Identifying Causes of Social Evolution: Contextual Analysis, the Price Approach, and Multilevel Selection

Kin selection theory and multilevel selection theory are distinct approaches to explaining the evolution of social traits. The latter claims that it is useful to regard selection as a process that can occur on multiple levels of organisation such as the level of individuals and the level of groups. This is reflected in a decomposition of fitness into an individual component and a group component. This multilevel view is central to understanding and characterising evolutionary transitions in individuality, e.g., from unicellular life to multicellular organisms, but currently suffers from the lack of a consistent, quantifiable measure. Specifically, the two major statistical tools to determine the coefficients of such a decomposition, the multilevel Price equation and contextual analysis, are inconsistent and may disagree on whether group selection is present. Here we show that the reason for the discrepancies is that underlying the multilevel Price equation and contextual analysis are two non-equivalent causal models for the generation of individual fitness effects (thus leaving different “remainders” explained by group effects). While the multilevel Price equation assumes that the individual effect of a trait determines an individual's relative success within a group, contextual analysis posits that the individual effect is context-independent. Since these different assumptions reflect claims about the causal structure of the system, the correct approach cannot be determined on general theoretical or statistical grounds but must be identified by experimental intervention. We outline interventions that reveal the underlying causal structure and thus facilitate choosing the appropriate approach. We note that kin selection theory with its focus on the individual is immune to such inconsistency because it does not address causal structure with respect to levels of organisation. In contrast, our analysis of the two approaches to measuring group selection demonstrates that multilevel selection theory adds meaningful (falsifiable) causal structure to explain the sources of individual fitness and thereby constitutes a proper refinement of kin selection theory. Taking such refined causal structure into account seems indispensable for studying evolutionary transitions in individuality because these transitions are characterised by changes in the selection pressures that act on the respective levels.

Sex-biased demography modulates male harm across the genome

Recent years have seen an explosion of theoretical and empirical interest in the role that kin selection plays in shaping patterns of sexual conflict, with a particular focus on male harming traits. However, this work has focused solely on autosomal genes, and as such it remains unclear how demography modulates the evolution of male harm loci occurring in other portions of the genome, such as sex chromosomes and cytoplasmic elements. To investigate this, we extend existing models of sexual conflict for application to these different modes of inheritance. We first analyse the general case, revealing how sex-specific relatedness, reproductive value and the intensity of local competition combine to determine the potential for male harm. We then analyse a series of demographically explicit models, to assess how dispersal, overlapping generations, reproductive skew and the mechanism of population regulation affect sexual conflict across the genome, and drive conflict between nuclear and cytoplasmic genes. We then explore the effects of sex biases in these demographic parameters, showing how they may drive further conflicts between autosomes and sex chromosomes. Finally, we outline how different crossing schemes may be used to identify signatures of these intragenomic conflicts.

No evidence that relatedness or familiarity modulate male harm in wild Drosophila melanogaster

Sexual selection frequently promotes the evolution of aggressive behaviours that help males compete against their rivals, but which may harm females and hamper their fitness. Kin selection theory predicts that optimal male-male competition levels can be reduced when competitors are more genetically related to each other than to the population average, contributing to resolve this sexual conflict. Work in Drosophila melanogaster has spearheaded empirical tests of this idea, but studies so far have been conducted in lab-adapted populations in homogeneous rearing environments that may hamper kin recognition, and used highly skewed sex ratios that may fail to reflect average natural conditions. Here, we performed a fully factorial design with the aim of exploring how rearing environment (i.e. familiarity) and relatedness affect male-male aggression, male harassment, and overall male harm levels in a natural population of Drosophila melanogaster, under more natural conditions. Namely, we: a) manipulated relatedness and familiarity so that larvae reared apart were raised in different environments, as is common in the wild, and b) studied the effects of relatedness and familiarity under average levels of male-male competition in the field. We show that, contrary to previous findings, groups of unrelated-unfamiliar males were as likely to fight with each other and harass females than related-familiar males, and that overall levels of male harm to females were similar across treatments. Our results suggest that the role of kin selection in modulating sexual conflict is yet unclear in Drosophila melanogaster, and call for further studies that focus on natural populations and realistic socio-sexual and ecological environments.

Non-kin Cooperation in Ants

Eusociality represents an extreme form of social behavior characterized by a reproductive division of labor. Eusociality necessarily evolved through kin selection, which requires interactions among related individuals. However, many eusocial taxa also show cooperation between non-kin groups, challenging the idea that cooperative actions should only occur among relatives. This review explores the causes and consequences of non-kin cooperation in ants. Ants display a diversity of behaviors that lead to non-kin cooperation within and between species. These interactions occur among both reproductive and non-reproductive individuals. The proximate and ultimate mechanisms leading to non-kin cooperative interactions differ substantially depending on the biotic and abiotic environment. We end this review with directions for future research and suggest that the investigation of non-kin cooperative actions provides insight into processes leading to social evolution.

Living with relatives offsets the harm caused by pathogens in natural populations

Living with relatives can be highly beneficial, enhancing reproduction and survival. High relatedness can, however, increase susceptibility to pathogens. Here, we examine whether the benefits of living with relatives offset the harm caused by pathogens, and if this depends on whether species typically live with kin. Using comparative meta-analysis of plants, animals, and a bacterium (nspecies = 56), we show that high within-group relatedness increases mortality when pathogens are present. In contrast, mortality decreased with relatedness when pathogens were rare, particularly in species that live with kin. Furthermore, across groups variation in mortality was lower when relatedness was high, but abundances of pathogens were more variable. The effects of within-group relatedness were only evident when pathogens were experimentally manipulated, suggesting that the harm caused by pathogens is masked by the benefits of living with relatives in nature. These results highlight the importance of kin selection for understanding disease spread in natural populations.

Looking Like a Million Dollars: Does Attractiveness Priming Increase Altruistic Behavior in Experimental Games?

The emergence of altruistic behavior constitutes one of the most widely studied problems in evolutionary biology and behavioral science. Multiple explanations have been proposed, most importantly including kin selection, reciprocity, and costly signaling in sexual selection. In order to test the latter, this study investigated whether people behave more altruistically when primed by photographs of attractive faces and whether more or less altruistic people differ in the number of sexual and romantic partners. Participants in the general population (N = 158, 84 F, 74 M) first rated the attractiveness of photographs of 20 faces of the opposite (sexually preferred) sex and then played the Dictator and Ultimatum Games (DG and UG). The photograph rating acted as priming; half the participants received photographs of people rated as more attractive than average in an earlier study, and the other half received photographs previously rated as less attractive. The attractiveness-primed participants, especially men, were expected to behave more altruistically—signaling that they are desirable, resource-possessing partners. We also expected altruists to self-report more sexual and romantic partners. The observed difference between altruistic behaviors in the attractiveness- and unattractiveness-primed groups occurred in UG offers, however, in the opposite than expected direction in women. The number of sexual partners was positively correlated to minimum acceptable offers (MAOs) in the UG, in line with expectations based on the theory of costly signaling.

Sexual competition and kin recognition co-shape the traits of neighboring dioecious Diospyros morrisiana seedlings

Plants respond differently to the identity of their neighbors, such as their sex and kinship, showing plasticity in their traits. However, how the functional traits of dioecious trees are shaped by the recognition of neighbors with different sex and kinship remains unknown. In this study, we set up an experiment with different kin/nonkin and inter/intrasexual combinations for a dioecious tree species, Diospyros morrisiana. The results showed that plants grew better with nonkin and intrasexual neighbors than with kin and intersexual neighbors. Kin combinations had significantly shorter root length in the resource-overlapping zone than nonkin combinations, suggesting that kin tended to reduce competition by adjusting their root distribution, especially among female siblings. Our study suggested that the seedling growth of D. morrisiana was affected by both the relatedness and sexual identity of neighboring plants. Further analysis by gas chromatography-mass spectrometry showed that the root exudate composition of female seedlings differed from that of male seedlings. Root exudates may play important roles in sex competition in dioecious plants. This study indicates that sex-specific competition and kin recognition interact and co-shape the traits of D. morrisiana seedlings, while intrasexual and nonkin neighbors facilitate the growth of seedlings. Our study implies that kin- and sex-related interactions depend on different mechanisms, kin selection, and niche partitioning, respectively. These results are critical for understanding how species coexist and how traits are shaped in nature.

Prospective evolutionary drivers of allocare in wild belugas

Allocare, investment in offspring from non-parents, poses an evolutionary enigma. While the fitness trade-offs driving parental care are universal, alloparents may be driven by kin selection, reciprocation, the need to acquire parenting skills (‘learning-to-parent’), an indiscriminate attraction towards infants (‘natal attraction’), or a combination of multiple drivers. Among belugas (Delphinapterus leucas), allocare has been reported in wild and captive populations, but its underlying mechanisms remain untested. Using over 1800 focal observations, we quantified alloparental associations in St. Lawrence Estuary (SLE) belugas to determine whether the learning-to-parent and natal attraction hypotheses are consistent with patterns of allocare in this population. We found that subadults showed little interest in providing allocare and that alloparental investment remained constant across offspring age classes. As the observed patterns of allocare are inconsistent with both the learning-to-parent and natal attraction hypotheses, allocare in SLE belugas is likely driven by kin selection, reciprocation, or a combination thereof.

Genomic imprinting drives eusociality

The origin of eusociality, altruistically foregoing personal reproduction to help others, has been a long-standing paradox ever since Darwin. Most eusocial insects and rodents likely evolved from subsocial precursors, in which older offspring “helpers” contribute to the development of younger siblings without a permanent sterile caste. The driving mechanism for the transition from subsociality (with helpers) to eusociality (with lifelong sterile workers) remains an enigma because individuals in subsocial groups are subject to direct natural selection rather than kin selection. Our genomic imprinting theory demonstrates that natural selection generates eusociality in subsocial groups when parental reproductive capacity is linked to a delay in the sexual development of offspring due to sex-antagonistic action of transgenerational epigenetic marks. Focusing on termites, our theory provides the missing evolutionary link to explain the evolution of eusociality from their subsocial wood-feeding cockroach ancestors, and provides a novel framework for understanding the origin of eusociality.