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Concept: Kin selection

267

Why females of some species cease ovulation prior to the end of their natural lifespan is a long-standing evolutionary puzzle [1-4]. The fitness benefits of post-reproductive helping could in principle select for menopause [1, 2, 5], but the magnitude of these benefits appears insufficient to explain the timing of menopause [6-8]. Recent theory suggests that the cost of inter-generational reproductive conflict between younger and older females of the same social unit is a critical missing term in classical inclusive fitness calculations (the “reproductive conflict hypothesis” [6, 9]). Using a unique long-term dataset on wild resident killer whales, where females can live decades after their final parturition, we provide the first test of this hypothesis in a non-human animal. First, we confirm previous theoretical predictions that local relatedness increases with female age up to the end of reproduction. Second, we construct a new evolutionary model and show that given these kinship dynamics, selection will favor younger females that invest more in competition, and thus have greater reproductive success, than older females (their mothers) when breeding at the same time. Third, we test this prediction using 43 years of individual-based demographic data in resident killer whales and show that when mothers and daughters co-breed, the mortality hazard of calves from older-generation females is 1.7 times that of calves from younger-generation females. Intergenerational conflict combined with the known benefits conveyed to kin by post-reproductive females can¬†explain why killer whales have evolved the longest post-reproductive lifespan of all non-human animals.

Concepts: Evolution, Reproduction, Human, Scientific method, Male, Inclusive fitness, Natural selection, Kin selection

227

Despite its short-term costs, behaviour that appears altruistic can increase an individual’s inclusive fitness by earning direct (selfish) and/or indirect (kin-selected) benefits. An evolved preference for other-regarding or helping behaviour in potential mates has been proposed as an additional mechanism by which these behaviours can yield direct fitness benefits in humans.

Concepts: Motivation, Evolutionary psychology, Evolutionary biology, Richard Dawkins, Inclusive fitness, The Selfish Gene, Altruism, Kin selection

214

Recent work has revealed a new class of “zero-determinant” (ZD) strategies for iterated, two-player games. ZD strategies allow a player to unilaterally enforce a linear relationship between her score and her opponent’s score, and thus to achieve an unusual degree of control over both players' long-term payoffs. Although originally conceived in the context of classical two-player game theory, ZD strategies also have consequences in evolving populations of players. Here, we explore the evolutionary prospects for ZD strategies in the Iterated Prisoner’s Dilemma (IPD). Several recent studies have focused on the evolution of “extortion strategies,” a subset of ZD strategies, and have found them to be unsuccessful in populations. Nevertheless, we identify a different subset of ZD strategies, called “generous ZD strategies,” that forgive defecting opponents but nonetheless dominate in evolving populations. For all but the smallest population sizes, generous ZD strategies are not only robust to being replaced by other strategies but can selectively replace any noncooperative ZD strategy. Generous strategies can be generalized beyond the space of ZD strategies, and they remain robust to invasion. When evolution occurs on the full set of all IPD strategies, selection disproportionately favors these generous strategies. In some regimes, generous strategies outperform even the most successful of the well-known IPD strategies, including win-stay-lose-shift.

Concepts: Kin selection, Biology, Nash equilibrium, Natural selection, Evolution, The Evolution of Cooperation, Prisoner's dilemma, Game theory

198

The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.

Concepts: Population genetics, Inclusive fitness, Natural selection, The Selfish Gene, Evolutionary biology, Altruism, Evolution, Kin selection

76

Humans often cooperate with strangers, despite the costs involved. A long tradition of theoretical modeling has sought ultimate evolutionary explanations for this seemingly altruistic behavior. More recently, an entirely separate body of experimental work has begun to investigate cooperation’s proximate cognitive underpinnings using a dual-process framework: Is deliberative self-control necessary to reign in selfish impulses, or does self-interested deliberation restrain an intuitive desire to cooperate? Integrating these ultimate and proximate approaches, we introduce dual-process cognition into a formal game-theoretic model of the evolution of cooperation. Agents play prisoner’s dilemma games, some of which are one-shot and others of which involve reciprocity. They can either respond by using a generalized intuition, which is not sensitive to whether the game is one-shot or reciprocal, or pay a (stochastically varying) cost to deliberate and tailor their strategy to the type of game they are facing. We find that, depending on the level of reciprocity and assortment, selection favors one of two strategies: intuitive defectors who never deliberate, or dual-process agents who intuitively cooperate but sometimes use deliberation to defect in one-shot games. Critically, selection never favors agents who use deliberation to override selfish impulses: Deliberation only serves to undermine cooperation with strangers. Thus, by introducing a formal theoretical framework for exploring cooperation through a dual-process lens, we provide a clear answer regarding the role of deliberation in cooperation based on evolutionary modeling, help to organize a growing body of sometimes-conflicting empirical results, and shed light on the nature of human cognition and social decision making.

Concepts: Decision making, Evolutionary biology, Kin selection, Reciprocal altruism, Altruism, Game theory, Cognition, The Evolution of Cooperation

70

When we contract an infection, we typically feel sick and behave accordingly. Symptoms of sickness behavior (SB) include anorexia, hypersomnia, depression, and reduced social interactions. SB affects species spanning from arthropods to vertebrates, is triggered nonspecifically by viruses, bacteria, and parasites, and is orchestrated by a complex network of cytokines and neuroendocrine pathways; clearly, it has been naturally selected. Nonetheless, SB seems evolutionarily costly: it promotes starvation and predation and reduces reproductive opportunities. How could SB persist? Former explanations focused on individual fitness, invoking improved resistance to pathogens. Could prevention of disease transmission, propagating in populations through kin selection, also contribute to SB?

Concepts: Sickness behavior, Symptoms, Kin selection, Immune system, Evolutionary biology, Evolution, Natural selection, Bacteria

48

Prolonged life after reproduction is difficult to explain evolutionarily unless it arises as a physiological side effect of increased longevity or it benefits related individuals (i.e., increases inclusive fitness). There is little evidence that postreproductive life spans are adaptive in nonhuman animals. By using multigenerational records for two killer whale (Orcinus orca) populations in which females can live for decades after their final parturition, we show that postreproductive mothers increase the survival of offspring, particularly their older male offspring. This finding may explain why female killer whales have evolved the longest postreproductive life span of all nonhuman animals.

Concepts: Kin selection, Reproduction, Killer whales, Michael Bigg, Beached whale, Whale, Killer whale

34

Kin selection theory provides one important explanation for seemingly altruistic helping behaviour by non-breeding subordinates in cooperative breeding animals. However, it cannot explain why helpers in many species provide energetically costly care to unrelated offspring. Here, I use comparative analyses to show that direct fitness benefits of helping others, associated with future opportunities to breed in the resident territory, are responsible for the widespread variation in helping effort (offspring food provisioning) and kin discrimination across cooperatively breeding birds. In species where prospects of territory inheritance are larger, subordinates provide more help, and, unlike subordinates that cannot inherit a territory, do not preferentially direct care towards related offspring. Thus, while kin selection can underlie helping behaviour in some species, direct benefits are much more important than currently recognised and explain why unrelated individuals provide substantial help in many bird species.

Concepts: Scientific method, Theory, Altruism, Ethology, Evolution, Natural selection, Bird, Kin selection

34

Kin selection theory predicts that, where kin discrimination is possible, animals should typically act more favorably toward closer genetic relatives and direct aggression toward less closely related individuals. Contrary to this prediction, we present data from an 18-y study of wild banded mongooses, Mungos mungo, showing that females that are more closely related to dominant individuals are specifically targeted for forcible eviction from the group, often suffering severe injury, and sometimes death, as a result. This pattern cannot be explained by inbreeding avoidance or as a response to more intense local competition among kin. Instead, we use game theory to show that such negative kin discrimination can be explained by selection for unrelated targets to invest more effort in resisting eviction. Consistent with our model, negative kin discrimination is restricted to eviction attempts of older females capable of resistance; dominants exhibit no kin discrimination when attempting to evict younger females, nor do they discriminate between more closely or less closely related young when carrying out infanticidal attacks on vulnerable infants who cannot defend themselves. We suggest that in contexts where recipients of selfish acts are capable of resistance, the usual prediction of positive kin discrimination can be reversed. Kin selection theory, as an explanation for social behavior, can benefit from much greater exploration of sequential social interactions.

Concepts: Mongoose, Eviction, Discrimination, Theory, Sociology, Kin selection, Scientific method, Explanation

30

Until recently, inclusive fitness has been widely accepted as a general method to explain the evolution of social behavior. Affirming and expanding earlier criticism, we demonstrate that inclusive fitness is instead a limited concept, which exists only for a small subset of evolutionary processes. Inclusive fitness assumes that personal fitness is the sum of additive components caused by individual actions. This assumption does not hold for the majority of evolutionary processes or scenarios. To sidestep this limitation, inclusive fitness theorists have proposed a method using linear regression. On the basis of this method, it is claimed that inclusive fitness theory (i) predicts the direction of allele frequency changes, (ii) reveals the reasons for these changes, (iii) is as general as natural selection, and (iv) provides a universal design principle for evolution. In this paper we evaluate these claims, and show that all of them are unfounded. If the objective is to analyze whether mutations that modify social behavior are favored or opposed by natural selection, then no aspect of inclusive fitness theory is needed.

Concepts: Richard Dawkins, Genetics, Population genetics, Evolutionary psychology, Evolutionary biology, Kin selection, Natural selection, Evolution