OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

CHAPTER 12 Cooperative breeding systems

Michael A. Cant

12.1 Introduction future fitness, and between direct and indirect components of their inclusive fitness. In this way Cooperative breeding is a type of social system cooperative breeders differ from eusocial species in which some group members (referred to as which have distinct reproductive and worker castes ‘helpers’) routinely provide care for offspring that and helpers remain functionally or morphologically are not their own, but retain the potential to repro- sterile throughout their lives (Bourke 2011). duce themselves either currently or in the future. Cooperative breeders have been the focus of This broad definition (which derives from those intense research in behavioural ecology for two suggested by Cockburn 1998; Crespi and Yanega main reasons. First, they embody a major puzzle of 1995; Emlen 1991) includes a range of species, from evolutionary theory: how can altruistic behaviour primitively eusocial insects such as paper wasps, be favoured by natural selection? Helpers pay a hover wasps, halictid bees, and ambrosia beetles; fitness cost to boost the reproductive output of to avian, mammalian, and fish ‘helper-at-the-nest’ other group members. For example, subordinate systems in which offspring delay dispersal and foundresses of the paper wasp Polistes dominulus help dominant breeders with subsequent breeding risk their lives foraging to feed larvae to which attempts; and also larger animal societies with mul- they are often unrelated (Leadbeater et al. 2010; tiple male and female breeders and helpers per Queller et al. 2000). Using the classification of social group (Fig. 12.1). From current information, 9% of behaviours introduced by Hamilton (1964), help- birds (852 species; Cockburn 2006) around 2% of ing is a form of altruism when it involves a life- mammals (Lukas and Clutton-Brock in press; Ried- time direct fitness cost to the helper, and results in man 1982), <0.5% of fishes (20–38 species; Taborsky a lifetime direct fitness benefit to the recipient of 1994; Taborsky 2009), and hundreds of species of help. In the case of paper wasps, foraging involves insect can be classed as cooperative breeders. There clear fitness costs because foundresses that do more are also examples from arachnids (Salomon and foraging suffer higher mortality (Cant and Field Lubin 2007) and crustaceans (Duffy and Macdon- 2001). Cooperative breeding systems provide con- ald 2010). These societies, while very diverse in crete examples of altruism together with the pos- terms of social structure and basic biology, share sibility of measuring the fitness consequences of some common features. Populations are usually helping, and hence an opportunity to test evolution- subdivided into groups of kin (although non-kin ary theories of cooperation. individuals may also be present) with strong eco- Second, cooperative breeders have proved to be logical constraints on dispersal or independent excellent models for the study of evolutionary con- breeding (Hatchwell 2009). Within groups, there is flict and its consequences for behaviour and group usually (but not always) a reproductive division dynamics. Evolutionary conflict arises whenever of labour in which high ranked or socially domi- the optimum fitness outcomes for the participants nant individuals breed, and lower ranked individ- in an interaction cannot all be achieved simulta- uals help (Field and Cant 2009b). Because helpers neously. In the case of cooperative breeders, the retain the ability to reproduce themselves, their role of breeder is usually more profitable (in terms behaviour reflects a trade-off between current and of fitness) than the role of helper, which generates

The Evolution of Parental Care. First Edition. Edited by Nick J. Royle, Per T. Smiseth, and Mathias Kölliker. © Oxford University Press 2012. Published 2012 by Oxford University Press. OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 207 evolutionary conflict over reproductive roles and as sexual conflict over mating and conflict between shares of reproduction. Conflict arises over helping parents (Chapter 9), and between parents and off- effort because investment in helping usually trades spring over parental investment (Chapter 7). off against a helper’s own residual reproductive The topic of cooperative breeding has been well- value, so each helper would prefer other group reviewed in birds (Cockburn 1998; Hatchwell 2009; members to invest more. Studies of within-group Koenig and Dickinson 2004; Stacey and Koenig conflicts in cooperative breeders have provided 1990) and mammals (Russell 2004; Solomon and insights into how groups remain stable despite French 1997). Insect cooperative breeders are usu- selection for selfishness, and the ways in which evo- ally described as ‘primitively eusocial’ (because lutionary conflicts of interest within groups can be they lack sterile castes) and are not usually consid- resolved on an evolutionary time scale, for example, ered alongside vertebrates, although there are clear by the evolution of morphological specialization similarities between insect and vertebrate systems (Bourke 1999), or fertility schedules which elimi- (Field and Cant 2009a). Here I focus on four ques- nate reproductive overlap within groups (Cant and tions that are of interest to researchers working on Johnstone 2008); and also on a behavioural time both taxa. First I discuss current understanding of scale, through mechanisms of ‘negotiation’ (Cant evolutionary routes to cooperative breeding, and 2011; McNamara et al. 1999). The general principles the constraints on dispersal that can lead to the arising from these studies can help us to understand formation of cooperative groups. Second, I outline how conflict is resolved in a range of contexts, such the main hypotheses for the evolution of helping

(a) (c) (e)

(b) (d) (f)

Figure 12.1 Examples of cooperative breeding systems. (a) Tropical hover wasps (Stenogastrinae; such as this group of Parischnogaster alternata) breed year round in South East Asia in semi-permanent mud nests. Females mate and either attempt to breed independently or form a strict age-based queue to inherit the position of breeder (Field et al. 2006; Photo by Adam Cronin). (b) A group of cooperatively breeding spiders Stegodyphus dumicola preying upon a cricket. This species forms colonies of tens to hundreds of individuals in which a large proportion of females are non-breeders. These females help by regurgitating food for the offspring of other females, and are eventually consumed by them (Salomon and Lubin 2007; photo by Mor Salomon-Botner). (c) The African cichlid Neolamprologus pulcher forms cooperative groups in which reproduction is monopolized by a single breeding pair. Subordinates delay dispersal and help if there is a shortage of suitable breeding habitat, and prefer to settle with non-kin over kin (Heg et al. 2008; photo by Michael Taborsky). (d) Pied babblers Turdoides squamiceps form cooperative groups of 2–10 individuals in the Kalahari Desert. Helpers engage in sophisticated sentinel behaviour, vocal negotiation over cooperation, and active teaching of fledglings (Raihani and Ridley 2008; photo by Alex Thornton). (e) Banded mongooses Mungos mungo in Uganda live in groups of 8–60 individuals in which multiple females give birth together in each breeding attempt. After pups emerge from the den they form one-to-one relationships with adult ‘escorts’ who guard and provision them (Bell et al. 2010; Cant et al. 2010; photo by the author). (f) Human reproductive life-history is characterized by a short-interbirth interval and long period of offspring dependency (Mace and Sear 2005). Offspring are reliant upon the investment of their parents, grandparents, and older siblings for many years, and are cooperative breeders par excellence (photo of members of the forager-horticulturalist Phari Korwa tribe, India, by Shakti Lamba). OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

208 THE EVOLUTION OF PARENTAL CARE behaviour based on direct and indirect fitness bene- death of the mother and defend offspring against fits, and assess the evidence for these in insects and predators and parasites while mothers forage (Field vertebrates. I focus in particular on recent develop- and Brace 2004; Gadagkar 1990). ments in kin selection theory which examine the In insects two main evolutionary routes to impact of demography on the evolution of social cooperative breeding and eusociality have been behaviour and life-history in cooperative species. proposed. The subsocial route (Wheeler 1928) is sim- Third, I discuss recent attempts to incorporate ilar to that proposed for cooperative vertebrates, behavioural negotiation into evolutionary models namely, that transitions to cooperation occurred of parental care and cooperation. Fourth, I consider through offspring remaining in their natal nest reproductive conflicts that arise within groups over to help their mother (or mother and father, in helping effort and reproduction, and theory and the case of termites; Korb 2008). The second, empirical tests of how evolutionary conflict over semisocial route (Lin and Michener 1972; Michener reproduction is resolved. Much of this conflict the- 1958), suggests that cooperation arose among same- ory applies equally well to non-cooperative species generation females who could gain mutualistic and and can be used to derive insights into how within- kin-selected benefits from breeding together. Same- family conflict over parental care is resolved on generation associations are commonly seen in some evolutionary and behavioural time scales (see also bees, ants, and polistine wasps (Lin and Mich- Chapters 7, 8, and 9). ener 1972). Phylogenetic analysis suggests that high relatedness as a consequence of monogamy is asso- 12.2 Routes to cooperative breeding ciated with evolutionary transitions from solitary breeding to cooperative breeding and eusociality In most cooperatively breeding fish, birds, and in Hymenoptera (Hughes et al. 2008) and in ter- mammals, groups form when offspring delay dis- mites (Boomsma 2009). Ancestral monogamy in persal and remain on their natal territory to help Hymenoptera has been taken as evidence in sup- their parents rear subsequent broods. In birds, 852 port of the subsocial route to cooperative breed- out of 9268 bird species for which parental care ing, because in subsocial associations helpers can systems are known or can be inferred are coop- expect to raise full rather than half siblings, whereas erative breeders (Cockburn 2006). Avian coopera- monogamy would appear to offer no clear advan- tive breeders almost always evolved from socially tage to sociality via the semisocial route (Boomsma monogamous biparental ancestors, the mating sys- 2009). tem exhibited by around 80% of extant birds (Cock- These comparative analyses emphasize the burn 2006; Cornwallis et al. 2010). The ancestral importance of kin structure for cooperative mating system of mammals is polygyny rather than transitions, but it is clear that ecological conditions social monogamy (Clutton-Brock 1989), but recent also play a major role in the origin and maintenance phylogenetic analysis suggests that most coopera- of cooperative breeding. In birds, offspring delay tively breeding mammals evolved from monoga- dispersal when there is a shortage of suitable mous ancestors (Lukas and Clutton-Brock in press). breeding habitat (e.g. Komdeur et al. 1995), where In both birds and mammals, therefore, monogamy there are high indirect or direct fitness benefits appears to set the stage for the evolution of cooper- of philopatry, for example through inheritance of ative breeding. breeding positions (Dickinson and Hatchwell 2004); In many cooperative insect lineages an impor- and, across species, where ecological environments tant precursor to cooperative breeding is the evo- are temporally variable, since this allows groups to lution of progressive provisioning, where mothers breed in both harsh and benign years (Rubenstein remain to guard and provision their offspring and Lovett 2007). Similar factors may also promote during development (Field and Brace 2004). Pro- group formation in cooperatively breeding cichlids gressive provisioning and extended parental care (Wong and Balshine 2011). In mammals, delayed facilitate the evolution of cooperation because addi- dispersal of offspring does not appear to be the tional helpers can provide insurance against the result of habitat saturation, since vacant habitat OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 209 often remains unutilized (Russell 2004). Rather, From this brief survey it is clear that multi- dispersal is often costly in mammals because ple factors may contribute to delayed dispersal males aggressively defend access to mates and of offspring and subsequent evolution of coopera- because dispersing individuals are susceptible to tive breeding. Monogamy makes the transition to predation and attack by conspecifics. By delaying cooperative breeding easier for both insects and dispersal, young adults can remain in a ‘safe vertebrates, and in insects progressive provision- haven’ and may inherit breeding status if same-sex ing sets the stage for cooperative breeding because dominants die. Such are the benefits of philopatry helpers then become particularly useful. In verte- for young adults that in many species of mammal brates, delayed dispersal arises where there is a dominant individuals often go to considerable shortage of suitable habitat or mates or strong bar- lengths to forcibly evict subordinates, while the riers to group entry. In insects helpers may do best subordinates themselves appear highly reluctant to remain in their natal group because independent to leave (Clutton-Brock 2002; Johnstone and Cant nesting entails high mortality, and in Hymenoptera 1999). from a life-history in which solitary breeders have a In insects harsh ecological conditions and high high chance of dying before their offspring are fully adult mortality are suggested to promote the for- developed. In each case the consequence of con- mation of groups via the subsocial or semisocial straints on dispersal is a genetically structured pop- routes. In primitively eusocial wasps, for example, ulation, in which relatedness to local group mem- dispersal is typically not constrained by a lack of bers is on average greater than relatedness to the available breeding habitat: nests can be constructed breeding population at large (Hatchwell 2010). In on a range of vegetation types or substrates. There the next section I explore how population structure are nevertheless severe constraints on independent influences selection for any traits that have social breeding because mothers have a high probability effects, such as helping or breeding. of dying in the extended period for which offspring are dependent upon their care. Offspring that stay 12.3 Selection for helping behaviour to help their mother or join the nesting associations of same-generation females can provide insurance Helpers contribute to the rearing of offspring in a against the failure of the nest due to the death of variety of ways: assisting with nest construction, their mother or the dominant female on the nest provisioning of offspring, babysitting young, and (Gadagkar 1990; Queller 1994). In addition, insect defence of a nest or territory against conspecifics cooperative breeders frequently form social queues and predators. These behaviours involve measur- and can often gain greater direct fitness from queu- able survival costs or costs to attributes which are ing than they can from independent nesting (Field likely to correlate with direct fitness, such as mat- and Cant 2009b; Leadbeater et al. 2011). In some ing success or condition. A central challenge has socially polymorphic species (e.g. some halictine been to explain how these behaviours can evolve bees and Polistes species) individuals adopt a coop- and persist in populations despite these costs. Selec- erative or non-cooperative life history depending tion will favour alleles for helping behaviour only on latitude and length of the summer breeding sea- if the fitness costs are offset by benefits either to son. In the bee Halictus rubicundus, for example, the helper themselves or to other individuals in overwintering females transplanted from northern which copies of the ‘helping’ alleles reside. This to more southern latitudes switched from a solitary has led to four main hypotheses to explain help- to a cooperative life-history; bees transplanted in ing behaviour, the first two of which are usually the reverse direction switched to solitary breeding lumped together as forms of ‘kin selection’: 1) indis- (Field et al. 2010; Fig. 12.2). The key ecological vari- criminate helping may be favoured if dispersal is able in this case is the length of the summer season: limited so that the recipients of help are on average at the more southern latitudes foundresses can raise more closely related than the population at large two broods in a season rather than one, so that first (Hamilton 1964); 2) individuals may recognize kin brood offspring have the option to become helpers. and preferentially direct care towards them (Hamil- OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

210 THE EVOLUTION OF PARENTAL CARE

(a) (b) (c)

80

60 Peebles.

Belfas. t B 40 % Social nests

Wicklow. C 20

Su. ssex SO SOTR TR

Figure 12.2 Sweat bees (Halictinae) include both solitary and cooperatively breeding species, and in some species cooperative behaviour varies between populations. Females of Halictus rubicundus dig a nest burrow in spring. In southern Ireland, Halictus rubicundus (Wicklow, Eire) breeds cooperatively. Mated overwintering females dig a burrow nest in spring and produce a first brood of 5–7 offspring which remain to help their mother raise a second, larger brood of reproductives. In Northern Ireland populations (Belfast), nests are started later in spring and only one brood is produced per season, with no helping among offspring. Transplantation of overwintered females to southern and northern latitudes of Great Britain (a) resulted in females switching from cooperative to non-cooperative life-histories (b) and (c). Panel (b) shows the percentage of nests from the cooperative Wicklow population that became cooperative at the source site (SO) and at the site to which they were transplanted (TR). Panel (c) shows the results for the transplant experiment on the Belfast population. Reproduced from Field et al. (2010) with permission from Elsevier. ton 1964); 3) there may be immediate or delayed breeding may be very different from those that direct fitness benefits which outweigh the imme- select for cooperative behaviour in extant systems. diate fitness costs (Kokko et al. 2001); and 4) help- ing may be enforced by social punishment, so that 12.3.1 Demography and indiscriminate the alternative, not helping, results in even greater altruism fitness costs (Clutton-Brock and Parker 1995; Gas- ton 1978). It is important to recognize that these Altruistic traits can be favoured by natural selection hypotheses are not mutually exclusive: for example, if they satisfy Hamilton’s rule (Hamilton 1964) helping may benefit relatives while at the same time r B − C > 0 (12.1) result in direct fitness benefits to the actor. xy Given that the great majority of cooperatively In which C is the lifetime direct fitness cost to the breeding species are composed of groups of genetic focal bearer of a trait; B is the lifetime direct fit- relatives, mechanisms based on kin selection seem ness benefit to social partners resulting from the to offer a plausible and general explanation for the trait; and rxy is the coefficient of relatedness of evolution of helping behaviour. However, the dis- the focal individual x to its social partner y, that covery of hardworking, unrelated helpers in both is, their genetic similarity relative to the popula- insect (Leadbeater et al. 2010; Queller et al. 2000) tion mean (Hamilton 1964). Since costs and benefits and vertebrate (Clutton-Brock et al. 2000; Reyer are defined in terms of lifetime fitness effects, acts 1984) systems indicates that direct fitness benefits which involve immediate costs need not be altruis- or coercion must also be important in maintain- tic. For example, an actor who pays an immediate ing helping behaviour, at least in some systems. cost to help another is not behaving altruistically if Moreover, it is important to remember that the fac- this cost is repaid later, for example, through recip- tors that could have initially promoted cooperative rocation by the recipient. Failure to consistently OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 211 employ Hamilton’s definition of altruism in terms of the helping act. Note that this inequality can of lifetime fitness effects has caused much misun- equally be used to predict selection for ‘harming’ derstanding in the past, and is one of the sources of behaviour or traits, which are defined as traits that confusion underlying recent attacks on Hamilton’s reduce the fecundity of local breeders, such that b is theory (e.g. Nowak et al. 2010; but see Rousset and negative (Johnstone and Cant 2008; West et al. 2002).

Lion 2011 for a counter-critique). Note also that a Where competition is global rxe = 0 because dis- focus on Hamilton’s rule doesn’t mean ignoring the placed individuals are a genetically random sample > role of ecology in the evolution of cooperation, such of the population. When competition is local rxe as whether animals build a safe nest or live in sat- 0, and hence inequality (12.2) is harder to satisfy urated habitats. Factors such as these can raise the for a given (positive) b and c. In fact the first model benefits, B, and lower the costs, C, of helping, and to examine explicitly the consequences of local kin thereby favour the evolution of altruism (Alexander competition for the evolution of altruism (Taylor et al. 1991). 1992, building on the ‘infinite island’ population From the outset Hamilton recognized two dis- genetic model of Wright 1943) found that the posi- tinct ways in which altruism may evolve. First, tive effect of limited dispersal on selection for altru- actors might recognize and preferentially direct ism was exactly cancelled by the negative effects of help toward their genetic relatives. Second, and increased competition. In other words, according to more controversially, constraints on dispersal may Taylor’s model, Hamilton’s second mechanism for ensure that actors interact primarily with close the evolution of altruism didn’t work. kin. The problem with this second mechanism Subsequent theoretical work by Taylor and oth- is that limited dispersal (or population ‘viscos- ers has shown that this ‘cancelling’ result arises ity’) increases both average relatedness between because of the simplifying assumptions of the social partners and the intensity of local competi- model, and that incorporating plausible demo- tion for resources or reproductive opportunities. To graphic and life-history features (e.g. overlapping illustrate, suppose that an actor engages in some generations, sex-biased dispersal, budding disper- behaviour (such as guarding the nest, or provision- sal, individual variation in fecundity) recovers the ing young) which results in b extra offspring for a prediction that dispersal constraints select for help- recipient, at a cost of c fewer offspring for the actor. ing (Lehmann and Rousset 2010). Empiricists know As a consequence of the act, the overall change in that experimental manipulation of ecological con- the number of offspring produced locally is (b − c). straints can affect individual dispersal and help- Will this act be favoured by natural selection? If all ing decisions on a behavioural time scale (see Sec- these extra offspring disperse away from the patch tion 12.2 above)—what the new models suggest and compete with unrelated individuals, there are is that severe ecological constraints on dispersal no further fitness consequences of helping and the over many generations can favour the evolutionary bsandcs (which measure numbers of offspring) origin of local helping. Indeed, not only helping can be used as reasonable proxies for the Bs and Cs behaviour but any social trait which increases the in Hamilton’s rule (which measure lifetime fitness fecundity of local group members is more likely to effects) to determine the direction of selection on the evolve when there are strong dispersal constraints. helping act. If, however, there are constraints on dis- Two factors which promote the evolution of persal then extra offspring produced may remain indiscriminate altruism are particularly relevant to locally and compete with offspring to which the both insect and vertebrate systems: sex-biased dis- actor may be related (through local density depen- persal and budding dispersal. These are considered dent regulation). Selection will then favour helping below. if the following extended version of Hamilton’s rule is satisfied (Queller 1992): 12.3.1.1 Sex biased dispersal In most cooperative breeders one sex disperses − − − > rxyb c rxe(b c) 0 (12.2) more frequently, or further, from their natal patch where rxe is mean relatedness of the actor to the off- than the other (Lawson Handley and Perrin 2007). spring that are displaced by competition as a result Sex biased dispersal of this kind likely evolved as OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

212 THE EVOLUTION OF PARENTAL CARE a strategy to reduce inbreeding and its associated the strength of selection for helping and harm- deleterious effects, and because the advantages of ing across the lifespan (Johnstone and Cant 2010). philopatry are often different for males and females Specifically, local mating and male-biased disper- (Lawson Handley and Perrin 2007). But it also has sal, the demographic pattern exhibited by most profound consequences for the evolution of social cooperative mammals, results in females becom- behaviour in males and females, and hence social ing less closely related to local group members structure and mating system. as they get older, and hence stronger selection Johnstone and Cant (2008) extended Taylor’s for helping early in life compared to later. How- (1992) approach to explore how sex differences ever, two unusual (and different) demographic pat- in dispersal influence selection for ‘helping’ and terns result in the opposite pattern. Specifically, a ‘harming’ behaviour. They showed that where there pattern of female-biased dispersal and local mat- is a strong sex bias in dispersal, selection favours ing (thought to characterize ancestral humans), harming behaviour among adults of the dispers- and non-local mating with low dispersal by both ing sex; and in general favours helping among sexes (characteristic of pilot whales Globicephala adults of the philopatric sex. This prediction agrees spp and killer whales Orcinus orca, the two other with observations of dispersal and helping in coop- species which exhibit menopause), results in selec- eratively breeding birds and mammals, where in tion for early reproductive cessation and late life general it is the philopatric sex which provides helping. most help (Cockburn 1998; Russell 2004). In coop- eratively breeding cichlids, both sexes disperse 12.3.1.2 Budding dispersal and both sexes provide help (Stiver et al. 2004). The usual assumption of infinite island models is Extending the model to haplodiploid organisms that individual offspring disperse alone and join (Johnstone et al. 2012) show that male-biased dis- groups in which there are no other relatives present. persal, which is widespread in social Hymenoptera, Gardner and West (2006), however, explored selec- strongly selects for helping among females. Thus, tion for helping under ‘budding dispersal’, that is, incorporating sex biased dispersal and local compe- when juveniles disperse in groups. Budding dis- tition into Hamilton’s rule suggests that Hamilton persal is conducive to the evolution of helping (1964) was in fact correct in his original claim that behaviour because it decouples the positive and ‘family relationships in Hymenoptera are poten- negative consequences of dispersal: extra offspring tially very favourable to the evolution of reproduc- produced as a result of help can disperse away from tive altruism’. their parents (so avoiding competition with kin) but An important message of these models is that still form groups in which relatedness is high. not only behaviour but also life-history traits are This model helps to explain the evolution of shaped by kin selection in the same way as are acts group dispersal in cooperative insects and verte- of helping or harming. Decisions such as whether brates. In many species, young adults form dis- to breed or not and how many offspring to produce, persal coalitions to seek out or compete for vacant and life-history traits such as the rate of senescence, territories, or to take over existing groups. In will affect the fitness of other local group mem- acorn woodpeckers (Melanerpes formicivorus), for bers and thus constitute forms of indiscriminate example, helpers form sibling groups which com- help or harm. Consider, for example, the timing pete intensely for any reproductive vacancies that of reproduction. Where selection favours helping appear (Koenig et al. 1998; similar dispersal coali- early in life and harming later, females may gain tions are found in other cooperatively breeding from delaying reproduction and instead helping birds and mammals, e.g. Port et al. 2010; Sharp early in life; where the reverse is true, females may et al. 2008). Dispersal coalitions may also arise gain from early reproductive cessation and late- because multiple young adults are evicted by life helping, in other words, menopause (Cant and older dominant breeders (e.g. Cant et al. 2010). A Johnstone 2008). It turns out that sex biased dis- form of budding dispersal occurs in ‘independent- persal and patterns of mating interact to determine founding’ social vespid wasps of the genera Polistes, OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 213

Belonogaster, Mischocyttarus, Parapolybia,andRopa- the more common such markers became the less lidia, in which colonies are founded by multi- useful they would be in distinguishing kin from ple inseminated foundresses, independently of any non-kin (Crozier 1986). For genetic kin recognition workers (Gadagkar 1991; Reeve 1991). The bene- systems to work and to promote the evolution of fits of joining a dispersal coalition will depend on altruism requires that genetic ‘rarity’ is associated social structure and the distribution of reproduction with some other fitness advantage, such as resis- within groups, for example, whether breeding is tance to parasites or pathogens (Rousset and Roze monopolized by a single individual (as is the case in 2007). This may explain why known examples of most independent founding wasps) or shared more genetic kin recognition in mice and humans involve evenly among group members (as occurs in banded detection of similarity at major histocompatibility mongooses). The evolution of group dispersal may (MHC) genes which are highly polymorphic and also involve an element of positive feedback: once involved in immune function (Rousset and Roze group dispersal is common, dispersers may be 2007). selected to join larger coalitions which can compete Helpers may potentially be able to discriminate more effectively; or evictors selected to expel larger kin from non-kin using learned or genetic cues, but numbers of their offspring, but these benefits will do they use these cues when allocating help? In eventually be offset by the costs of elevated within- cooperative birds and mammals, some studies find group competition. Group dispersal in cooperative evidence of kin-directed care while others do not: breeders is a promising area for further theoret- across 9 species, variation in relatedness explains ical and empirical work, and may have hitherto 10% of the variation between helpers in the prob- unexplored impacts on individual behaviour, group ability of helping (Cornwallis et al. 2009; Griffin structure, and population dynamics. and West 2003). One result to emerge from these comparative analyses is that there is typically no relationship between relatedness and helping effort 12.3.2 Discriminate altruism: kin directed (as opposed to the probability of helping; Corn- care wallis et al. 2009; Griffin and West 2003). This sug- Kin discrimination should promote the evolution gests that the costs and benefits of helping are more of helping because Hamilton’s rule is easier to sat- important determinants of individual helping effort isfy if helpers can direct care towards more closely than is variation in relatedness (Cornwallis et al. related group members. In this case relatedness rxy 2009). is by definition higher than the average related- In cooperatively breeding insects, there is little ness to all potential recipients. Since the ability to evidence that helpers discriminate between kin and preferentially aid kin increases the inclusive fitness non-kin within groups. Typically helpers distin- pay-off of costly helping, we might expect selec- guish between nestmates and non-nestmates, but tion for mechanisms which enable helpers to single do not distinguish degrees of relatedness among out close relatives among members of their social nestmates (Keller 1997). In Polistes dominulus,for group. Helpers could learn to recognize kin if other example, 20–30% of helpers are non-relatives but factors ensured that individuals with whom helpers there is no difference between related and unrelated interact most frequently, or those in closest physi- helpers in foraging effort, nest defence, aggression cal proximity, were reliably genetically related. In or inheritance rank (Leadbeater et al. 2010; Queller cooperatively breeding birds, kin recognition is typ- et al. 2000). As with vertebrates, kin-biased helping ically based on cues that are learnt during develop- may not be favoured because of the costs of recog- ment in the nest (Komdeur et al. 2008). There is less nition errors. In insects that share a nest, there may evidence that genetic similarity can be recognized be few environmental cues to distinguish kin from directly and there are some theoretical difficulties non-kin. In paper wasps, for example, it has been with this idea. Selection could in principle favour argued that cues based on cuticular hydrocarbons the spread of ‘marker’ alleles which allow relatives (implicated in kin discrimination among larvae in to recognize and direct care toward each other, but solitary insects) may be unreliable since these can be OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

214 THE EVOLUTION OF PARENTAL CARE acquired from contact with the nest (Gamboa 2004). a good chance of inheriting breeding status, and However, recent studies have shown that unre- where large group size is associated with elevated lated helpers in Polistes dominulus have measurably survival or reproductive output—two conditions different hydrocarbon profiles (E. Leadbeater and which commonly hold in cooperatively breeding J. Field, personal communication). While cues to insects and vertebrates. The key assumptions to test discriminate kin exist, therefore, they are not used are 1) that helping leads to increased recruitment by wasps in helping decisions. and larger future group size, and 2) that a larger group size is beneficial to the direct fitness of helpers (Wong and Balshine 2011). Studies of insect 12.3.3 Direct fitness benefits and vertebrate cooperative breeders often report Examples of species with hardworking, unrelated an association between group size and breeder helpers (for example, Polistes dominulus, Leadbeater productivity, but do not show that helping per et al. 2010; Queller et al. 2000) suggest that help- se leads to elevated future fitness for helpers. In ing can also yield direct fitness benefits, and that paper wasps and hover wasps group augmentation in some cases these direct benefits alone may be benefits do not appear to be a major determinant sufficient to outweigh the fitness costs of help- of helper effort: helpers reduce their helping ing. When considering direct fitness benefits of effort as they get closer to inheriting, a pattern helping it is useful to distinguish those benefits which is opposite to that predicted by the group that are non-enforced or enforced (Gardner and augmentation hypothesis (Field and Cant 2007). In Foster 2008). In both cases helping is more prof- birds there is also scant evidence that variation in itable than non-helping, but in the case of enforced group augmentation benefits underlies variation in benefits it is the threat or action of social part- helping effort (but see Kingma et al. 2011 for one ners that reduces the pay-off of the non-helping such case). option. The prestige hypothesis suggests that helping evolves as a costly signal of quality, and that the 12.3.3.1 Non-enforced benefits costs of helping are offset by the fitness benefits Helping can be readily explained if it results in of improved mating access or dominance status some form of immediate or delayed direct fitness that result from this honest advertisement of qual- benefit which offsets the initial cost of the help- ity. Initial evidence for the hypothesis came from ful act. In this case helping is a form mutualism observations of Arabian babbler Turdoides squam- (Gardner and Foster 2008; West et al. 2007). Several iceps helpers competing with each other to help behavioural mechanisms which result in delayed (Carlisle and Zahavia 1986); although a subsequent benefits of helping have been proposed to operate study on the same species did not replicate this in cooperative breeders, including the acquisition finding (Wright 1999). The key predictions of the of parenting skills; the recruitment of offspring into prestige hypothesis are 1) that helpers should help the group which later become helpers themselves; more in the presence of an audience; and 2) that ele- and elevated social status or dominance (reviewed vated helping effort should causally increase social by Dickinson and Hatchwell 2004; Koenig and Wal- status or mating success. McDonald et al. (2008) ters 2011). The last two mechanisms have received tested the first of these predictions in cooperatively some theoretical attention under the terms ‘group breeding bell miners, but found that helpers did not augmentation’ (Kokko et al. 2001) and ‘prestige’ adjust their helping effort to the presence or absence (Zahavi 1995) respectively. of an audience (the breeding male or female). In An actor can gain group augmentation benefits if other species, helpers that invest most have a higher the extra offspring produced as a result of helping probability of obtaining breeding status, but this remain in their natal group and boost the actor’s may simply reflect variation in helper quality rather future survival or reproductive success (Kokko a causal link between helping and future mating et al. 2001). The delayed direct fitness of helping success (Cant and Field 2005). Overall, evidence for will be especially important where helpers have the prestige hypothesis is scarce. OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

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12.3.3.2 Enforced benefits In the paper wasp Polistes fuscatus, the removal Much theoretical interest in evolutionary biology or inactivation of dominant foundresses (by cool- has focused on the use of punishment and threats ing them) leads to reduced helper effort (Reeve to induce cooperation and helping (Cant 2011; Rat- and Gamboa 1987); and wing-clipping of subor- nieks and Wenseleers 2008). In the context of coop- dinate helpers leads to increased aggression from erative breeding, the pay to stay hypothesis (Gaston dominants (Reeve and Nonacs 1997), as expected 1978) suggests that dominants can exploit the gains if aggression is used to enforce help. A difficulty that subordinates derive from group membership with these studies is that the function of behaviours to charge ‘rent’ in the form of help. This mecha- classed as aggressive is often unclear. In Polistes nism is based on the use of a threat or ‘last move’ for example, ‘dart’ behaviour is usually classed as in the interaction: helpers work to rear the off- aggression but may instead serve as a cooperative spring of dominants to avoid expulsion from the signal to coordinate worker activity (Nonacs et al. group. When the threat is clear and credible, no 2004). In P. dominulus, dominants are often aggres- evictions will be observed, so an effective threat is sive to subordinates, but this appears to be linked a highly cost-effective means of social control (Cant to conflict over social rank rather than conflict over 2011). Alternatively, dominants might coerce sub- help (Cant et al. 2006). ordinates into helping via the use of punishment. In summary, patterns of helping in cooperative Punishment differs from threat in that it involves a breeders provide general evidence for Hamilton’s repeated interaction rather than a last move: domi- first mechanism based on indiscriminate altruism, nants might pay an immediate cost to punish a lazy namely that increasing constraints on dispersal and helper if this act induces the helper to reciprocate by the presence of relatives should promote helping working harder in the future. and inhibit harming behaviour. Inclusive fitness The key prediction of the pay to stay hypothe- models which incorporate demography and popu- sis is that experimental reduction of helper effort lation structure are also an important step toward should lead to eviction from the group. In splendid an evolutionary theory of ‘cooperative life history’. fairy wrens and cooperative cichlids, experiments Variation in relatedness does not correlate well with to temporarily remove subordinates helpers or helping effort within groups, which parallels find- reduce their helping effort typically led to increased ings on the relationship between parentage and aggression from dominants and higher rates of parental care (Chapter 11). There is little evidence subordinate helping thereafter (Balshine-Earn et al. that threats of eviction induce helping, although 1998; Bergmüller and Taborsky 2005; Mulder and dominants in some species do use punishment Langmore 1993). However, none of these experi- to enforce helping. In some cooperatively breed- mental manipulations led to helpers being expelled ing insects, helpers adjust their effort according to from the group, as would be expected if helpers their expected future fitness (Field and Cant 2009b). were induced to help because of the hidden threat However, more research is required to understand of eviction by dominants. individual variation in helping and, importantly, In other species, there is evidence that domi- variation in the consistency of individual contri- nants use aggression to activate lazy workers. In butions to helping (their ‘cooperative personality’ naked mole rats (Heterocephalus glaber), for example, Bergmuller et al. 2010; English et al. 2010). queens direct aggression (in the form of ‘shoves’) toward lazy workers to increase their activity level 12.4 Negotiation over help (Reeve 1992). In meerkats (Suricata suricatta), hard- working male helpers are subject to less aggression The preceding discussion highlights the evolution- from dominant breeders than lazy male helpers, ary conflicts that exist within cooperatively breed- and males that ‘false feed’ (i.e. bring food over ing groups over levels of investment. Coercion—via to a pup but then eat the item themselves) are punishment and threats—is one behavioural mani- subject to more aggression than those that do not festation of this conflict. In many species, however, engage in this behaviour (Clutton-Brock et al. 2005). coercion may be impractical or inefficient: in birds, OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

216 THE EVOLUTION OF PARENTAL CARE for example, the targets of punishment can fly away. (2011) adapted McNamara’s negotiation approach Nevertheless, individuals may be able to induce to show that helping may often benefit mothers others to help more by adjusting their own helping and fathers (via ‘load lightening’) as much as off- effort contingent on the helping effort of their social spring, so that relatedness of helpers to each parent partners, in a process of bargaining or ‘negotiation’. and the responsiveness of parents may be a more Negotiation is by definition a behavioural interac- important determinant of helping effort than aver- tion: a process of bid and counter-bid. By contrast, age relatedness to the brood. The predictions of this classic models of parental care exclude bargaining model have not yet been tested. Moreover, there because they solve for evolutionarily stable com- have been no tests of the assumptions or predictions binations of genetically specified fixed ‘sealed bid’ of any negotiation model in cooperatively breeding efforts, so called because it is assumed that play- insects. ers can’t change their effort after observing that of McNamara et al.’s (1999) model is an impor- their partner (Houston and Davies 1985). Sealed tant first step towards an evolutionary theory of bid models have the advantage of mathematical behavioural negotiation, but there are many other tractability, but their assumptions are at odds with forms that bargaining or negotiation might take. a wealth of evidence that animals typically observe Some biological interactions, for example, can be and adjust their helping effort to that of their thought of as consisting of a sequence of ‘moves’, social partners (Johnstone 2011; McNamara et al. in which one player commits to a level of invest- 1999). Allowing players to observe and respond to ment which is observed and responded to by their each other’s helping effort on a behavioural time social partners. For example, in birds and mammals scale can render sealed bid equilibria evolutionarily mothers effectively make a ‘first move’ by allocat- unstable, at least in cases where there is some vari- ing resources to the egg, while their mate (or a ation in individual efforts due to noise or variation helper) is placed in the role of a ‘second mover’ in quality (McNamara et al. 1999; Johnstone 2011). who must choose how much effort to invest after To address this issue, McNamara et al (1999) birth or hatching. Selection should favour moth- developed one type of ‘negotiation’ model (again in ers that adjust their investment in eggs accord- the context of biparental care) in which they solved ing to the amount of help their offspring will for evolutionarily stable levels of behavioural receive later (Russell et al. 2007). Empirical tests responsiveness or ‘rules for responding’, rather of this idea present an interestingly mixed picture. than evolutionarily stable fixed efforts. Where In splendid fairy wrens (Malurus splendens; Russell increasing investment brings diminishing produc- et al. 2007), carrion crows (Corvus corone;Canes- tivity returns, and each party has perfect informa- trari et al. 2011), and cooperative cichlids (Neo- tion about offspring need, the ESS rule for respond- lamprologus pucher; Taborsky et al. 2007), mothers ing is to partially compensate for changes in each reduce their investment in eggs when helpers are other’s effort levels. However, other response rules present, but in the wrens and crows this reduction (for example, effort ‘matching’, where an increased is offset by the investment received from helpers effort by one parent results in increased effort by post-hatching. By contrast, in acorn woodpeckers its partner) can be evolutionarily stable where par- (Melanerpes formicivorus), mothers do not decrease ents have incomplete information about the level of investment per egg when helpers are present, but offspring need, and use each other’s effort levels instead lay a greater number of eggs, so each off- to estimate this (Johnstone and Hinde 2006). Vari- spring is worse off overall (Koenig et al. 2009). A ation in how parents obtain information may help recent model by Savage et al. (in press) suggests to explain the range of responses to experimen- that these contrasting empirical patterns might be tal manipulation of parental effort that have been explained by variation in the personal fitness costs observed in biparental birds, including no change of increasing clutch size. Where clutch size is con- in partner effort level, partial or full compensa- strained by high costs of egg production, mothers tion, and effort matching (Hinde 2006; Chapter 9). are predicted to reduce their investment per egg, In the context of cooperative breeding, Johnstone and helpers to compensate for this reduction so that OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 217 each offspring receives greater resources overall. the concession model, and produced quite differ- Where clutch size is more flexible, females should ent predictions. For example, ‘incomplete control’ produce more eggs in the presence of helpers, to the models (Cant 1998; Reeve et al. 1998) assumed detriment of each individual offspring (a situation that no single individual had cost-free control over similar to the results found in acorn woodpeckers). the allocation of reproduction, but rather that both More work is needed to test the specific predictions dominants and subordinates could invest costly of the model, and to determine the general condi- effort to increase their share of reproduction; while tions for which mothers might gain from 1) produc- the ‘restraint’ model (Johnstone and Cant 1999) ing fragile offspring to attract compensatory care assumed that subordinate reproduction was limited from helpers; versus 2) producing hardy clutches, only by the threat of eviction from the group. These or perhaps a mixture of hardy and fragile young, and other models led to a confusing array of pre- when helpers are present. dictions and a tangled theoretical picture, at least initially. As Gardner and Foster (2008) put it:

12.5 Reproductive conflict From this simple beginning skew theory diver- Within cooperatively breeding groups there are sified into a comedy of additional models, each differing in their specific assumptions about the usually strong asymmetries in fitness between power of individuals, the information available, breeders and helpers which leads to evolutionary and whether and how individuals negotiate their conflict over reproduction, and often to intense reproductive share. competition among group members to monopo- lize reproduction (Cant and Johnstone 2009). Much The problem with skew research, however, does research over the last 30 years has focused on not lie in the diversification of models: as a rule understanding how this conflict is resolved, and the development of different models represents a the evolutionary causes of variation in the distribu- progression in the understanding of a natural sys- tion of reproduction, or the degree of reproductive tem, since models can only be rejected by com- skew, between groups and between species. Many parison with other models (Hilborn and Mangel researchers were drawn to working on reproduc- 1997; Lakatos 1978). In the case of skew theory, tive skew because there existed a simple candidate the various models can be classified into those that model which potentially applied very widely (the assume the resolution of conflict is influenced by ‘concession’ model; Reeve 1991; Vehrencamp 1983). threats to exercise ‘outside options’ (such as leaving This model assumed that a single dominant indi- the group, or evicting a competitor), versus those vidual controlled reproduction in the group, but that assume outside options are irrelevant. This that subordinates could use the threat of depar- distinction provides an opportunity to distinguish ture from the group to extract a reproductive con- between and eliminate models, and to clear away cession or ‘staying incentive’ from dominant indi- some of the theoretical tangle. viduals, at least in cases where the presence of The main problem with the research on subordinates boosted the reproductive success of reproductive skew has been a dearth of empirical dominants. Thus in this model the level of skew tests of the models’ assumptions, particularly in groups was determined by the inclusive fitness experimental tests. Two notable exceptions are value of ‘outside options’ to subordinates, that is, the experimental studies of Langer et al. (2004) their fitness pay-off should they choose to disperse (on a social bee Exoneura nigrescens)andHeget to breed elsewhere. The model suggested that vari- al. (2006) (on a cooperative cichlid Neolamprologus ation in skew both within and between species was pulcher), both of which manipulated the value of explicable by variation in three parameters: relat- outside options (i.e. breeding opportunities outside edness, ecological constraints, and the productivity the group) to subordinates to test whether this benefit of retaining subordinates. influenced the outcome of reproductive conflict. Starting in the 1990s a number of other mod- In both cases varying outside options had no els appeared which relaxed the assumptions of effect on skew, suggesting that threats of departure OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

218 THE EVOLUTION OF PARENTAL CARE do not determine the pattern of reproduction in for example through egg destruction, nest destruc- natural groups. In cooperatively breeding birds, tion, infanticide, and aggression (Cant 2012). An experimental suppression of paternity share (by important question is whether evolutionarily sta- removing males during the female’s fertile period) ble resolution of conflict always requires individ- has not been shown to lead to the departure of sub- uals to invest costly effort in conflict, or whether ordinates, as expected if the pattern of reproductive selection can favour less costly and more efficient sharing among males reflects a subordinate’s threat resolutions mechanisms. Theory suggests two ways of departure (Cant 2006). In banded mongooses in which evolutionary conflicts need not be man- (Mungos mungo), experimental suppression of dom- ifested in actual conflict: 1) through the use of an inant or subordinate breeders (using short-acting effective deterrent threat (Cant 2011; Cant et al. contraceptives) never leads to their departure from 2010); and 2) through mechanisms which make con- the group, or to the eviction of subordinates. Sup- flict investment unprofitable (Cant 2012). Threats pression does, however, trigger mass infanticide can lead to efficient conflict resolution because they shortly after birth. In banded mongooses, therefore, need only be carried out when the social rules it appears that low reproductive skew arises from they enforce are broken. For a threat (e.g. of depar- a ‘Mexican standoff’—any female that attempts to ture, eviction, or attack) to be effective in this monopolize reproduction is very likely to have her way requires effective communication and the abil- litter killed (see also Hodge et al. 2011; Fig. 12.3). ity to discriminate transgressors. Data from social Current evidence, therefore, suggests that the hymenoptera, social fish, and mammals indicates value or availability of outside options does not that such effective communication exists in some determine the level of reproductive skew within systems, because threats of attack or infanticide groups, although more experiments are needed. do successfully deter subordinates from breeding This fits with recent theory which suggests that out- or challenging the position of dominant (reviewed side options will be least relevant in groups of rel- in Cant 2011). In fish size hierarchies, for exam- atives and where the productivity benefits of asso- ple, dominant fish use the threat of eviction from ciation are high—exactly the conditions that apply the group to limit the growth and competitive to most cooperative breeders (Cant and Johnstone ability of subordinates, but conflict is resolved 2009). Rather, the outcome of reproductive conflict without them having to carry out this threat within groups appears to depend on the ability of (Cant 2011). one party to suppress the reproductive attempts Second, evolutionary conflict (i.e. a disparity of other group members, and the costs of these between the fitness optima of social partners; Chap- attempts at suppression. Consequently, the hope ter 9) may exist, but need not be manifested in costly that the simple framework offered by early skew or destructive acts. Outcomes featuring zero actual models could provide a universal explanation for conflict are possible when biological conflict takes variation in skew both within and between species the form of ‘suppression competition’ (for exam- seems to have faded. The spotlight has shifted to ple, infanticide, policing, mate guarding) in which understanding the evolution of conflict strategies success in competition depends on eliminating or within cooperative groups: how animals suppress nullifying the competitive acts of others. By con- each other’s breeding attempts, how conflicts are trast overt conflict is always expected in ‘produc- settled on a behavioural time scale, and why the tion competition’ where success depends on max- outcome of reproductive conflict is so variable. The imizing proportional effort or competitive acts (as study of ‘reproductive skew’ has therefore given is the case, for example, in biological ‘scrambles’; way to the study of ‘reproductive conflict’, which Chapter 8). To illustrate the biological distinction highlights conflict mechanisms that operate on a between production and suppression competition, behavioural time scale as well as evolutionary out- consider two female birds laying eggs in a shared comes, and the value of experiments over correla- nest. Where competition takes the form of a scram- tions (see also Chapters 7, 8, and 9). ble between offspring after hatching, each female’s In many cooperative species, reproductive con- fitness pay-off will depend on her proportional rep- flict is resolved in a costly and wasteful manner, resentation in the communal clutch. A female who OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 219

(a)

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0 0 First Middle Last Sync Async Birth order

Figure 12.3 Extreme birth synchrony and evidence of infanticide in banded mongooses. In this species most adult females breed in each breeding attempt and typically give birth on exactly the same day. (a) Frequency histogram of synchronous and asynchronous breeding attempts. Females give birth on the same day in 63% of breeding attempts. (b) Synchronous communal litters are less likely to fail in the den. (c) In those litters that are asynchronous, females that give birth first are very likely to fail in the first week compared to those that give birth last. This dependency of early pup survival on the pregnancy status of co-breeders is a signature of infanticide. Extreme birth synchrony in this species appears to be an adaptation to avoid infanticide and minimize competitive disparities between young. Reproduced with permission from Hodge et al. (2011). invests nothing in competition (i.e. lays no eggs) tion and shows that asymmetry in strength and is certain to get zero fitness pay-off. If, however, uncertainty about strength or conflict effort can pro- competition takes the form of infanticide after eggs mote peaceful resolution of evolutionary conflict, are laid, females who invest nothing in infanticide even among unrelated individuals (Cant 2012). The may still achieve some reproductive success, partic- level of information in the contest has a strong ularly if egg discrimination is not perfect. A recent effect on the costliness of behavioural conflict res- model explores this type of suppression competi- olution, and can be expected to shape signalling OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

220 THE EVOLUTION OF PARENTAL CARE strategies and dominance interactions (e.g. Chap- can result in heritable changes in patterns of gene ters 7 and 8). Experiments to manipulate the status expression in adulthood, but much less is known quo distribution of reproduction to reveal hidden about these mechanisms in wild populations and threats, or to alter the level of uncertainty about their ecological and evolutionary significance (Boss- relative strength, would help to test these models dorf et al. 2008). For example, the level of invest- in the context of reproductive conflict and conflict ment received in early life offers a strong candi- over parental care. date explanation for observed differences in later life-history and the consistency of contributions to helping in some cooperatively breeding species 12.6 Conclusion and future research (e.g. English et al. 2010). Moreover, individuals that Cooperative breeding species are excellent subjects receive greater investment when young may be for research on the evolution of parental and allo- more or less likely to help themselves as adults, or parental care; how cooperation evolves; and the more or less likely to disperse from the group, lead- behavioural mechanisms by which animals resolve ing to positive or negative feedback in the quality conflicts and exercise control over each other’s of early versus late cooperative environments and behaviour. A recurring theme of this chapter is potentially dramatic impacts on group stability and the need for more experimental tests of models of population dynamics over time. helping and reproductive conflict. Any proposed Third, there is much scope for research on the behavioural mechanism of social control (such as behavioural processes by which animals resolve punishments or threats) can only be investigated conflict over reproduction and helping. For exam- rigorously through the use of manipulation exper- ple, low-level social aggression is a conspicuous iments. Manipulations of this type are often chal- feature of animal societies, but the function of lenging logistically, but without them there is a dan- aggressive interactions is often unclear. Are aggres- ger of developing a biased and inaccurate picture sive dominants advertising their strength to deter of the forces sustaining cooperation and resolving subordinates from challenging their status? Does reproductive conflict in natural systems. For exam- submissive behaviour serve to conceal a subordi- ple, where threats of attack or infanticide are effec- nate’s true strength or motivation to challenge dom- tive, observed acts of aggression may be just the inants? How frequently should dominants interact tip of the iceberg of forces influencing behaviour with subordinates to maintain their social status, in cooperative groups. Detecting hidden threats and how often should subordinates probe domi- requires experiments to disturb the status quo. nant strength? Research on these questions would There are many promising areas for future help to understand why some societies are peaceful research; I mention four here. First, detailed lon- while others are overtly fractious, and how social gitudinal studies of cooperative animals in their conflict influences the evolution of cognitive and natural environment provide an opportunity to neural processes such as individual recognition and investigate selection on aging in highly viscous social memory. populations. Field studies have an enormous Fourth, current research is starting to reveal advantage over laboratory studies to address these the neural and hormonal mechanisms controlling questions because key life-history trade-offs might cooperative behaviour, and how these mechanisms only be manifested in an environment where indi- are themselves shaped by natural selection. This viduals are exposed to their natural predators, par- is helping to break down the traditional barriers asites, and pathogens. between studies of proximate mechanism and ulti- Longitudinal studies of cooperative breeders mate function. This barrier can be traced to an influ- also offer unparalleled opportunities to examine ential paper by Tinbergen (1963) which divided transgenerational effects and epigenetic inheritance research questions into four categories (sometimes under natural conditions (see also Chapters 14 and called the ‘four whys’): physiological causation, 17). Studies of laboratory rodents have revealed development, evolutionary history, and adaptive mechanisms by which pre- and post-natal care value. However, in that paper Tinbergen was at OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

COOPERATIVE BREEDING SYSTEMS 221 pains to point out that these four research foci bird. Proceedings of the Royal Society B-Biological Sciences should be viewed as complementary and their pro- 277, 3233–28. tagonists united by a common aim, that is, to under- Bergmuller, R., Schurch, R., and Hamilton, I. M. (2010). stand why animals behave in the way that they do. Evolutionary causes and consequences of individual ‘Cooperation between all these workers is within variation in cooperative behaviour. Philosophical Trans- actions of the Royal Society B 365, 2751–64. reach’, he wrote, ‘and the main obstacle seems to Bergmüller, R. and Taborsky, M. (2005). Experimental be a lack of appreciation of the fact that there is manipulation of helping in a cooperative breeder: a common aim’. In cooperative breeding species, helpers ‘pay-to-stay’ by pre-emptive appeasement. Ani- research on physiological mechanisms would help mal Behaviour 69, 19–28. to understand the proximate control of helping, Boomsma, J. J. (2009). Lifetime monogamy and the evolu- punishment, winner–loser effects, and reproductive tion of eusociality. Philosophical Transactions of the Royal suppression (see also Chapter 3). All of these social Society B-Biological Sciences 364, 3191–207. responses have large impacts on inclusive fitness Bossdorf, O., Richards, C. L., and Pigliucci, M. and hence the mechanisms controlling their devel- (2008). Epigenetics for ecologists. Ecology Letters 11, opment and expression are subject to selection and 106–15. will be shaped by the social and ecological envi- Bourke, A. F. G. (1999). Colony size, social complexity and reproductive conflict in social insects. Journal of Evolu- ronment. Research programmes which blend evolu- tionary Biology 12, 245–57. tionary theory, life-history analysis, and investiga- Bourke,A.F.G.(2011).Principles of Social Evolution. Oxford tion of physiological mechanism offer exciting pos- University Press, Oxford. sibilities to advance knowledge about cooperation Canestrari, D., Marcos, J. M., and Baglione, V. (2011). and parental care. Much of this information may Helpers at the nest compensate for reduced maternal be relevant to ourselves: after all, our morphology, investment in egg size in carrion crows. Journal of Evolu- physiology, fertility, rate of senescence, and long tionary Biology 24, 1870–8. period of offspring dependency all reflect an evo- Cant, M. A. (1998). A model for the evolution of repro- lutionary history of cooperative breeding, not more ductive skew without reproductive suppression. Animal recent technological developments. Behaviour 55, 163–9. Cant, M. A. (2006). A tale of two theories: parent-offspring conflict and reproductive skew. Animal Behaviour 71, Acknowledgements 255–63. Cant, M. A. (2011). The role of threats in animal coopera- Thanks to Jeremy Field, Mathias Kölliker, Nick tion. Proceedings of the Royal Society B-Biological Sciences Royle, Andy Russell, Michael Taborsky, and an 278, 170–8. anonymous referee for helpful comments. Fund- Cant, M. A. (2012). Suppression of social conflict and evo- lutionary transitions to cooperation. American Naturalist ing was provided by a Royal Society University 179, 293–301. Research Fellowship. Cant, M. A. and Field, J. (2001). Helping effort and future fitness in cooperative animal societies. Proceedings of the Royal Society of London Series B-Biological Sciences 268, References 1959–64. Cant, M. A. and Field, J. (2005). Helping effort in a domi- Alexander, R. D., Noonan, K. M., and Crespi, B. (1991). The nance hierarchy. Behavioral Ecology 16, 708–15. evolution of eusociality. In P. W. Sherman, J. Jarvis, and Cant, M. A., Hodge, S. J., Gilchrist, J. S., Bell, M. B. V., R. D. Alexander, eds. The Biology of the Naked Mole Rat. and Nichols, H. J. (2010). Reproductive control via evic- Princeton University Press, Princeton. tion (but not the threat of eviction) in banded mon- Balshine-Earn, S., Neat, F. C., Reid, H., and Taborsky, M. gooses. Proceedings of the Royal Society of London B 277, (1998). Paying to stay or paying to breed? Field evidence 2219–26. for direct benefits of helping behavior in a cooperatively Cant, M. A. and Johnstone, R. A. (2008). Reproductive breeding fish. Behavioral Ecology 9, 432–8. conflict and the separation of reproductive generations Bell, M. B. V., Radford, A. N., Smith, R. A., Thompson, in humans. Proceedings of the National Academy of Sciences A. M., and Ridley, A. R. (2010). Bargaining babblers: of the United States of America 105, 5332–6. vocal negotiation of cooperative behaviour in a social OUP CORRECTED PROOF – FINAL, 12/7/2012, SPi

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