Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.     

The definition of eusociality

We describe more precise definitions for the term "eusociality"and other social systems. Our criterion for eusociality is thepresence of castes, which are groups of individuals that becomeirreversibly behaviorally distinct at some point prior to reproductivematurity. Eusocial societies are characterized by two traits:(1) helping by individuals of the less-reproductive caste, and(2) either behavioral totipotency of only the more reproductivecaste (facultative eusociality) or totipotency of neither caste(obligate eusociality). We define "cooperative breeding" asalloparental care without castes. Cooperatively breeding societiesmay comprise two types, semisocial (distribution of lifetimereproductive success bimodal), and quasisocial (distributionof lifetime reproductive success unimodal), but this hypothesisrequires empirical analysis. Our definitions conceptually unifystudies of arthropod and vertebrate sociality.     

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.     

The Soldiers in Societies: Defense,Regulation, and Evolution

The presence of reproductively altruistic castes is one of the primary traits of the eusocial societies. Adaptation and regulation of the sterile caste, to a certain extent, drives the evolution of eusociality. Depending on adaptive functions of the first evolved sterile caste, eusocial societies can be categorized into the worker-first and soldier-first lineages, respectively. The former is marked by a worker caste as the first evolved altruistic caste, whose primary function is housekeeping, and the latter is highlighted by a sterile soldier caste as the first evolved altruistic caste, whose task is predominantly colony defense. The apparent functional differences between these two fundamentally important castes suggest worker-first and soldier-first eusociality are potentially driven by a suite of distinctively different factors. Current studies of eusocial evolution have been focused largely on the worker-first Hymenoptera, whereas understanding of soldier-first lineages including termites, eusocial aphids, gall-dwelling thrips, and snapping shrimp, is greatly lacking. In this review, we summarize the current state of knowledge on biology, morphology, adaptive functions, and caste regulation of the soldier caste. In addition, we discuss the biological, ecological and genetic factors that might contribute to the evolution of distinct caste systems within eusocial lineages.     

Eusociality Shapes Convergent Patterns of Molecular Evolution across Mitochondrial Genomes of Snapping Shrimps

Eusociality is a highly conspicuous and ecologically impactful behavioral syndrome that has evolved independently across multiple animal lineages. So far, comparative genomic analyses of advanced sociality have been mostly limited to insects. Here, we study the only clade of animals known to exhibit eusociality in the marine realm—lineages of socially diverse snapping shrimps in the genus Synalpheus. To investigate the molecular impact of sociality, we assembled the mitochondrial genomes of eight Synalpheus species that represent three independent origins of eusociality and analyzed patterns of molecular evolution in protein-coding genes. Synonymous substitution rates are lower and potential signals of relaxed purifying selection are higher in eusocial relative to noneusocial taxa. Our results suggest that mitochondrial genome evolution was shaped by eusociality-linked traits—extended generation times and reduced effective population sizes that are hallmarks of advanced animal societies. This is the first direct evidence of eusociality impacting genome evolution in marine taxa. Our results also strongly support the idea that eusociality can shape genome evolution through profound changes in life history and demography.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Brood care and social evolution in termites

Cooperative brood care is assumed to be the common driving factor leading to sociality. While this seems to be true for social Hymenoptera and many cooperatively breeding vertebrates, the importance of brood care for the evolution of eusociality in termites is unclear. A first step in elucidating this problem is an assessment of the ancestral condition in termites. We investigated this by determining the overall level of brood care behaviour across four termite species that cover the phylogenetic diversity of the lower termites. Brood care was low in the three species (all from different families) that had an ancestral wood-dwelling lifestyle of living in a single piece of wood that serves as food and shelter. In the fourth species, a lower termite that evolved outside foraging, brood care was more common. Together with data for higher termites, this suggests that brood care in termites only becomes important when switching from a wood-dwelling to a foraging lifestyle. These results imply that early social evolution in termites was driven by benefits of increased defence, while eusociality in Hymenoptera and cooperative breeding in birds and mammals are primarily based on brood care.     

The risk‐return trade‐off between solitary and eusocial reproduction

Social insect colonies can be seen as a distinct form of biological organisation because they function as superorganisms. Understanding how natural selection acts on the emergence and maintenance of these colonies remains a major question in evolutionary biology and ecology. Here, we explore this by using multi‐type branching processes to calculate the basic reproductive ratios and the extinction probabilities for solitary vs. eusocial reproductive strategies. We find that eusociality, albeit being hugely successful once established, is generally less stable than solitary reproduction unless large demographic advantages of eusociality arise for small colony sizes. We also demonstrate how such demographic constraints can be overcome by the presence of ecological niches that strongly favour eusociality. Our results characterise the risk‐return trade‐offs between solitary and eusocial reproduction, and help to explain why eusociality is taxonomically rare: eusociality is a high‐risk, high‐reward strategy, whereas solitary reproduction is more conservative.     

Kin selection versus sexual selection: why the ends do not meet

I redevelop the hypothesis that lifetime monogamy is a fundamental condition for the evolution of eusocial lineages with permanent non-reproductive castes, and that later elaborations--such as multiply-mated queens and multi-queen colonies--arose without the re-mating promiscuity that characterizes non-social and cooperative breeding. Sexually selected traits in eusocial lineages are therefore peculiar, and their evolution constrained. Indirect (inclusive) fitness benefits in cooperatively breeding vertebrates appear to be negatively correlated with promiscuity, corroborating that kin selection and sexual selection tend to generally exclude each other. The monogamy window required for transitions from solitary and cooperative breeding towards eusociality implies that the relatedness and benefit-cost variables of Hamilton's rule do not vary at random, but occur in distinct and only partly overlapping combinations in cooperative, eusocial, and derived eusocial breeding systems.     

The weird eusociality of polyembryonic parasites

Some parasitoid wasps possess soldier castes during their parasitic larval stage, but are often neglected from our evolutionary theories explaining caste systems in animal societies. This is primarily due to the polyembryonic origin of their societies. However, recent discoveries of polyembryonic trematodes (i.e. flatworms) possessing soldier castes require us to reconsider this reasoning. I argue we can benefit from including these polyembryonic parasites in eusocial discussions, for polyembryony and parasitism are taxonomically vast and influence the evolution of social behaviours and caste systems in various circumstances. Despite their polyembryony, their social evolution can be explained by theories of eusociality designed for parent–offspring groups, which are the subjects of most social evolution research. Including polyembryonic parasites in these theories follows the trend of major evolutionary transitions theory expanding social evolution research into all levels of biological organization. In addition, these continued discoveries of caste systems in parasites suggest social evolution may be more relevant to parasitology than currently acknowledged.     

Origin and evolution of eusociality: a perspective from studying primitively eusocial wasps

Eusocial insects are those that show overlap of generations, cooperative brood care and reproductive caste differentiation. Of these, primitively eusocial insects show no morphological differences between reproductive and worker castes and exhibit considerable flexibility in the social roles that adult females may adopt. This makes them attractive model systems for investigations concerning the origin of eusociality. The rapidly accumulating information on primitively eusocial wasps suggests that haplodiploidy is unlikely to have an important role in the origin of eusociality. General kin selection (without help from haplodiploidy) could however have been an important factor due to the many advantages of group living. Pre-imaginal caste bias leading to variations in fertility is also likely to have some role. Because workers often have some chance of becoming reproductives in future, mutualism and other individual selection models suggest themselves as important factors. A hypothesis for the route to eusociality which focuses on the factors selecting for group living at different stages in social evolution is presented. It is argued that group living originates owing to the benefit of mutualism (the ‘Gambling Stage’) but parental manipulation and subfertility soon become important (the ‘Manipulation Stage’) and finally the highly eusocial state is maintained because genetic asymmetries created by haplodiploidy are exploited by kin recognition (the ‘Recognition Stage’).     

Eusociality and the success of the termites: insights from a supertree of dictyopteran families

Sociality in insects may negatively impact on species richness. We tested whether termites have experienced shifts in diversification rates through time. Supertree methods were used to synthesize family‐level relationships within termites, cockroaches and mantids. A deep positive shift in diversification rate is found within termites, but not in the cockroaches from which they evolved. The shift is responsible for most of their extant species richness suggesting that eusociality is not necessarily detrimental to species richness, and may sometimes have a positive effect. Mechanistic studies of speciation and extinction in eusocial insects are advocated.     

Multiple origins of eusociality among sponge-dwelling shrimps (Synalpheus)

Abstract.— As the most extreme expression of apparent altruism in nature, eusociality has long posed a central paradox for behavioral and evolutionary ecology. Because eusociality has arisen rarely among animals, understanding the selective pressures important in early stages of its evolution remains elusive. Employing a historical approach to this problem, we used morphology and DNA sequences to reconstruct the phylogeny of 13 species of sponge-dwelling shrimps ( Synalpheus ) with colony organization ranging from asocial pair-bonding through eusociality. We then used phylogenetically independent contrasts to test whether sociality was associated with evidence of enhanced competitive ability, as suggested by hypotheses invoking an advantage of cooperation in crowded habitats. The molecular, morphological, and combined data each strongly supported three independent origins of monogynous, multigenerational (eusocial) colony organization within this genus. Phylogenetically independent contrasts confirmed that highly social taxa, with strong reproductive skew, have significantly higher relative abundance within the host sponge than do less social taxa, a result that was robust to uncertainty in tree topology and varying models of character change. A similar tendency for highly social species to share their sponge with fewer congener species was suggestive, but not significant. Because unoccupied habitat appears to be limiting for many sponge-dwelling shrimp species, these data are consistent with hypotheses that cooperative social groups enjoy a competitive advantage over less organized groups or individuals, where independent establishment is difficult, and that enemy pressure is of central importance in the evolution of animal sociality.     

昆虫社会行为的进化与生态适应

一、引言昆虫社会行为的进化涉及两大问题:(1)社会行为的起源和进化过程;(2)社会行为的适应意义。这两个问题都曾使达尔文感到困惑。达尔文曾详尽地描述过蜜蜂复杂的造巢行     

Recent and simultaneous origins of eusociality in halictid bees

Eusocial organisms are characterized by cooperative brood care, generation overlap and reproductive division of labour. Traits associated with eusociality are most developed in ants, termites, paper wasps and corbiculate bees; the fossil record indicates that each of these advanced eusocial taxa evolved in the Late Cretaceous or earlier (greater than 65 Myr ago). Halictid bees also include a large and diverse number of eusocial members, but, in contrast to advanced eusocial taxa, they are characterized by substantial intra- and inter-specific variation in social behaviour, which may be indicative of more recent eusocial evolution. To test this hypothesis, we used over 2400 bp of DNA sequence data gathered from three protein-coding nuclear genes (opsin, wingless and EF-1a) to infer the phylogeny of eusocial halictid lineages and their relatives. Results from relaxed molecular clock dating techniques that utilize a combination of molecular and fossil data indicate that the three independent origins of eusociality in halictid bees occurred within a narrow time frame between approximately 20 and 22 Myr ago. This relatively recent evolution helps to explain the pronounced levels of social variation observed within these bees. The three origins of eusociality appear to be temporally correlated with a period of global warming, suggesting that climate may have had an important role in the evolution and maintenance of eusociality in these bees.     

Corpse Management in Social Insects

Undertaking behavior is an essential adaptation to social life that is critical for colony hygiene in enclosed nests. Social insects dispose of dead individuals in various fashions to prevent further contact between corpses and living members in a colony. Focusing on three groups of eusocial insects (bees, ants, and termites) in two phylogenetically distant orders (Hymenoptera and Isoptera), we review mechanisms of death recognition, convergent and divergent behavioral responses toward dead individuals, and undertaking task allocation from the perspective of division of labor. Distinctly different solutions (e.g., corpse removal, burial and cannibalism) have evolved, independently, in the holometabolous hymenopterans and hemimetabolous isopterans toward the same problem of corpse management. In addition, issues which can lead to a better understanding of the roles that undertaking behavior has played in the evolution of eusociality are discussed.     

Eusociality in African mole-rats: new insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis)

After the discovery of eusociality in the naked mole-rat, it was proposed that inbreeding and high colony relatedness in this species were the major underlying factors driving cooperative breeding in African molerats. By contrast, field and laboratory studies of the eusocial Damaraland mole-rat (Cryptomys damarensis) have raised the possibility that this species is an obligate outbreeder, although the build-up of inbreeding over several generations could still occur. Using microsatellite markers, we show that most breeding pairs in wild colonies of the Damaraland mole-rat are indeed unrelated (R = 0.02 +/- 0.04) and that mean colony relatedness (R = 0.46 +/- 0.01), determined across 15 colonies from three separate populations, is little more than half that previously identified in naked mole-rats. This finding demonstrates that normal familial levels of relatedness are sufficient for the occurrence of eusociality in mammals. Variation in the mean colony relatedness among populations provides support both for the central role played by ecological constraints in cooperative breeding and for the suggestion that inbreeding in naked mole-rats is a response to extreme constraints on dispersal. Approaches that determine the relative importance of an array of extrinsic factors in driving social evolution in African mole-rats are now required.     

Policing and punishment across the domains of social evolution

Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment‐relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements. Synthesis Researchers have long observed that individuals in animal societies punish (and by extension, police) each other, but they have rarely investigated whether general principles underlie this behavior across social arrangements. In this paper, we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punisher roles in animal societies. We apply the approach to eusocial insects and cooperatively breeding vertebrates and outline extensions towards the control of cancer cell lineages and punishment in human groups. We highlight how variation in specific social variables may drive differences in punishing/policing across the social domains.     

Social life: the paradox of multiple-queen colonies

The evolution of animal societies in which some individuals forego their own reproductive opportunities to help others to reproduce poses an evolutionary paradox that can be traced to Darwin. Altruism may evolve through kin selection when the donor and recipient of altruistic acts are related to each other, as generally is the case in social birds and mammals. Similarly, social insect workers are highly related to the brood they rear when colonies are headed by a single queen. However, recent studies have shown that insect colonies frequently contain several queens, with the effect of decreasing relatedness among colony members. How can one account for the origin and maintenance of such colonies? This evolutionary enigma presents many of the same theoretical challenges as does the evolution of cooperative breeding and eusociality.     

Dufour’s gland secretion,sterility and foraging behavior: Correlated behavior traits in bumblebee workers

Bombus terrestris colonies go through two major phases: the “pre-competition phase” in which the queen is the sole reproducer and aggression is rare, and the “competition phase” in which workers aggressively compete over reproduction. Conflicts over reproduction are partially regulated by a group of octyl esters that are produced in Dufour’s gland of reproductively subordinate workers and protect them from being aggressed. However, workers possess octyl esters even before overt aggression occurs, raising the question of why produce the ester-signal before it is functionally necessary?In most insect societies, foragers show reduced aggression and low dominance rank. We hypothesize that ester production in B. terrestris is not only correlated with sterility but also with foraging, signaling cooperative behavior by subordinate workers. Such a signal helps to maintain social organization, reduce the cost of fights between reproductives and helpers, and increase colony productivity, enabling subordinates to gain greater inclusive fitness. We demonstrate that foragers produce larger amounts of esters compared to non-foragers, and that their amounts positively correlate with foraging efforts. We further suggest that task performance, potential fecundity, and aggression are interlinked, and that worker–worker interactions are involved in regulating foraging behavior.B. terrestris, being an intermediate phase between primitive and derived eusocial insects, provides an excellent model for understanding the evolution of early phases of eusociality. Our results, combined with those in primitively eusocial wasps, suggest that at early stages of social evolution, reproduction was regulated by a “primordial division of labor”, that comprised foragers and reproducers, which further evolved to a more complex division of labor, a hallmark of eusociality.