices: in species such as salamanders, for instance, females assess males they happen to encounter and accept or reject them then and there (Houck & Reagan, 1990); in species such as bowerbirds, females visit different males in their territories or display sites, traveling back and forth to compare them (Borgia, 1985b,1995); in species such as peacocks and grouse, females go to a congregational display area called a lek, where they can compare many males at the same time (Petrie, Halliday, & Sanders, 1991; Alatalo, et al., 1991; Gibson & Bradbury, 1985).
In species like these, in which the primary breeding criterion is the choice of the female, traits of males are selected which, rather than allowing them to compete aggressively with other males, allow them to compare themselves favorably in displaying themselves to females. Recall that this process is known as intersexual selection or epigamic selection; like intrasexual selection, it results in sexual dimorphism (Andersson, 1994).
When a female chooses a mate but does not choose a territory, she has to be choosy, because the possible mate will offer no territorial resources and will be contributing nothing but his genes to her future offspring. In a circumstance like this, the female uses cues to assess a potential mate in terms of probable genetic quality. It is more difficult, however, to assess the quality of genes than it is to assess the quality of resources available on a territory, which are more readily apparent. So, how does a female go about determining which male has the best genes?
One theory is that females seek out potential mates who will have male offspring who will, in turn, be attractive to other females; this is called the “sexy son” model, or the “Fisherian” model. According to this model, whether a male is attractive to other females is the criterion by which a female finds a male attractive. Females mandrills choose to mate with males, displaying brightly colored, gaudily colored faces (Small, 1992). Thus, a male’s success with other females is as important to assess as physical and behavioral traits are to the scrutinizing female looking for a potential mate (Dugatkin, 1992; Pruett-Jones, 1992). Since the males who are the most successful with females are the most attractive to other females, the outcome often is that one male may achieve all or most of the matings in a geographical area. When some males have very high success rates while other males have complete reproductive failure, the result is the strong selection for those traits which increase attractiveness, even slightly, to females. In elephant seals, only the harem master mates with the females while many bachelors are unable to reproduce at all. Since a harem master may have forty mates, thirty-nine males are reproductive failures. Approximately ten percent of male elephant seals fertilize nearly ninety percent of the females during each breeding season and pass their traits to the next generation.
Over time and through many generations, even slight incremental trait changes can become substantial; the final result of this selection over time can be greatly disproportionate exaggeration of certain desired characteristics. This is, for instance, how birds like peacocks, widowbirds, and birds of paradise wound up with their distinctively elaborate, long tails (Andersson, 1982; Harvey & Arnold, 1982). In the male widowbird, individuals with the longest tails are known to have the most nests in their territories. This means that the longer tail attracts mates, leading to more pairings and more nests for resultant offspring (who also possess the attractive trait of a long tail) (Small, 1992).
There are strong biological penalties for non-conformity in systems like this. If a female does not follow the crowd in her mate preference and chooses to mate with a male whom her peers do not find attractive, she may be successful reproductively, but only in the short run. She may succeed in raising offspring, but any sons she has will have a distinct disadvantage compared to other males of the same group. These sons will not have the same traits that most females find attractive, and their ability to find mates themselves will be seriously compromised. The daughters of such a female, like their mother, will tend to shun the trait preferred by their peers; they, too, may be successful in breeding, but their sons will suffer the same fate as their brothers, being unsuccessful in the mating game.
Over time, the lineage of females who do not prefer the selected trait will thus disappear, and the population of females who prefer the trait will increase. When the feedback between the preferred male trait and the female preference for it increases greatly, a situation gradually arises called “runaway selection”; in such a process, traits which were once functional for survival and thus attractive to females become attractive in and of themselves in the long run.
Runaway traits may evolve through intersexual (epigamic) selection, or even through intrasexual selection, such as the exaggerated size of elephant seal harem masters. Traits like this, which evolve only because of their value in attracting mates, and not for any other purpose, may actually be a threat to the survival of the males who exhibit them (Andersson, 1994). For instance, a peacock’s long, elaborate tail feathers make it very difficult for him to fly to escape danger; predators such as tigers also can easily grab peacocks by their long tail feathers, a direct liability to safety and survival. Male widowbirds are handicapped as well by their long tails; males with the longest tails actually are at the absolute limit of their size while still being able to marginally fly (Thomas, 1993). This limit has been reached because the potentially fatal cost of having tails any longer offsets the potential benefits longer tails might offer in terms of mating (see Figure 7.7). Peacocks and widowbirds actually shed their long tail feathers between mating seasons, a powerful demonstration that the liability of hauling them around is simply not worth the cost when mating is not an issue.
It also costs a male a great deal to maintain such exaggerated traits in terms of the energy it takes to grow and maintain them. This may actually be a factor in female selection of a mate.
The “handicap model” is another way to look at female choice systems (Johnstone, 1995; Zahavi, 1975). According to this model, a male exhibiting an exaggerated trait which is in itself a physical handicap (long, elaborate tail feathers; a huge beak, etc.) is in effect displaying an advertisement. He is signaling to females the fitness of his genes that enable survival, since he would need to have strong energy reserves, sharp perceptual skills to find energy resources, and an efficient metabolism to develop and maintain the handicapping trait, as well as swiftness and agility to be able to elude predators despite the handicap.
The sons of these males will inherit the genes for these traits, and will be able to attract mates with them because of the survival assets they imply. The survival and reproductive benefits will also be passed down to the daughters, as well, though the handicap will not. Thus, the daughters will be able to reserve and channel more energy into reproduction and raising offspring, because of the inherent survival benefits in the genes they have inherited. The survival benefits of these genes is the crux of this model of female selection; the handicap model theorizes that females select mates with handicaps which are well-maintained at great expense, because of the good genes for other survival-enhancing traits this expense implies.
We have seen two models of female choice systems; a third is the “parasite model” (Hamilton & Zuk, 1982). This is related to the handicap model, although it focuses on being able to evade a different kind of predator: mainly microscopic, parasitic ones. According to this model, when a male displays well-maintained features which are obviously expensive metabolically, it implies that he has good genes, as well as something else: it also reveals that he must have a healthy immune system to be able to have this extra energy to keep up this extra expense, despite having to spend energy to ward off not only predators he can see, but the numerous microscopic parasites which are a constant threat to everyday survival. When an individual is not successful at doing both simultaneously, he will display this vulnerability through lack of maintenance of the physical features, or even visible deformity or damage. For example, in studies of pigeons in which the parasite load has been manipulated, it has been found that the plumage of birds with greater parasite loads are less well-maintained; it has also been found that such parasitically overburdened birds have less energy for courtship display, which may affect their ability to attract mates (Clayton, 1990).
The handicap model and the parasite model both theorize that the expensive sexually-selected traits are advertisements of male fitness; thus they are not mutually exclusive, although they do differ in subtle ways. The handicap model suggests that females choose males for mating partners who display evidence of a better genotype for physical fitness; such genotypes generally remain similar over many generations. The parasite model suggests that females make their selection based on evidence of a better immunoconfiguration, which may change drastically even from one season to the next, because of swift parasite mutations and changing host vulnerability. In the parasite model, the best male one season may actually be the worst the following season. In both models, the present state of a male’s physical condition is highly significant to selective females; this is because, when it comes to the survival capacity of her potential offspring, it is the upcoming season that is important (Clayton, 1991).
Many traits which are sexually-dimorphic are due to testosterone, which is, in fact, a handicap itself; testosterone production has been found to inhibit immune system functioning (Folstad & Karter 1992, Nelson & Demas 1996). So, according to both the handicap and parasite models, males displaying expensive, well-maintained testosterone-caused characteristics are advertising both their good genes and their strong immune system. The fact that they exhibit maintenance of these testosterone-related features shows that their immune systems are capable of fighting off parasites even while compromised by high production of testosterone (Zuk, Johnsen, & MacLarty, 1995).
Good genes and a strong immune system are also advertised by another very important feature: body symmetry. Bilaterally symmetric body parts, such as eyes and ears, come from genes which are not duplicated in the genome. Thus, the set of genes which determines the code for the right eye also determines the left. Asymmetry of features which normally are symmetric is known as fluctuating asymmetry, as opposed to genetically-encoded symmetry. Any fluctuating asymmetry which is apparent indicates that at some point during development, some environmental insult (usually a nutritional deficiency or an infection) disturbed the epigenetic process enough to cause different outcomes from the same genetic code. Such asymmetry also suggests that the individual’s ability to cope with environmental challenge has been weakened (Moller, 1990; Parsons, 1990; Polak & Trivers, 1994; Van Valen, 1962).
Symmetry is highly attractive to selective mates, perhaps because it portends better performance in adulthood; generally individuals with more symmetry perform better than individuals with some asymmetry (Manning & Ockenden, 1994; Waldrop, Pedersen, & Bell, 1968). This improved performance may be a direct result of the underlying genotype and/or immunoconfiguration, or it may be an aftereffect of the resulting symmetry. In either case, it has been shown that individuals of many species, including humans, possessing more symmetric features are, in general, more attractive to, and successful with, potential mates (Thornhill & Gangestad, 1993,1994).
Polyandry occurs when one female is mated simultaneously with more than one male. It is very rare, both across animal species and in human cultures. It is rare because it reduces the reproductive success of males.
When form of mating strategy is seen, it is usually in species in which the male is has high assurance of genetic paternity, and is mainly responsible for parental investment in offspring. For example, in many species of birds, after a clutch is laid, the male is responsible for incubation while the female searches for nourishment to replace the resources she used in producing the eggs. If she is indeed successful in foraging, she may lay another clutch, which would be advantageous to her reproductive success. She may use the original mate to father her second clutch; however, this choice will leave her with the responsibility of incubating the second clutch. Therefore, if the female is able to find a second male to father her second clutch, she will once again be freed from the responsibility of incubating the eggs (Barash, 1982). As in the polygynous mating strategy, the better the territory a female inhabits, the more likely she will be successful in producing a large number of offspring.
In order for males to invest time and energy into fathering offspring, there must be a high confidence of paternity (Barash, 1982). Beyond the initial incubation period, offspring generally have little need for paternal investment. When a female lays large eggs, producing precocial young that are able to survive upon hatching, she provides them the nourishment needed for development. As in the Jacana spinosa shorebirds, females are freed of all parental duty by leaving the male responsible for incubating the eggs and defending the nest. With the time she saves from parental responsibilities, a female uses to defend her large territory, to mate, and to lay eggs.
Polyandry is divided into three classifications: synchronous, classic, and cooperative. In synchronous polyandry, more than one male may mate with a female, and in most cases, neither sex participates in parental care of the offspring. In classic polyandry, females compete for mates and leave a mating partner for the next. All parental investment becomes the responsibility of the father. In this form of polyandry, the sexual dimorphism is noticeable between the sexes as the females are larger, aggressive, and exhibit more behavioral and physical displays. Finally, cooperative polyandry occurs when females, along with two or more males, divide and share parental responsibilities among themselves. Little to no sexual dimorphism is noticed in the species practicing this form of sexual dimorphism.
Although females benefit reproductively from polyandry, they do so at a high cost to males. Males who father a clutch of eggs with a female may become entirely responsible for the parental investment of the offspring until they hatch. During this period of incubation, males cannot reproduce with any other females as they will not be able to invest in her offspring. Therefore, a male must be certain the female he invests in is healthy and is able to produce viable offspring so that he does not waste precious time incubating her eggs that may be harmed by poor genes or bad health.
Furthermore, a male must be certain he is the father of a clutch prior to investing valuable time and resources towards parenting. In order to do this, he must be certain the female has not mated with another male and left him with the responsibility of incubating another male’s offspring.
Not every species falls into one category or another in terms of the mating system that they utilize. Polygynandry is a mating system that may integrate components of the strategies previously discussed. Polygynandry occurs when several females as well as several males inhabit and nest within a territory, sharing in mating relationships and the consequent parental responsibilities associated with the resulting offspring. Although this type of relationship may sound promiscuous and random, it may actually be highly structured, integrating components of monogamy, polygyny, and polyandry. In fact, dominance and social structures most likely exist between both sexes as well as between individuals of the same sex. Furthermore, mating rights and parental duties may follow strict guidelines due to the rules of the social hierarchy in place among the mating individuals.
Evidence of multimale-multifemale mating systems were seen in a variety of primate species including macaques (Seyfarth, 1978) and chimpanzees (Tutin, 1979; Goodall, 1986). A relationship between a male and a female may last from several hours up to many days; however, exclusive relations between the two animals is not guaranteed. Van Noordwijk (1985) observed among primates that both males and females copulated with several partners but always returned to the original pairing afterwards. As mentioned above, the pairings that did occur were far from random as they were influenced by the individual’s social rank, familial relations, age, sexual appeal and attractiveness, and sexual preferences.
In the species that utilize multimale-multifemale mating systems, females generally engage in numerous copulations prior to conception. This is where sperm competition plays a significant role in a male’s reproductive success. For instance, in the ring-tailed lemur, data on one female shows that she mated with five males and received 27 ejaculations during a four hour period in which she was sexually receptive (Koyama, 1988). Similarly, as in rhesus monkeys (Manson, 1992) and in chimpanzees (Hiraiwa-Hasegawa, 1990) copulations can be as frequent as 50-90 times and 135 times, respectively, prior to conception. Therefore, the males that are successful in producing offspring with a female must be aggressive as sperm competitors.
As in human beings, promiscuity in animals refers to the absence of any pair-bond contracts between mates. However, promiscuous does not refer to a lack of discrimination of choice in species that utilize this mating strategy. On the contrary, secondary sexual characteristics may be extremely elaborate which indicates a high level of importance towards sexual mate selection (Barash, 1982). Many mammalian species have this mating system since female mammals can nourish her offspring without the aid of a male mate. Within these mammalian species, such as in most rodents, males defend a territory, and mate with females that enter their territory and are in estrus (Barash, 1982). In general, they do not remain with any one female for a long period of time.
Passerine birds such as brown-headed cow-birds are promiscuous animals that do not even rear their own young. Instead of the male or female becoming solely responsible for parental investment of offspring, these birds deposit their eggs in the nests of a host species, who unknowingly raise the offspring of another species (Barash, 1982). Furthermore, monogamy is not practiced in these bird species as cow-birds feed near grazing cattle who disturb insects from their habitats. These insects become the food resources on which the cow-birds depend, requiring no defense by a potential mate (Barash, 1982).