Reproductive Social Behavior: Cooperative Games to Replace Sexual Selection
Science 17 February 2006:Vol. 311. no. 5763, pp. 965 - 969DOI: 10.1126/science.1110105
A recent review of diversity in animal reproductive social behavior (1) raises questions about Darwin's 1871 theory of sexual selection (2). Unlike the theories of evolution through common descent and of evolutionary change by natural selection, Darwin's theory of sexual selection has continually drawn criticism from evolutionists, notably Huxley in 1938 (3). Darwin wrote "Males of almost all animals have stronger passions than females" and "the female... with the rarest of exceptions is less eager than the male... she is coy." Darwin explained these templates as resulting from females choosing mates who are "vigorous and well-armed... just as man can improve the breed of his game-cocks by the selection of those birds which are victorious in the cock-pit." He continues, "Many female progenitors of the peacock must... have... by the continued preference of the most beautiful males, rendered the peacock the most splendid of living birds."
Since 1871, sexual selection theory has often been restated (4), yet contemporary definitions share Darwin's central narrative: "We now understand... Males, who can produce many offspring with only minimal investment, spread their genes most effectively by mating promiscuously... Female reproductive output is far more constrained by the metabolic costs of producing eggs or offspring, and thus a female's interests are served more by mate quality than by mate quantity" (5). This narrative is taught in biology textbooks (6), is axiomatic to evolutionary psychology (7), and is broadcast in popular media (8).
The reproductive social behavior of most species has not been studied, but a great many of those that have been do not conform to Darwinian sexual-selection templates. We suggest that sexual selection is always mistaken, even where gender roles superficially match the Darwinian templates.
There are fundamental problems that universally undercut all applications of sexual selection theory to any species, including the contradiction between sexual selection's rationale and the reason for sexual versus asexual reproduction, the difficulty of sustaining a stable hierarchy of genetic quality within a gene pool in the face of continued directional selection for high-ranked genotypes, and the use of different fitness definitions for males and females. These and other fatal problems are detailed in the references accompanying table S1.
We think that the notion of females choosing the genetically best males is mistaken. Studies repeatedly show that females exert choice to increase number, not genetic quality, of offspring and not to express an arbitrary feminine aesthetic. Instead, we suggest that animals cooperate to rear the largest number of offspring possible, because offspring are investments held in common. We therefore propose replacing sexual selection theory with an approach to explaining reproductive social behavior that has its basis in cooperative game theory. We introduce a notion of allocating time into various relationships to maximize cooperative, or "team," fitness. In this theory, we can observe that diverse social organizations emerge from how individuals accrue direct benefits from the relationships they develop with one another within diverse ecological contexts.
Cooperative Games in Reproductive Social Behavior
Here, we explain reproductive social behavior in developmental time, not evolutionary time. A social system develops from the interaction of individuals just as body parts develop from the interaction of tissues. In our model, each animal acts continually as an individual or as a team member, and the value of an action is scored by how it contributes to that animal's average fitness accumulation rate (9). An individual's actions involve obtaining and exchanging direct benefits to increase the number of offspring successfully reared (10–14). We further envision a future two-tier theory that will embed this phenotypic treatment within an overarching evolutionary-genetic model.
Maynard Smith introduced game theory to biology in the 1980s, including the evolutionary stable strategy (ESS), a population-genetic counterpart to the Nash competitive equilibrium (NCE) of game theory (15). A competitive game ends when an NCE is attained, i.e., the state where each player cannot better its position, given the positions of the other players. In competitive games, the players do not communicate.
In cooperative games, players make threats, promises, and side payments to each other; play together as teams; and form and dissolve coalitions. Cooperative games usually end up at different solutions to an NCE. Nash also investigated cooperative games and introduced the concept of a Nash bargaining solution (NBS) as an outcome of these games (16).
Logic of bargaining and side payments. To illustrate, consider a "payoff matrix" that indicates the direct benefit each player receives in every scenario (17)
......
A recent review of diversity in animal reproductive social behavior (1) raises questions about Darwin's 1871 theory of sexual selection (2). Unlike the theories of evolution through common descent and of evolutionary change by natural selection, Darwin's theory of sexual selection has continually drawn criticism from evolutionists, notably Huxley in 1938 (3). Darwin wrote "Males of almost all animals have stronger passions than females" and "the female... with the rarest of exceptions is less eager than the male... she is coy." Darwin explained these templates as resulting from females choosing mates who are "vigorous and well-armed... just as man can improve the breed of his game-cocks by the selection of those birds which are victorious in the cock-pit." He continues, "Many female progenitors of the peacock must... have... by the continued preference of the most beautiful males, rendered the peacock the most splendid of living birds."
Since 1871, sexual selection theory has often been restated (4), yet contemporary definitions share Darwin's central narrative: "We now understand... Males, who can produce many offspring with only minimal investment, spread their genes most effectively by mating promiscuously... Female reproductive output is far more constrained by the metabolic costs of producing eggs or offspring, and thus a female's interests are served more by mate quality than by mate quantity" (5). This narrative is taught in biology textbooks (6), is axiomatic to evolutionary psychology (7), and is broadcast in popular media (8).
The reproductive social behavior of most species has not been studied, but a great many of those that have been do not conform to Darwinian sexual-selection templates. We suggest that sexual selection is always mistaken, even where gender roles superficially match the Darwinian templates.
There are fundamental problems that universally undercut all applications of sexual selection theory to any species, including the contradiction between sexual selection's rationale and the reason for sexual versus asexual reproduction, the difficulty of sustaining a stable hierarchy of genetic quality within a gene pool in the face of continued directional selection for high-ranked genotypes, and the use of different fitness definitions for males and females. These and other fatal problems are detailed in the references accompanying table S1.
We think that the notion of females choosing the genetically best males is mistaken. Studies repeatedly show that females exert choice to increase number, not genetic quality, of offspring and not to express an arbitrary feminine aesthetic. Instead, we suggest that animals cooperate to rear the largest number of offspring possible, because offspring are investments held in common. We therefore propose replacing sexual selection theory with an approach to explaining reproductive social behavior that has its basis in cooperative game theory. We introduce a notion of allocating time into various relationships to maximize cooperative, or "team," fitness. In this theory, we can observe that diverse social organizations emerge from how individuals accrue direct benefits from the relationships they develop with one another within diverse ecological contexts.
Cooperative Games in Reproductive Social Behavior
Here, we explain reproductive social behavior in developmental time, not evolutionary time. A social system develops from the interaction of individuals just as body parts develop from the interaction of tissues. In our model, each animal acts continually as an individual or as a team member, and the value of an action is scored by how it contributes to that animal's average fitness accumulation rate (9). An individual's actions involve obtaining and exchanging direct benefits to increase the number of offspring successfully reared (10–14). We further envision a future two-tier theory that will embed this phenotypic treatment within an overarching evolutionary-genetic model.
Maynard Smith introduced game theory to biology in the 1980s, including the evolutionary stable strategy (ESS), a population-genetic counterpart to the Nash competitive equilibrium (NCE) of game theory (15). A competitive game ends when an NCE is attained, i.e., the state where each player cannot better its position, given the positions of the other players. In competitive games, the players do not communicate.
In cooperative games, players make threats, promises, and side payments to each other; play together as teams; and form and dissolve coalitions. Cooperative games usually end up at different solutions to an NCE. Nash also investigated cooperative games and introduced the concept of a Nash bargaining solution (NBS) as an outcome of these games (16).
Logic of bargaining and side payments. To illustrate, consider a "payoff matrix" that indicates the direct benefit each player receives in every scenario (17)
......
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