How and Why Female Sexual Selection Influences Male Characters

Secondary sexual characteristics have puzzled biologists for years. These characteristics appear to be worthless ornaments that are costly for the organism in terms of energy and increased visibility to predators. Peacock's tails, deer antlers, and brightly colored plumage are all examples of these seemingly useless and deleterious traits, which are now believed to be extremely important to males' reproductive success. Numerous theories have been proposed concerning why and how certain traits develop, how and if they are beneficial, and why specific traits are chosen over others. Hamilton and Zuk proposed the most central of these theories in 1982; this theory proposes, among other things, that female choice is based on heritable variation in resistance to parasites which males display through ornamentation or physical displays. Although this theory has some flaws, the idea that secondary sexual characteristics display fitness and that females are able to assess fitness from these displays appears to be true in many cases.

One of the major assumptions for these theories is that females choose their mates; this is called sexual selection. Sexual selection of males occurs in species that are polygynous, in which females are able to choose from a variety of males, females must invest significant energy into their offspring, and males must compete to pass on their genes. The idea that females are picky about which males they are willing to mate with and pick the "best" male possible also assumes that heritable variations confer genetic advantages to their offspring. Females choose males based on phenotype and displays, which demonstrate the males' superior genes; males that are able to grow exaggerated characteristics and invest energy and time in displays of physical fitness are thought to have a genetic advantage over males who cannot. Because these females invest energy in their offspring, both before their birth and after, they are more selective about which males they allow to contribute genes. Males that have a less than optimal genotype and phenotype are not worth the female's effort. These males are weeded out by sexual selection based on mating displays and ornaments. The exception to this includes an indirect benefit to the female; females will mate with less than desirable males if their offspring will have increased viability. The "sexy son" hypothesis postulates that females may forgo direct benefits to increase the chance of their offspring reproducing and thus carrying their genes into another generation.

Female sexual selection drives the evolution of male sexual ornaments and display, but what is unclear is how females judge males and how variations in male fitness are physically manifested. The latter is the topic of most of the theoretical writing and experiments reviewed here. Female choice models include the good genes and runaway models and heritable variation in viability models theorize on why male sexual characteristics may be highly variable within a population (Sullivan). The good genes model assumes that female preference and male characteristics can coevolve for any number of reasons. One explanation for coevolution may be that female sensory organs are biased to prefer specific male embellishments. Another explanation for coevolution may be that females incur direct benefits by mating with certain types of males. Indirect benefits to females may take the form of increased viability for offspring when the father is selected, which leads to further selection for traits demonstrating fitness and can result in coevolution. Hamilton and Zuk proposed the idea that mating with male birds possessing bright plumage may indirectly benefit female birds. Males that are able to survive the increased energetic demands of growing and maintaining bright feathers and increased visibility, and thus risk of predation, may have an increased resistance to parasites. Mating with these birds confers indirect benefits on the female by providing good genes for their offspring, who will potentially also be more resistant to parasites (Sullivan).

An argument against directional sexual selection makes the point that if only certain males are allowed to breed then the population will decrease in genetic variation. Decreases in genetic variability often lead to more homogeneity, which makes species more vulnerable to genetic disorders, disease, and parasites, which is not the case in all species exhibiting sexual characteristics. However, Pomiankowski argued that this objection is overstated since many genetic mechanisms can work against sexual selection to increase variation. Recurrent mutations, natural selection acting in opposition to sexual selection, and other factors can increase genetic variation in a population and thus maintain heritable variation (Sullivan).

Male sexual traits are generally accepted as injurious; they have high energetic costs and increase risk of predation. This means that males with very developed sexual characteristics have reduced viability, but not developing these exaggerated traits would decrease their viability further by making it unlikely that they will reproduce. This loss of viability must be present for handicap theories to work. The basic handicap principle is a sports analogy; Zahavi and Zahavi write that, "the investment that animals make in signals is similar to the 'handicaps' imposed on the stronger contestant in a game or sporting event" (Getty). This means that animals with extreme sexual characteristics carry heavy parasite loads. The idea behind this is the economic concept of conspicuous consumption; "By wasting one proves conclusively that one has enough assets to waste and more" (Getty). More flashy signalers show that they have enough energy to waste some and still survive, lower-quality signalers signal less because they do not have access to the same resources or are less fit overall, and therefore cannot afford to waste large amounts of energy on sexual displays. These males are not chosen as mates because they are less visible; they have a less fit phenotype, which is the physical manifestation of their genotype; and, in species where males help with parenting, are not able to offer sufficient resources to the offspring and mother. Regardless of whether a handicap model is used, parasites are the focus of much of the literature surrounding sexual selection and the evolution of secondary sexual traits.

Parasites seem to be the most variable factor that could affect an organism's viability. Hamilton and Zuk focused on the effects of parasites as well; they predicted that signals of good health are dependant on low parasite loads, which would contribute to reproductive viability and stated that their hypothesis would be contradicted if a species generally chose mates with the most parasites (Getty). This hypothesis has been difficult to prove and to disprove, because the type of ornament and display varies widely in cost across species and because determining the actual number and negative effects of parasites is difficult. Sexual characteristics can range from traits that may be otherwise useful to the organism to extreme ornamentation that makes them vulnerable to predators and unable to defend their selves, and may include traits that are unidentified and therefore not measurable, even if the known traits could be measured in terms of loss of viability. More important is the fact that parasite load and the harm done by parasites is both parasite and species specific. Because each host-parasite relationship for a species is not fully understood, determining harm is not possible, nor can the amount of parasites in an organism be accurately measured. Hamilton and Zuk's theory does work if, instead of trying to measure how many parasites are in each organism and comparing their viability, researchers are able to find instances of lower and higher parasite loads in the same species and correlate those instances with reproductive viability.

Folstad, Arneberg, and Karter were able to examine the effects of lowered parasite loads in a population of reindeer by examining the affects parasites had on antler symmetry. The premise for this is that symmetry of ornamental characters is important to sexual selection and may be caused by environmental stressors that affect the ability to develop identically on both sides of the body. In "Antlers and Parasites" the authors cite a study conducted by Moller that supports the idea that environmental stresses, such as parasites, can influence development of symmetry. Moller found that increased parasite loads made the tail feathers of Hirundo rustica develop asymmetrically and decreased parasite loads resulted in more symmetrical tail ornamentation. However, fluctuations in parasite loads were visible in traits evident only in males. The authors used female reindeer, which have antlers, to test if parasite load changes would affect the symmetry and size of their antlers, because they are presumably not useful in sexual displays. Half the females were treated for nematode parasites and the other half was a control. At the end of the study, antler symmetry was determined and the treated reindeer were found to have significantly more symmetrical antlers than those that had not been treated for nematodes (Folstad). These studies support the idea that increased parasite loads decrease reproductive viability by decreasing symmetry, an important factor in which individuals mate and pass on their genes.

Males tend to be most affected by sexual selection because their energetic input into the creation of an offspring tends to be smaller than the female's and because, in mammals, males tend to be larger, and thus more prone to parasites. In polygynous groups, where sexual characteristics tend to be pronounced, the most effective strategy for males is to mate with many partners. Sperm are less costly to produce than eggs and male parental investment may be small; it is often less than a female's. This is also why females can be, and are, picky about their mate; successful females invest more in fewer offspring than successful males. Males that do not confer any benefit to the mother or offspring are simply not worth the energy required to produce young. Female selection and competition from other males also has a tendency to result in sexual dimorphism, usually for larger males than females. Moore and Wilson researched the affect of increased body size on parasite load.

By comparing the parasite loads of sexually dimorphic mammals, they were able to find a trend toward greater parasitism of males in more sexually dimorphic mammals. Moore and Wilson concluded that "increased parasitism is a cost of sexual selection in mammals." They went on to hypothesize that the larger sex is simply more exposed because it offers a larger target for vectors or "some limiting resource constrains both somatic growth and immune function". This means that enhanced growth may come at the cost of reduced immune systems (Moore).
Although some sources argue against parasite load as an indicator of health and search for other factors that may affect sexual viability, most would agree that parasite loads have some affect on which males are able to mate. Through the process of sexual selection females choose males, presumably based on secondary sexual characteristics. Males display to attract the attention of females through ornamentation and displays of physical health. These displays may be hampered by parasites, which may make the male less able devote energy to growing large ornaments and competing with other males. Displays of male health are costly, but necessary, because in species that practice female mate choice, only the males that are able to display breed. By reducing their personal health males are able to increase their reproductive viability. Parasites do not only affect male health, but they are more likely to affect males because males tend to be larger and probably devote more energy to ornamentation than to keeping their immune systems in good order. Males are forced to demonstrate their good genes because sperm are far less costly to produce than an egg, they must prove that their genes are worth the energy put into creating an egg and caring for the young.

Works Cited
Able, D. J. (1996). The contagion indicator hypothesis for parasite-mediated sexual selection. Pro. National Academy of Science, USA. 93, 2229-2233.

Folstad I., P. Arneberg, A. J. Karter (1996). Antlers and parasites. Oecologia. 105, 556-558.

Getty, T. (2001). Signaling health versus parasites. The American Naturalist. 159, 363-370.

Moore, S. L. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science. 297.

Sullivan, B. K. (1991). Review: Parasites and sexual selection: separating causes and effects. Herpetologica. 47, 250-264.