Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders?

Optimal skew models explain reproductive sharing within social groups as resulting from reproductive incentives given by controlling dominants to subordinates in return for peaceful cooperation. We explore two versions of an alternative, the incomplete control model, for the evolution of reproductive sharing within groups. In this model, dominants have only limited control over the allocation of reproduction and must expend effort to increase their share of the total group output We show that, when the relatedness between dominant and subordinate is symmetrical, (1) the subordinate's fraction of reproduction either increases with, or is insensitive to, the subordinate's genetic relatedness, r, to the dominant in both versions of the incomplete control model, whereas the subordinate's fraction of reproduction decreases with increasing r in the optimal skew model, (2) the subordinate's share of reproduction in the incomplete control model must exceed that in the optimal skew model, and (3) ecological factors affecting solitary breeding success do not directly affect the subordinate's share of reproduction in incomplete control model but do in the optimal skew model. When dominant-subordinate relatedness is asymmetrical (as is often the case in parent-offspring associations), the incomplete control model predicts no reproduction by the subordinate offspring regardless of group size for groups containing any mixture of unrelated and full-sibling subordinates, whereas the optimal skew models predict that such reproduction is possible when the group size is three or more. The available evidence indicates a negative relationship between relatedness and a subordinate's reproductive share in both vertebrate and hymenopteran societies, apparently supporting the predictions of the optimal skew, not incomplete control, class of models. However, such a negative relationship is not necessarily inconsistent with the incomplete control model when, as is true for some vertebrate studies, it results from a comparison of skews in genetically monogamous, nonincestuous groups of parents and their offspring (asymmetric relatednesses) with skews in groups of nonkin (symmetric relatednesses). Both models predict higher skews in parent-offspring associations. Occasional reproduction by subordinate offspring in groups of asymmetrical relatedness when such groups are larger than dyads is more consistent with the optimal skew model, however. Overall, current data on reproductive skew and its relationships to intragroup aggression and ecological constraints support the optimal skew model, but more data are needed to rule out the incomplete control model. These models are examples of two different general views of intrasocietal evolution: the tug-of-war view, in which group members engage in a struggle over resources, and the transactional view, in which group members exchange parcels of reproduction to induce beneficial behavior from each othe

Promiscuous Honey Bee Queens Increase Colony Productivity by Suppressing Worker Selfishness

SummaryQueen monogamy is ancestral among bees, ants, and wasps (Order Hymenoptera), and the close relatedness that it generates within colonies is considered key for the evolution of eusociality in these lineages [1]. Paradoxically, queens of several eusocial species are extremely promiscuous [2], a derived behavior that decreases relatedness among workers and fitness gained from rearing siblings but benefits queens by enhancing colony productivity [3–9] and inducing workers to rear queens’ sons instead of less related worker-derived males [10–13]. Selection for promiscuity would be especially strong if productivity in a singly inseminated queen’s colony declined because selfish workers invested in personal reproduction at the expense of performing tasks that contribute to colony productivity. We show in honey bees that workers’ ovaries are more developed when queens are singly rather than multiply inseminated and that increasing ovary activation is coupled with reductions in task performance by workers and colony-wide rates of foraging and waggle-dance recruitment. Increased investment in reproductive physiology by selfish workers might result from greater incentive for them to favor worker-derived males or because low mating frequency signals a queen’s diminished quality or future fecundity. Either possibility fosters selection for queen promiscuity, revealing a novel benefit of it for eusocial insects

Evolutionarily stable communication between kin: a general model

At present, the most general evolutionary theory of honest communication is Grafen's model of Zahavi's 'handicap' signalling system, in which honesty of signals about the signaller's quality (e.g. mate suitability or fighting ability) is maintained by the differentially high cost of signals to signallers having lower quality. The latter model is here further generalized to include any communication between signallers and receivers that are genetically related (e.g. parents and begging offspring, cooperative or competing siblings). Signalling systems involving relatives are shown to be evolutionarily stable, despite a potential pay-off for false signalling, if the Zahavian assumption of differential signal costs holds and there are diminishing reproductive returns to the signaller as the receiver's assessed value of its attribute increases, or if, regardless of whether the Zahavian assumption holds, signallers with high values of the attribute benefit more from a given receiver assessment than signallers with low values (e.g. begging chicks that are hungrier benefit more from being fed). In stable systems of signalling among kin, it is also shown to be generally true that (i) levels of signalling and thus observed signal costs will decline as relatedness increases or as the receiver's reproductive penalty for erroneous assessment increases, and (ii) receivers will consistently, altruistically overestimate the true value of the signalled attribute

Partial ovary development is widespread in honey bees and comparable to other eusocial bees and wasps

Honey bee workers have few opportunities for direct reproduction because their ovary development is chemically suppressed by queens and worker-laid eggs are destroyed by workers. While workers with fully developed ovaries are rare in honey bee colonies, we show that partial ovary development is common. Across nine studies, an average of 6% to 43% of workers had partially developed ovaries in queenright colonies with naturally mated queens. This shift by workers toward potential future reproduction is linked to lower productivity, which suggests that even small investments in reproductive physiology by selfish workers reduce cooperation below a theoretical maximum. Furthermore, comparisons across 26 species of bees and wasps revealed that the level of partial ovary development in honey bees is similar to that of other eusocial Hymenoptera where there is reproductive conflict among colony members. Natural variation in the extent of partial ovary development in honey bee colonies calls for an exploration of the genetic and ecological factors that modulate shifts in cooperation within animal societies

Predicting the temporal dynamics of reproductive skew and group membership in communal breeders

Reproductive skew models attempt to predict the fraction of reproduction contributed by each individual that participates in a communal brood. One potential limitation of these models is that individuals make a single, fixed decision about group membership and reproductive allocation at the beginning of the breeding period. While this is appropriate for animals that reproduce in a synchronous bout, many cooperative breeders produce offspring over a prolonged period of time. It is likely that these species adjust reproductive allocation and group membership over time in response to temporal shifts in group productivity and ecological constraints. In this paper we adapt transactional models of reproductive skew to a continuous form, generating time-dependent functions of reproductive allocation. We derive a general method for predicting temporal changes in group membership as well as a general expression for reproductive skew across the regions over which a group is stable. Using a linear approximation for time-dependent reproduction, we derive new expressions for reproductive skew in cases where the subordinate departs during the breeding period. In this case we find that the traditional model always overestimates the subordinate's share of reproduction when dominants are in control of both reproductive shares and group membership (i.e., concessions models). Conversely, we find that the traditional model always underestimates the subordinate's share of reproduction when subordinates are in control of reproductive shares (i.e., constraint models). We discuss the implications of these new calculations in relation to the traditional skew models and more recent empirical tests of reproductive skew in animal societies. Copyright 2005.communal breeding; dynamic model; kin selection; reproductive skew

Mating games: the evolution of human mating transactions

We propose a new, evolutionary, game-theoretic model of conditional human mating strategies that integrates currently disconnected bodies of data into a single mathematically-explicit theory of human mating transactions. The model focuses on the problem of how much resource a male must provide to a female to secure and retain her as a mate. By using bidding-game models, we show how the male's minimally required resource incentive varies as a function of his own mate value, the value of the female, and the distribution of the mate values of their available alternative mates. The resulting theory parsimoniously accounts for strategic pluralism within the sexes, mate choice differences between the sexes, and assortative mating, while generating a rich set of testable new predictions about human mating behavior. Copyright 2004.assortative mating; evolution; game theory; human mating; mate choice; mating strategies