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Abstract Background Phylogenetic analyses strongly associate nonsocial ancestors of cooperatively-breeding or eusocial species with monogamy. Because monogamy creates high-relatedness family groups, kin selection has been concluded to drive the evolution of cooperative breeding (i.e., the monogamy hypothesis). Although kin selection is criticized as inappropriate for modeling and predicting the evolution of cooperation, there are no examples where specific inclusive fitness-based predictions are intrinsically wrong. The monogamy hypothesis may be the first case of such a flawed calculation. Results A simulation model mutated helping alleles into non-cooperative populations where females mated either once or multiply. Although multiple mating produces sibling broods of lower relatedness, it also increases the likelihood that one offspring will adopt a helper role. Examining this tradeoff showed that under a wide range of conditions polygamy, rather than monogamy, allowed helping to spread more rapidly through populations. Further simulations with mating strategies as heritable traits confirmed that multiple-mating is selectively advantageous. Although cooperation evolves similarly regardless of whether dependent young are close or more distant kin, it does not evolve if they are unrelated. Conclusions The solitary ancestral species to cooperative breeders may have been predominantly monogamous, but it cannot be concluded that monogamy is a predisposing state for the evolution of helping behavior. Monogamy may simply be coincidental to other more important life history characteristics such as nest defense or sequential provisioning of offspring. The differing predictive outcome from a gene-based model also supports arguments that inclusive fitness formulations poorly model some evolutionary questions. Nevertheless, cooperation only evolves when benefits are provided for kin: helping alleles did not increase in frequency in the absence of potential gains in indirect fitness. The key question, therefore, is not whether kin selection occurs, but how best to elucidate the differing evolutionary advantages of genetic relatedness versus genetic diversity.

Ants exhibit a size-associated colony founding trait that is characterized by the degree to which foundresses rely on internal reserves to raise their first brood of workers (claustrality). The reliance on stored reserves is positively correlated with degree of claustrality (claustral > facultative > semi-claustral) and is variable across species of Pogonomyrmex harvester ants. Three species of harvester ant foundresses that differ in degree of claustrality were observed initiating nests under laboratory conditions over 2 years. P. rugosus is fully claustral, P. salinus is facultative, and P. californicus is semi-claustral. Across species, degree of claustrality was positively associated with mean digging rate and nest depth over the first 3 days of nest initiation, total nest depth, and degree of nest closure. Branching and abundance of peripheral nodes were higher in semi-claustral and facultative nests than in claustral nests. The facultative species dug for the longest time and achieved the greatest tunnel length. Within each species, there were trends associating mass with digging rate, but these were not consistent in all species. There were no intraspecific trends of mass with nest depth. Also within species, a foundress’s mass did not affect her tendency to open or close her nest. These results reveal degree of claustrality is correlated across species with several nest initiation characteristics that together may represent different colony founding syndromes.

The invasive success of the exotic Argentine ant [ Linepithema humile (Mayr)] is often closely tied to year-round availability of water sources. Previous studies suggest that the location of such water sources can strongly influence activity patterns of colonies and may be a key predictor of building infestations. We studied activity patterns of Argentine ants in relation to water and food resources in two open-air structures (aviaries). In one series of manipulations, ant activity inside the aviaries was significantly reduced with the placement of numerous water sources around the outside. Inside activity increased again when the outside water sources were removed. A second series of manipulations involved the placement of water sources at targeted locations outside of the structures. Ant activity inside the aviaries consistently shifted significantly closer to these targeted sites. The results suggest that providing a reliable water source to Argentine ant colonies exterior to buildings can be a non-chemical method of integrated pest management for reducing ant infestations. Independent of our manipulations, L. humile activity levels predictably declined with time of day, but these changes were uncorrelated with observed surface temperatures. In fact, activity was often noted at surface temperatures higher than those that cause worker mortality under laboratory conditions. This suggests that L. humile exhibits a consistent temperature-independent circadian activity pattern of reduced foraging in afternoons relative to mornings. [ABSTRACT FROM AUTHOR]

The authors discuss the implications of the exposure of foetus to untreated maternal depression and selective serotonin reuptake inhibitors (SSRIs) on neurodevelopment. Topics include the reproductive safety of SSRIs, the risk related to SSRIs exposure during pregnancy, and the association between SSRI exposure and disorders of language, speech, and neuromotor function in children.

Ant queens often cooperate in starting colonies (pleometrosis), but not all foundresses are likely to achieve equal reproductive success. Therefore, joining decisions may be influenced by queens' perceptions of a partner's likelihood to be of mutualistic benefit or to be a successful competitor in eventually controlling reproduction. Large queen size (as measured by weight) was assumed to be a desired characteristic in a mutualistic partner, but to be avoided in a potential competitor. With respect to this variable, Lasius pallitarsis queens appeared to join others in a manner consistent with increasing their competitive advantage. When given a choice between joining another queen or nesting alone, only queens with a large weight advantage were significantly likely to join. When given a choice between joining either a light or a heavy queen, queens of all weights preferentially joined the lighter resident. Moreover, when queen condition was improved by feeding, changes in joining behavior were consistent with predictions of improved competitive ability. Finally, lighter queens were more likely to leave nest sites when joined by others. However, queens significantly aggregated when in high densities, which may be consistent with gaining mutualistic benefits. Pleometrosis appears to have an evolutionary dynamic between mutualistic group benefits and individual competition to monopolize those benefits. [ABSTRACT FROM AUTHOR]

Lasius pallitarsis ants were placed in situations where they encountered unfamiliar areas and had to choose between one of two directions for further exploration. Workers advancing onto new ground apparently leave behind some chemical signature to which later ants orient. This orientation occurred under two types of experimental conditions. First, ants show a significant tendency to follow each other as they advance out from their colony into unexplored areas. The same ants transferred into an entirely novel situation, in which there is no obvious 'homeward' direction, show similar behavior. When ants are coming from familiar ground, following tends to increase as the number of ants passing the decision point increases. However, following decreases when ants are on entirely novel ground. The results are discussed in relation to models describing foraging responses. [ABSTRACT FROM AUTHOR]

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Two of John et al.'s examples of proxy failures in ecological situations are not failures: Runaway sexual selection and marsupial neonate competition. Instead, more appropriate ecological examples may be paternal genetic kin recognition and warning coloration. These differ in proxy effectiveness and failure in ways that illustrate the importance of "costs" in the evolution of ecological proxy traits.

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., (© 2023 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.)

In viral infections and cancer tumours, negative health outcomes often correlate with increasing genetic diversity. Possible evolutionary processes for such relationships include mutant lineages escaping host control or diversity, per se , creating too many immune system targets. Another possibility is social heterosis where mutations and replicative errors create clonal lineages varying in intrinsic capability for successful dispersal; improved environmental buffering; resource extraction or effective defence against immune systems. Rather than these capabilities existing in one genome, social heterosis proposes complementary synergies occur across lineages in close proximity. Diverse groups overcome host defences as interacting 'social genomes' with group genetic tool kits exceeding limited individual plasticity. To assess the possibility of social heterosis in viral infections and cancer progression, we conducted extensive literature searches for examples consistent with general and specific predictions from the social heterosis hypothesis. Numerous studies found supportive patterns in cancers across multiple tissues and in several families of RNA viruses. In viruses, social heterosis mechanisms probably result from long coevolutionary histories of competition between pathogen and host. Conversely, in cancers, social heterosis is a by-product of recent mutations. Investigating how social genomes arise and function in viral quasi-species swarms and cancer tumours may lead to new therapeutic approaches., (© 2021 The Authors.)

A multitude of factors may determine reproductive skew among cooperative breeders. One explanation, derived from inclusive fitness theory, is that groups can partition reproduction such that subordinates do at least as well as noncooperative solitary individuals. The majority of recent data, however, fails to support this prediction; possibly because inclusive fitness models cannot easily incorporate multiple factors simultaneously to predict skew. Notable omissions are antagonistic selection (across generations, genes will be in both dominant and subordinate bodies), constraints on the number of sites suitable for successful reproduction, choice in which group an individual might join, and within-group control or suppression of competition. All of these factors and more are explored through agent-based evolutionary simulations. The results suggest the primary drivers for the initial evolution of cooperative breeding may be a combination of limited suitable sites, choice across those sites, and parental manipulation of offspring into helping roles. Antagonistic selection may be important when subordinates are more frequent than dominants. Kinship matters, but its main effect may be in offspring being available for manipulation while unrelated individuals are not. The greater flexibility of evolutionary simulations allows the incorporation of species-specific life histories and ecological constraints to better predict sociobiology., Competing Interests: The author has no conflict of interest., (© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

While strict vertical transmission insures the durability of intracellular symbioses, phylogenetic incongruences between hosts and endosymbionts suggest horizontal transmission must also occur. These horizontal acquisitions can have important implications for the biology of the host. Wolbachia is one of the most ecologically successful prokaryotes in arthropods, infecting an estimated 50-70% of all insect species. Much of this success is likely due to the fact that, in arthropods, Wolbachia is notorious for manipulating host reproduction to favor transmission through the female germline. However, its natural potential for horizontal transmission remains poorly understood. Here we evaluate the fundamental prerequisites for successful horizontal transfer, including necessary environmental conditions, genetic potential of bacterial strains, and means of mediating transfers. Furthermore, we revisit the relatedness of Wolbachia strains infecting the Panamanian leaf-cutting ant, Acromyrmex echinatior , and its inquiline social parasite, Acromyrmex insinuator , and compare our results to a study published more than 15 years ago by Van Borm et al. (2003). The results of this pilot study prompt us to reevaluate previous notions that obligate social parasitism reliably facilitates horizontal transfer and suggest that not all Wolbachia strains associated with ants have the same genetic potential for horizontal transmission.

Competing Interests: I declare that I have no competing interests.

Parents often face an investment trade-off between either producing many small or fewer large offspring. When environments vary predictably, the fittest parental solution matches available resources by varying only number of offspring and never optimal individual size. However when mismatches occur often between parental expectations and true resource levels, dynamic models like multifaceted parental investment (MFPI) and parental optimism (PO) both predict offspring size can vary significantly. MFPI is a "realist" strategy: parents assume future environments of average richness. When resources exceed expectations and it is too late to add more offspring, the best-case solution increases investment per individual. Brood size distributions therefore track the degree of mismatch from right-skewed around an optimal size (slight underestimation of resources) to left-skewed around a maximal size (gross underestimation). Conversely, PO is an "optimist" strategy: parents assume maximally good resource futures and match numbers to that situation. Normal or lean years do not affect "core" brood as costs primarily fall on excess "marginal" siblings who die or experience stunted growth (producing left-skewed distributions). Investment patterns supportive of both MFPI and PO models have been observed in nature, but studies that directly manipulate food resources to test predictions are lacking. Ant colonies produce many offspring per reproductive cycle and are amenable to experimental manipulation in ways that can differentiate between MFPI and PO investment strategies. Colonies in a natural population of a harvester ant (Pogonomyrmex salinus) were protein-supplemented over 2 years, and mature sexual offspring were collected annually prior to their nuptial flight. Several results support either MFPI or PO in terms of patterns in offspring size distributions and how protein differentially affected male and female production. Unpredicted by either model, however, is that supplementation affected distributions more strongly across years than within (e.g., small females are significantly rarer in the year after colonies receive protein). Parental investment strategies in P. salinus vary dynamically across years and conditions. Finding that past conditions can more strongly affect reproductive decisions than current ones, however, is not addressed by models of parental investment., (© 2018 The Authors. Journal of Animal Ecology © 2018 British Ecological Society.)

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation., (© 2015 The Author(s) Published by the Royal Society. All rights reserved.)

The role of the ant colony largely consists of non-reproductive tasks, such as foraging, tending brood, and defense. However, workers are vitally linked to reproduction through their provisioning of sexual offspring, which are produced annually to mate and initiate new colonies. Gynes (future queens) have size-associated variation in colony founding strategy (claustrality), with each strategy requiring different energetic investments from their natal colony. We compared the per capita production cost required for semi-claustral, facultative, and claustral gynes across four species of Pogonomyrmex harvester ants. We found that the claustral founding strategy is markedly expensive, costing approximately 70% more energy than that of the semi-claustral strategy. Relative to males, claustral gynes also had the largest differential investment and smallest size variation. We applied these investment costs to a model by Brown and Bonhoeffer (2003) that predicts founding strategy based on investment cost and foraging survivorship. The model predicts that non-claustral foundresses must survive the foraging period with a probability of 30-36% in order for a foraging strategy to be selectively favored. These results highlight the importance of incorporating resource investment at the colony level when investigating the evolution of colony founding strategies in ants., (Copyright © 2014 Elsevier Ltd. All rights reserved.)

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.

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 Hamilton's 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.

Social castes of eusocial insects may have arisen through an evolutionary modification of an ancestral reproductive ground plan, such that some adults emerge from development physiologically primed to specialize on reproduction (queens) and others on maternal care expressed as allo-maternal behaviour (workers). This hypothesis predicts that variation in reproductive physiology should emerge from ontogeny and underlie division of labour. To test these predictions, we identified physiological links to division of labour in a facultatively eusocial sweat bee, Megalopta genalis. Queens are larger, have larger ovaries and have higher vitellogenin titres than workers. We then compared queens and workers with their solitary counterparts-solitary reproductive females and dispersing nest foundresses-to investigate physiological variation as a factor in caste evolution. Within dyads, body size and ovary development were the best predictors of behavioural class. Queens and dispersers are larger, with larger ovaries than their solitary counterparts. Finally, we raised bees in social isolation to investigate the influence of ontogeny on physiological variation. Body size and ovary development among isolated females were highly variable, and linked to differences in vitellogenin titres. As these are key physiological predictors of social caste, our results provide evidence for developmental caste-biasing in a facultatively eusocial bee.

Social Hymenoptera have played a leading role in development and testing of kin selection theory. Inclusive fitness models, following from Hamilton's 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 Hamilton's 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.