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Linksvayer T.A. (2010) Subsociality and the of . In: Breed M.D. and Moore J., (eds.) Encyclopedia of Animal Behavior, volume 3, pp. 358- 362 Oxford: Academic Press.

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Subsociality and the

T. A. Linksvayer, University of Copenhagen, Copenhagen, Denmark

ã 2010 Elsevier Ltd. All rights reserved.

Introduction and Definitions attention of many evolutionary biologists since Darwin.

The evolution of permanently sterile individuals, as found Social interactions are ubiquitous in . In some in many , is paradoxical because alleles , social interactions are confined to interactions reducing fertility should be disfavored by natural selec- between the sexes during . Species at the other tion. The ecological and evolutionary success of the euso- extreme have complex societies in which individuals live cial makes this evolutionary enigma even more in intimate association with nestmates, and social interac- compelling. There have been a range of complementary tions are fundamental to all aspects of . An array of terms hypotheses that attempt to explain various aspects of the has been used to categorize types of animal . evolution of eusociality: evolutionary mechanisms that For example, the following categories were developed by have enabled the evolution of eusociality; selection pres- CharlesMichener andEdward O. Wilson to describe degrees sures that have favored the evolution of eusociality; fac- of sociality in the social insects, particularly the insect order tors that facilitate or enable the evolution of eusociality; (, , and ): communal, sub-, the general pathways and specific scenarios by which quasi-, semi-, para-, pre-, and eu-social (see Table 1). eusociality can evolve; and the genetic and developmental Subsocial animals live in groups consisting of mechanisms underlying traits involved in the evolution of Table 2 parents and immature offspring, and are characterized by eusociality ( ). brood defense or brood provisioning by parents. Such Whenever possible, empirical studies of these hypoth- parental care is taxonomically widespread and found eses are described. In many cases, studying these hypotheses in some , spiders, mites, scorpions, millipedes, empirically has proven difficult because of the absence of insects, and vertebrates. Besides parental care, alloparen- an obvious study system for elucidating the evolutionary tal care, in which adults provide protection or provision- origin of eusociality. Eusocial lineages with sterile workers ing to nonoffspring is found in some insects, , and and large societies are highly derived and have been euso- . Semisocial animals live together in same- cial for millions of years. The selection pressures and traits generation groups, have cooperative brood care (i.e., allo- of these taxa are likely to be very different than those at the parental care occurs), and have a reproductive division of origin of eusociality. Other lineages such as xylocopine labor such that some individuals mainly reproduce, while bees, halictid bees, and vespid wasps, contain species or others mainly perform other tasks such as foraging and populations that range from subsocial to eusocial. The brood-care. Finally, eusocial, or truly social groups contain traits and selective pressures found in these lineages may multiple adult generations, have cooperative brood care, be more relevant to understanding the origin of eusocial- and have a reproductive division of labor such that nonre- ity. However, in most cases, these lineages likely have also productive helpers remain so more or less permanently. had the same degree of sociality for millions of years.

Determining the animal societies that qualify for the eusocial label has been at the center of a lot of attention. In the older literature, only , some bees and wasps (all in Hymenoptera), and the were recognized as Evolutionary Mechanisms for the being eusocial. More recent studies show that a wide Evolution of Eusociality variety of animals such as naked mole rats, , an and Multilevel Selection ambrosia , , and snapping shrimp fit the strict definition of eusociality. Several authors have suggested The question of the evolutionary mechanism by which amending the categories in Table 1, in particular, broad- eusociality can evolve has been asked more broadly as: eningthe definition of eusociality to include taxa having How can reproductive evolve? Darwin suggested only temporary helpers that provide alloparental care, that selection at the family-level could result in the evo- and also removing the focus of the current classification lution of sterile helpers, as found in eusocial insects. That system on characteristics found in the Hymenoptera. is, even though sterile helpers do not reproduce, their In this article, I discuss the evolution of eusociality, in close relatives, who are also likely to carry genes underly- particular, how eusociality evolves from subsociality. ing conditionally expressed helper traits, do reproduce I focus mainly on the well-studied Hymenoptera. The and pass on the conditional helper genes. William D. question of how eusociality evolves has occupied the Hamilton formalized these ideas in his theory of inclusive

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Subsociality and the Evolution of Eusociality 359

Table 1 Levels of social organization in insects, after Michener and Wilson

Parental care Alloparental care Reproductive division of labor Overlapping adult generations

Presocial Subsocial þ Parasocial Communal þ Quasisocial þþ Semisocial þþ þ Eusocial þþ þ þ

Table 2 Summary of hypothesis providing different levels of explanation for the evolution of eusociality

Level of explanation List of relevant theories, hypotheses, scenarios, and factors

Ultimate selective pressures Increased productivity, defense, assured returns Evolutionary mechanism Kin selection/multilevel selection Preconditions and facilitating factors Haplodiploid hypothesis, subsociality, demographic factors, strict lifetime monogamy Pathways Subsocial route, semisocial route Behavioral and physiological mechanisms Parental manipulation, subfertility hypothesis, nutritional hypothesis Genetic and developmental mechanisms Reproductive groundplan hypothesis, heterochrony hypothesis

*See text for further explanation of the placement of various hypotheses.

fitness and showed that altruistic behaviors evolve single, singly mated reproductive (i.e., there is strict when the fitness benefits (b) to recipients of altruistic lifetime monogamy). r acts times the relatedness between social partners ( )is greater than the fitness costs to the performer of altruis- Parental Manipulation and Mutualism as tic acts: rb c > 0. This relationship is called Hamilton’s Alternatives to Kin Selection? rule and is the foundation of or kin selection theory. Parental manipulation and mutualism are often presented Kin selection can also be described in the mathemati- as alternative hypotheses to kin selection for the evolution cally equivalent levels of selection framework (sometimes of eusociality. The mutualism hypothesis proposes that referred to simply as , although this is less eusociality can evolve through mutualistic benefits to correct because multiple levels of selection, e.g., within- groups of individuals that live together and reciprocally and among-groups are always simultaneously considered). assist one another. However, many authors argue that

In this case, whether altruistic behaviors evolve depend mutualism alone cannot lead to eusociality. The parental on the balance between selection within social groups and manipulation hypothesis suggests that mothers restrict selection among social groups. In fact, kin selection is a the reproductive options of some offspring so that they special type of multilevel selection, involving between- assist in the rearing of additional fully fertile offspring. and within-kin-group selection. Selection among social However, parental manipulation is not a mutually exclu- groups (i.e., colonies) in social insects is clearly important, sive alternative to kin selection, and each may operate and can arise due to direct competition between colonies sequentially or in concert. Furthermore, parental manip- for resources, or any other factor that causes some colo- ulation involves parent–offspring interactions and need nies to survive better and produce more reproductive not be considered distinct from kin selection theory. individuals relative to other colonies. As a result, some The genetic underpinnings of parental manipulation authors have suggested that selection among colonies by mothers and kin selected expression of altruistic could be important for the evolutionary origin of eusoci- behavior by workers differ, and as a result there are ality, irrespective of kin selection. This is theoretically expected differences in the evolutionary dynamics of possible, but it seems likely that social groups at the origin these genes for these two routes to eusociality. In most of eusociality are actually always composed of relatives, kin selection models, genes causing altruistic behaviors so that, in this case, kin selection can be said to be the are located and expressed in the genomes of helpers that ultimate evolutionary mechanism for how eusociality provide care to relatives. These behaviors can be consid- evolves. Supporting this supposition, phylogenetic analy- ered to be under ‘offspring control,’ because whether an sis of extant eusocial lineages indicates that the ancestral offspring expresses the altruistic helping behaviors condition is always closely related kin groups with a depends directly on its own genotype. In contrast, under

Encyclopedia of Animal Behavior (2010), vol. 3, pp. 358-362

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360 Subsociality and the Evolution of Eusociality parental manipulation models, whether an offspring hypothesis suggests that eusociality has evolved more expresses helping behavior to its sibs depends on its frequently in the haplodiploid Hymenoptera because of mother’s genotype. While both alleles causing parental the asymmetry in relatedness between haplodiploid manipulation and worker altruism alleles must satisfy females and their relatives. Specifically, full-sibling hap- Hamilton’s rule, the differences in the genetic basis of lodiploid females are more closely related to one another r ¼ these traits means that the benefit to cost ratio necessary on average ( 0.75) than they are to their brothers for parental manipulation alleles to spread is often less (r ¼ 0.25) or to their offspring (r ¼ 0.5), while full-sibling than for worker altruism alleles. diploid males and females are equally related to one r ¼ Michener and Brothers observed the behavior of another and their own offspring ( 0.5). As a result of mother–offspring groups of halictid bees to determine this relatedness asymmetry, alleles causing haplodiploid whether offspring became helpers as a result of parental females to help care for their sisters instead of their own manipulation or offspring control. Mother bees were offspring should spread more readily in haplodiploids observed to frequently nudge their most fertile offspring relative to in diploids. back into the nest where brood care behaviors occurs, The haplodiploid hypothesis is pleasingly simple and suggesting that behavioral parental manipulation may was initially widely embraced. However, its importance play an important role in the evolution of eusociality. in explaining the taxonomic distribution of eusociality has now been long doubted for several reasons. Averaged across both male and female siblings, haplodiploid

Selective Factors Favoring the Evolution females are equally related to their full sibs or offspring of Eusociality (r ¼ 0.5), just as diploids. In order to capitalize on the high relatedness of haplodiploid females to their brothers, female helpers must invest relatively more resources in Ultimately, whether alleles influencing eusocial traits, such as sib-care behavior, spread in a population depends rearing sisters, and this female-biased investment must on the specific benefits of helping and group-living rela- be associated with helping behavior. Factors such as mul- tive to independently reproducing; that is the underlying tiple queens and multiple mating that decrease related- b ecological factors that influence the magnitude of the ‘ ’ ness are commonly found in the eusocial Hymenoptera, so and ‘c’ terms in Hamilton’s rule. These selective benefits that the theoretical benefit of disappears explain why eusociality evolves, whereas the other hypoth- or is greatly mitigated. While low observed relatedness Table 2 eses and factors summarized in explain at various values have been taken as evidence refuting the haplodi- levels how eusociality evolves. Possible advantages of join- ploid hypothesis, conditions found in highly eusocial ing a group and helping versus attempting independent populations likely do not reflect conditions at the evolu- tionary origin of eusociality. Indeed, as described above, reproduction include increased per capita productivity, increased nest defense against predators or parasites, and monogamy seems to be the ancestral condition in eusocial the potential to inherit proven nest sites. Furthermore, lineages. Finally, the phylogenetic association between helping has higher assurance of fitness returns because haplodiploidy and eusociality may not be as strong as was even if a helper dies before its immature nestmates reach once perceived. Several large taxonomic groups are hap- adulthood, other helpers can potentially finish rearing the lodiploid but do not have eusocial members (e.g., some immature, whereas if an independently nesting parent mites, scale insects, whiteflies, and ), and eusociality dies before its offspring reach adulthood, there is no occurs in several diploid groups, including termites, naked chance the parent will achieve any fitness returns for its mole rats, aphids, snapping shrimp, and an . investment. Similarly, if partially grown immatures are Traits besides the relatedness asymmetry caused by hap- lodiploidy may help to explain the apparent prevalence of available to receive help, individuals that remain and help may have a ‘reproductive head start’ relative to indi- eusociality in the Hymenoptera. For example, maternal care viduals that disperse and reproduce on their own. Empiri- (i.e., subsociality), nest-building, mandibulate mouthparts, cal studies with various social lineages suggest that all of the female sting, above average numbers, short these factors are important in the evolution of eusociality, lifespan of adults relative to juvenile development time, and often these factors may be lineage-specific. strict lifetime monogamy, and protogyny enabled by haplo- diploidy have all been proposed to facilitate the evolution of eusociality. These traits are sometimes termed ‘preadapta- Factors Promoting the Evolution of Eusociality: tions’ for colonial life. In contradiction, some authors suggest Haplodiploidy and Subsociality that there are unlikely to be a small number of factors For much of the twentieth century, biologists believed important in the evolutionary origin of eusociality across that eusociality originated more than ten times within all eusocial lineages. the insect order Hymenoptera and only once in a non- Nevertheless, one factor, subsociality, does seem to be hymenopteran insect (termites). Hamilton’s haplodiploid a universal and necessary precondition for the evolution

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Subsociality and the Evolution of Eusociality 361 of eusociality. Indeed, it is widely accepted that allopar- Proximate Hypotheses for the Evolution ental care, one of the defining characteristics of eusociality, of Eusociality is derived from parental care, which defines subsociality. Interestingly, maternal care (i.e., subsociality) is found more Because kin selection theory provides an ultimate evolu- commonly in the Hymenoptera than in any other tionary explanation for how eusociality can evolve, but group. Population genetic models demonstrate that mater- does not provide insight into the more proximate devel- nal care evolves more readily in haplodiploids relative opmental, physiological, or genetic basis of eusociality, to diploids. Some authors have pointed out that haplodi- several authors have sought additional levels of expla- is likely more closely associated with subsociality nation. For example, parental manipulation provides a than eusociality. For example, subsociality is only found specific behavioral mechanism for the evolution of euso- in those mites and ticks (subclass Acari) that are haplodi- ciality, namely, ‘mom made me do it.’ According to the ploid. Haplodiploidy and subsociality also co-occur in some subfertility hypothesis, some offspring have reduced fer- thrips (Thysanoptera), bees and wasps (aculeate Hymenop- tility and are incapable of nesting alone, but can still tera), and ambrosia beetles (Coleoptera: Xyleborini). If provide help at their natal nest. If helping behavior is haplodiploidy facilitates the evolution of subsociality, and only expressed when offspring are in poor condition, sub- subsociality is a necessary precondition for eusociality, then fertility provides a scenario by which helping behavior can eusociality should also be more likely in haplodiploids. spread. Indeed, in all cases, helping behavior must be Thus, there are still strong reasons to expect an association conditionally expressed for it to evolve. Hunt’s nutritional between haplodiploidy and eusociality. scenario, based on observations and experiments with social wasps, provides further explicit ecological and behavioral mechanistic details for the evolution of eusoci- Evolutionary Pathways to Eusociality: ality in wasps. Specifically, in this scenario, the exchange of Subsocial Versus Semisocial protein-rich saliva between larvae and adults underlies a reproductive division of labor between well-nourished Two primary evolutionary routes to eusociality have been reproductive individuals and undernourished helpers. proposed: the subsocial route and the semisocial route. In the subsocial route, some offspring do not disperse and reproduce, but instead remain at the nest and help rear The Genetic and Developmental Basis siblings. In this route, the mother survives, so her repro- duction continues after the emergence of her first off- of Eusociality spring. The nondispersal of some offspring together with alloparental care leads to overlap of adult generations West-Eberhard’s ovarian groundplan scenario, and the and cooperative brood care that occurs by definition related reproductive groundplan hypothesis, elaborated in eusociality. Because the subsocial route starts with a by James Hunt and Gro Amdan, have a developmental single family unit, helpers provide care to close relatives focus and describe how queen and worker phenotypes

(siblings), and kin selection can act efficiently. diverge based on an ancestral developmental program. In the semisocial route, individuals from the same Specifically, solitary insects all have more or less similar generation form aggregations. Some of these individuals reproductive cycles with corresponding behavioral cycles, become helpers that rear the offspring of their nestmates, involving foraging and reproducing components. Under and if some of these offspring remain to also become the groundplan hypothesis, these components of the helpers, and individuals from both generations coexist, ancestral reproductive groundplan can be separated dur- eusociality can evolve. In this semisocial route, helpers ing the course of social evolution and used to build potentially provide care to offspring of unrelated adults, societies composed of reproductive and nonreproductive or if founding members are sisters, helpers provide care individuals, that is, queens and workers. Studies with to nieces. Semisocial colonies sometimes form when the honeybees support the link between reproductive state mother dies prior to the emergence of her offspring; and behavior in workers, suggesting that evolutionarily the resulting group of sibs in a semisocial . conserved genetic and physiological mechanisms may con- The benefit to cost ratio must be higher for the semisocial tribute to division of labor in eusocial lineages. Similarly, Polistes route to work relative to the subsocial route, as prescribed studies with wasps suggest that simple modification by Hamilton’s rule, because the relatedness between non- of conserved life history traits associated with diapause reproductives in the colony and the next generation is cycles may underlie the origin of queen and worker castes lower than in a subsocial colony. Since phylogenetic anal- in these wasps. ysis identifies the ancestral condition of eusocial lineages The heterochrony hypothesis proposes that prerepro- to be a monogamous family unit, it seems that eusociality ductive alloparental care of offspring towards their sibs has evolved via the subsocial route. (i.e., sib care) is caused by the early expression of maternal

Encyclopedia of Animal Behavior (2010), vol. 3, pp. 358-362

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362 Subsociality and the Evolution of Eusociality care genes, so that just like the groundplan hypotheses, for how it can evolve. Currently, empirical study of complex social traits characterizing eusociality can arise the evolution of eusociality largely lags behind theory. from simple changes in preexisting genetic and develop- Observational and experimental studies of the selective mental machinery. It is widely accepted that alloparental benefits of social living, together with emerging studies care behaviors are developmentally homologous with and of the developmental, genetic, and behavioral underpin- evolutionarily derived from parental care behaviors. nings of social traits will change this, and will increase Ancestrally, maternal care genes are expressed only after our understanding of the evolution of sociality. mating. The heterochrony hypothesis proposes that in See also: , and Social Evolution; Coopera- the derived condition, genes for maternal care are condi- tionally expressed prereproductively in female helpers tion and Sociality; Social Evolution; Kin towards siblings instead of offspring. In this view, sib Selection and Relatedness; Levels of Selection; Sex care behavior is a derived trait and the evolution of the and Social Evolution; Social Evolution in ‘Other’ Insects capacity for females to provide care prereproductively and Arachnids; Social Insects: Behavioral Genetics; towards their sibs is a first step in the evolutionary origin Spiders: Social Evolution; Termites: Social Evolution; of eusociality from subsociality. There may often be a William Donald Hamilton. small number of genes underlying this behavioral hetero- chrony, permitting rapid social evolution given the appro- priate . In some cases, conditionally Further Reading expressed sib care, a first step from subsociality to eusoci- ality, may occur without the subsequent evolution of any Alexander RD, Noonan KM, and Crespi BJ (1991) The evolution of other eusocial traits. eusociality. In: Sherman PW, Jarvis JUM, and Alexander RD (eds.) The Biology of the Naked Mole Rat, pp. 3–44. Princeton, NJ: The heterochrony hypothesis also makes explicit pre- Princeton University Press. dictions about the genetic basis of sib care behavior. Many Boomsma JJ (2007) Kin selection versus : Why the ends of the same genes should be expressed in adults do not meet. Current Biology 17: R673–R683. Bourke AFG and Franks NR (1995) Social Evolution in Ants. Princeton, performing sib care behaviors as in adults performing NJ: Princeton University Press. maternal care behaviors. This will especially be true in Choe JC and Crespi BJ (eds.) (1997) The Evolution of in Insects and Arachnids. Cambridge: Cambridge University Press. populations of incipiently eusocial species but less so in Costa JT (2006) The Other Insect Societies. Cambridge, MA: Belknap those with an advanced degree of eusociality, where more Press.

Gadagkar R (2001) The Social Biology of marginata: Toward genes are expected to have caste-limited expression due Understanding the Evolution of Eusociality. Cambridge, MA: Harvard to selection for the elaboration of queen–worker diver- University Press. gence. However, because the evolutionary elaboration of Hamilton WD (1964) The genetical evolution of social behaviour. I, II. sib care behaviors and queen–worker phenotypic differ- Journal of Theoretical Biology 7: 1–16, 17–52. ences is likely based upon simple modification of preex- Ho¨ lldobler B and Wilson EO (2009) The : The Beauty, Elegance, and Strangeness of Insect Societies. Cambridge, MA: isting physiological, behavioral, and genetic machinery, Harvard University Press. queen and worker traits even in highly eusocial species are Hughes WOH, Oldroyd BP, Beekman M, and Ratnieks FLW (2008) Ancestral monogamy shows kin selection is key to the evolution of expected to have a common molecular basis. Recent stud- Polistes eusociality. Science 320: 1213–1216. ies of patterns of gene expression in wasps and Hunt JH (2007) The Evolution of Social Wasps. Oxford University Press. honeybees support these predictions. Linksvayer TA and Wade MJ (2005) The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: Maternal effects, sib-social effects, and heterochrony. Quarterly Review of Biology 80: 317–336. Conclusions Michener CD (1974) The Social Behavior of the Bees. Cambridge, MA: Harvard University Press. Queller DC (1989) The evolution of eusociality: Reproductive head starts The evolution of sociality is considered to be one of of workers. Proceedings of the National Academy of Sciences USA the major transitions of evolution. A range of hypotheses 86: 3224–3226. explain why sociality evolves, the evolutionary mecha- Wade MJ (2001) Maternal effect genes and the evolution of sociality in haplo-diploid organisms. Evolution 55: 453–458. nism for how it can evolve, as well as novel, more proxi- West-Eberhard MJ (2003) Developmental Plasticity and Evolution. mate developmental, genetic, and behavioral details Oxford: Oxford University Press.

Encyclopedia of Animal Behavior (2010), vol. 3, pp. 358-362