Toward greater realism in inclusive fitness models: the case of caste fate conflict in insect societies.

In the field of social evolution, inclusive fitness theory has been successful in making a wide range of qualitative predictions on expected patterns of cooperation and conflict. Nevertheless, outside of sex ratio theory, inclusive fitness models that make accurate quantitative predictions remain relatively rare. Past models dealing with caste fate conflict in insect societies, for example, successfully predicted that if female larvae can control their own caste fate, an excess should opt to selfishly develop as queens. Available models, however, were unable to accurately predict levels of queen production observed in Melipona bees-a genus of stingless bees where caste is self-determined-as empirically observed levels of queen production are approximately two times lower than the theoretically predicted ones. Here, we show that this discrepancy can be resolved by explicitly deriving the colony-level cost of queen overproduction from a dynamic model of colony growth, requiring the incorporation of parameters of colony growth and demography, such as the per-capita rate at which new brood cells are built and provisioned, the percentage of the queen's eggs that are female, costs linked with worker reproduction and worker mortality. Our revised model predicts queen overproduction to more severely impact colony productivity, resulting in an evolutionarily stable strategy that is approximately half that of the original model, and is shown to accurately predict actual levels of queen overproduction observed in different Melipona species. Altogether, this shows how inclusive fitness models can provide accurate quantitative predictions, provided that costs and benefits are modeled in sufficient detail and are measured precisely.

Microbial Primer: Cooperation in bacteria.

The growth and success of many bacteria appear to rely on a stunning range of cooperative behaviours. But what is cooperation and how is it studied?

Fitness as the organismal performance measure guiding adaptive evolution.

A long-standing problem in evolutionary theory is to clarify in what sense (if any) natural selection cumulatively improves the design of organisms. Various concepts, such as fitness and inclusive fitness, have been proposed to resolve this problem. In addition, there have been attempts to replace the original problem with more tractable questions, such as whether a given gene or trait is favored by selection. Here, we ask what theoretical properties the concept fitness should possess to encapsulate the improvement criterion required to talk meaningfully about adaptive evolution. We argue that natural selection tends to shape phenotypes based on the causal properties of individuals and that this tendency is, therefore, best captured by a fitness concept that focuses on these properties. We highlight a fitness concept that meets this role under broad conditions but requires adjustments in our conceptual understanding of adaptive evolution. These adjustments combine elements of Dawkinsian gene selectionism and Egbert Leigh's "parliament of genes."

Michener's group-size paradox in cooperatively breeding birds.

According to Michener's paradox, most altruistic groups in nature should be small and large groups should not exist. This is because per capita productivity is thought to decrease as groups get larger, meaning that the share of indirect fitness available to each group member declines, which favours dispersal. The empirical evidence for a decrease in per capita productivity is contradictory, however, and limited to the social Hymenoptera. I report that per capita reproductive success decreased with increasing group size across 26 cooperatively breeding bird species. Small groups comprising two or three individuals were the most common (79% of 16,101 groups), and these had the highest per capita reproductive success. This close fit between per capita reproductive success and the distribution of group sizes in nature suggests that it may indeed be difficult for large groups to evolve through indirect fitness benefits alone.

Alloparental Support and Infant Psychomotor Developmental Delay.

Receiving social support from community and extended family has been typical for mothers with infants in human societies past and present. In non-industrialised contexts, infants of mothers with extended family support often have better health and higher survival through the vulnerable infant period, and hence shared infant care has a clear fitness benefit. However, there is scant evidence that these benefits continue in industrialised contexts. Better infant health and development with allocare support would indicate continued evolutionary selection for allocare. The research reported here used multiple logistic regression analysis to test whether a lack of family and other social support for mothers was associated with an increased risk of developmental delay in 9-month-old infants in the UK Millennium Cohort (analysis sample size, 15,696 infants). Extended family-based childcare during work hours and more maternal time spent with friends were the most influential kin and social support variables: infants of mothers with kin-based childcare versus all other childcare arrangements had a lower risk of developmental delay (OR = 0.61, 95% CIs: 0.46-0.82). Infants of mothers who spent no time with friends when compared with those who saw friends every day had double the odds of delay. Greater paternal involvement in infant care was associated with a lower odds of developmental delay. In conclusion, shared care of infants and social support for mothers may influence fitness-related traits in industrialised societies rather than being factors that influenced selection only in the past and in societies which retain close kin networks and a strong local community focus.

Crozier's paradox and kin recognition: Insights from simplified models.

Crozier's paradox suggests that genetic kin recognition will not be evolutionarily stable. The problem is that more common tags (markers) are more likely to be recognised and helped. This causes common tags to increase in frequency, eliminating the genetic variability that is required for genetic kin recognition. In recent years, theoretical models have resolved Crozier's paradox in different ways, but they are based on very complicated multi-locus population genetics. Consequently, it is hard to see exactly what is going on, and whether different theoretical resolutions of Crozier's paradox lead to different types of kin discrimination. I address this by making unrealistic simplifying assumptions to produce a more tractable and understandable model of Crozier's paradox. I use this to interpret a more complex multi-locus population genetic model where I have not made the same simplifying assumptions. I explain how Crozier's paradox can be resolved, and show that only one known theoretical resolution of Crozier's paradox - multiple social encounters - leads without restrictive assumptions to the type of highly cooperative and reliable form of kin discrimination that we observe in nature. More generally, I show how adopting a methodological approach where complex models are compared with simplified ones can lead to greater understanding and accessibility.

Colony level fitness analysis identifies a trade-off between population growth rate and dauer yield in Caenorhabditis elegans.

BACKGROUND: In the evolution from unicellular to multicellular life forms, natural selection favored reduced cell proliferation and even programmed cell death if this increased organismal fitness. Could reduced individual fertility or even programmed organismal death similarly increase the fitness of colonies of closely-related metazoan organisms? This possibility is at least consistent with evolutionary theory, and has been supported by computer modelling. Caenorhabditis elegans has a boom and bust life history, where populations of nematodes that are sometimes near clonal subsist on and consume food patches, and then generate dauer larva dispersal propagules. A recent study of an in silico model of C. elegans predicted that one determinant of colony fitness (measured as dauer yield) is minimization of futile food consumption (i.e. that which does not contribute to dauer yield). One way to achieve this is to optimize colony population structure by adjustment of individual fertility. RESULTS: Here we describe development of a C. elegans colony fitness assay, and its use to investigate the effect of altering population structure on colony fitness after population bust. Fitness metrics measured were speed of dauer production, and dauer yield, an indirect measure of efficiency of resource utilization (i.e. conversion of food into dauers). We find that with increasing founder number, speed of dauer production increases (due to earlier bust) but dauer yield rises and falls. In addition, some dauer recovery was detected soon after the post-colony bust peak of dauer yield, suggesting possible bet hedging among dauers. CONCLUSIONS: These results suggest the presence of a fitness trade-off at colony level between speed and efficiency of resource utilization in C. elegans. They also provide indirect evidence that population structure is a determinant of colony level fitness, potentially by affecting level of futile food consumption.

Child and adolescent foraging: New directions in evolutionary research.

Young children and adolescents in subsistence societies forage for a wide range of resources. They often target child-specific foods, they can be very successful foragers, and they share their produce widely within and outside of their nuclear family. At the same time, while foraging, they face risky situations and are exposed to diseases that can influence their immune development. However, children's foraging has largely been explained in light of their future (adult) behavior. Here, we reinterpret findings from human behavioral ecology, evolutionary medicine and cultural evolution to center foraging children's contributions to life history evolution, community resilience and immune development. We highlight the need to foreground immediate alongside delayed benefits and costs of foraging, including inclusive fitness benefits, when discussing children's food production from an evolutionary perspective. We conclude by recommending that researchers carefully consider children's social and ecological context, develop cross-cultural perspectives, and incorporate children's foraging into Indigenous sovereignty discourse.

Conflict and conflict resolution in the major transitions.

Conflict and conflict resolution have been argued to be fundamental to the major transitions in evolution. These were key events in life's history in which previously independently living individuals cooperatively formed a higher-level individual, such as a multicellular organism or eusocial colony. Conflict has its central role because, to proceed stably, the evolution of individuality in each major transition required within-individual conflict to be held in check. This review revisits the role of conflict and conflict resolution in the major transitions, addressing recent work arguing for a minor role. Inclusive fitness logic suggests that differences between the kin structures of clones and sexual families support the absence of conflict at the origin of multicellularity but, by contrast, suggest that key conflicts existed at the origin of eusociality. A principal example is conflict over replacing the founding queen (queen replacement). Following the origin of each transition, conflict remained important, because within-individual conflict potentially disrupts the attainment of maximal individuality (organismality) in the system. The conclusion is that conflict remains central to understanding the major transitions, essentially because conflict arises from differences in inclusive fitness optima while conflict resolution can help the system attain a high degree of coincidence of inclusive fitness interests.

Signatures of kin selection in a natural population of the bacteria Bacillus subtilis.

Laboratory experiments have suggested that bacteria perform a range of cooperative behaviors, which are favored because they are directed toward relatives (kin selection). However, there is a lack of evidence for cooperation and kin selection in natural bacterial populations. Molecular population genetics offers a promising method to study natural populations because the theory predicts that kin selection will lead to relaxed selection, which will result in increased polymorphism and divergence at cooperative genes. Examining a natural population of Bacillus subtilis, we found consistent evidence that putatively cooperative traits have higher polymorphism and greater divergence than putatively private traits expressed at the same rate. In addition, we were able to eliminate alternative explanations for these patterns and found more deleterious mutations in genes controlling putatively cooperative traits. Overall, our results suggest that cooperation is favored by kin selection, with an average relatedness of r = .79 between interacting individuals.

Why do Hymenopteran workers drift to non-natal groups? Generalized reciprocity and the maximization of group and parental success.

Eusocial Hymenoptera are often characterized by having facultatively or obligately sterile worker castes. However, findings across an increasing number of species are that some workers are non-natal-they have 'drifted' away from where they were born and raised. Moreover, drifters are often indistinguishable from natal workers in the work and benefits provided to joined groups. This seems an evolutionary paradox of providing benefits to potentially unrelated individuals over close kin. Rather than being mistakes, drifting is proposed to be adaptive if joiners either gain inclusive fitness by preferentially moving to other kin groups or through generalized reciprocity in which exchanging workers across groups raises group-level genetic diversity and creates social heterosis. It is unclear, however, if reciprocity is unlikely because of a susceptibility to cheating. In resolving this question, a series of evolutionary simulations show: (1) Reciprocity can persist under a range of genetic assumptions and scenarios of cheating, (2) cheating almost always evolves, but can be expressed in a variety of ways that are not always predictable, (3) the inclusive fitness hypothesis is equally or more susceptible to cheating. Moreover, existing data in Hymenoptera (although not extensive) are more consistent with generalized reciprocity. This supports a hypothesis that drifting, as a phenomenon, may more often reflect maximization of group and parental fitness rather than fitness gains for the individual drifters.

Microchimerism as a source of information on future pregnancies.

Small numbers of fetal cells cross the placenta during pregnancy turning mothers into microchimeras. Fetal cells from all previous pregnancies accumulate forming the mother's fetal microchiome. What is significant about microchimeric cells is that they have been linked to health problems including reproductive and autoimmune diseases. Three decades after the discovery of fetal microchimerism, the function of these cells remains a mystery. Here, we contend that the role of microchimeric cells is to inform the fetus about the likelihood that its genes are present in future pregnancies. We argue that, when genes are more likely than average to be in future maternal siblings, fetuses will send a fixed number of cells that will not elicit a maternal immune response against them. However, when genes are less likely to be in future maternal siblings, fetuses will send an ever-increasing number of cells that will elicit an ever-stronger maternal immune response. Our work can explain the observed clinical association between microchimeric cells and pre-eclampsia. However, our work predicts that this association should be stronger in women with a genetically diverse microchiome. If supported by medical tests, our work would allow establishing the likelihood of pregnancy or autoimmune problems advising medical interventions.

Impact of genetic relatedness on reproductive behavior in Pelvicachromis pulcher, a biparental cichlid fish with mutual mate choice and ornamentation.

Inbreeding can result in inbreeding depression. Therefore, many species seek to avoid inbreeding. However, theory predicts that inbreeding can be beneficial. Accordingly, some species tolerate inbreeding or even prefer mating with close relatives. Evidence for active inbreeding, i.e., kin-mating preference was reported in the biparental African cichlid fish Pelvicachromis taeniatus. Related mating partners revealed better parental cooperation due to kin selection, a potential benefit of inbreeding. In this study, we investigated kin-mating preference in a genetically diverse, outbred F2-lab population of Pelvicachromis pulcher, a closely related species to P. taeniatus. Like P. taeniatus, this species shows mutual ornamentation and mate choice as well as intense biparental brood care. The F1 P. pulcher generation had revealed signs of inbreeding depression but no inbreeding avoidance. We studied mating behavior and aggression in trios consisting of a male P. pulcher, an unfamiliar sister, and an unfamiliar, unrelated female. Because the study focused on kin-mating patterns, female pairs were matched for body size and coloration. The results provide no evidence for inbreeding avoidance but rather suggest inbreeding preference. We also found no significant impact of inbreeding on offspring survival. The results suggest no inbreeding avoidance in P. pulcher; however, the strength of inbreeding preference and inbreeding depression seems to be variable. We discuss possible causes for this variation like context-dependent inbreeding depression. The number of eggs positively correlated with female body size and coloration. Furthermore, the female aggressiveness was positively correlated with female coloration indicating that coloration signal female dominance and quality.

Relatedness modulates reproductive competition among queens in ant societies with multiple queens.

Reproductive sharing in animal groups with multiple breeders, insects and vertebrates alike, contains elements of both conflict and cooperation, and depends on both relatedness between co-breeders, as well as their internal and external conditions. We studied how queens of the ant Formica fusca adjust their reproductive efforts in response to experimental manipulations of the kin competition regime in their nest. Queens respond to the presence of competitors by increasing their egg laying efforts, but only if the competitors are highly fecund and distantly related. Such a mechanism is likely to decrease harmful competition among close relatives. We demonstrate that queens of Formica fusca fine-tune their cooperative breeding behaviors in response to kinship and fecundity of others in a remarkably precise and flexible manner.

No Signs of Inclusive Fitness or Reciprocal Altruism in Advantageous Inequity Aversion.

Advantageous inequity aversion (i.e., the tendency to respond negatively to unfairness that benefits oneself) usually develops in 6-8-year-olds. However, little is known about the selection pressures that might have shaped this phenomenon. Using data collected from 120 4-8-year-old Finnish children, we tested two evolutionary explanations for the development of advantageous inequity aversion: reciprocal altruism (i.e., benefiting from sharing when the roles are likely reversed in the future) and inclusive fitness (i.e., benefiting from sharing with biological relatives that carry the same alleles). We first successfully replicated a previous experiment, showing that 6-8-year-olds display advantageous inequity aversion by preferring to throw away a resource rather than keep it for themselves. Here, this behavior was also displayed in 5-year-olds. Using a novel experiment, we then asked children to distribute five erasers between themselves, a sibling, a peer, and a stranger. That is, an equal distribution was only possible if throwing away one eraser. We found no support for advantageous inequity aversion being shaped by either inclusive fitness or reciprocal altruism. Future studies could investigate costly signaling and adherence to social norms to avoid negative consequences as ultimate explanations for advantageous inequity aversion.

Lifetime inclusive fitness effects of cooperative polygamy in the acorn woodpecker.

Although over 50 y have passed since W. D. Hamilton articulated kin selection and inclusive fitness as evolutionary explanations for altruistic behavior, quantifying inclusive fitness continues to be challenging. Here, using 30 y of data and two alternative methods, we outline an approach to measure lifetime inclusive fitness effects of cooperative polygamy (mate-sharing or cobreeding) in the cooperatively breeding acorn woodpecker Melanerpes formicivorus. For both sexes, the number of offspring (observed direct fitness) declined while the number of young parented by related cobreeders (observed indirect fitness effect) increased with cobreeding coalition size. Combining these two factors, the observed inclusive fitness effect of cobreeding was greater than breeding singly for males, while the pattern for females depended on whether fitness was age-weighted, as females breeding singly accrued greater fitness at younger ages than cobreeding females. Accounting for the fitness birds would have obtained by breeding singly, however, lifetime inclusive fitness effects declined with coalition size for males, but were greater for females breeding as duos compared to breeding singly, due largely to indirect fitness effects of kin. Our analyses provide a road map for, and demonstrate the importance of, quantifying indirect fitness as a powerful evolutionary force contributing to the costs and benefits of social behaviors.

An evolutionary perspective on the association between grandmother-mother relationships and maternal mental health among a cohort of pregnant Latina women.

Grandmothers are often critical helpers during a mother's reproductive career. Studies on the developmental origins of health and disease demonstrate how maternal psychological distress can negatively influence fetal development and birth outcomes, highlighting an area in which soon-to-be grandmothers (henceforth "grandmothers") can invest to improve both mother and offspring well-being. Here, we examine if and how a pregnant woman's mental health- specifically, depression, state-anxiety, and pregnancy-related anxiety- is influenced by her relationship with her fetus' maternal and paternal grandmother, controlling for relationship characteristics with her fetus' father. In a cohort of pregnant Latina women in Southern California (N = 216), we assessed social support, geographic proximity, and communication between the fetus' grandmothers and pregnant mother. We assessed maternal mental health with validated questionnaire-based instruments. We find that both social support from and communication with the maternal grandmother were statistically associated with less depression, while no paternal grandmother relationship characteristics were statistically significant in association with any mental health variable. These results align with the idea that maternal grandmothers are more adaptively incentivized to invest in their daughters' well-being during pregnancy than paternal grandmothers are for their daughters-in-law. Results suggest that the positive association of maternal grandmothers with mothers' mental health may not hinge on geographic proximity, but rather, potentially function through emotional support. This work represents a novel perspective describing a psychological and prenatal grandmaternal effect.

Early-life sibling conflict in Canada jays has lifetime fitness consequences.

While delaying natal dispersal can provide short-term benefits for juveniles, lifetime fitness consequences are rarely assessed. Furthermore, competition for limited positions on a natal territory could impose an indirect fitness cost on the winner if the outcome has negative effects on its siblings. We use radio-tracking and 58 years of nesting data in Ontario, Canada to examine the lifetime fitness consequences of sibling expulsion in the Canada jay (Perisoreus canadensis). Six weeks after fledging, intra-brood dominance struggles result in one 'dominant juvenile' (DJ) remaining on the natal territory after expelling its subordinate siblings, the 'ejectees' (EJs). Despite an older age-at-first-reproduction, DJs produced more recruits over their lifetime and had higher first-year survival than EJs, leading to substantially higher direct fitness. Even though DJs incurred an indirect fitness cost by expelling their siblings and there was no evidence that their presence on the natal territory increased their parents' reproductive output the following year, they still had substantially higher inclusive fitness than EJs. Our results demonstrate how early-life sibling conflict can have lifetime consequences and that such fitness differences in Canada jays are driven by the enhanced first-year survival of DJs pursuant to the early-summer expulsion of their sibling competitors.

A kin-selection model of fairness in heterogeneous populations.

Humans and other primates exhibit pro-social preferences for fairness. These preferences are thought to be reinforced by strong reciprocity, a policy that rewards fair actors and punishes unfair ones. Theories of fairness based on strong reciprocity have been criticized for overlooking the importance of individual differences in socially heterogeneous populations. Here, we explore the evolution of fairness in a heterogeneous population. We analyse the Ultimatum Game in cases where players' roles in the game are determined by their status. Importantly, our model allows for non-random pairing of players, and so we also explore the role played by kin selection in shaping fairness. Our kin-selection model shows that, when individuals condition their behaviour on their role in the game, fairness can be understood as either altruistic or spiteful. Altruistic fairness directs resources from less valuable members of a genetic lineage to more valuable members of the same lineage, whereas spiteful fairness keeps resources away from the competitors of the actor's high-value relatives. When individuals express fairness unconditionally it can be understood as altruistic or selfish. When it is altruistic, unconditional fairness again serves to direct resources to high-value members of genetic lineages. When it is selfish, unconditional fairness simply improves an individual's own standing. Overall, we expand kin-selection based explanations for fairness to include motivations other than spite. We show, therefore, that one need not invoke strong reciprocity to explain the advantage of fairness in heterogeneous populations.