Sexual selection theory postulates that males will compete with one another to inseminate the largest number of females possible. The ability of the male to be a successful polygynist allows him to pass on his genetic information to a large number of progeny. Thus it is difficult to explain males who do not seek out more than one partner per breeding season, males who stay with a single partner for a long period of time (monogamy), and males who share a single female with several other males (polyandry).
The mate-guarding hypothesis maintains monogamy may be adaptive. A female left by one male would acquire another partner, whose sperm would then fertilize her eggs (Emlen, 215). Thus it is in the best interest of the first male to remain with his partner if receptive females are scarce. For example, the male clown shrimp, Hymenocera picta, will spend many weeks with a single female rather than try to inseminate as many females as possible.
An alternative to the mate guarding hypothesis, the mate-assistance hypothesis, theorizes that males will remain with a single partner to help rear offspring in environments in which male parental care can greatly promote offspring survival. The number of progeny that survive as a result of male monogamy is decidedly higher than the number that would survive if the male abandoned and fathered many more offspring with several other females.
In some species, the female will try to block the male's attempts at polygyny. For example, paired females of the beetle Nicrophorus defodiens assault their mate when they release sex pheromones to attract other potential female mates. The couple will pair to bury a carcass on which the female will later lay her eggs. Once the carcass is buried, the male will try to attract another female partner by releasing pheromones. The first female will push him from the perch or bite him to stop him from attracting other females that might lay eggs on the carcass. This eliminates competition between the two female's larvae for survival on the same carcass. This is known as female-enforced monogamy.
When a paired female beetle is experimentally tethered and unable to prevent her male from releasing sex pheromones after the burial of a carcass, the amount of time the male spends releasing hormones increases dramatically. Graph reproduced from Eggert and and Sakaluk, 334.
Monogamy is exceptionally rare in mammals. The mate-assistance hypothesis suggests that males who make a parental investment in their young are usually monogamous. Although fewer than ten percent of male mammals give substantial parental care, most of these exceptional males are monogamous (Alcock 487). Males who make a large parental investment increase the likelihood that their offspring will survive and pass on their genetic information, thus it serves the same genetic purpose as the paternal animal not making an investment in his offspring, trying to fertilize as many females as possible, and having many litters with low survival rates. There are rare cases of males being sexually monogamous and not making a large parental investment in the offspring. This is known as facultative monogamy.
Because of their lack of paternal care and voluntary sexual monogamy, Kirk's dikdik (Madoqua kirki), a dwarf African antelope, are considered to be an example of practitioners of extreme facultative monogamy. Photo courtesy Andrew Waddington.
Birds, one of the largest groups of animals that are often monogamous, sometimes demonstrate a behavior known as extra-pair copulation. For males, these extra-pair copulations have many costs: there is a great deal of time spent away from the alpha pairing in search of beta females. Also, the alpha female may mate and be fertilized by a beta male while the alpha male is away searching for a partner. It has been shown that males tend to guard their primary mates much more closely during her fertile period and spend time in search of other mates only after this period is over. Whether these extra-pair copulations prove worthwhile for the males involved depends entirely on whether or not a beta female's egg is fertilized. With the use of DNA fingerprinting to determine paternity, it has been demonstrated that extra-pair copulation is advantageous for males and that the beta female's eggs are in fact fertilized quite frequently.
What do females stand to gain from extra-pair copulation? Most females resist philandering males, however some seek out copulation from more than one male. The table below lists hypotheses on why females might seek out several partners.
Table 1. Hypotheses on why females might benefit by mating voluntarily with more than one male. Reproduced from Alcock, 493.
Genetic Benefits of Polyandry
1. Egg fertilization insurance via acquisition of sufficient numbers of competent sperm.
2. Better sperm with genes acquired from preferred sexual partners.
3. Genetic variety gained via acquisition of genetically diverse sperm.
Material Benefits of Polyandry
1. Acquisition of resources controlled by mating partners.
2. Acquisition of parental care from mating partners.
3. Improved foraging success via distraction of a male foraging competitor.
4. Reduced risk of sexual harassment form non-partners.
It has been shown that sometimes females actively seek out extra-pair copulations also. Agelaius phoeniceus, the red winged blackbird, has been studied extensively as an example of female initiated extra-pair copulation. In the study population, females initiate courtship and copulation outside their social bond.
"...between 18 and 43% of all breeding females engaged in extra-pair copulations each breeding season. The peak of extra-pair copulation occurred 2 days before the first egg was laid and 1 day closer to egg laying compared to the peak of within-pair copulation, suggesting that extra-pair copulations conferred a genetic advantage to females. Females that copulated with extra-pair males improved their reproductive success by hatching a significantly greater proportion of eggs and fledging a significantly greater proportion of young than females that did not copulate with extra-pair males. Improved hatching success was probably due to female avoidance of temporary male sperm depletion. Improved fledging success resulted from significantly lower depredation rates of clutches laid by females that copulated with multiple males. In addition, a lower proportion of nestlings tended to starve in broods containing extra-pair fertilized offspring." (Gray)