Polygyny Threshold (Behavioral Ecology)
KeywordsFemale Choice Paternal Care Great Reed Warbler Territory Quality Unmated Male
The polygyny threshold is the minimum difference in quality of male territories that is sufficient to make a female choose to mate with a male that is already mated, instead of mating with a male that has no mates.
For decades, polygynous mating systems – in which a male is paired to two or more females – were seen as a reflection of the population sex ratio. Under this rationale, a 1:1 adult sex ratio (one male for each female in the population) would predict that males would mate, on average, with one female during the breeding period, and females would behave the same way; i.e., the mating system would be monogamous. Following this rationale, in a biased sex ratio scenario of 1:3 (one male for three females), it would be expected that males would acquire more than one mating partner; i.e., a polygynous mating system would be predicted. However, through the accumulation of data on sex ratios and mating system characteristics, it was noted that there are cases that rebut the already mentioned rationale to explain the evolution and development of polygynous mating systems. For instance, there are monogamous species with biased sex ratios, and polygynous species with even sex ratios.
In the light of the inconsistence of the sex ratio hypothesis, in the 1950s, researchers started to develop hypotheses to explain the evolution of polygyny. Verner (1964) noticed that in a population of the long-billed marsh wren, Telmatodytes palustris, despite the even sex ratio, there were several cases in which females chose already mated males, while there were unmated males available. If females choose a mated male instead of a bachelor, they should gain fitness benefits from this behavior and, thus, there should be selection acting on females to mate polygynously. Given this scenario, Verner (1964), and Verner and Willson (1966) developed the hypothesis that when differences exist in the qualities of male territories, if the difference between two territories is large enough, females will choose the male in the better territory even if this territory already has a female and the other territory has no females. This led to the idea that there must be a threshold that determines whether a female must remain in monogamous relationships or join polygynous ones, i.e., the polygyny threshold.
From Monogamy to Polygyny
Every trait or behavior that enhances the fitness of an individual is expected to be selected. If a male acquires more offspring by mating with several females, one can expect the evolution of polygyny. However, if the male provides parental care to the offspring, the evolution of polygyny may be disadvantageous to females, given that a polygynous male will have to share his parental effort among the offspring obtained with different females – each female receives less help than she would obtain in a monogamous relationship. If polygyny is disadvantageous to females (i.e., reduces their fitness), one can expect polygyny to be counter-selected.
If a female in a polygynous group receives less help in caring for her offspring, what could also make polygyny advantageous to females, to the point that polygyny would be selected? Mating with already mated males would be expected in situations in which the female may gain greater direct (e.g., food, protection, nest sites) and/or indirect (e.g., genes of higher quality to her offspring) benefits from polygyny. Given the potential benefits, females should choose among males basing their decision on: genetic male quality, potential paternal care, and the quality of the territory held by each male. Every time these benefits overcome the costs of polygyny (e.g., less help in caring for young, greater competition for resources), polygyny is expected to evolve. This evolution is likely to take place when there is variance in the distribution of a particular resource (e.g., food) in the environment. Such variance allows the existence of territories that contain greater amounts of resource than others. Once the territories are different in quality, if the male population is large enough, some males will occupy low-quality territories. Once males occupy territories that vary in quality, they cannot offer equivalent reproductive benefits to females.
Hypothetically, the first female to choose a mate has all the n mature males available to her choice. If the territories held by these males differ in quality, the female is predicted to choose the male holding the best territory. The second female to make a choice faces a different situation; she may choose between a number of n – 1 unmated males, and one mated male holding the best territory. If this second female gains more offspring by choosing the male with the second best territory than mating with the mated male, she is expected to become monogamous. However, if despite the costs of sharing the best territory with another female, the second female gains more offspring by choosing the mated male with the best territory instead of the bachelor holding the second best territory, she is expected to establish a polygynous relationship. This shift from monogamy to polygyny is created by the differences in quality between the males’ territories. This polygyny threshold can only be crossed once a female joining a polygynous group can achieve reproductive success at least as high as if she would by mating with a bachelor. If the differences in territory quality are of great magnitude, it is possible that some males will be able to monopolize a larger proportion of females, leading some low-quality males with low-quality territories to stay unmated.
The Polygyny Threshold Model
The polygyny threshold model (PTM) was developed by Orians (1969) in order to propose a hypothesis for the evolution of mating systems in birds and mammals based on individual fitness, and in opposition to a hypothesis based on group selection. Through the analyses of female choice possibilities, the PTM provides theoretical basis to predict the development of mating systems, specifically the shift from monogamy to polygyny. Polygyny is always expected to be advantageous to males, thus to understand the evolution of polygyny, one should focus on benefits and costs to females. Hence, the PTM is based on female choice.
The PTM promoted a great amount of empirical tests, and received support from different sources of data, for instance: polygynous females of great reed warblers, Acrocephalus arundinaceus, indigo buntings, Passerina cyanea, and lark buntings, Calamospiza melanocorys, show similar reproductive success when compared to monogamous females; the majority of red-winged blackbird females chose polygyny when they were experimentally faced with mated males with territories containing more nest sites, and bachelors with territories containing fewer nest sites; by breeding in high-quality territories, these polygynous females gained fitness benefits that surpassed the costs of mating polygynously (Pribil and Searcy 2001), which makes the polygyny option adaptive.
Counter-Evidences and Criticism
The PTM was also refuted by other studies, which leads to the idea that the applicability of the PTM may be restricted to some contexts and systems, in a way that some species and even particular populations in generally polygynous species may not behave as predicted by the model. For example, in the work of Pleszczynska (1978), some females that could mate with a mated male with a better territory chose to mate with a bachelor. In red-winged blackbirds (different study from the mentioned above), females do not even pay a cost of polygyny. Moreover, other studies report that second females to mate with the male gain lower fitness than monogamous females. Given the difficulties in interpreting the contrasting evidence, alternative or complementary hypotheses to the PTM have been proposed. For instance, it has been argued that, if females settle asynchronously in a male territory, the overlap in urgency for paternal care by each brood may be reduced, which diminishes the polygyny threshold (Leonard 1990). The sexy son hypothesis has been proposed to explain cases of lower fitness of second females (Weatherhead and Robertson 1979). This hypothesis states that a second female to cross the polygyny threshold may gain less reproductive success than a monogamous female at a first moment. But, their young will be of higher quality – since the young received alleles from a high-quality polygynous father – thus, she will gain greater fitness in future generations through the offspring of her sons.
Another limitation of the PTM is that it assumes that females may choose mates freely (i.e., PTM is an ideal free model), but, in many cases, females are not free to choose partners. For instance, second females may not be allowed to settle by resident females of mated males (e.g., red-winged blackbirds), thus they may not be able to cross the polygyny threshold. Besides that, sometimes, females may mate with an already mated male just because it is difficult to find unmated males, distinguish mated from unmated males (Alatalo et al. 1981), and/or properly sample males and territories. Lastly, contrary to the PTM, sometimes it seems that females do not suffer costs from polygyny and just settle at random, which led to a neutral mate choice hypothesis (Lightbody and Weatherhead 1988).
The polygyny threshold is an important idea that helped to explain the evolution of polygynous mating systems. The concept led to the development of several theoretical models, especially the PTM. This model provided theoretical base and many predictions for empirical tests. The limitations of the PTM stressed in the last four decades are important and must be considered in the construction of the paradigm. Nevertheless, the PTM and, particularly, the concept of a polygyny threshold remain key points in the continuous effort to understand the evolution of mating systems.