Content, cost, and context: A framework for understanding human signaling systems.

Humans frequently perform extravagant and seemingly costly behaviors, such as widely sharing hunted resources, erecting conspicuous monumental structures, and performing dramatic acts of religious devotion. Evolutionary anthropologists and archeologists have used signaling theory to explain the function of such displays, drawing inspiration from behavioral ecology, economics, and the social sciences. While signaling theory is broadly aimed at explaining honest communication, it has come to be strongly associated with the handicap principle, which proposes that such costly extravagance is in fact an adaptation for signal reliability. Most empirical studies of signaling theory have focused on obviously costly acts, and consequently anthropologists have likely overlooked a wide range of signals that also promote reliable communication. Here, we build on recent developments in signaling theory and animal communication, developing an updated framework that highlights the diversity of signal contents, costs, contexts, and reliability mechanisms present within human signaling systems. By broadening the perspective of signaling theory in human systems, we strive to identify promising areas for further empirical and theoretical work.

Evolution of male and female choice in polyandrous systems.

We study the evolution of male and female mating strategies and mate choice for female fecundity and male fertilization ability in a system where both sexes can mate with multiple partners, and where there is variation in individual quality (i.e. in the availability of resources individuals can allocate to matings, mate choice and production of gametes). We find that when the cost of mating differs between sexes, the sex with higher cost of mating is reluctant to accept matings and is often also choosy, while the other sex accepts all matings. With equal mating costs, the evolution of mating strategies depends on the strength of female sperm limitation, so that when sperm limitation is strong, males are often reluctant and choosy, whereas females tend to accept available matings. Male reluctance evolves because a male's benefit per mating diminishes rapidly as he mates too often, hence losing out in the process of sperm competition as he spends much of his resources on mating costs rather than ejaculate production. When sperm limitation is weaker, females become more reluctant and males are more eager to mate. The model thus suggests that reversed sex roles are plausible outcomes of polyandry and limited sperm production. Implications for empirical studies of mate choice are discussed.

Unmatedness promotes the evolution of helping more in diplodiploids than in haplodiploids.

The predominance of haplodiploidy (where males develop from unfertilized haploid eggs and females from fertilized diploid eggs) among eusocial species has inspired a body of research that focuses on the possible role of relatedness asymmetries in the evolution of helping and eusociality. Previous theory has shown that in order for relatedness asymmetries to favor the evolution of helping, there needs to be variation in sex ratios among nests in the population (i.e., split sex ratios). In haplodiploid species, unmated females can produce a brood of all males, and this is considered the most likely mechanism for split sex ratios at the origin of helping. In contrast, in diploidiploids unmatedness means total reproductive failure. We compare the effect of unmatedness on selection for male and female helping in haplodiploids and diplodiploids. We show that in haplodiploids, unmatedness promotes helping in females but not in males within the empirical range. In diplodiploids, unmatedness promotes helping by both sexes, and the effect is stronger than in haplodiploids, all else being equal. Our study highlights the need to consider interactions between ecological and genetic factors in the evolution of helping and eusociality.

Unravelling the many facets of human cooperation in an experimental study.

Humans readily cooperate, even with strangers and without prospects of reciprocation. Despite thousands of studies, this finding is not well understood. Most studies focussed on a single aspect of cooperation and were conducted under anonymous conditions. However, cooperation is a multi-faceted phenomenon, involving generosity, readiness to share, fairness, trust, trustworthiness, and willingness to take cooperative risks. Here, we report findings of an experiment where subjects had to make decisions in ten situations representing different aspects of cooperation, both under anonymous and 'personalised' conditions. In an anonymous setting, we found considerable individual variation in each decision situation, while individuals were consistent both within and across situations. Prosocial tendencies such as generosity, trust, and trustworthiness were positively correlated, constituting a 'cooperativeness syndrome', but the tendency to punish non-cooperative individuals is not part of this syndrome. In a personalised setting, information on the appearance of the interaction partner systematically affected cooperation-related behaviour. Subjects were more cooperative toward interaction partners whose facial photographs were judged 'generous', 'trustworthy', 'not greedy', 'happy', 'attractive', and 'not angry' by a separate panel. However, individuals eliciting more cooperation were not more cooperative themselves in our experiment. Our study shows that a multi-faceted approach can reveal general behavioural tendencies underlying cooperation, but it also uncovers new puzzling features of human cooperation.

Costly punishment prevails in intergroup conflict.

Understanding how societies resolve conflicts between individual and common interests remains one of the most fundamental issues across disciplines. The observation that humans readily incur costs to sanction uncooperative individuals without tangible individual benefits has attracted considerable attention as a proximate cause as to why cooperative behaviours might evolve. However, the proliferation of individually costly punishment has been difficult to explain. Several studies over the last decade employing experimental designs with isolated groups have found clear evidence that the costs of punishment often nullify the benefits of increased cooperation, rendering the strong human tendency to punish a thorny evolutionary puzzle. Here, we show that group competition enhances the effectiveness of punishment so that when groups are in direct competition, individuals belonging to a group with punishment opportunity prevail over individuals in a group without this opportunity. In addition to competitive superiority in between-group competition, punishment reduces within-group variation in success, creating circumstances that are highly favourable for the evolution of accompanying group-functional behaviours. We find that the individual willingness to engage in costly punishment increases with tightening competitive pressure between groups. Our results suggest the importance of intergroup conflict behind the emergence of costly punishment and human cooperation.

High cooperation and welfare despite-and because of-the threat of antisocial punishments and feuds.

Cooperation can be difficult to sustain when there is a temptation to free-ride on the efforts of others. In experiments, peer punishment often stabilizes cooperation but fails to improve earnings because of the costs associated with punishment. In addition, antisocial use of punishment-punishing cooperators, counterpunishing, and feuding-often leads to lower cooperation and earnings. The current study investigated if powerful individuals-individuals who can punish without cost or who are immune from punishment-police the antisocial use of punishment, thus reducing the undesirable effects of punishment. In order to create ample opportunities for antisocial punishment and identify the motives for the use of punishment, our modified public goods game implemented fixed groups, fixed participant identifiers, 2 punishment stages, and full information about participant actions. The powerful participants with cost-free punishment or immunity punished low contributors more often, and immune participants also punished those who punished cooperators. Intriguingly, we found that whenever all participants could be punished-regardless of the cost of punishing or asymmetry in the cost-cooperation and net earnings reached very high levels. However, participants who were immune cooperated at a markedly low level, reducing earnings in the group. The results show that in an environment with repeated interactions, plenty of information, and everyone being accountable, even inefficient punishment can maintain high cooperation and earnings, but immunity of the powerful leads to corrupt behavior and reduced efficiency. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

The good-genes and compatible-genes benefits of mate choice.

Genetic benefits from mate choice could be attained by choosing mates with high heritable quality ("good genes") and that are genetically compatible ("compatible genes"). We clarify the conceptual and empirical framework for estimating genetic benefits of mate choice, stressing that benefits must be measured from offspring fitness because there are no unequivocal surrogates for genetic quality of individuals or for compatibility of parents. We detail the relationship between genetic benefits and additive and nonadditive genetic variance in fitness, showing that the benefits have been overestimated in previous verbal treatments. We point out that additive benefits readily arise from nonadditive gene action and that the idea of "heritable nonadditive benefits" is a misconception. We review the empirical evidence of the magnitude of benefits of good genes and compatible genes in animal populations, and we outline the most promising future directions for empirical research on the genetic benefits of mate choice.

Between-group competition and human cooperation.

A distinctive feature of human behaviour is the widespread occurrence of cooperation among unrelated individuals. Explaining the maintenance of costly within-group cooperation is a challenge because the incentive to free ride on the efforts of other group members is expected to lead to decay of cooperation. However, the costs of cooperation can be diminished or overcome when there is competition at a higher level of organizational hierarchy. Here we show that competition between groups resolves the paradigmatic 'public goods' social dilemma and increases within-group cooperation and overall productivity. Further, group competition intensifies the moral emotions of anger and guilt associated with violations of the cooperative norm. The results suggest an important role for group conflict in the evolution of human cooperation and moral emotions.

Extended haplodiploidy hypothesis.

Evolution of altruistic behavior was a hurdle for the logic of Darwinian evolution. Soon after Hamilton formalized the concept of inclusive fitness, which explains how altruism can evolve, he suggested that the high sororal relatedness brought by haplodiploidy could be why Hymenopterans have a high prevalence in eusocial species, and why helpers in Hymenoptera are always female. Later it was noted that in order to capitalize on the high sororal relatedness, helpers would need to direct help toward sisters, and this would bias the population sex ratio. Under a 1:3 males:females sex ratio, the inclusive fitness valuation a female places on her sister, brother, and an own offspring are equal-apparently removing the benefit of helping over independent reproduction. Based on this argumentation, haplodiploidy hypothesis has been considered a red herring. However, here we show that when population sex ratio, cost of altruism, and population growth rate are considered together, haplodiploidy does promote female helping even with female-biased sex ratio, due the lowered cost of altruism in such populations. Our analysis highlights the need to re-evaluate the role of haplodiploidy in the evolution of helping, and the importance of fully exploring the model assumptions when comparing interactions of population sex ratios and social behaviors.

The evolutionary dynamics of adaptive virginity, sex-allocation, and altruistic helping in haplodiploid animals.

In haplodiploids, females can produce sons from unfertilized eggs without mating. However, virgin reproduction is usually considered to be a result of a failure to mate, rather than an adaptation. Here, we build an analytical model for evolution of virgin reproduction, sex-allocation, and altruistic female helping in haplodiploid taxa. We show that when mating is costly (e.g., when mating increases predation risk), virginity can evolve as an adaptive female reproductive strategy. Furthermore, adaptive virginity results in strongly divergent sex-ratios in mated and virgin queen nests ("split sex ratios"), which promotes the evolution of altruistic helping by daughters in mated queen nests. However, when helpers evolve to be efficient and increase nest production significantly, virgin reproduction is selected against. Our results suggest that adaptive virginity could have been an important stepping stone on the pathway to eusociality in haplodiploids. We further show that virginity can be an adaptive reproductive strategy also in primitively social haplodiploids if workers bias the sex ratio toward females. By remaining virgin, queens are free to produce sons, the more valuable sex in a female-biased population. Our work brings a new dimension to the studies linking reproductive strategies with social evolution.

Assortment, but not knowledge of assortment, affects cooperation and individual success in human groups.

The success or failure of human collective action often depends on the cooperation tendencies of individuals in groups, and on the information that individuals have about each other's cooperativeness. However, it is unclear whether these two factors have an interactive effect on cooperation dynamics. Using a decision-making experiment, we confirm that groups comprising individuals with higher cooperation tendencies cooperate at a higher level than groups comprising individuals with low cooperation tendencies. Moreover, assorting individuals with similar cooperation tendency together affected behaviour so that the most cooperative individuals tended to cooperate more and the least cooperative individuals cooperated less, compared to their behaviour in randomly formed groups. In line with predictions of evolutionary models of cooperation, there was a strong positive association between individuals' cooperation tendency and success when groups were formed assortatively, whereas such association did not exist when groups were formed randomly. Surprisingly, information about group members' cooperativeness in assorted groups had no effect on cooperation levels. We discuss potential explanations for why information about cooperativeness of others may be disregarded in certain circumstances.

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights.

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.

Human cooperation in groups: variation begets variation.

Many experiments on human cooperation have revealed that individuals differ systematically in their tendency to cooperate with others. It has also been shown that individuals condition their behaviour on the overall cooperation level of their peers. Yet, little is known about how individuals respond to heterogeneity in cooperativeness in their neighbourhood. Here, we present an experimental study investigating whether and how people respond to heterogeneous behaviour in a public goods game. We find that a large majority of subjects does respond to heterogeneity in their group, but they respond in quite different ways. Most subjects contribute less to the public good when the contributions of their peers are more heterogeneous, but a substantial fraction of individuals consistently contributes more in this case. In addition, we find that individuals that respond positively to heterogeneity have a higher general cooperation tendency. The finding that social responsiveness occurs in different forms and is correlated with cooperativeness may have important implications for the outcome of cooperative interactions.

Genetic variability and drift load in populations of an aquatic snail.

Population genetic theory predicts that in small populations, random genetic drift will fix and accumulate slightly deleterious mutations, resulting in reduced reproductive output. This genetic load due to random drift (i.e., drift load) can increase the extinction risk of small populations. We studied the relationship between genetic variability (indicator of past population size) and reproductive output in eight isolated, natural populations of the hermaphroditic snail Lymnaea stagnalis. In a common laboratory environment, snails from populations with the lowest genetic variability mature slower and have lower fecundity than snails from genetically more variable populations. This result suggests that past small population size has resulted in increased drift load, as predicted. The relationship between genetic variability and reproductive output is independent of the amount of nonrandom mating within populations. However, reproductive output and the current density of snails in the populations were not correlated. Instead, data from the natural populations suggest that trematode parasites may determine, at least in part, population densities of the snails.

The effects of mating system and genetic variability on susceptibility to trematode parasites in a freshwater snail, Lymnaea stagnalis.

The amount and distribution of genetic variability in host populations can have significant effects on the outcome of host-parasite interactions. We studied the effect of mating system and genetic variability on susceptibility of Lymnaea stagnalis snails to trematode parasites. Mating system of snails from eight populations differing in the amount of genetic variability was manipulated, and self- and cross-fertilized offspring were exposed to naturally occurring trematode parasites in a controlled lake experiment. Susceptibility of snails varied between populations, but mating-system treatment did not have a significant effect. Heterozygosity of snails was negatively correlated with the probability of trematode infection, however, suggesting that parasitic diseases may pose a serious threat to populations lacking genetic variability.

Mate-search efficiency can determine the evolution of separate sexes and the stability of hermaphroditism in animals.

Limited availability of mating partners has been proposed as an explanation for the occurrence of simultaneous hermaphroditism in animals with pair mating. When low population density or low mobility of a species limits the number of potential mates, simultaneous hermaphrodites may have a selective advantage because, first, they are able to adjust the allocation of resources between male and female functions in order to maximize fitness; second, in a hermaphroditic population the likelihood of meeting a partner is higher because all individuals are potential mates; and, third, in the absence of mating partners, many simultaneously hermaphroditic animals have the option of reproducing through self-fertilization. Recognizing that mate availability is central to the existing theory of hermaphroditism in animals, it is important to examine the effects of mate search on predictions of the stability of hermaphroditism. Many hermaphroditic animals can increase the number of potential mates they contact by active searching. However, since mate search has costs in terms of time and energy, the increased number of potential mates will be traded off against the amount of resources that can be allocated to the production of gametes. We explore the consequences of this trade-off to the evolution of mating strategies and to the selective advantage of self-fertilization. We show that in low and moderate population densities, poor mate-search efficiency and high costs of searching stabilize hermaphroditism and bias sex allocation toward female function. In addition, in very low population densities, there is strong selective advantage for self-fertilization, but this advantage decreases considerably in species with high mate-search efficiency. Most important, however, we present a novel evolutionary prediction: when mate search is efficient, disruptive frequency-dependent selection on time allocation to mate search leads to the evolution of searching and nonsearching phenotypes and, ultimately, to the evolution of males and females.

The effect of inbreeding rate on fitness, inbreeding depression and heterosis over a range of inbreeding coefficients.

Understanding the effects of inbreeding and genetic drift within populations and hybridization between genetically differentiated populations is important for many basic and applied questions in ecology and evolutionary biology. The magnitudes and even the directions of these effects can be influenced by various factors, especially by the current and historical population size (i.e. inbreeding rate). Using Drosophila littoralis as a model species, we studied the effect of inbreeding rate over a range of inbreeding levels on (i) mean fitness of a population (relative to that of an outbred control population), (ii) within-population inbreeding depression (reduction in fitness of offspring from inbred versus random mating within a population) and (iii) heterosis (increase in fitness of offspring from interpopulation versus within-population random mating). Inbreeding rate was manipulated by using three population sizes (2, 10 and 40), and fitness was measured as offspring survival and fecundity. Fast inbreeding (smaller effective population size) resulted in greater reduction in population mean fitness than slow inbreeding, when populations were compared over similar inbreeding coefficients. Correspondingly, populations with faster inbreeding expressed more heterosis upon interpopulation hybridization. Inbreeding depression within the populations did not have a clear relationship with either the rate or the level of inbreeding.

Inbreeding rate modifies the dynamics of genetic load in small populations.

The negative fitness consequences of close inbreeding are widely recognized, but predicting the long-term effects of inbreeding and genetic drift due to limited population size is not straightforward. As the frequency and homozygosity of recessive deleterious alleles increase, selection can remove (purge) them from a population, reducing the genetic load. At the same time, small population size relaxes selection against mildly harmful mutations, which may lead to accumulation of genetic load. The efficiency of purging and the accumulation of mutations both depend on the rate of inbreeding (i.e., population size) and on the nature of mutations. We studied how increasing levels of inbreeding affect offspring production and extinction in experimental Drosophila littoralis populations replicated in two sizes, N = 10 and N = 40. Offspring production and extinction were measured over 25 generations concurrently with a large control population. In the N = 10 populations, offspring production decreased strongly at low levels of inbreeding, then recovered only to show a consistent subsequent decline, suggesting early expression and purging of recessive highly deleterious alleles and subsequent accumulation of mildly harmful mutations. In the N = 40 populations, offspring production declined only after inbreeding reached higher levels, suggesting that inbreeding and genetic drift pose a smaller threat to population fitness when inbreeding is slow. Our results suggest that highly deleterious alleles can be purged in small populations already at low levels of inbreeding, but that purging does not protect the small populations from eventual genetic deterioration and extinction.