Peter Nonacs

The past, present and future of reproductive skew theory and experiments

A major evolutionary question is how reproductive sharing arises in cooperatively breeding species despite the inherent reproductive conflicts in social groups. Reproductive skew theory offers one potential solution: each group member gains or is allotted inclusive fitness equal to or exceeding their expectation from reproducing on their own. Unfortunately, a multitude of skew models with conflicting predictions has led to confusion in both testing and evaluating skew theory. The confusion arises partly because one set of models (the ‘transactional’ type) answer the ultimate evolutionary question of what ranges of reproductive skew can yield fitness‐enhancing solutions for all group members. The second set of models (‘compromise’) give an evolutionarily proximate, game‐theoretic evolutionarily stable state (ESS) solution that determines reproductive shares based on relative competitive abilities. However, several predictions arising from compromise models require a linear payoff to increased competition and do not hold with non‐linear payoffs. Given that for most species it may be very difficult or impossible to determine the true relationship between effort devoted to competition and reproductive share gained, compromise models are much less predictive than previously appreciated. Almost all skew models make one quantitative prediction (e.g. realized skew must fall within ranges predicted by transactional models), and two qualitative predictions (e.g. variation in relatedness or competitive ability across groups affects skew). A thorough review of the data finds that these three predictions are relatively rarely supported. As a general rule, therefore, the evolution of cooperative breeding appears not to be dependent on the ability of group members to monitor relatedness or competitive ability in order to adjust their behaviour dynamically to gain reproductive share. Although reproductive skew theory fails to predict within‐group dynamics consistently, it does better at predicting quantitative differences in skew across populations or species. This suggests that kin selection can play a significant role in the evolution of sociality. To advance our understanding of reproductive skew will require focusing on a broader array of factors, such as the frequency of mistaken identity, delayed fitness payoffs, and selection pressures arising from across‐group competition. We furthermore suggest a novel approach to investigate the sharing of reproduction that focuses on the underlying genetics of skew. A quantitative genetics approach allows the partitioning of variance in reproductive share itself or that of traits closely associated with skew into genetic and non‐genetic sources. Thus, we can determine the heritability of reproductive share and infer whether it actually is the focus of natural selection. We view the ‘animal model’ as the most promising empirical method where the genetics of reproductive share can be directly analyzed in wild populations. In the quest to assess whether skew theory can provide a framework for understanding the evolution of sociality, quantitative genetics will be a central tool in future research.

Kinship, greenbeards, and runaway social selection in the evolution of social insect cooperation

Social Hymenoptera have played a leading role in development and testing of kin selection theory. Inclusive fitness models, following from Hamiltons rule, successfully predict major life history characteristics, such as biased sex investment ratios and conflict over parentage of male offspring. However, kin selection models poorly predict patterns of caste-biasing nepotism and reproductive skew within groups unless kin recognition constraints or group-level selection is also invoked. These successes and failures mirror the underlying kin recognition mechanisms. With reliable environmental cues, such as the sex of offspring or the origin of male eggs, predictions are supported. When only genetic recognition cues are potentially available, predictions are not supported. Mathematical simulations demonstrate that these differing mechanisms for determining kinship produce very different patterns of behavior. Decisions based on environmental cues for relatedness result in a robust mixture of cooperation and noncooperation depending on whether or not Hamiltons rule is met. In contrast, cooperation evolves under a wider range of conditions and to higher frequencies with genetic kin recognition as shared greenbeard traits. This “excess of niceness” matches the existing patterns in caste bias and reproductive skew; individuals often help others at an apparent cost to their inclusive fitness. The results further imply a potential for greenbeard-type kin recognition to create arbitrary runaway social selection for shared genetic traits. Suggestive examples in social evolution may be alloparental care and unicoloniality in ants. Differences in kin recognition mechanisms also can have consequences for maintenance of advantageous genetic diversity within populations.

Foundress polyphenism and the origins of eusociality in a facultatively eusocial sweat bee, Megalopta genalis (Halictidae)

The reproductive (queen) and nonreproductive (worker) castes of eusocial insect colonies are a classic example of insect polyphenism. A complementary polyphenism may also exist entirely among females in the reproductive caste. Although less studied, reproductive females may vary in behavior based on size-associated attributes leading to the production of daughter workers. We studied a bee with flexible social behavior, Megalopta genalis, to better understand the potential of this polyphenism to shape the social organization of bee colonies and, by extension, its role in the evolution of eusociality. Our experimental design reduced variation among nest foundresses in life history variables that could influence reproductive decisions, such as nesting quality and early adulthood experience. Within our study population, approximately one third of M. genalis nests were eusocial and the remaining nests never produced workers. Though they do not differ in survival, nest-founding females who do not attempt to produce workers (which we refer to as the solitary phenotype) are significantly smaller and become reproductive later than females who attempt to recruit workers (the social phenotype). Females with the social phenotype are more likely to produce additional broods but at a cost of having some of their first offspring become nonreproductive workers. The likelihood of eusocial organization varies with body size across females of the social phenotype. Thus, fitness consequences associated with size-based plasticity in foundress behavior has colony level effects on eusociality. The potential for size-based polyphenisms among reproductive females may be an important factor to consider in the evolutionary origins of eusociality.

Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a ‘monogamy window’, because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that ‘point of view’ is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamiltons rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.

Extreme Polygyny: Multi-seasonal “Hypergynous” Nesting in the Introduced Paper Wasp Polistes dominulus

In temperate climates, female paper wasps typically initiate new colonies in the spring. Several nest-founding tactics have been documented in Polistes species, including solitary nest initiation, joining a cooperative association, usurping an existing nest, or adopting an abandoned nest. Occasionally, exceptionally large groups of females have also been found reusing nests from the previous season. Here we report this phenomenon in introduced populations of the Eurasian species Polistes dominulus. We describe in detail the demographic and genetic characteristics of one such spring colony from Los Angeles, California, USA, which was collected with 84 associated adults and all stages of developing brood in its 613 cells. Genetic and morphological data indicate the presence of multiple reproductively active females of varying relatedness, as well as many nonbreeding females, including probable early-produced offspring. Despite some evidence of chaotic social conditions, the colony appeared to have been highly productive. Additional observations of similar colonies are needed to determine how control is maintained within such a large breeding aggregation.

Testing models of parental investment strategy and offspring size in ants

Parental investment strategies can be fixed or flexible. A fixed strategy predicts making all offspring a single ‘optimal’ size. Dynamic models predict flexible strategies with more than one optimal size of offspring. Patterns in the distribution of offspring sizes may thus reveal the investment strategy. Static strategies should produce normal distributions. Dynamic strategies should often result in non-normal distributions. Furthermore, variance in morphological traits should be positively correlated with the length of developmental time the traits are exposed to environmental influences. Finally, the type of deviation from normality (i.e., skewed left or right, or platykurtic) should be correlated with the average offspring size. To test the latter prediction, we used simulations to detect significant departures from normality and categorize distribution types. Data from three species of ants strongly support the predicted patterns for dynamic parental investment. Offspring size distributions are often significantly non-normal. Traits fixed earlier in development, such as head width, are less variable than final body weight. The type of distribution observed correlates with mean female dry weight. The overall support for a dynamic parental investment model has implications for life history theory. Predicted conflicts over parental effort, sex investment ratios, and reproductive skew in cooperative breeders follow from assumptions of static parental investment strategies and omnipresent resource limitations. By contrast, with flexible investment strategies such conflicts can be either absent or maladaptive.

Preference for straight-line paths in recruitment trail formation of the Argentine ant, Linepithema humile

Linepithema humile (Mayr, 1868) ants self-organize mass recruitment to food sources by laying pheromone trails to direct foragers. Initial exploration may occur randomly, but selection of the shortest route is often derived from positive feedback mechanisms rather than individual intelligence or decision-making. In this study, we examined whether L. humile foraging routes minimize travel distance and maximize linearity (i.e., have the fewest turns). Colonies of L. humile foraged in an artificial grid containing a number of possible routes to a long-lasting food source. In the design, there were three possible shortest routes that varied only in the number of turns that the ants had to make. The majority of foraging ants preferred one of the three shortest routes to the food, and significantly favored the path with the fewest turns. Selection of the shortest, straightest route may maximize mass recruitment to the food source by decreasing the chance of foraging ants losing the trail.

Urban Infestation Patterns of Argentine Ants, Linepithema humile, in Los Angeles

Infestations of buildings by Argentine ants, Linepithema humile (Mayr), were monitored on the campus of the University of California, Los Angeles. Foraging ant activity peaked during the hotter months of the year. The mean monthly maximum temperature, but not rainfall, positively correlated with indoor infestation frequency. Neither garden size nor the predominant groundcover vegetation correlated with the number of foraging ants at baits within gardens. Although the number of foraging ants outside a building varied over 40-fold, ant density in gardens did not predict the likelihood of infestation within the building. Also, the type of vegetative groundcover employed did not predict infestation frequency. There was, however, a significant negative relationship between the size of the garden outside of a building and the number of infestations. Given the large foraging area of L. humile workers, buildings next to small gardens may be infested simply because they lie within the “normal” foraging area of a colony. The best predictor of which rooms were infested within buildings was the presence of a water source. Thus providing water for ant colonies outside and away from buildings may be one method of integrated pest management to reduce the proclivity of ants to infest structures.

Cultural evolution and emergent group-level traits through social heterosis.

Smaldino proposes emergent properties of human groups, arising when individuals display both differentiation and organization, constitute a novel unit of cultural selection not addressed by current evolutionary theory. We propose existing theoretical frameworks for maintenance of genetic diversity - social heterosis and social genomes - can similarly explain the appearance and maintenance of human cultural diversity (i.e., group-level traits) and collaborative interdependence.

Evaluating an Open-Exam Approach to Engaging Students in Evolutionary Paradoxes: Cheating to Learn

Abstract Game theory is used in biology to understand why otherwise rational individuals make nonintuitive decisions regarding cooperation and competition. Recently, biology teachers engaged their students in game theory curricula by presenting them with a real-world game theory challenge: the opportunity to cheat on a game theory exam. Here we present a guide for other teachers to employ this provocative and educational classroom exercise, and discuss the results of the Cheating to Learn exercise in a biology class.