Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Strange bedfellows: A Russian prince, A Scottish Economist, and the role of empathy in early theories for the evolution of cooperation.

From 1888 to his death in 1921, Russian Prince Peter Kropotkin forced biologists to ask themselves whether natural selection inevitably led to a dog-eat-dog world, or whether pro-social behavior could also be a product of the evolutionary process. In this historical vignette, I focus on Kropotkin's theory of "mutual aid," with emphasis on the role that empathy played in that theory, and the unexpected source--economist Adam Smith's 1759 book, The Theory of Moral Sentiments--of Kropotkin's ideas on empathy in animals.

Jump-Starting Evolution.

Since How to Tame a Fox (and Build a Dog) appeared in 2017, molecular genetics research connected to the silver fox domestication experiment has been published in Nature and Proceedings of the National Academy of Science. Lee Alan Dugatkin writes about his connection to the project, the role of neural crest cells in domesticating foxes, and how dogs, bonobos, and humans fit into the picture.

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm.

The evolution of group-beneficial traits potentially allows the survival of 'cheaters' that would otherwise be unfit. Here we describe experimental work on group-beneficial traits and the consequences of frequency-dependent selection in the context of bacterial antibiotic resistance. We constructed a 'self-limited antibiotic resistant' (SLAR) strain of Escherichia coli in which a TEM-1 beta-lactamase was anchored to the inner membrane. In pairwise competition experiments between the SLAR strain and ampicillin-sensitive strains, only the SLAR strain survived in the presence of ampicillin. We also constructed a 'shared antibiotic resistant' (SAR) strain in which TEM-1 beta-lactamase protected both the SAR strain and nearby sensitive cells, thus acting as a model for a genetically defined group-beneficial trait. In pairwise competition experiments of the SAR strain against two different sensitive strains of E. coli, we found that the sensitive strains maintained themselves at frequencies of 5-12% in the presence of ampicillin. When the relative cost of the SAR strain was lowered, its equilibrial frequency rose. Sensitive strains also arose from pure cultures of the SAR strain. In these cases, too, the sensitive 'cheaters' were maintained in ampicillin at frequencies comparable to those observed in the previous competitions. These results suggest that traits which benefit other group members can permit survival of genotypes that otherwise would be eliminated by natural selection, and allow the maintenance of greater genetic variation upon which evolution can operate.

Eavesdropping on visual cues in green swordtail (Xiphophorus helleri) fights: a case for networking.

Aggressive contests probably occur in networking environments where information about fighting ability is conveyed both to an opponent and to individuals peripheral to the fight itself, the bystanders. Our primary aim was to investigate the relative influences of eavesdropping and prior social experience on the dynamics of aggressive contests in Xiphophorus helleri. A bystander's ability to witness an encounter was manipulated using clear, one-way mirror, and opaque partitions. After watching (or not watching) the initial contest, the bystander encountered either the winner or loser of the bout. Treatment comparisons of bystander-winner or bystander-loser contest dynamics indicated the presence or absence of winner, loser, or eavesdropping effects. Winner and loser effects had negligible influences on bystander contest dynamics. Eavesdropping significantly reduced the bystander's propensity to initiate aggression, escalate, and win against seen winners regardless of whether the watched bout had escalated or not. Though eavesdropping had relatively little effect on bystander-loser contest dynamics, bystanders were less prone to initiate aggression and win against losers that had escalated in the witnessed bout. Thus, bystanders appear to preferentially retain and utilize information gained about potentially dangerous opponents (winners or persistent losers). Our data lend clear support for the importance of eavesdropping in visually based aggressive signalling systems.

Individual recognition, dominance hierarchies and winner and loser effects.

Winner and loser effects are defined as an increased probability of winning an aggressive interaction at time T, based on victories at time T-1, T-2, etc., and an increased probability of losing at time T, based on losses at time T-1, T-2, etc., respectively. Prior theoretical work on dominance hierarchy formation has demonstrated that when players are not capable of individual recognition, loser effects always produce a clear top-ranked (alpha) individual, but all other ranks in a group remain unclear; whereas winner effects always produce strict linear hierarchies in which the rank of each individual is clear. Paradoxically, however, when individual recognition--a phenomenon long thought to stabilize hierarchies--is possible, winner and loser effects have no impact on the probability of forming strict linear hierarchies.

The social implications of winner and loser effects.

Winner and loser effects have now been documented in a number of species. To our knowledge, experimental work, however, has focused exclusively on pairwise interactions, and not the extent to which winner and loser effects impact hierarchy formation. We report the results of experimentally manipulated winner and loser effects on hierarchy formation in a socially living species, the green swordtail, Xiphophorus helleri. Our results demonstrate that randomly chosen winners in pairwise aggressive contests were more likely to emerge as top-ranked individuals in a hierarchy, whereas randomly chosen losers were more likely to emerge as the lowest-ranking individuals, and that 'winner-neutral-loser' hierarchies were significantly overrepresented.

The evolution of risk-taking.

Many animal species besides humans show evidence of individuality. Knowing how a risk-taker differs from its stay-at-home counterpart could not only help humans live more easily with our fellow creatures, says Lee Dugatkin of the University of Louisville, but also tell us a few things about ourselves and how we got this way.

Overestimating resource value and its effects on fighting decisions.

Much work in behavioral ecology has shown that animals fight over resources such as food, and that they make strategic decisions about when to engage in such fights. Here, we examine the evolution of one, heretofore unexamined, component of that strategic decision about whether to fight for a resource. We present the results of a computer simulation that examined the evolution of over- or underestimating the value of a resource (food) as a function of an individual's current hunger level. In our model, animals fought for food when they perceived their current food level to be below the mean for the environment. We considered seven strategies for estimating food value: 1) always underestimate food value, 2) always overestimate food value, 3) never over- or underestimate food value, 4) overestimate food value when hungry, 5) underestimate food value when hungry, 6) overestimate food value when relatively satiated, and 7) underestimate food value when relatively satiated. We first competed all seven strategies against each other when they began at approximately equal frequencies. In such a competition, two strategies--"always overestimate food value," and "overestimate food value when hungry"--were very successful. We next competed each of these strategies against the default strategy of "never over- or underestimate," when the default strategy was set at 99% of the population. Again, the strategies of "always overestimate food value" and "overestimate food value when hungry" fared well. Our results suggest that overestimating food value when deciding whether to fight should be favored by natural selection.

Cheating on the edge.

We present the results of an individual agent-based model of antibiotic resistance in bacteria. Our model examines antibiotic resistance when two strategies exist: "producers"--who secrete a substance that breaks down antibiotics--and nonproducers ("cheats") who do not secrete, or carry the machinery associated with secretion. The model allows for populations of up to 10,000, in which bacteria are affected by their nearest neighbors, and we assume cheaters die when there are no producers in their neighborhood. Each of 10,000 slots on our grid (a torus) could be occupied by a producer or a nonproducer, or could (temporarily) be unoccupied. The most surprising and dramatic result we uncovered is that when producers and nonproducers coexist at equilibrium, nonproducers are almost always found on the edges of clusters of producers.

Developmental environment, cultural transmission, and mate choice copying.

Using female mate choice copying as a rudimentary form of cultural transmission, this study provides evidence that social environment during development has a significant effect on the tendency to use culturally acquired information. Groups of newborn guppies (Poecilia reticulata) were raised for 35 days in 1 of 5 "developmental environments". Groups of 15 newborns were raised in pools with no adults (treatment 1), both adult male and female guppies (treatments 2 and 3), only adult females (treatment 4) or only adult males (treatment 5). Mature females raised in treatments 1 and 2, but not treatments 3, 4, and 5, copied the mate choice of others. Treatments 1 and 2 correspond to social structures that guppies experience during their development in the wild. Newborn guppies swim together in shoals (analogous to treatment 1). As they mature, juveniles join schools of adult males and females (analogous to treatments 2). At no time during the normal developmental process are juveniles found with males, but only unreceptive females (as was the case for long periods in treatment 3) or in the presence of adults of only one sex (analogous to treatments 4 and 5). As such, normal developmental environments prime guppies for cultural transmission, while unnatural environments fail to do so.

Extrinsic effects, estimating opponents' RHP, and the structure of dominance hierarchies.

We examined the impact of winner and loser effects on dominance hierarchy formation when individuals are capable of estimating their opponent's resource holding power (RHP). The accuracy of such estimates was a variable in our simulations, and we considered cases in which all individuals err within the same bounds, as well as cases in which some individuals consistently overestimate, while others consistently underestimate their opponent's fighting RHP. In all cases, we found a clearly defined linear hierarchy. In most simulations, the vast majority of interactions were 'attack-retreats', and the remainder of interactions were almost all 'fights'. Error rates had no effect on the linearity of the hierarchy or the basic attack-retreat nature of interactions, and consistent over and underestimation did not affect the ultimate position of an individual in a hierarchy.

Antibiotic resistance and the evolution of group-beneficial traits. II: a metapopulation model.

Inspired by the evolution of antibiotic resistance in bacteria, we have developed a model that examines the evolution of "producers" (who secrete a substance that breaks down antibiotics) and non-producers. In a previous study, we found that frequency-dependent selection could favor an intermediate frequency of producers in a single, large population. Here we develop a metapopulation model that examines the evolution of producers and non-producers. Our results indicate that in a metapopulation with many groups, each of size N, the equilibrial frequency of producers decreases with group size. Even when N is high (e.g. 150 individuals/group), however, a significant frequency of producers is still predicted. We also found that the equilibrial frequency of producers increases as the minimum numbers of producers necessary to provide protection to non-producers increases. Lastly, increasing the benefit/cost ratio (b/c) for producers increases their equilibrial frequency.

Animal cooperation among unrelated individuals.

The evolution of cooperation has long been a topic near and dear to the hearts of behavioral and evolutionary ecologists. Cooperative behaviors run the gamut from fairly simple to very complicated and there are a myriad of ways to study cooperation. Here I shall focus on three paths that have been delineated in the study of intraspecific cooperation among unrelated individuals: reciprocity, byproduct mutualism, and group selection. In each case, I attempt to delineate the theory underlying each of these paths and then provide examples from the empirical literature. In addition, I shall briefly touch upon some recent work that has attempted to examine (or re-examine) the role of cognition and phylogeny in the study of cooperative behavior. While empirical and theoretical work has made significant strides in the name of better understanding the evolution and maintenance of cooperative behavior in animals, much work remains for the future. "From the point of view of the moralist, the animal world is on about the same level as the gladiator's show. The creatures are fairly well treated, and set to fight; whereby the strongest, the swiftest and the cunningest live to fight another day. The spectator has no need to turn his thumb down, as no quarter is given em leader the weakest and the stupidest went to the wall, while the toughest and the shrewdest, those who were best fitted to cope with their circumstances, but not the best in any other way, survived. Life was a continuous free fight, and em leader a war of each against all was the normal state of existence." (Huxley 1888)

Play and the evolution of fairness: a game theory model.

Bekoff [J. Consci. Stud. 8 (2001) 81] argued that mammalian social play is a useful behavioral phenotype on which to concentrate in order to learn more about the evolution of fairness. Here, we build a game theoretical model designed to formalize some of the ideas laid out by Bekoff, and to examine whether 'fair' strategies can in fact be evolutionarily stable. The models we present examine fairness at two different developmental stages during an individual's ontogeny, and hence we create four strategies-fair at time 1/fair at time 2, not fair at time 1/not fair at time 2, fair at time 1/not fair at time 2, not fair at time 1/fair at time 2. Our results suggest that when considering species where fairness can be expressed during two different developmental stages, acting fairly should be more common than never acting fairly. In addition, when no one strategy was evolutionarily stable, we found that all four strategies we model can coexist at evolutionary equilibrium. Even in the absence of an overwhelming database from which to test our model, the general predictions we make have significant implications for the evolution of fairness.