Volume 92, No. 1 THE QUARTERLY REVIEW OF BIOLOGY March 2017

THE ROLE OF BROOD IN EUSOCIAL

Eva Schultner Centre of Excellence in Biological Interactions, Department of Biosciences, University of Helsinki 00014 Helsinki, Finland Tvärminne Zoological Station 10900 Hanko, Finland Institut für Zoologie, Universität Regensburg 93053 Regensburg, Germany e-mail: [email protected]

Jan Oettler Institut für Zoologie, Universität Regensburg 93053 Regensburg, Germany e-mail: [email protected]

Heikki Helanterä Centre of Excellence in Biological Interactions, Department of Biosciences, University of Helsinki 00014 Helsinki, Finland Tvärminne Zoological Station 10900 Hanko, Finland e-mail: [email protected]

keywords eusocial Hymenoptera, brood, development, cooperation, conflict

abstract Study of social traits in offspring traditionally reflects on interactions in simple family groups, with famous examples including parent-offspring conflict and sibling rivalry in and . In contrast, studies of complex social groups such as the societies of , , and focus mainly on adults and, in particular, on traits and interests of queens and workers. The social role of developing individuals in complex societies remains poorly understood. We attempt to fill this gap by illustrating

The Quarterly Review of Biology, March 2017, Vol. 92, No. 1 Copyright © 2017 by The University of Chicago Press. All rights reserved. 0033-5770/2017/9201-0002$15.00

39 40 THE QUARTERLY REVIEW OF BIOLOGY Volume 92

that development in social Hymenoptera constitutes a crucial life stage with important consequences for the individual as well as the colony. We begin by describing the complex social regulatory network that modulates development in Hymenoptera societies. By highlighting the inclusive fitness interests of developing individuals, we show that they may differ from those of other colony members. We then demonstrate that offspring have evolved specialized traits that allow them to play a functional, coop- erative role within colonies and give them the potential power to act toward increasing their inclusive fitness. We conclude by providing testable predictions for investigating the role of brood in colony interactions and giving a general outlook on what can be learned from studying offspring traits in hymenopteran societies.

Introduction can even display different levels of social ity IFE is social and it is the interactions depending on environmental conditions L among molecules, cells, or individuals (e.g., in bees; Michener 1974). Second, euso- that have created functional genomes from ciality within the Hymenoptera has evolved simple replicators, multicellular organisms several times independently ( Johnson et al. from a unicellular ancestor, and so- 2013). Finally, there is large variation in so- cieties from solitary organisms. Across these cial ecological complexity even within euso- evolutionary transitions (Maynard Smith and cial Hymenoptera, from the annual, simple Szathmáry 1995), similar ultimate factors family groups of bumble bees to the com- underlie how single entities form and main- plex nest networks of supercolonial wood tain cohesive social groups. On one hand, ants (Schultner et al. 2016), making this genetic relatedness between individual enti- taxon ideal for understanding the evolu- ties facilitates cooperation because partners tionary dynamics that govern the formation, gain indirect fitness from helping relatives maintenance, and cohesion of complex so- (Hamilton 1964). On the other hand, be- cial groups (Bourke 2011). cause partners are rarely genetically identical The evolution of in the Hy- and do not overlap perfectly in their fitness menoptera is anchored in simple family interests, potential for conflict remains and groups, with adult offspring staying in their complex control mechanisms are predicted parental nest to help their mother repro- to evolve in order to keep selfishness in check duce instead of dispersing and reproducing (Bourke 2011). Both cooperation and con- themselves (Hughes et al. 2008). A typical flict are thus crucial determinants of social eusocial Hymenoptera colony is charac- cohesion. terized by reproductive division of labor have evolved an especially large between adult females of overlapping gen- range of social complexity (Figure 1), which erations—the reproductive queen(s) and reaches its apex in the colonies of eusocial her (facultatively) sterile daughter workers. insects that are characterized by reproduc- In primitively eusocial species, differences tive division of labor between individuals, between queens and workers are subtle, in- cooperative brood care, and the presence of volving mainly changes in adult physiology individuals from overlapping generations and/or behavior (O’Donnell 1998), and in- (Wilson 1971). The Hymenoptera—ants, dividuals are capable of switching between bees, and wasps—stand out across the range roles. Although the reproductive capacity of sociality for several reasons. First, of workers is constrained, for instance, via this group exhibits the entire range of soci- dominance hierarchies or queen phero- ality, from the solitary lifestyles of parasitic monal control (Van Oystaeyen et al. 2014), wasps over the semisocial groups of sweat they usually retain the ability to reproduce bees to the irreversibly eusocial superorgan- sexually, for example, in wasps (Suzuki ismal societies of ants and honey bees, with 1985; Chandrashekara and Gadagkar 1991) their morphologically separated queen and and bees (Michener 1990). When a queen worker castes and high levels of social co- dies, one of her daughters will take over the hesion (Helanterä 2016). The same species nest—in many cases her success depends March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 41 on her physical dominance over nestmates potent, leaving developing individuals with (Michener 1990; Kukuk and May 1991; more reproductive options (Khila and Abou- Kukuk 1994). In advanced eusocial species, heif 2008, 2010). Hymenoptera develop with reproductive division of labor is generally complete metamorphosis (so-called holo- permanent and queens and workers exhibit metabolous development) and individuals strong morphological differences. Queens undergo several developmental steps from are specialized for dispersal, colony found- egg to adult (Figure 2). An important con- ing, and egg laying, and workers are struc- sequence of development with complete turally adapted for cooperative tasks such metamorphosis is that growth occurs only as colony defense, nursing, and foraging during development so that morphological (Wilson 1953, 1971; Oster and Wilson 1978; traits such as overall body size and size and Wheeler 1986). Workers are morphologi- allometry of specific body parts are irre- cally constrained in their reproductive op- versibly determined by the time individuals tions because they lack functional organs reach the adult stage. For advanced eusocial for sexual reproduction (e.g., loss of func- Hymenoptera species with morphol ogical tional sperm-storing organs in honey reproductive castes, holometabolous devel- workers, Gotoh et al. 2013, 2016; and most opment has particularly important conse- ants, Hölldobler and Wilson 1990; Gobin quences: whether a female egg develops into et al. 2008; Gotoh et al. 2016). Although a reproductive queen or a sterile worker is workers of many advanced eusocial species irreversibly determined during larval devel- have retained the ability to produce unfer- opment (Wheeler 1986). As a result, adult tilized eggs that develop into males (Bourke queens and workers are fixed in their re- 1988; Helanterä and Sundström 2007), productive roles when they reach the adult some species have lost worker reproductive stage. Development is similarly decisive for organs altogether (Hölldobler and Wilson males, who typically produce sperm only 1990; Boleli et al. 1999; Gotoh et al. 2016). during this life stage, after which the testes The presence of individuals from several degenerate (Hölldobler and Bartz 1985; generations within the same nest adds a Boomsma et al. 2005; Stürup et al. 2013). layer of social complexity to eusocial col- Within Hymenoptera colonies, develop- onies compared to subsocial or semisocial ing individuals embody future generations taxa (Figure 1), and social interactions in of sexuals and workers with individual fit- eusocial species involve parent-offspring ness interests. At the same time, they rep- and offspring-offspring interactions on resent the combined current reproductive several levels: between queens and work- investment of all colony members and much ers, between queens and their developing of a colony’s social life revolves around offspring, between workers and develop- brood care and the attempts of adult in- ing individuals, and among developing dividuals to follow their inclusive fitness in- individ uals. Nevertheless, study of eusocial terests by influencing offspring production Hymenoptera has largely concentrated on and development. Brood becomes a source the social interactions between adult queens of conflict within colonies when adults fol- and workers, and colony offspring produc- low contrasting fitness interests (Sundström tion has been seen as a simple consequence and Boomsma 2001; Beekman and Rat- of adult actions. This is perhaps not sur- nieks 2003; Beekman et al. 2003; Helanterä prising, since queens and workers share ex- and Ratnieks 2009), making them central pensive stakes in colony reproduction and, to the evolution of both cooperation and consequently, in lifetime fitness. However, as conflict within societies. mentioned above, adult queens and work- Fully understanding the social complexity ers can be behaviorally, physiologically, and of Hymenoptera societies therefore hardly morphologically restricted to their repro- seems possible without a closer look at the ductive roles. biology of brood. Surprisingly, however, de- In contrast to adults, the eggs of euso- veloping individuals as a distinct social en- cial Hymenoptera species are generally toti- tity have been largely neglected in studies 42 THE QUARTERLY REVIEW OF BIOLOGY Volume 92

Figure 1. Insect Sociality and the Role of Offspring in the Other Insect Societies Insects have evolved a wide range of social lifestyles (Wilson 1971; Costa 2006). Main characteristics of this sociality continuum are variation in the social interactions between offspring and adults and among offspring (Wong et al. 2013), and variation in the contributions of indirect and direct fitness to overall inclusive fitness of individuals within groups. In solitary insects offspring typically develop in isolation from parents, so that parent-offspring interactions are nonexistent or limited to short-term such as egg guarding and . However, solitary juveniles can display intense social interactions. Well-known examples include cannibalism among developing stages (e.g., in ladybugs and fruit flies; Michaud and Grant 2004; Vijendravarma et al. 2013) and cooperative foraging in caterpillars (Fitzgerald and Peterson 1988). In subsocial species, parents exhibit extended periods of offspring care, for instance, by engaging in . With longer periods of parental care, developing individuals also spend more time together, providing further opportunities for interaction. Earwigs are one intriguing example; here mothers defend and provision their mobile offspring for several weeks after hatching (Costa 2006). During this time, offspring can engage in competitive interactions such as cannibalism (Dobler and Kölliker 2010, 2011), but also behave cooperatively by sharing food via direct feedings and consumption of broodmate feces (Falk et al. 2014). Cooperative food sharing has been linked to the transition from simple to highly social groups in the order Blattodea, which contains social cockroaches and (Lihoreau et al. 2012). In the lineage, food sharing may have played a role in the evolution of eusociality by facilitating transfer of the microbial fauna needed for wood digestion (Bell et al. 2007). Social insect species comprise communal, quasisocial, semisocial, and primitive and superorganismal eusocial species. In communal species members of the same generation live together but do not engage in cooperative brood care. Quasisocial and semisocial species form groups of members of the same generation and engage in cooperative brood care, and sometimes even division of reproductive labor. Nesting behavior of adults creates a novel social environment, which now includes adult-juvenile interactions that do not involve parents and their offspring. Quasisocial and semisocial insect groups are often only temporary—occurring throughout the colony cycle of several species of bees and wasps (Crespi and Yanega 1995). Social complexity is most pronounced in obligately eusocial insects, which form permanent social groups characterized by reproductive division of labor, cooperative brood care, and the presence of individuals from overlapping generations. With individuals from several generations living in the same nest, social interactions in eusocial species involve parent-offspring and offspring-offspring interactions on several different levels. This complexity can be further increased by the huge variation in colony structures exhibited by eusocial species, which ranges from family groups with a single pair of reproductives and their offspring to huge colonies containing hundreds of reproductives and their respective helper and developing offspring. The diversity of social lifestyles is striking even within the eusocial insects, ranging from the small colonies of primitively March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 43 of social Hymenoptera. In fact, developing ranging from clonal species with mono- Hymenoptera are often thought to possess morphic queens and workers to leafcutter little power, i.e., the ability to act (Beek- ants with several morphological worker man and Ratnieks 2003), because of their castes), ecological strategies (exemplified low mobility and overall dependence on by differential nesting and brood-rearing workers. This is in contrast to the other ma- strategies in bees and wasps compared to jor group of eusocial insects—the termites. ants), and social structures (from tight-knit Termites are hemimetabolous insects that family groups to large, genetically diverse develop with incomplete metamorphosis. colonies; Figure 2). Termite colonies are largely comprised of We begin our review by presenting an juvenile workers in different larval (with- overview of the social regulatory network out visible wing buds) and nymphal (with that modulates development in eusocial visible wing buds) stages, in addition to species and describing the complex fitness reproductive adults (the queen and king). interactions between developing individ- This allows for a more flexible determina- uals and their adult nestmates. We go on tion of reproductive caste since workers can to illustrate that, contrary to the common develop into reproductives late in life. These view that brood is powerless, developing fundamental differences in developmental individuals are a diverse, functional group strategies have important consequences for that plays an active role in colony life. We individual and colony life history. Further- conclude by presenting promising avenues more, the ultimate factors driving coop- of future research on brood biology that erative behavior appear to differ between will help provide new perspectives on social eusocial Hymenoptera (benefits from brood evolution. care) and termites (benefits from cooper- ative nest defense). We therefore restrict this review to the role of brood in euso- Development in a Social Environment cial Hymenoptera and refer to Korb et al. There are several features of social hy- (2012) for a discussion of brood from a ter- me nopteran biology that are important for mite perspective. understanding the developmental, ecolog- In the following review, we demonstrate ical, and evolutionary processes shaping that development in eusocial Hymenoptera brood traits within societies. For simplicity, constitutes a crucial life stage with impor- we have summarized these characteristics tant consequences for the individual as well in Figure 2. We begin our review by focus- as the colony. We focus mainly on the de- ing on one of these fundamental proper- veloping stages of eusocial species because ties—polyphenic development of female these have been studied most closely. The eggs into queens or workers—to illustrate wealth of literature on queen-worker inter- the complex regulation of development in actions underlines that eusocial Hymenop- the social environments of hymenopteran tera are especially intriguing for study of colonies. We then zoom in on the fitness social traits because of the large variation interests of developing individuals, who are in the magnitude of division of labor (e.g., predicted to evolve traits that allow them

eusocial species lacking morphological reproductive castes (e.g., hover wasps, sweat bees) to the huge societies of superorganismal eusocial species with distinct morphological castes (e.g., termites, army ants, honey bees). The social role of developing individuals is surely most pronounced in termites, where juveniles resemble adults in morphology and can carry out all kinds of colony tasks. One of the most fascinating social offspring behaviors is displayed by Ambrosia larvae that cooperate with their adult siblings in brood care, gallery maintenance, and fungus gardening (Biedermann and Taborsky 2011). Discovery of such elaborate behaviors affirms that it is worthwhile to take a closer look at the social role of brood in insect societies. Photo credits: R. Vijendravarma (fly), J. Meunier (earwig), P. Biedermann (beetle), E. Schultner (termite). See the online edition for a color version of this figure. 44 THE QUARTERLY REVIEW OF BIOLOGY Volume 92

Figure 2. Fundamental Features of Social Hymenoptera Biology March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 45 to maximize their inclusive fitness, and core developmental pathways (West-Eber- explore how these tie-in with the inclusive hard 2003) that are cis-regulated by meth- fitness interests of other colony members. ylation (Bonasio et al. 2012; Simola et al. 2013) and transcription factors (Schrader et al. 2015; Klein et al. 2016). Alternative complex social regulation developmental trajectories can be initiated of development by factors such as genetic predisposition Like in other organisms, developmental ( Ju lian et al. 2002; Volny and Gordon 2002; outcome in social Hymenoptera depends on Helms Cahan and Keller 2003; Anderson individual genotype, environment, and di- et al. 2006, 2008; Schwander and Keller rect maternal effects (West-Eberhard 2003). 2008), maternal effects (Bier 1952, 1954a; Social environment adds another layer of Schwander et al. 2008; Libbrecht et al. complexity to this regulatory developmen- 2013), and by social developmental environ- tal network (Wheeler 1986, 1991; Linksva- ment, particularly nutrition (Michener 1974; yer and Wade 2005) as expression of larval Ishay et al. 1976; Wheeler 1986, 1994; Höll- phenotypes can be regulated by the gen- dobler and Wilson 1990; Gadagkar et al. otypes of adult colony members through 1991; Kukuk 1994; O’Donnell 1998; Karsai modification of the internal environment and Hunt 2002; Smith et al. 2008a; Jeanne independently of outside factors (Links- and Suryanarayanan 2011; Kamakura 2011; vayer and Wade 2005; Linksvayer 2006, Linksvayer et al. 2011; Judd et al. 2015). 2007; Linksvayer et al. 2009, 2011). Devel- Food quality and quantity, in particular, oping in a Hymenoptera colony thus entails seem to play a role in triggering worker de- exposure to an intricate social network, pro- velopment by acting on diverse molecular viding developing individuals with ample and physiological processes (Corona et al. opportunity to participate in social pro- 2016). In primitively eusocial species, envi- cesses, while at the same time allowing adult ronmental variation in resource levels can nestmates to influence larval environment. underlie female caste differences (Knerer The complexity of social regulation of de- and Atwood 1966). In most species, how- velopment is best exemplified by differential ever, nutrition levels of larvae are assumed queen-worker development. This funda- to be (at least to some extent) under worker mental property of eusocial Hymenoptera control. In mass provisioning species such colonies has received much atten tion and as stingless bees, for example, larvae are presenting a comprehensive account of the reared in closed cells and workers deposit proximate mechanisms involved is outside more than twice the amount of food in the the scope of this review—we instead refer larger queen cells compared to worker cells readers to more thorough reviews of this (Sakagami 1982). Workers can also manipu- topic (e.g., Wheeler 1986; Anderson et al. late the quality of larval provisions. In prim- 2008; Smith et al. 2008b; Corona et al. 2016; itively eusocial sweat bees, larvaereared on Kapheim 2016). In the following we use provisions with relatively higher sugar con- differential queen-worker development to tent are more likely to attain queen status illustrate the complexity of developmental (Richards and Packer 1994). Similarly, in regulation in eusocial colonies. the progressively provisioning Contrasting queen and worker pheno- where cells remain open until pupation and types result from differential expression of larvae are fed successively, workers exert

Photo credits: S. Fuchs (bee), L. Schrader (ant). Adult C. obscurior queen and wingless, sterile male photo- graphs reproduced from L. Schrader et al. Sphingolipids, transcription factors, and conserved toolkit genes: developmental plasticity in the ant Cardiocondyla obscurior. Molecular Biology and Evolution (2015) 32:1474 -1486. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution (SMBE) on- line at: http://mbe.oxfordjournals.org/content/32/6/1474.abstract. See the online edition for a color version of this figure. 46 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 control over caste determination by feed- the help of cross-fostering approaches, ing queen-destined larvae with high-quality experimental studies are now beginning royal jelly instead of pollen ( Jung-Hoffmann to reveal how these factors interact to cre- 1966). Apart from provisioning behavior, ate different phenotypes. In ants, for ex- workers can also influence female develop- ample, caste fate of female larvae can be ment via mechanical signals ( Jeanne 2009) determined by an interaction between or directed aggression (Brian 1973; Penick larval genotypes and genotypes of adult and Liebig 2012). nestmates (Linksvayer 2006, 2007; Teseo In many cases, worker brood care behav- et al. 2014; Villalta et al. 2016b). These in- ior is modulated by the queen(s). Indeed, teractions are likely modulated by individ- queens play a role in social control of caste ual differences between larvae regarding fate, for example, via pheromonal control sensitivity to social environmental input of worker feeding behavior (Vargo and Pas- and individual worker differences in key sera 1991; Vargo 1998), through mechani- behaviors like provisioning. Similar effects cal signals directed at developing females of worker genotypes on female caste de- ( Jeanne 2009; Jeanne and Suryanarayanan velopment have been demonstrated in 2011; Suryanarayanan et al. 2011), via pher- the honey bee (Linksvayer et al. 2011), omones that cause workers to kill sexual where interplay between larval and nurse larvae (Edwards Adas 1991; Vargo and Pas- worker gene expression regulates dif- sera 1991; Keller et al. 1996; Klobuchar and ferential development of female larvae (Vo- Deslippe 2002), or through direct phero- jvodic et al. 2015). Interplay of individual monal inhibition (Röseler and Röseler 1974; genotypic, maternal, and sibsocial ef fects Passera 1980). Although queen signaling can also influence expression of more gen- appears to act like an enforcement strat- eral traits, such as body size and survival. In egy, the widespread occurrence and evolu- acorn ants, interaction between larval and tionary stability of inhibitory signals (Van worker genotypes determines adult worker Oystaeyen et al. 2014) suggests that the body size (Linksvayer 2007). In contrast, colony as a whole, and possibly individual worker and larvae genotypes interact to mod- larvae, may benefit from queen control of ulate survival but not worker size in the al- female caste (Keller and Nonacs 1993). pine ant (Purcell and Chapuisat 2012). Conditions experienced by queens may also Further excellent evidence for the com- translate into different female phenotypes plexity and flexibility of the social develop- via maternal effects (Schwander et al. 2008; mental regulatory network comes from the Meunier and Chapuisat 2009; Cahan et al. study of ants, where so-called intercastes 2011; Libbrecht et al. 2013). In wood ants, commonly occur (cf. Heinze 1998). Inter- for example, queens develop from eggs laid caste individuals are thought to result from in spring, while summer eggs develop into abnormal development because they dis- workers (Bier 1954a). Predisposition toward play an uncoordinated expression of queen queen caste in the egg stage arises because and worker traits. However, aberrantly pro- spring eggs are associated with larger nurse duced intercastes can become accommo- cells in the ovaries (Bier 1952, 1954b). How- dated into stable intermorph phenotypes ever, predetermination of caste in these when their presence increases colony fit- species is not absolute and worker-modu- ness (Molet et al. 2012), underlining the im- lated nutritional conditions experienced by portance of development for evolutionary female larvae play a substantial role in in- processes. Intermorphs with a functional fluencing adult caste (Bier 1954a; Göss- spermatheca and active ovaries have been wald and Bier 1954). found in a ponerine ant (Ohkawara et al. These examples show that the influence 1993), where they may represent a novel of individual genotype, environment, ma- caste specialized in brood production. In ternal effects, and sibsocial effects on de- Crematogaster ants intermorph-laid eggs are velopment are often difficult to tease redistributed to the queen and the larvae apart (Linksvayer and Wade 2005). With (Heinze et al. 1999; Peeters et al. 2013) and March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 47 thus serve as food sinks without affecting these concur or are in conflict with the male parentage or sexual production (Oet- inclusive fitness interests of other colony tler et al. 2013), indicating that developing members. Furthermore, we highlight the into an intermorph is altruistic at the col- features that determine whether individ- ony level. uals are able to capitalize on potentially To conclude, the wealth of studies on conflicting inclusive fitness interests and female caste determination in eusocial Hy- the factors that may constrain them from menoptera provide an excellent backbone doing so. for investigating regulation of development in social environments. In the future, the Female Caste Fate combination of experimental and molec- Perhaps the most important trait for a de- ular methods should help further unravel veloping female is whether she develops into the mechanisms associated with such geno- a reproductive queen or a (functionally) type by (social) environment interactions. sterile worker. Because a female is more closely related to her own offspring than to offspring of other developing individuals, fitness interests of female larvae are predicted to be under se- developing individuals lection to increase their chances of devel- Evolution of social developmental regula- oping into a queen rather than a worker tion is tightly linked with selective processes (Bourke and Ratnieks 1999; Ratnieks 2001; acting on individual as well as colony-level Reuter and Keller 2001; Wenseleers et al. traits (Figure 3). On one hand, male and fe- 2003; Dobata 2012). Adult queens and male sexuals mate and produce offspring, workers generally differ in their relatedness which allows them to gain direct fitness to developing females because of haplodip- from reproduction. Workers in species with loidy, with workers more closely related to distinct morphological castes, on the other their queen-destined sisters than to their hand, are typically restricted to gaining in- mother queen. This can cause them to ex- direct fitness by helping to rear related off- hibit differing fitness interests regarding spring. Both sexuals and workers ultimately allocation of resources toward new queens depend on colony reproductive output for versus workers (Strassmann et al. 2002; inclusive fitness, and total offspring produc- Ratnieks et al. 2006). Additionally, varia- tion depends on the quality of the queen(s) tion in colony queen number or queen and her mate(s) as well as on the ability of mating frequency may lead them to differ workers to cooperate efficiently (Korb and in their interests regarding the identity of Heinze 2016). Colonies as groups of co- queen-destined larvae (i.e., nepotism; Rat- operating individuals can thus become nieks et al. 2006). Similarly, decreasing re- direct targets of selection and be seen as latedness may increase levels of selfishness adaptive “superorganismal” units if within in developing females, resulting in conflict group competition is obviated (Gardner over female caste both among female lar- and Grafen 2009), e.g., when efficient con- vae and between female larvae and their trol of brood rearing by workers resolves adult nestmates (Dobata 2012). However, the conflict over caste fate of developing conflict between queens and workers over females (Ratnieks et al. 2006; Ratnieks and which individual female develops into Helanterä 2009). When the fitness interests a queen may be constrained from break- of developing individuals differ from those ing out because within-colony kin discrim- of their nestmates based, for instance, on ination and the cues that underlie it are relatedness asymmetries within complex predicted to be selected against (Ratnieks societies, potential for social conflict exists 1991; Keller 1997). Similarly, multiple mat- (Ratnieks and Reeve 1992; Ratnieks et al. ing by queens should reduce actual levels 2006). In the next section, we zoom in on of within-colony conflict over female caste key traits linked to the fitness interests of de- fate by increasing caste fate policing (Do- veloping individuals, and explore whether bata 2012). 48 THE QUARTERLY REVIEW OF BIOLOGY Volume 92

Figure 3. Determinants of Fitness in Hymenoptera Colonies The life cycle of a stereotypical social hymenopteran colony begins with a single queen. Prior to colony foundation, the queen mates with one or several males whose sperm she stores in her spermatheca for the entire duration of her life. Although the males die soon after mating, the queen goes on to found a new colony. During the early phases of colony foundation, she produces female eggs that develop into the first generations of work- ers. After a phase of colony growth during which only workers are reared, the queen starts to lay male eggs and workers begin rearing female larvae into new queens. Upon maturation, males and new queens leave their natal nest to mate, and the cycle starts anew. Individual fitness depends on an array of factors in each life stage, includ- ing caste (e.g., queen or worker), morphology, physiology, fecundity, and behavior. These fitness-determining factors are in turn strongly influenced by genes, epigenetic mechanisms, and abiotic and social environment. Colony fitness is also determined by these factors and their interactions, as well as by their consequences on col- lective behavior, colony efficiency, and social cohesion. See the online edition for a color version of this figure.

There are many potential ways in which immense fitness benefits. At the same time, a female larva can influence her caste fate; selfish female larvae are costly to the colony these are strongly linked to species-specific overall, probably because queen develop- mechanisms of caste determination. The ment demands high resource investment. best example for selfish queen caste deter- Workers kill a large proportion of excess mination comes from taxa where queen- queens immediately after emergence (Engels worker size dimorphism is absent (Ratnieks and Imperatriz-Fonseca 1990; Wenseleers 2001). In stingless bees, queens et al. 2004a), which suggests that individ- and workers are reared in identically sized ual- and colony-level selection are opposing cells provisioned with the same amount of forces in this conflict. Alternatively, produc- food. Around one-fifth of female larvae de- tion and culling of excess queens may be a velop into queens (Kerr 1950; Wenseleers way for workers to select the highest qual- and Ratnieks 2004), even though very few ity queen. Although these bees have long of them end up as swarming queens (Bourke served as models in social insect research, and Ratnieks 1999; Wenseleers et al. 2003). how selfish larvae actually influence their However, queens that do manage to join caste fate is not well understood. With to- a swarm and found a new colony reap day’s genomic resources (Kapheim et al. March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 49

2015), this fascinating system seems pre- nest or join already established nests in- destined for studying the proximate link stead of founding their own colonies (Le- between genetic and/or environmental fac- noir et al. 2010). Theory predicts potential tors and selfish queen de termination, and conflict among workers, resident queens, and promises to shed light on general processes the future queens regarding queen develop- coordinating developmental switches in eu- ment, recruitment, and dispersal in polyg- social insects. ynous species (Crozier and Pamilo 1996), Another way female larvae may selfishly but empirical tests are still lacking. attain queen caste is by developing into miniature queens (Bourke and Ratnieks 1999; Wolf and Seppä 2016). Females that Female Quality develop into queens in spite of only being In holometabolous insects, morphological fed worker rations have been observed in traits such as overall body size are irrevers- ants (McInnes and Tschinkel 1995; Rüppell ibly determined during development (Shin- et al. 1998; Lenoir et al. 2010) and stingless gleton et al. 2007). Substantial evidence bees, where developing into a miniature shows that these traits play a role in deter- queen has clear fitness benefits as “dwarf ” mining adult fitness (Roff 1992; Stearns queens are frequently observed to head 1992). For instance, overall body size is colonies (Wenseleers et al. 2005; Ribeiro positively correlated with female potential et al. 2006). Instead of founding their own fecundity in butterflies (Bauerfeind and colonies, small queens of the fire ant Sole- Fischer 2005; Boggs and Freeman 2005). nopsis invicta take over unrelated, queen- Likewise, large ant queens have higher less nests (McInnes and Tschinkel 1995) in chances of surviving independent colony order to exploit the resident worker force foundation (Bourke and Franks 1995; Wier- (Tschinkel 1996). Over one-third of colo- nasz and Cole 2003; Enzmann et al. 2014). nies produce small queens in the field, in- In addition, queen body weight is positively dicating that conspecific colony takeover correlated with oviposition rate (Wagner pays off (McInnes and Tschinkel 1995). and Gordon 1999) and overall brood pro- Here, developing into a small queen allows duction (Fjerdingstad and Keller 2004). Al- female larvae to engage in an alternative though increased weight can be a result of reproductive tactic (Wolf and Seppä 2016), both pre- and posteclosion feeding, these potentially resulting in large fitness benefits. studies indicate that well-endowed queens This mode of colony foundation is com- outcompete smaller conspecifics. Similarly, mon in socially parasitic (inquiline) ants, a queen that concludes development with where queens are of similar size as their het- a slight size advantage may increase her erospecific host workers; miniaturization chances of winning struggles over reproduc- of queens appears to be an evolutionary tive dominance that involve direct aggres- mechanism allowing parasites to produce sion or fighting (Bernasconi and Strassmann queens even when larvae are fed worker ra- 1999; Beekman and Ratnieks 2003; Beek- tions (Nonacs and Tobin 1992; Aron et al. man et al. 2003; Ratnieks et al. 2006). This 1999). When female larvae in nonpara- is the case in the fire ant Solenopsis invicta sitic species employ similar tactics to attain (Bernasconi and Keller 1998) and the gar- queen status, they may in fact be acting as den ant Lasius niger (Aron et al. 2009), intraspecific parasites (Savolainen and Ve- where the largest queens typically win con- psäläinen 2003; Lenoir et al. 2010). Preva- tests among cooperatively founding queens. lence of clear queen-size dimorphism and Queen-destined larvae may be confronted altogether smaller queen sizes in polygy- with a tradeoff between adult body size and nous species (Heinze and Tsuji 1995; Rüp- timing of emergence if fast development pell and Heinze 1999; Heinze and Keller confers a fitness advantage but results in 2000; Rüppell et al. 2002) suggests that small smaller adult size with potentially lower queens may represent a successful strategy fecundity and/or longevity. In the honey in species where queens stay in their natal bee, the virgin queen that hatches first rou- 50 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 tinely attempts to kill any remaining queen responses (Linksvayer 2006). Cross-foster- pupae in order to assure her takeover of ing approaches that take differential larval the maternal colony (Seeley 1985). Here, responses into account can help resolve competition over future reproductive dom- whether variability in queen size reflects the inance between queen-destined larvae may outcome of conflict between developing become apparent in differential develop- queens and workers, or simply represents mental rates. noise in the system. The outcome of competition between females in species without morphological Male Quality castes may also be influenced by size ad- Eusocial Hymenoptera males spend the vantages accumulated during development majority of their lives as developing individ- (Kukuk 1994). In the eusocial halictine bee uals, usually surviving as adults only long Lasioglossum zephyrum, for instance, the prob- enough to mate (Hölldobler and Bartz ability that a female will emerge as queen in- 1985). Male reproductive success has been creases with body size (Michener 1990) and linked to sperm quantity and quality (Wier- large queens are better at inhibiting worker nasz et al. 2001; Baer and Boomsma 2004; reproduction (Kukuk and May 1991). Finally, Lawson et al. 2012), seminal fluid composi- it is often overlooked that developmentally tion (den Boer et al. 2009, 2010; King et al. determined adult traits can play a role for 2011), and the presence of mating plugs worker inclusive fitness. For example, in a (Roberston 1995; Duvoisin et al. 1999; Baer carpenter ant where workers have retained et al. 2001). Because of their short adult life the ability to produce haploid, male-destined span males typically only produce sperm eggs, worker size is positively correlated with during development, after which the testes ovariole number (Wheeler 1994). In honey degenerate (Hölldobler and Bartz 1985; bees, workers that are pollen-deprived during Passera and Keller 1992; Simmons 2001; development grow up to be poor foragers Boomsma et al. 2005); the only known ex- (Scofield and Mattila 2015). ception to this rule are the wingless males Generally, workers should have an inter- in the ant genus Cardiocondyla (Heinze and est in controlling female size if a certain Hölldobler 1993). With spermatogenesis re- size is linked to higher fitness per unit of stricted to development, ejaculate quan- investment (Fjerdingstad 2005), whereas tity and viability are invariably fixed by the a developing female might simply prefer time the adult male emerges. Given the fit- larger size. Variation in resource availabil- ness benefits from lifelong pair-bonding, ity should lead workers to adjust the num- male larvae should thus have a strong in- ber of queens they rear, while maintaining terest in maximizing ejaculate production optimal queen size (Rosenheim et al. 1996; (Boomsma et al. 2005). However, few studies Fjerdingstad 2005). However, many species have investigated how conditions experi- show considerable variability when it comes enced during development impact charac- to queen size (Sundström 1995; Fjerding- teristics of the male ejaculate. Correlative stad and Boomsma 1997; Rüppell et al. 2002; evidence for the importance of develop- Wiernasz and Cole 2003; Fjerdingstad 2004, ment and growth in determining male re- 2005; Meunier and Chapuisat 2009), which productive success has been found in the indicates that although workers may retain harvester ant, where large males transfer up partial control of size through allocation of to five times more sperm than small males provisions to larvae, plastic developmental (Wiernasz et al. 2001). Similarly, large honey responses may limit their ability to control bee drones carry significantly more sperm female size (Fjerdingstad 2005). Indeed, size than small drones (Schlüns et al. 2003). Re- variation within species or even colonies cently, it has also been shown that protein likely reflects variation in developmental intake during adulthood does not affect trajectories brought about by environmen- sperm viability in drones, indicating that tal factors, worker provisioning behavior, larval nutrition plays a central role in de- and larval developmental and behavioral termining male fitness (Stürup et al. 2013). March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 51

Prior to mating a male must search for, or selectively bias the caste fate of female lar- find, and court a prospective queen while vae, thus decreasing production of workers facing strong competition from rival males but increasing allocation to female sexuals (Shik et al. 2013). Similar to queens, adult (Hammond et al. 2002). Because of the body size and timing of emergence is thus extreme consequences of such behavior, predicted to be crucial for male quality and each male larva should prefer to escape reproductive success. An association be- execution (Nonacs 1993) while each fe- tween overall male body size and fitness male larva should prefer to be a recipient has been demonstrated in harvester ants of preferential treatment (as long as they (Davidson 1982; Wiernasz et al. 1995; Abell can effectively turn the extra resources into et al. 1999), where the size and the shape of fitness). As is the case among adults, colony legs and wings correlate with male mating kin structure may play a role in determin- success (Wiernasz et al. 1995). In the honey ing the potential for this conflict. In par- bee, mating flights seem to have selected ticular, selection on workers to detect and for wing symmetry in males, a trait linked to remove queen-laid male larvae should be developmental stability ( Jaffé and Moritz stronger in singly mated, single-queen col- 2010). Male quality may be particularly onies. Male larvae in single-queen colonies linked to fitness when competition for mat- should therefore, both as individuals and ings is fierce (Wiernasz et al. 1995; Abell as a collective (since they prefer an equal et al. 1999; Boomsma et al. 2005). As is the sex ratio, as do the queens), have an in- case for queens, workers should prefer male creased interest in escaping detection by sizes with the highest fitness payoff per unit workers compared to their counterparts in investment (Fjerdingstad 2005), and worker multiple-queen colonies. Female larvae in and larval genotypes together with envi- single-queen colonies may benefit from ad- ronmental factors likely determine adult vertising their sex in order to facilitate se- male size. Although social Hymenoptera lective removal of males. Although queens males are generally short-lived and do not determine primary sex ratios via control of contribute to social life, there are excep- egg fertilization, brood phenotype is deci- tions such as the long-lived males in the ant sive in influencing the ability of workers to genus Cardiocondyla, which allow for more manipulate secondary sex ratios via selec- detailed study of the dynamics of male tive brood rearing (Mehdiabadi et al. 2003). quality (Heinze 2016). Brood Parentage Brood Sex In species where workers have retained The fitness optima of queens and workers the ability to produce haploid male eggs, a in regard to brood sex allocation are deter- further conflict arises over male parentage. mined by relatedness asymmetries between Al though male larvae and their worker individuals resulting from haplodiploidy, mothers share an interest in individual variation in queen mating frequency, queen male survival, nestmate workers and queens number and relatedness, and the pro duc- should prefer to lay their own eggs and/or tion of males by workers (Bourke and Franks rear only queen-laid male eggs. The poten- 1995; Ratnieks et al. 2006). In the simplest tial for conflict is predicted to vary with kin scenario with one singly mated queen as structure, with higher levels of worker re- sole reproductive, workers should prefer production in colonies with a single, singly threefold investment in female sexuals while mated queen where workers are on average the queen prefers equal investment in both more related to sons of other workers than sexes (Trivers and Hare 1976). Conflict be- to sons of the queen. Here, workers are tween these parties of interest becomes ap- predicted to be under selection to produce parent when workers execute male brood their own sons instead of rearing the queen’s (Keller et al. 1996; Passera and Aron 1996; sons. Accordingly, worker-laid males in such Sundström et al. 1996; Chapuisat et al. 1997) colonies should have an interest in signaling 52 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 their maternity to promote preferential trated how social environment influences rearing. In contrast, in colonies with mul- individual development. We now change tiply mated queens, workers are selected to perspective and examine how developing police other egg-laying workers as they are individuals themselves can influence social more closely related to queen sons than processes within a colony. worker sons, even if each individual worker The mere presence or absence of brood is still most closely related to her own sons affects ecological, behavioral, and physio- (Ratnieks 1988; Wenseleers et al. 2013). logical processes within colonies. For ex- Here, worker-laid males should have an ample, ant larvae influence periodic activity, interest in masking maternity. Although re- foraging strategies, and ovarian activity of latedness variation seems to explain a con- workers (Cole and Hoeg 1996; Dussutour siderable proportion of variation in worker and Simpson 2009; Ulrich et al. 2016). In policing (Bourke 1988; Wenseleers and Rat- wasps, absence of brood causes workers to nieks 2006b), worker policing can also evolve abandon colonies (Kumano and Kasuya if there are substantial costs to unchecked 2001) and can induce physiological changes worker reproduction, i.e., through decreases in individual workers that lead to the devel- in colony efficiency (Ratnieks 1988; Ham- opment of queen-like features (Solis and mond and Keller 2004). Ultimately, polic- Strassmann 1990). Brood can also be in- ing behavior should select against worker volved in influencing ecological processes egg laying (Wenseleers et al. 2004b), which outside the colony—larval demand for pro- has been shown to be the case in honey tein in aphid-tending ants, for instance, di- bees and social wasps (Wenseleers and Rat- rectly impacts growth rates of aphid colonies nieks 2006a). (Oliver et al. 2012). Conflict over parentage of both male and Brood thus clearly modulates processes female brood can arise between queens in on both the individual and the colony multiple queen colonies (Reeve and Rat- level. Such modulation can be passive (e.g., nieks 1993; Keller and Reeve 1994; Keller when workers respond to larger numbers 1995, 1997). Here, kin-preferential behav- of larvae by increasing foraging efforts) and ior or nepotism is predicted to evolve because thus strongly resemble the limited parent- individual workers and groups of workers offspring interactions in subsocial insects vary in their relatedness to brood produced (Wong et al. 2013). Brood can also actively by different queens. Brood may be selected influence the behavior and physiology of to either signal maternity in order to facil- their nestmates, as well as their own devel- itate kin-preferential rearing or mask ma- opment. This seems intuitive when think- ternity to avoid nepotistic brood removal. ing of social interactions in simple groups Although theory predicts selection against such as the classic case of family conflict in sufficient chemical information for kin- birds, where chicks adjust their begging in- preferential rearing (Ratnieks 1991), it does tensities to maximize their own food intake not preclude selection on larvae to adver- (Smith and Montgomerie 1991; Ottosson tise parentage and empirical data show that et al. 1997), often to the detriment of their genetic relatedness can be reflected by siblings or parents (Mock and Parker 1998; chemical similarity (Dani et al. 2004; Neh- Johnstone 2004). So far, little attention has ring et al. 2011; Helanterä et al. 2013; Hel- been paid to active manipulation by euso- anterä and d’Ettorre 2015). cial Hymenoptera offspring and few stud- ies have aimed at distinguishing between passive and active mechanisms. Similarly, The Social Role of the importance of brood traits for deter- Developing Individuals mining individual and colony developmen- In the previous section, we described why tal processes and their effects on fitness development is an important life stage both trajectories remains underappreciated. So for the individual and the colony and illus- although there is ample evidence that de- March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 53 veloping individuals are as social as adults, structures that are used to hold solid food in many cases it remains unclear to which items (Petralia and Vinson 1978, 1979; Busch- extent brood social traits serve cooperative inger and Schaefer 2006). Others carry spe- and selfish purposes, whether they can be cialized tubercles through which they secrete used in different contexts, and how they in- substances that workers ingest dur ing fluence social processes. brood care (Wheeler 1918; Villet et al. 1990). In the second part of our review, we pro- Brood has also evolved features that are vide a synthesis on the morphological, be- important to colony survival, defense, and havioral, and physiological traits that allow organization. Ant colonies take advantage developing offspring to modulate individual- of the superior buoyancy of brood and its and colony-level processes. We roughly clas- resistance to submersion by forming living sify offspring traits according to features rafts with which they escape floods in their of social life, but ask readers to remember unpredictable habitats (Adams et al. 2011; that traits may be used in different con- Purcell et al. 2014). In the weaver ant Poly- texts. We highlight cases where developing rhachis muelleri, larvae and pupae possess individuals may be actively manipulating mimetic green coloration that is thought their social environment and discuss the to reduce the conspicuousness of nest con- relevance of specific traits for the acting de- tents in this tree-living species (Dorow et al. veloping individual, its nestmates, and the 1990). Weaver ant larvae are also unique in colony as a collective whole. that their silk glands, instead of being used to spin cocoons, have been co-opted to produce nest construction material (Höll- brood exhibits morphologies dobler and Wilson 1977). Strikingly, in some adapted to social life taxa, mainly female larvae are used for silk Compared to the striking diversity of spinning, which represents a kind of divi- adult ants, bees, and wasps, at first glance sion of labor among larvae (Wilson and brood looks surprisingly similar across taxa. Hölldobler 1980). In other cases, morpho- Legless and grub-like, social Hymenoptera logical adaptations are restricted to certain larvae seem to display few distinct features. development stages, for example, in the However, a closer look reveals a large diver- desert ant Pheidole rhea, whose fourth instar sity in morphology (Wheeler and Wheeler larvae have anchor-tipped hairs that serve to 1976) even within single groups—e.g., in attach them to the ceiling of underground ants (Wheeler 1918; Wheeler and Wheeler nests (Penick et al. 2012). In wood ants, larval 1953; Petralia and Vinson 1979; Hölldobler hairs help attach larvae to one another, thus and Wilson 1990; Masuko 1990a, 2008; Pee- facilitating their transport by workers (Otto ters and Hölldobler 1992; Baratte et al. 2005; 2005), while ponerine ant larvae exhibit Bueno et al. 2011; Solis et al. 2010a,b, 2011, sticky tubercles which serve to attach them to 2012). Indeed, morphological specializa- nest walls (Peeters and Hölldobler 1992). tions linked to the specific ecology of larvae Recent studies suggest that morpholog- are visible in developing stages. Larvae of ical characters also play a role in commu- many ant species use their sharp, sclerotized nication between adults and brood. mandibles to feed directly on insect prey larvae are thought to use specialized hairs brought back to the nest (Wheeler 1918; to sense vibrations caused by workers and Wilson 1958). Myrmecina ant larvae have queens (Suryanarayanan et al. 2011), while specialized, elongated head morphol ogies Myrmica ant pupae possess stridulatory or- that allow them to consume the contents gans with which they signal their status to of their mite prey (Masuko 1994, 2008). In attending workers (Casacci et al. 2013). contrast, in ants with largely immobile lar- These studies highlight how studying the vae that are fed directly by workers, mandi- functional morphology of brood can help bles are often rudimentary (Wheeler and in understanding its social role in hyme- Wheeler 1953). Some ant larvae have unique nopteran societies. 54 THE QUARTERLY REVIEW OF BIOLOGY Volume 92

brood as a food source val secretions is thus a key feature of brood- One passive way for brood to take part in adult interactions in social Hymenop- colony life is as a direct food source for nest- tera colonies (Hölldobler and Wilson 1990; mates (Wilson 1971); in the context of this Hunt and Nalepa 1994). A prime example review, such cannibalism of viable brood is of larval food processing is found in ponero- not to be confused with consumption of morph ants, whose larvae digest solid in- nonviable, trophic eggs produced by adult sect prey extra-intestinally with the help females in many species (Crespi 1992; of proteolytic salivary secretions (Wheeler Hunt and Nalepa 1994; Khila and Abouheif 1918). Larval predigestion of prey is then 2008). Across species, adults resort to brood followed by ingestion and redistribution of cannibalism and/or feed eggs and pupae the liquefied food by workers (Cassill et al. to larvae in times of resource shortages 2005). Larvae also act as a digestive caste (Woyke 1977; Sorensen et al. 1983a; Höll- due to the high levels of proteases and amy- dobler and Wilson 1990; Heinze et al. 1999; lases in their labial secretions and midgut Schmickl and Crailsheim 2001; Kudô and (Wheeler 1918; Went et al. 1972; Petralia Shirai 2012) and high brood-to-worker ra- et al. 1980; So rensen et al. 1983b). Enzymes tios can significantly increase colony resis- and degraded proteins that are passed from tance to starvation (Rueppell and Kirkman larvae to adults during trophallaxis lead to a 2005). Selective destruction of viable brood sig nificant increase of proteinase activity in by workers and queens is typically seen as a worker midguts (Sorensen et al. 1983b)— consequence of conflict over reproductive which do not usually contain proteases (Pe- dominance, male production, and/or sex tralia et al. 1980; Hölldobler and Wilson allocation (e.g., in ants; Bourke and Franks 1990). In wasps, larval saliva resembles flo- 1995; Hora et al. 2007), but can have a sim- ral nectar and contains essential amino ac- ple trophic function as well (Oettler et al. ids (Hunt et al. 1982). Many of these are not 2013). In some ants, workers and/or queens produced by adults themselves, and thus regularly drink larval hemolymph by punc- queens and workers must solicit saliva do- turing the larval cuticle (Masuko 1986) nations to aid in protein degradation (Ishay through hemolymph ducts located on the and Ikan 1968; Hunt 1984). abdomen of larvae (Masuko 1989, 1990b) For colony as well as individual fitness, or by squeezing a larva’s neck until it pro- the importance of this social interaction is duces a droplet of saliva (Traniello 1982). immense. In ants, brood can process ex- This provides adults with essential nutri- cess protein that otherwise would have det- ents but does not kill the larvae. In this way, rimental effects on individual worker and brood plays a cooperative role in within- colony survival (Dussutour and Simpson colony interactions. 2012). Lack of protein-processing late in- star larvae prohibits production of new sex- uals in pharaoh ants, giving larvae a role in brood modulates colony nutrition caste regulation (Warner et al. 2016). When Adult ants, bees, and wasps cannot pro- paper wasp adults are denied access to lar- cess large food items due to their thread val saliva, nests exhibit decreased survival, waist, which restricts the size of food par- smaller size, and produce fewer offspring ticles that can pass through their esopha- (Hunt and Dove 2002). Wasp larvae respond gus to the midgut (Hölldobler and Wilson actively to solicitation with specialized ap- 1990; Hunt 1991, 1994). Processing of solid pendages that they use to signal their reluc- prey—in many species a colony’s main pro- tance to share (Hunt 1988) and retain saliva tein source—is therefore often performed in response to lateral vibrations caused by by larvae earning them the name “commu- queens, showing that larvae actively respond nal stomach” (Wheeler 1918; Markin 1970; to physical cues (Cummings et al. 1999). Went et al. 1972; Sorensen et al. 1983b; In fire ants, queen egg-laying rate is sig- Cassill and Tschinkel 1999; Dussutour and nificantly correlated with the number of Simpson 2009). Nestmate solicitation of lar- protein-processing larvae (Tschinkel 1995; March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 55

Cassill and Vinson 2007). Addition of lar- more frequently by workers (Creemers et al. vae to colonies maximizes egg laying, while 2003), while others signal their hunger by removal of larvae causes egg-laying rates to swaying, with hungry larvae displaying this drop to almost zero (Tschinkel 1988). When begging behavior more often than well-fed larval secretions constitute the main food nestmates (Kaptein et al. 2005). Vespa wasp source of queens (Wilson 1974; Børgesen larvae signal hunger acoustically by scrap- 1989; Børgesen and Jensen 1995), the ef- ing their mandibles against the cell walls, fects of abstinence can be far-reaching. which attracts feeding workers (Ishay and Pharaoh ant queens that are denied access Landau 1972; Barenholz-Paniry et al. 1986). to larvae have lower levels of both vitello- Worker, male, and queen larvae produce genin and vitellin in their abdomens ( Jen- distinct hunger signals (Ishay and Schwartz sen and Børgesen 1995) and significantly 1973), which suggests that workers may re- decrease their egg production (Børgesen spond differently to varying signals. Likewise, 1989; Børgesen and Jensen 1995). Intrigu- stridulation of mandible surfaces (Wheeler ingly, larvae seem to only respond to solic- and Bailey 1920) and nonvolatile chemical itation by mature, mated queens but deny cues (Cassill and Tschinkel 1995) may func- young, mated queens and virgin queens tion as hunger signals in ant larvae. In access to saliva (Børgesen 1989). This indi- bumble bees, differential feeding behavior cates that larvae can differentiate between of workers has been associated with hunger queens of varying fecundity, perhaps with status of larvae (Smeets and Duchateau the help of honest chemical signals, and 2001; Pereboom et al. 2003), and recently suggests that secretion donation is an ac- this has been linked to differences in the tive behavioral response. chemical compounds on the cuticles of hun gry and satiated larvae (den Boer and Duchateau 2006). brood actively regulates food intake Larvae may also increase their food con- The quantity and quality of nutrition is sumption directly. How a larva goes about one of the most important factors implicated doing this is strongly linked to species biol- in insect development (Scriber and Slansky ogy. In social bees and wasps, brood is reared 1981), and has been linked to a diversity of in cells that are either mass-provisioned fitness-related traits such as survival (Hódar prior to ovipositioning and then sealed, or et al. 2002), developmental rate (Shafiei progressively provisioned throughout devel- et al. 2001), body size (Chapman 1998; Da- opment. Brood rearing in mass provisioned, vidowitz et al. 2003), and reproductive suc- sealed cells limits resources available to cess (Delisle and Hardy 1997; Engels and brood, but also removes some of the con- Sauer 2007). In social Hymenoptera, devel- trol workers may exert over larval nutri- opmental nutrition is furthermore tightly tion, thus giving larvae potential power linked to female reproductive caste and the over food intake (Bourke and Ratnieks fitness payoffs associated with developing 1999; Ratnieks 2001). A prime example is into a queen. Selection should therefore egg cannibalism in the Trigona favor traits that allow developing individu- postica, which occurs when several eggs are als to regulate their food intake. laid in the same cell (Beig 1972). Similarly, One common way offspring influence larvae in some mass-provisioning wasps their food intake is through begging (Kil- increase their provisions by entering neigh- ner and Johnstone 1997; Johnstone 2004; boring brood cells and consuming their Mas and Kölliker 2008). Although the first con tents (Engels and Imperatriz-Fonseca observations of begging in social Hyme- 1990; Velthuis and Sommeijer 1991; Faus- noptera date back some 60 years (Le Masne tino et al. 2002). 1953; Brian 1966), the consequences of this In contrast to bees and wasps, ant brood behavior have only been studied more re- is reared in piles without any physical bound- cently. In a Myrmica ant, larvae that beg for aries between individuals (Hölldobler and food by extending the head upward are fed Wilson 1990). This has important conse- 56 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 quences for both the developing individ- omone furthermore increases foraging uals and the colony as a whole because time (Traynor et al. 2015) and worker pol- ant larvae typically have the opportunity to len consumption (Pankiw et al. 2008), and selfishly increase provisions by cannibaliz- primes preforagers to begin pollen forag- ing nearby brood items (Hölldobler and Wil- ing (Pankiw and Page 2001), resulting in an son 1990). Indeed, ant larvae increase their increase in the number of foragers (Pankiw provisions by feeding on larvae (Rüger et al. et al. 1998) and their pollen loads (Pankiw 2008) and cannibalizing eggs (Baroni Ur- 2004). Specific compounds in brood pher- bani 1991; Heinze et al. 1996; Schultner et al. omone modulate worker feeding behavior, 2013, 2014), a behavior that can increase and experimental application of these com- their survival (Schultner et al. 2013). Can- pounds on larval cuticle results in increased nibalism levels in Formica ant larvae are me- deposition of royal jelly and higher larvae diated by inclusive fitness constraints, with weights (Le Conte et al. 1995). In queen- larvae cannibalizing less often when pre- less colonies, brood pheromone in duces sented with highly related eggs (Schultner emergency queen rearing, and workers are et al. 2014). However, although female lar vae more likely to choose female larvae that significantly decreased cannibalism inten- exhibit high pheromone concentrations as sities in high-relatedness broods, cannibal- future queens (Le Conte et al. 1994). Many ism levels in male larvae remained constant of these behavioral changes seem modu- (Schultner et al. 2014). Together with data lated by brood pheromone effects on worker showing that larvae preferentially cannibal- physiology. In particular, decreasing titres ize eggs from a foreign population com- of juvenile hormone (Le Conte et al. 2001), pared to sibling eggs (Schultner et al. 2013), inhibition of ovary development and/or this confirms that factors such as individual activation (Arnold et al. 1994; Mohammedi genotype and colony kin structure play a et al. 1998; Maisonnasse et al. 2010; Tray- decisive role in mediating larval behavior. nor et al. 2014), increasing activity of hy- Finally, cannibalism provides a good exam- popharyngeal glands (Moham medi et al. ple for how interactions among developing 1996), and decreasing vitellogenin stores individuals can have far-reaching conse- (Smedal et al. 2009) have all been linked quences for colony organization: the spa- to brood pheromone. tial separation of brood by age and/or size Numerous past studies have attempted in many ant taxa has been suggested to be to characterize brood pheromones in ants a means for colonies to prevent costly can- (Watkins and Cole 1966; Walsh and Tsch- nibalism among brood (Wheeler 1910; Le inkel 1974; Bigley and Vinson 1975; Brian Masne 1953; Carlin 1988; Baroni Urbani 1975), but unequivocal evidence for brood 1991)—and thus qualifies as an example of pheromone-mediated effects on worker be- coercion. havior has proven difficult to obtain (see the review by Morel and Vander Meer 1988). brood modulates division of Since then, however, several studies have labor within colonies demonstrated that brood regulates worker Excellent evidence for how brood can egg-laying in ants (Heinze et al. 1996; End- mod ulate division of labor comes from the ler et al. 2004; Teseo et al. 2013; Ebie et al. study of honey bee brood pheromone. De- 2015; Ulrich et al. 2016), and it appears that veloping honey bee larvae secrete brood both queen-derived odors on egg surfaces pheromone, a blend of substances produced (Morel and Vander Meer 1988; Endler et al. by their salivary glands (Le Conte et al. 2006; Holman et al. 2010) and larval odors 2006) that induces workers to cap brood (Villalta et al. 2015) are responsible for cells (Le Conte et al. 1990; Trouiller et al. inducing changes in worker behavior and 1991). Adult workers exposed to the pher- physiology. With the availability of modern omone also begin foraging later (Le Conte quantitative technologies, now is the time et al. 2001) and decrease their foraging to readdress the question of ant brood turnaround time (Pankiw 2007). Brood pher- pheromones in more detail. March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 57

An important consequence of physio- (van Zweden and d’Ettorre 2010), and like logical changes induced by brood odors adults brood can display nest-specific odor is worker sterility; thus brood can signal profiles (Klahn and Gamboa 1983; Cotone- workers to refrain from egg laying and in- schi et al. 2007). Additionally, information stead concentrate their efforts on brood about sex is conveyed in wasp brood odor rearing (Keller and Nonacs 1993). Brood profiles, although workers do not seem to odors also provide a way for offspring to ad- use this information (Cotoneschi et al. vertise their status or quality and influence 2009). Ant workers can discriminate be- provisioning behavior of workers (He et al. tween brood according to sex, parentage, 2016). Seen from this perspective, brood and/or caste ( Jemielity and Keller 2003; odors are no different than the chemical Endler et al. 2004, 2006; Shimoji et al. begging signals employed by offspring of 2012; Ebie et al. 2015; Villalta et al. 2016a). other insect taxa to manipulate parental Intriguingly, discrimination abilities of adult provisioning behavior (Mas and Kölliker workers appear to be linked to their expe- 2008). Because brood odors signal workers rience as larvae (Signorotti et al. 2013), provid- to refrain from egg laying and their pro- ing yet another argument to include brood duction influences colony ecology and sur- when studying insect societies. vival (Smedal et al. 2009), they are a crucial Brood odors can play a key role in regu- determinant of the inclusive fitness of de- lating adult traits, for instance, in the honey veloping individuals. Although clearly a bee where queens mate multiply and work- brood phenotype, brood odors are often ers have retained the ability to lay male seen as a chemical means for queens to eggs. Honey bee workers are selected to re- suppress worker reproduction. Indeed, it move eggs laid by other workers, since the is likely that queens benefit from inhibi- inclusive fitness interests of workers align tion of worker reproduction mediated by with both the queen and her sons (Beek- the odors of their offspring. Thus mother man and Ratnieks 2003). Indeed, queen- and offspring interests may align concern- laid eggs differ from worker-laid eggs in ing brood odor production, adding an ad- their odor profiles (Katzav-Gozansky et al. ditional level of complexity to this central 2003; Martin et al. 2005) and removal rates social interaction. As brood pheromone ef- (Ratnieks and Visscher 1989), indicating fects are so strongly associated with the reg- that queens are under selection to produce ulation of social processes such as worker male eggs that display maternal origin in foraging and brood rearing behavior, brood order to facilitate discrimination and avoid signaling is also likely to play a key role in destruction through policing workers (See- the evolution of cooperative brood care in ley 1985, 1995; Ratnieks 1988, 1995; Keller bees and other social Hymenoptera (Tray- and Nonacs 1993; Oldroyd et al. 2002). How- nor et al. 2014). ever, low removal rates of worker-laid eggs in so-called anarchistic honey bee so cieties suggest that worker-laid males can some- brood odors mediate times escape detection (Oldroyd et al. conflict among adults 1994; Oldroyd and Ratnieks 2000; Barron Brood odors are furthermore associated et al. 2001), possibly by carrying queen-like with selective brood treatment (Klahn and odors (Oldroyd and Ratnieks 2000; Ol- Gamboa 1983; Page et al. 1989; Panek and droyd et al. 2002). In ants, differences in Gamboa 2000; Hannonen and Sundström odor profiles of worker and queen-laid eggs 2003), for instance, in the context of sex al- can allow workers to selectively kill worker- location conflict where workers need to dis- laid eggs (d’Ettorre et al. 2004; van Zweden criminate between male and female brood. et al. 2009). Brood odors may also play a role Here, brood phenotype directly influences in regulating the production of new sexuals, worker behavior. Social Hymenoptera typ- for instance, in the ant Aphaenogaster senilis, ically use long-chained hydrocarbons em- where workers preferentially kill queen- bedded in the cuticle as discrimination cues destined larvae even though the chemical 58 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 profiles of worker and queen-destined lar- Hunt and Nalepa 1994) has been suggested vae are highly similar (Villalta et al. 2016a). to play a key role in the repeated evolution Clearly, brood odor regulation of adult be- of eusociality in the Hymenoptera (Hunt havior is complex and the mere presence 1991; Johnson et al. 2013). The food-shar- or absence of odor variation does not jus- ing behavior that is also found in subsocial tify inferences about differential behavior. taxa such as earwigs provides support to the Overall, the diversity of brood odors ap- idea that offspring feeding interactions lie pears to play a crucial role in determining at the basis of complex sociality in insects adult treatment of offspring. For now, how- (Falk et al. 2014). In several eusocial taxa, ever, data on individual variation in odor this has turned into an obligately expressed profiles is too scarce to provide conclusive offspring behavior without which colonies evidence that offspring are under selection cannot function optimally (e.g., decreased to mask or advertise their parentage, sex, egg-laying rates in fire ant queens denied or caste. Moreover, we are only beginning access to larval saliva, Tschinkel 1995; fail- to understand the proximate mechanisms ure to produce new queens in pharaoh associated with odor perception (Gronen- ant colonies deprived of larvae, Warner berg 2008; Zube et al. 2008; Brandstaetter et al. 2016; lower survival of larvae-deprived, et al. 2011; Roat and Cruz-Landim 2011; green-headed ant colonies due to the inabil- Brill et al. 2013; Sharma et al. 2015; McKen- ity to process excess proteins, Dussutour and zie et al. 2016; Wang et al. 2016). Under- Simpson 2009; and lower survivorship and standing evolution of offspring odors in fecundity of paper wasp colonies deprived social Hymenoptera will therefore require of larval secretions, Hunt and Dove 2002). detailed exploration of offspring odor pro- Nevertheless, this crucial social interaction duction and adult perception and discrimi- has received very little attention from social nation abilities, as well as study of the fac tors insect researchers, with the exception of that facilitate and constrain odor diversity seminal work published over 20 years ago evolution. Together, such studies will be (Hunt 1991; Hunt and Nalepa 1994). Hunt paramount in providing a better under- (1991) also called attention to a conflict-re- standing of the role of brood odors in in- lated aspect of this behavior by suggesting fluencing colony social processes. that evolution of saliva donorism in wasps may be intertwined with developmental conflict. If, for example, donorism carries Studying Developing Individuals a developmental cost for larvae and/or re- Reveals a New Perspective duces future reproductive potential, re- on Social Evolution luctance to share saliva may in fact be the The above sections show how developing result of selection on larvae to control the ants, bees, and wasps play a crucial role in timing and amount of saliva surrendered colony life, and that they have both fitness (Hunt 1991). Possibly, larvae that selec- interests and the power to attempt to reach tively refuse soliciting adults benefit from their fitness optima. Table 1 summarizes increased growth rates compared to more central aspects of colony life that brood can cooperative brood mates. Should increas- influence, elaborates on how the fitness in- ing growth lead to queen development, the terests of brood, the power of conflicting incentive for females to withhold saliva may parties of interest, and taxon-specific con- be particularly strong. Such speculation is, straints may influence social processes, in our opinion, worth pursuing in empirical and provides testable predictions of brood tests in order to understand the proximate power. In the final section, we present a mechanisms (e.g., physiological regulation short overview of how the study of develop- of sharing/refusing) and ultimate factors ing individuals can provide a new perspec- (e.g., costs and benefits of sharing/refus- tive on the biology of social Hymenoptera. ing) underlying the evolution of this pri- Larval food processing (see the section, mary social interaction, and its role in the The Social Role of Developing Individuals; evolution of complex sociality. March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 59 continued processing) is shaped by similar evolutionary processes as adult behavior, degree of cooperative behaviors should increase with social complexity cannibalism, dishonest signaling of need) should be negatively correlated with and relatedness, both inter- intraspecifically degree of divergence between brood and worker interests, variation in, for example, offspring size and number should be higher in low-relatedness settings physiology should increase with decreasing relatedness Testable PREDICTIONS Testable If brood behavior (e.g., food Selfish behavior (e.g., begging, If kin structure affects the Primer effect on worker brood power brood POTENTIAL adult queens and workers intake and brood provisioning shaped by selection on queens as well CONSTRAINTS on Physical dominance of control resource Workers Brood pheromones are Workers outcome? Whole Colony affect conflict potential/ affect Does KIN STRUCTURE cooperation may be higher when relatedness is high offspring should be higher in low-relatedness societies over optimal allocation into offspring size versus number are predicted to diverge more strongly when relatedness is low egg-laying workers on male parentage depends on mating frequency of the queen and queen number Possibly—payoffs from of individual Yes—selfishness and brood interests Worker Yes—whether brood agrees with Yes—whether TABLE 1 TABLE c

a INTEREST? b in acting on worker physiology so that egg-laying workers refrain from costly reproduction individual offspring may have different optima in worker provisioning can disagree over optimal resource allocation if there is a tradeoff between optimal offspring size and number used in selfish contexts evolution of colony-level traits Are there CONFLICTS OF there Are Yes—brood has an interest Yes—brood Yes—brood as a whole and Yes—brood and individual brood Workers Yes—cooperative traits may be Yes—cooperative Selfish brood traits can underlie The influence of brood on individual and colony-level traits in eusocial Hymenoptera The influence of brood via pheromone) (e.g., brood pheromone) morphology, morphology, behavior BROOD influence Chemical signaling (e.g., brood Chemical signaling Presence, traits reproduction defense, foraging, productivity COLONY-LEVEL COLONY-LEVEL INDIVIDUAL- and Physiology and Provisioning behavior Begging Colony organization, 60 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 continued e offspring should differ in levels of selfishness across kin structures should increase with relatedness levels should increase with relatedness levels differ in the benefits gained from saliva retention, they may adjust donorism levels accordingly strong selection to signal sex in single queen colonies while male larvae should be selected to mask sex Testable PREDICTIONS Testable Individual male and female Honesty of brood signals Levels of saliva donorism If male and female larvae Female larvae should be under brood power brood POTENTIAL fertilization care advantage over larvae CONSTRAINTS on Queen controls control brood Workers Adults have a physical Queens Whole Brood outcome? parties of interest is highest in single-queen colonies where relatedness asymmetries are maximized from primer function in high- relatedness societies retain saliva more often or preferentially donate saliva to related queens in multiple queen colonies, if they are not equally related to all queens sacrifice less related brood affect conflict potential/ affect Does KIN STRUCTURE Yes—conflict potential among all Yes—conflict Brood signals should be released offspring may Yes—individual may be more likely to Workers Continued TABLE 1 TABLE d INTEREST? their own sons, but other workers may be selected to police an interest in maximizing survival and may refuse donorism if this negatively affects growth and development brood as a resource in multiple queen colonies if its increases fitness queens differ in their sex-ratio optima because of relatedness asymmetries brood align with worker interests while of male brood align with queen interests Are there CONFLICTS OF there Are Workers can prefer producing Workers offspring have Yes—individual Queens are predicted to exploit Yes—brood, workers, and Yes—brood, interests of female Generally, via donorism and retention intake competitors BROOD influence Self-sacrifice Removing Masking/ advertizing sex traits COLONY-LEVEL COLONY-LEVEL Fecundity Saliva/hemolymph Sex Allocation Regulating food INDIVIDUAL- and March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 61

k or

continued l reproductive dominance is fierce over their caste fate, the proportion of female larvae that develop into queens should reflect the larval rather than adult optimum should be higher in species where competition for matings, nesting sites, If female offspring retain power Degree of selfish behavior h i

g j j flow primer function dimorphism about colony size ability to recognize competitors flow physiological tradeoffs ability to recognize competitors Workers control resource Workers Queen pheromones with Large Q-W size Access to information Constraints on larval Maternal effects Brood rearing in cells Workers control resource Workers Allometric growth/ Constraints on larval e Individual offspring and workers to prefer rearing closely related female larvae into queens individual female larvae are predicted to increase when relatedness is low concerning optimal allocation into offspring size versus number are predicted to diverge more strongly when relatedness is low Continued TABLE 1 TABLE Low relatedness causes queens Yes—levels of selfishness in Yes—levels Yes—adult and brood interests Yes—adult

c prefer producing fewer new queens than is optimal for an individual female larva maximizing investment in themselves tradeoff between size and number of new queens and males Yes—queens and workers Yes—queens Individual offspring prefer Yes—workers prefer an optimal Yes—workers f developmental pathways competitors intake competitors pathways intake before nestmates Alternative Removing Masking identity Regulating food Removing Novel developmental Masking/ advertizing identity Attaining critical size quality Male and queen Female caste Regulating food 62 THE QUARTERLY REVIEW OF BIOLOGY Volume 92 continued retain partial control over development, variation in adult phenotype should be larger in low relatedness settings selection to signal parentage, worker sons should advertise their parentage in singly mated, single-queen colonies while queen sons should mask parentage; this should be reversed in multiply mated or multiple-queen colonies Testable PREDICTIONS Testable If both workers and larvae If male offspring are under brood power brood POTENTIAL quality in species with alternative sexual morphs? reproductive constraints restricts/limits worker reproduction constrained by lack of matriline-specific brood odors) CONSTRAINTS on Less worker control of Lack of functional ovaries/ Policing (which may be outcome? affect conflict potential/ affect Does KIN STRUCTURE interests of the queen and her sons align; workers collectively prefer workers’ sons based on kinship alone and interests of workers’ sons align with their mothers interests of queen sons, queens, and workers collectively align but individual workers prefer own sons over queen Yes—in single-queen colonies, Yes—in In multiple-queen colonies, Continued TABLE 1 TABLE INTEREST? workers, and queens are predicted to disagree about which males are reared to adulthood Are there CONFLICTS OF there Are Yes—individual male offspring, Yes—individual via BROOD influence advertizing parentage traits COLONY-LEVEL COLONY-LEVEL INDIVIDUAL- and Male parentage Masking/ March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 63 should produce female brood-carrying matriline specific odors in order to facilitate preferential rearing (unless costs of being discriminated against are high), irrespective of queen fitness—this can be tested by comparing matriline specificity of brood odors in single- and multiple- queen colonies of socially polymorphic species In multiple-queen nests, queens et al. 2008). In such populations, fitness interests of o queens if workers preferentially rear relatively larger e when they compete for matings (Wiernasz et al. 1995; sex ratios can be split so that singly mated/single-queen the same time, individuals should be selected to avoid nies together and then fight for reproductive dominance larvae potentially retain much more power to engage in cted to vary with mean nestmate relatedness, the size of sex- prevent costly cannibalism among brood (Wheeler 1910; Le llow for sufficient divergent growth periods (Wheeler 1986). brood odors may constrain preferential brood rearing ales and nestmates females (due to haplo- e cases larvae can overcome this constraint by biting through ourke and Ratnieks 1999). Access to information about colony n queens and workers may thus constrain larvae in their power aviors carry a cost and/or reduce future reproductive potential Lack of matriline-specific sharply with decreasing queen number (Schultner et al. 2014). of investment (Fjerdingstad 2005). A developing larva may prefer workers may attempt to preferentially rear full sisters into queens Continued TABLE 1 TABLE Yes—in multiple-queen colonies, Yes—in (Brian and Hibble 1963). mating societies, individual female offspring, workers, and queens are predicted to disagree over which queen- destined larvae are reared to adulthood Yes—in multiple-queen/ Yes—in Myrmica rubra advertising parentage Ratnieks 1991; Dobata 2012. Female larvae that reach a critical minimum size before their female brood mates may increase chances of being reared int Evolution of cooperative larval traits such as saliva donorism may be intertwined with developmental conflict, e.g., if beh Workers should have an interest in controlling the size of sexuals if a certain is linked to higher sexual fitness per unit Workers In populations where colonies are headed by both singly and multiply mated queens or contain single multiple queens, One example is spatial separation of brood by age and/or size in ants, which has been suggested to be a means for colonies Rearing of brood in separate cells social bees and wasps may limit the power to regulate their food intake. In som When larval selfishness in the form of egg cannibalism is modeled a kin selection framework, levels are predi In taxa with strong morphological differences between castes, developmental switches typically occur early in development to a

In annual species where queens and workers are reared in separate cohorts, colony size is the main trigger of queen rearing (B For larvae to selectively remove same-sex competitors, they need be able discriminate among brood of different sexes. At Competition over access to resources between queen-destined larvae may be especially strong in species where queens found colo specific benefits, and brood sex ratio. As variation in queen number relatedness differentially affects between m diploidy), cannibalism levels in male larvae are predicted to stay constant across relatedness levels, while female levels drop The need for relatively more resources to trigger queen development in particular species with large size differences betwee to influence caste, especially if they must act within a restricted time window. (Hunt 1991). Masne 1953; Carlin 1988; Baroni Urbani 1991). cell walls to enter and consume provisions of neighboring cells (Engels Imperatriz-Fonseca 1990; Faustino et al. 2002). Ant selfish provisioning because brood is reared in batches and larvae often have easy access to eggs (Hölldobler and Wilson 1990). size may therefore be another crucial determinant of larvae power. detection. until only one queen remains (Bernasconi and Keller 1998; Aron et al. 2009). Competition between males in some ants can be fierc Abell et al. 1999; Boomsma 2005). female larvae into queens, as is the case in ant colonies produce female-biased sex ratios while multiply mated/multiple-queen male-biased (Meunier workers will depend on their colony of origin. Female parentage Masking/ a b c d e f g h i j k l a larger size than the worker optimum. 64 THE QUARTERLY REVIEW OF BIOLOGY Volume 92

Another example of a social interaction evo-devo) spurs renewed interest in the worth pursuing in more detail is parent- role of development in evolution (West- offspring conflict—an interaction typically Eberhard 2003; Abouheif et al. 2014). So- studied from the perspective of both adults cial Hymenoptera are excellent models due and juveniles. Although Hymenoptera con- to their extreme developmental polyphen- flict studies are built on the same theoret- ism, which is regulated by genetic, epige - ical scaffold, the focus has mainly been on netic, environmental, and social factors. conflict between parents (i.e., queens/males) Much like the study of evolutionary conflict, and their adult helper offspring (i.e., work- traditionally the study of social insect poly- ers). This may explain why classic conflict phenism has focused on adult individuals. traits such as begging have been largely Only recently has this shifted to center on overlooked in social insects (with the few no- molecular traits of developing individuals. table exceptions mentioned in the section, This has revealed a central role of transcrip- The Social Role of Developing Individuals). tional regulation (Kucharski et al. 2008, Begging can function as an honest signal 2015; Kamakura 2011; Forêt et al. 2012; of need or reflect the competitive ability of Guo et al. 2013; Shi et al. 2013; Bonasio individuals, i.e., their ability to carry the costs 2014; Klein et al. 2016) underlying differ- of begging (Kilner and John stone 1997; ential gene expression during development Royle et al. 2002). The only study of begging (Corona et al. 1999; Evans and Wheeler honesty in eusocial Hymenoptera revealed 1999, 2001; Abouheif and Wray 2002; San- that hungry ant larvae beg more frequently tana et al. 2006; Wheeler et al. 2006, 2014; than well-fed ones, indicating that this sig- Barchuk et al. 2007; Hoffman and Goodis- nal honestly reflects needs (Kaptein et al. man 2007; Patel et al. 2007; Mackert et al. 2005). Insect offspring often signal their 2008; Hunt et al. 2010b; Li et al. 2010; Aze- hunger chemically (Mas and Kölliker 2008)— vedo et al. 2011; Colgan et al. 2011; Mutti social earwig offspring signal their quality et al. 2011; Wolschin et al. 2011; Chen et al. by secreting higher relative amounts of par- 2012; Cameron et al. 2013; Berens et al. ticular compounds on their cuticle, which 2015; Brito et al. 2015; Schrader et al. 2015; induces differential feeding behavior in Vojvodic et al. 2015), with important con- mothers (Mas et al. 2009). Again, to our sequences for gene evolution (Hunt et al. knowledge, only one study has looked at 2010a, 2011, 2013; Hall et al. 2013; Har- chemical signals as a way for individual lar- pur et al. 2014; Helanterä and Uller 2014; vae to signal hunger and directly influence Mikheyev and Linksvayer 2015; Schrader worker provisioning behavior in eusocial et al. 2016). These efforts have substan- Hymenoptera (den Boer and Duchateau tially heightened our understanding of 2006). Seeing how important chemical com- the proximate mechanisms associated with munication is in social insect colonies polyphenic development. Within the eco- (Blomquist and Bagnères 2010), offspring evo-devo framework, experimental studies chemical signaling traits such as honey bee on emerging social insect model species brood pheromones and ant larvae odors promise to provide answers to fundamental merit further attention. Understanding the questions in evolutionary biology. evolution of offspring signaling in social Hymenoptera will demand studies focusing on signal production and perception, as Conclusions well as exploration of the costs and benefits Social Hymenoptera have proven ideal of signaling, the effects of signaling on in- models for studying the evolution of social- dividuals and the colony, and the potential ity, contributing to our understanding of the effects of colony kin structure on signal interplay between cooperation and conflict intensity and honesty. At the moment, this in social systems, and the factors associated field is wide open. with maintaining social cohesion (Bourke Finally, the expanding field of ecological 2011). However, the majority of studies have evolutionary developmental biology (eco- focused on interactions between adults. March 2017 ROLE OF BROOD IN EUSOCIAL HYMENOPTERA 65

This is surprising, since important physio- and conflict in social insect brood promises logical processes that determine lifetime to be a fruitful avenue for future research. fitness coincide with development. In ad- dition, developing individuals often dom- acknowledgments inate colonies numerically and their needs dictate worker behavior, physiology, and The authors thank L. Sundström and several anon- colony-level task division. Far from power- ymous reviewers for comments on previous versions of this manuscript. This work was made possible by a less, developing individuals have evolved Finnish Cultural Foundation grant to Eva Schultner, specialized traits that serve complex inter- a DFG grant (He1623/31) to Jan Oettler, and Kone actions with nestmates and play a central Foundation, University of Helsinki and Academy of role in social cohesion. In light of the ideas Finland grants to Heikki Helanterä (135970) and the presented here, the study of cooperation Centre of Excellence in Biological Interactions (252411).

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