Eco-evolutionary routes towards animal sociality
Ma, Long
DOI:
10.33612/diss.160350920
IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below.
Document Version
Publisher's PDF, also known as Version of record
Publication date: 2021
Link to publication in University of Groningen/UMCG research database
Citation for published version (APA):
Ma, L. (2021). Eco-evolutionary routes towards animal sociality: Ecology, behaviour and communication in communal breeding of burying beetles. University of Groningen. https://doi.org/10.33612/diss.160350920
Copyright
Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons).
Take-down policy
If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim.
Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum.
Chapter 8
General discussion and synthesis
The evolution of animal sociality is a biological mystery that has puzzled ecologists for centuries. Unravelling social evolution requires us to understand one of main topics: how ecological, social and genetic factors jointly determine the process of animal societies and the underlying eco-evolutionary routes from solitary to sociality (e.g. group living and reproducing) in animals (Vehrencamp, 2000; Riehl and Strong, 2015; Kramer and Meunier, 2019). In some highly advanced societies, there is a strict division of labour among group members, with an extremely-skewed partitioning of reproduction (Lin and Michener, 1972; Langer et al., 2004). Communally or cooperatively breeding systems may represent the early stages of animal sociality. In these groups, individuals permanently or temporarily live and reproduce together, of which benefits are induced by kinship, ecological constraints and other fitness benefits of grouping (Scott, 1998; Hayes, 2000; Vehrencamp, 2000; Gilchrist et al., 2004). Each group member is expected to obtain enhanced fitness benefits from living in groups (Bourke and Heinze, 1994; Field and Brace, 2004; Cant, 2012). Understanding the ecology and behaviour of the communal or cooperative breeding systems will contribute to our understandings of social evolution in animals and humans.
In this thesis, using the European burying beetle, Nicrophorus vespilloides, I address three key evolutionary issues: (i) the eco-evolutionary process that drives the evolution of social groups and (ii) the associated benefits and costs for groups and group members, and (iii) how complex social interactions are organized in such groups, potentially via communication systems (Figure 8-1, Research summary of the thesis). Burying beetle individuals utilise ‘bonanza’ carcasses as breeding resources that are needed for their offspring and themselves, and provide extended care towards developing offspring on the buried carcasses (Scott, 1998; Parker et al., 2015). Intriguingly, these beetles can breed as pairs and also can form groups by sharing a single carcass (that is, communal breeding). These biological features make burying beetles as an outstanding model for studying the evolution of animal sociality. In Chapter 2, I explored the underlying ecological process that shape the formation of social groups (e.g. cooperative and communal breeding), by investigating the impact of several ecological and intrinsic factors on the occurrence of group living and the associated benefits and costs for groups and for each group member. To clarify the effect of individual intrinsic conditions (e.g. breeding experience) on benefits and costs of group living, I examined in Chapter 3 whether and how dominant and subordinate individuals change their behaviour depending on the prior breeding experience of themselves and other group members in communal groups. Subsequently, I tested the combined effects of breeding experience and dominance status on the reproductive outcome of groups, and verified whether these effects were associated with the direct benefits and costs from previous breeding attempts. In Chapter 4, I conducted experiments to examine the implications of communal breeding at the level of individuals on immediate fitness benefits (e.g. reproductive success and outcome during the communal breeding compared to pair breeding), as well as its carry-over effects on future fitness, including future parental investment and reproductive outcome. In communal breeding of burying beetles, where there is a tug-of-war competition over resources and reproduction, none of the group members is able to fully control the reproduction of the others. However, each group member is expected to pay fewer costs and/or gain more benefits from mutually tolerating each other (Eggert et al., 2008; Komdeur et al., 2013; Liu et al., 2019). To explore the underlying mechanism of such mutual tolerance between dominant and subordinate individuals, I examined in Chapter 5 whether subordinates pay by helping, to stay within groups (‘pay-to-stay’), and whether dominants pay costs from having subordinates (‘pay-from-staying’). In social groups, it has been suggested that a well-coordinated organization in behaviour of individuals benefits the resolution of conflicts over resources and reproduction, which mainly relies on communication systems, such as chemical cues/signals (Ratnieks et al., 2006). In Chapter 6, I analysed CHC profiles of individuals that varied in parenting and dominance status, and experimentally examined
whether these potential chemical signals are involved in determining mutual tolerance interactions in groups where individuals compete for limited resources and are able to reproduce. Also, I profiled the expression patterns of genes that are co-opted to influence individual behaviour, such as parenting behaviour and aggression, to understand the underlying molecular mechanisms of such mutual tolerance in communal groups. In this general discussion (Chapter 8) I review and discuss my research findings on the communal breeding and chemical communications in burying beetles and provide avenues for future studies.
Figure 8-1. Research summary of the thesis. Ecology, behaviour and communication systems of
communal breeding in burying beetles. (i) Ecological and intrinsic factors favouring the formation of groups; (ii) dominance hierarchy and mutual tolerance (including three behavioural precursors) in social groups; and (iii) limited control of reproduction in groups, including behavioural control/strategies and chemical control/signals.
1|Ecological and intrinsic factors influencing the formation of
groups
In many animal species, where individuals may facultatively form social groups, numerous studies have highlighted the importance of ecological forces for the formation of group living and reproduction (Lin and Michener, 1972; Heg et al., 2004). As one of the hypotheses, the ecological constraint hypothesis offers a satisfactory explanation for the formation of group living and enables us to understand underlying ecological processes that shape the formation of social groups in animals (Hatchwell and Komdeur, 2000; Heg et al., 2004; Stiver et al., 2006). Given that the costs of solitary living are high due to ecological factors, such as high predation risk or intense competition for resources, selection favours individuals that join or breed in a group because of enhanced fitness benefits for overall groups and each individual group member (Emlen, 1982; Brockmann et al., 1997; Ebensperger et al., 2012). Burying beetles offer an outstanding model for studying the formation of social groups as these beetles can breed as pairs or may facultatively form groups consisting of more than one pair (Trumbo and Fiore, 1994; Scott, 1998). Their life cycles and reproductive chances are strictly dependent on the availability of carcasses that are needed for developing offspring and themselves (Trumbo and Fiore, 1994; Liu et al., 2019). Previous studies on burying beetles have documented the importance of ecological forces, such as resource availability and population density, on group formation (Wilson and Fudge, 1984; Eggert and Müller, 1992; Liu et al., 2020). Some studies suggest that such groups may be maintained by mutualistic benefits, such as improved defence of a large carcass against intruders (Trumbo and Fiore, 1994; Komdeur et al., 2013; Sun et al., 2014; Chen et al., 2020). Furthermore, our study on burying beetles clarifies how ecological processes may promote group formation and determine the benefits and costs of group living (Chapter 2). First, we found that the likelihood of carcass detection and occupation by burying beetles was positively influenced by carcass availability (i.e. carcass size) and low interspecific competition (i.e. competition with fly maggots and Scarab beetles). These results demonstrate that, in burying beetles, individuals may be more likely to detect and occupy larger carcasses. Intraspecific aggregation likely occurs on larger carcasses because they are smellier than smaller carcasses (Trumbo, 1992; Trumbo and Fiore, 1994; Scott, 1998; Royle and Hopwood, 2017). Second, during the process of group formation, we found that individuals were more likely to stay within a group of conspecifics when carcasses were large, and when interspecific competition was low (i.e. the carcasses were not infested with fly maggots). A potential explanation of these findings is that an individual’s decision to stay with a carcass is largely influenced by the amount of direct reproductive benefits that an individual may gain, where large carcasses provide more resources, and individuals may benefit more in the absence of interspecific intruders (Eggert and Sakaluk, 1995; Chan et al., 2020). However, it seems that burying beetles have no enhanced group defence against fly maggots by forming groups if usurpation of the carcass by fly maggots is high (Scott, 1994; Sun et al., 2014; Chan et al., 2020). If groups have a low probability to reproduce successfully, e.g. when the carcass is occupied by fly maggots, a behavioural transition occurs for burying beetles, where individuals are more likely to disperse from such groups and search for a new carcasses that are more suitable for reproduction (Hopwood et al., 2014; Royle and Hopwood, 2017). These findings support the ecological constraint hypothesis (Trumbo and Wilson, 1993; Hatchwell and Komdeur, 2000; Komdeur et al., 2013; Liu et al., 2020), indicating that limited resource availability (e.g. carcass size) and ecological constraints of independent breeding (e.g. the intensity of inter-specific competition) promotes the occurrence of group living through resource sharing. It also reveals the importance of considering potential ecological factors when studying the evolution of social behaviour.
In animals, not only ecological forces but also intrinsic forces such as body size and breeding experience may drive group formation and group living (Hatchwell and Komdeur
2000; Ebensperger and Cofré, 2001; Heg et al., 2004; Bergmüller and Taborsky, 2010). Our study shows that in burying beetles an individual’s decision to stay with a group is influenced by its absolute size and the relative size compared with others. Such a decision is also associated with the timing of breeding during the reproductive episode (i.e. before or after larvae hatching)(Chapter 2). In particular, when competing for a carcass with inter- and intraspecific intruders, and before larvae hatching, larger individuals are more likely to abandon their current carcass and disperse from the group, but after the larvae hatch they are more likely to stay with their current broods, compared with smaller individuals. These results may be due to size-dependent individual specialization in resource use (Bergmüller and Taborsky, 2010; Hopwood et al., 2016). It can be that small individuals may benefit more from joining a group (e.g. sharing resources with other) than large ones, because small individuals have little preference for the size of a carcass. However, large individuals are expected to reject very small carcasses or larger carcasses that need to be shared with others, and are more likely to breed solitarily (Ward et al., 2009; Hopwood et al., 2016). This may be due to a difference in resource-holding potentials for individuals (Scott, 1994; Eggert and Sakaluk, 2000; Bergmüller and Taborsky, 2010). These findings suggest that the variation in body size influences an individual’s decision to stay within groups; smaller individuals are likely to reproduce together through group breeding due to high costs of solitary breeding, for example, when carcass availability is limited and the intensity of interspecific competition is high, while large individuals are favoured to breed independently (Scott, 1998; Müller et al., 2007; Hopwood et al., 2015; 2016). Such differences in choosing a specific carcass that is suitable for breeding may resolve intraspecific competition for resources through effects of niche specialization (Bergmüller and Taborsky, 2010; Royle and Hopwood, 2017). Hence, we suggest that such niche specialization associated with the size distribution of individuals can determine the individual variation in reproductive decisions, which may favour the reduced costs of within-species competition for resources and reproduction (Hopwood et al., 2014; Royle and Hopwood, 2017). Also, our results found that when competing for carcasses with others, each individual was more likely to stay in groups when its size relative with others was smaller. This suggests that there is a higher probability of being expelled by others (e.g. focal, dominant individuals) in larger individuals than in smaller ones, because for burying beetles larger competitors with high resource potentials (RHPs) may pose a greater threat to individuals that are dominant in carcass use, and are more likely to challenge their dominance positions compared with smaller competitors (Scott, 1998; Boscolo et al., 2011; Hopwood et al., 2015b). Although dominant individuals could largely monopolize the carcass, evicting others from the carcass or suppressing their reproduction are considerably costly (Eggert and Müller, 1992; Scott, 1998). It is likely that focal individuals show a higher acceptance towards or a lower eviction towards small individuals than large ones, by which each group members could mitigate the escalation of group conflicts in resources and reproduction, with a stable relationship in groups (Eggert and Müller, 2000; Komdeur et al., 2013; Liu et al., 2020). Therefore, our results support that for burying beetles, each individual’s decision to stay in groups or not is jointly influenced by its own size and the size of others, because this is a combined result of individual’s decision (i.e. join a group or disperse), as well as the decision of other group members (i.e. being accepted or expelled). However, the impact of intrinsic factors, including body size, on group membership decision needs to be more investigated.
It is well known that animal individuals can gain a range of experiences while interacting with others, such as fighting/contest and breeding experience (Hsu et al., 2006; Walling et al., 2008; Garcia et al., 2014). Variation in such experiences plays an important role in affecting an individual’s contesting ability and/or outcome and reproductive performance (Byholm et al., 2011; Benelli et al., 2015). Previous studies on burying beetles have demonstrated the impacts of prior contest, breeding and social experience on an individual’s aggressiveness and its parenting performance (Walling et al., 2008; Lee et al., 2013; Pilakouta et al., 2016). For
example, In N. vespilloides, the prior social experience of males significantly influences their contest behaviour but these changes in behaviour have no direct influence on contest outcome, where males with prior social experience have higher encounter rates than naive males while the intensity of aggression is similar for experienced and naive males (Lee et al., 2014). Also, in this species, a female’s prior contest experience, irrespective of its contest outcome, has a positive influence on the amount of care provided, and its reproductive outcome; both winners and losers spend increased time on food provisioning to their offspring and have enhanced benefits in reproduction (i.e. larger broods of offspring) compared to females with no contest experience (Pilakouta et al., 2016). Experienced females that have cared for a small brood are more successful when competing for a second carcass against a virgin competitor than females that have cared for a large brood (Richardson et al., 2020). This is due to the costs of previous reproduction which may affect the difference in competitive ability (Creighton et al., 2009; Richardson et al., 2020).
Our experimental studies showed the combined impact of prior breeding experience and dominance status on individual aggressiveness and reproductive performance in communal groups (Chapter 3). These findings highlight the importance of prior breeding experience of focal individuals and their group members in mediating social interaction in groups, by which individuals are better able to resolve the conflicts of interests over resources and reproduction. In particular, for both dominant and subordinate individuals in groups, prior breeding experience has no effect on their aggressiveness and the amount of time providing care on the carcass, while experienced dominants and subordinates present in the same group lose more weight compared to inexperienced individuals of both categories. Furthermore, dominants that are in a group with subordinates with prior breeding experience have fewer injuries than when in a group with inexperienced subordinates, as experienced subordinates may have a reduction in competitive ability when competing for a carcass with others. Compared to groups where subordinates are inexperienced, communal groups where subordinates are experienced have enhanced fitness benefits in reproduction (larger broods at larval dispersal). This may be due to the fact that experienced subordinate pairs show a reduced parental effort compared to inexperienced subordinate pairs. This result suggests that experienced individuals may be better able to avoid the escalation of aggressive interaction, while such an effect is not associated with the direct benefits and costs of previous reproduction for each individual. Moreover, we suggest that when there is a fierce competition for resources and reproduction, dominant individuals may obtain more benefits or pay fewer costs from having experienced subordinates, while this should be further studied in the future. In such groups, the influence of the prior breeding experience of focal individuals and their group members on an individual’s decision in aggressiveness and reproductive performance may act via self-assessment, as well as social-assessment (Creel et al., 1992; Cotter et al., 2011; Lee et al., 2013; Huchard et al., 2016). First, individuals that breed in groups could change their reproductive performance depending on their prior breeding experience (‘self-assessment’; Dietemann et al., 2008; Lee et al., 2013). In our study, even though both dominant and subordinate individuals with prior breeding experience spend a similar amount of time providing care as inexperienced individuals, they lose more weight than inexperienced individuals. Experienced subordinate pairs of individuals show a reduction in the amount of time spent on the carcass compared to inexperienced ones, while this difference is absent for dominant pairs. Second, we suggest an effect of prior breeding experience in mediating the levels of aggression and reproductive performance via social cues (‘social-assessment’; e.g. the presence of others and/or their prior experience), and this may reflect a competitive interaction over resources between individuals. In groups, there is a negative correlation in the access towards the resources (i.e. carcasses) between dominant and subordinate individuals. This may be due to the fact that dominants are able to restrict the access to the carcass of others (Eggert and Müller, 1992; Komdeur et al., 2013; Liu et al., 2019). In animals, including
burying beetles, individuals are supposed to obtain the ability to acquire and process social information while reproducing (Ward and Hart, 2003; Haberer et al., 2010; Cotter et al., 2011; Lee et al., 2013). Furthermore, the acquisition of social experience develops the variation in the behavioural decision of individuals, which may favour the evolution of social behaviour in animals (Faulkes and Abbott, 1993; Clutton-Brock, 1998; Eggert et al., 2008).
2|Benefits and costs of group-living and -breeding
Among conspecific individuals, group living and reproducing is largely promoted and maintained by non-kin selected benefits through either reciprocity or mutualism (Creel and Creel, 2001; Watts, 2002; Clutton-Brock, 2009). In such cases, unrelated individuals are expected to gain enhanced fitness benefits from living and reproducing in groups, such as the cooperative defence of territories and resources (Heinsohn and Packer, 1995; Crofoot and Gilby, 2012), and reduced workloads in parental effort (Hayes, 2000; Clutton-Brock, 2002). Prior work suggests that in burying beetles the formation of communal groups is associated with high costs of solitary breeding because of a limited availability of reproductive chances for each individual (Wilson and Fudge, 1984; Eggert and Müller, 1992; Liu et al., 2020), while individuals could gain mutualistic benefits from breeding in groups, such as a joint defence of a large carcass against conspecific and heterospecific intruders (Trumbo and Fiore, 1994; Sun et al., 2014; Chen et al., 2020). In contrast, our results showed that the probability of group formation and group living occurred more frequently on larger carcasses, whereas the reproductive success (e.g. probability of larvae hatching and dispersing) was similar for group and solitary breeding in the field and laboratory conditions (Chapters 2 and 4). The allocation of reproduction between individuals of a group should be further investigated in the field. Also, reproductive costs were associated with group reproduction, i.e., the per capita number of larvae produced was lower for individuals that reproduced in groups than individuals breeding as pairs (irrespective of the effect of carcass size). For burying beetles, living in groups can be costly in terms of reproduction because communally breeding females may produce fewer offspring than females that breed solitarily (Müller et al., 1990; Richardson and Smiseth, 2020). These findings are consistent with previous studies on burying beetles, where enhanced benefits in reproduction does not occur in group breeding compared to solitary breeding (Trumbo and Wilson, 1993; 2016; Komdeur et al., 2013; Sun et al., 2014). Our study provided no support for the ‘mutualistic benefits hypothesis’, which indicates that individual burying beetles benefit from group breeding through the improved defence of large carcasses against interspecific intruders (e.g. fly maggots)(Eggert and Sakaluk, 2000; Sun et al., 2014). Even though an individual’s prowess in carcass defence differs across species of burying beetles, and is associated with individual body size, the probability of successfully defending the carcass against fly maggots is negatively related to discovery time and population density (Trumbo and Wilson, 1993; Trumbo, 2016). However, the benefits and costs of breeding in groups can differ across species of burying beetles (Komdeur et al., 2013; Sun et al., 2014). InN.tomentosus, individuals that breed in groups have enhanced benefits in carcass defence against flies and reproduction compared to individuals that breed in pairs (Scott, 1994; 1998), whereas these benefits are not found in N.vespilloides (Scott, 1998; Komdeur et al., 2013). Also, our studies support the hypothesis that a tolerance interaction occurs between individuals that are enforced to share a carcass with others, especially when carcass availability is limited (‘mutual tolerance hypothesis’), which may mitigate the costs of aggression within groups, such as fierce fights and evictions from carcasses (Eggert and Müller, 1992; Trumbo and Fiore, 1994; Liu et al., 2020). Moreover, communal breeding can be considered as a best-of-a-bad-job situation where burying beetle individuals only do so if they would otherwise not achieve any reproductive success and individuals are unable to reject others from the carcass (Eggert and Sakaluk, 2000; Komdeur et al., 2013; Sun et al., 2014; Liu et al., 2020). This may be due to large carcasses becoming ‘reproductive arenas’ that could
offer more opportunities to forage or reproduce due to the low competition (Eggert and Sakaluk, 2000; Gilchrist et al., 2004; Hodge et al., 2011).
Our results show experimental evidence that there are no immediate fitness effects of communal breeding on reproductive outcome and mortality, but there are carry-over effects on reproduction and costs in terms of mortality (Chapter 4). Such carry-over effects are different for males and females in the subsequent reproductive attempts. In particular, during the subsequent reproduction as pairs, males that have originated from communal groups gain enhanced benefits in reproduction compared to males that have originated from non-communal groups. However, females that originate from communal groups show worse reproductive performance (i.e. lower rates of carcass burial) and produce larvae that hatch and disperse later, compared to females that originate from non-communal groups (i.e. pairs). Such difference with respect to carry-over effects may be due to males being able to save more resources than females (Ward et al., 2009; Chemnitz et al., 2017; Richardson and Smiseth, 2020). In burying beetles, individuals are expected to gain benefits from access to carcasses, because feeding from it may offset the energetic costs of reproduction and save more resources for future reproduction (Creighton et al., 2009; Chemnitz et al., 2017; Richardson et al., 2018). Our results demonstrate that the effects of communal breeding on fitness are not only associated with immediate costs and benefits, but also with carry-over effects on future fitness. Such effects are more pronounced for males than for females; higher carry-over effects on fitness benefits are observed for males than females. This may be due to sex differences in the allocation of parental effort between current and future reproduction (Pilakouta et al., 2016; Richardson et al., 2020). More specifically, males may reduce investment to current broods and allocate more resources to future reproduction if paternity is uncertain (Neff and Gross, 2001; Richardson and Smiseth, 2020), whereas communally breeding females are found to shift their resource allocation towards eggs (i.e. lay more and larger eggs) and have reduced post-hatching care to larvae compared with females that breed alone (Richardson et al., 2020; Richardson and Smiseth, 2020). Moreover, this sex difference in the allocation of parental care is influenced by sexual conflict and intraspecific competition during communal breeding (Ward et al., 2009; Lee et al., 2014; Eggert and Müller, 2011; Richardson and Smiseth, 2020). First, sexual conflict leads to sex difference in a trade-off between parental investment in current and future reproduction (Houston and Davies, 1985; Mattey and Smiseth, 2015; Richardson et al., 2020). Second, intraspecific competition in communal breeding may lead to a difference in the future fitness between females and males because males are able to save resources that could be allocated to future reproduction and enhance future benefits (Ward et al., 2009; Pilakouta et al., 2015; 2016). Furthermore, such difference in a trade-off between current and future reproduction may give rise for sexual conflict in communal breeding (Boncoraglio and Kilner, 2012; Richardson and Smiseth, 2020).
3|Social interaction and group organization in communal
breeding - ‘tug-of-war’ competition
In many social animals, individuals are expected to obtain enhanced fitness benefits by forming temporary or permanent groups, where individuals share common resources and live and reproduce together (Ratnieks et al., 2006; West and Ghoul, 2019). However, conflicts over resources and reproduction also occur in such groups, and such conflicts could incur different costs for each group member (Clutton-Brock and Parker, 1995). To reduce the costs of group living, especially when resource availability is limited, individuals may adjust their behavioural strategy, for example, a high level of aggression towards each other and eviction (i.e. direct eviction and the threats of eviction)(Aureli et al., 2002; Stephens et al., 2005; Fraser and Bugnyar, 2011). In communal breeding groups of burying beetles, dominants have a monopoly in carcass use, while subordinates have a restricted access to the carcass and are
always found to gain a small proportion of offspring in communal broods (Eggert et al., 2008; Komdeur et al., 2013). On small carcasses, dominants easily reject others from the carcass and even kill them, while on large carcasses, none of the group members is able to fully exclude others from the carcass and has a complete control of the reproduction of others (‘the incomplete control hypothesis’)(Eggert et al., 2008; Liu et al., 2020). This incomplete control may favour a mutual tolerance between dominant and subordinate individuals when utilising a communal resource. Such tolerance interaction is mainly characterized by a low level of aggression between dominants and subordinates (Eggert et al., 2008; Cant and Young, 2013; Royle and Hopwood, 2017). Furthermore, such tolerance interaction is the result of a tug-of-war competition over resource and reproduction between individuals that are able to reproduce in communal groups (Clutton-Brock, 1998; Gilchrist, 2006; Cant and Young, 2013). And the degree of reproductive partitioning, as well as the allocation of resource, may reflect a social negotiation between group members (Clutton-Brock, 1998; Bergmüller and Taborsky, 2005;Cant and Young, 2013). Our studies offer a satisfactory explanation for the evolution of social interactions in communal groups on the basis of the assumed prediction of tug-of-war models, and this can be supported from two perspectives (Chapter 5): from the perspectives of subordinates and from the perspectives of dominants.
From the subordinate’s point of view, we give evidence for the pay-to-stay hypothesis, and our results showed that subordinate pairs of individuals paid to stay within the group (i.e. pay to be tolerated on the carcass) by helping dominants in carcass burial; helping subordinates have a higher chance to be tolerated by dominants than non-helping subordinates. However, our studies have no support for the pay-to-reproduce hypothesis and show that subordinate individuals do not pay by helping (i.e. assistance in carcass burial) in exchange for enhanced benefits in reproductive sharing. These results suggest that the reciprocity of social services may have evolved to mediate the extent of mutual tolerance among potentially communal breeders as they are expected to reduce the costs of group living from the supposed tolerance interaction (Eggert et al., 2008; Heg and Hamilton, 2008; Taborsky et al., 2016; Liu et al., 2020). However, this exchange of social services between dominants and subordinates has no direct influence on the degree of reproductive skew in communal groups of burying beetles. This may be so because the direct benefits of helping behaviour in reproduction may translate into other benefits, for example, feeding from the carcass and sexual attractiveness in the future (Eggert et al., 2008; Heg and Hamilton, 2008; Richardson and Smiseth, 2020).
From the dominant’s point of view, we found that dominant individuals paid costs when having subordinates in communal groups, and these costs were different for dominant females and males. In the presence of their partners, dominants could effectively control subordinate’s access towards the carcass, while this cannot fully compensate the costs of having subordinates, especially when resources are limited. Moreover, our results showed that a single remaining dominant individual paid more costs from having subordinates in the absence of its dominant partner. This could be explained by two following reasons. First, there is a sex difference in the behaviour of subordinates in response to the absence or presence of dominants. Our results show that dominant females are more likely to reject subordinate females from the carcass when their dominant mates are removed, compared to dominant males, whereas subordinate males are similar in the access towards the carcass when either dominant females or males are removed. This is due to the different behaviour of dominants towards subordinates of the same- versus opposite sex (Eggert and Müller, 2000; Komdeur et al., 2013; Ratz et al., 2020). In groups, dominant individuals are more likely to show aggressive behaviour towards same-sex subordinates, than opposite-sex ones, because reproductive conflict is more frequent among same-sex individuals (Eggert and Müller, 1992; 2000; Müller and Manser, 2007; Mitchell et al., 2009). Second, there is sex difference in
compensation for the loss of mates in dominant individuals. In particular, in communal groups, dominant females still work at a maximum level of care and have no direct compensation for the loss of mates by either changing their investment or recruiting others (Eggert and Müller, 2000; Smiseth et al., 2005; Creighton et al., 2015; Ratz and Smiseth, 2018). However, dominant males may have a partial compensation for the costs of mates loss, which may be offset by the benefits from recruiting others or by increasing their own parental efforts to the current broods (McNamara et al., 1999; Rauter and Moore, 2004; Smiseth et al., 2005; Trumbo and Valletta, 2007; Suzuki and Nagano, 2009). Third, in communal groups, dominant males, but not dominant females, may benefit from the presence of subordinates, because the direct costs of loss of mates for dominant males may be offset by the benefits from recruiting other individuals. This may be due to the fact that the benefits and costs of communal breeding are different for females and males in burying beetles (Scott, 1998; Richardson and Smiseth, 2020). Furthermore, it is likely that a remaining dominant has a worse ability to control subordinates in the absence of its dominant mate, compared to in the presence of its dominant mate. This indicates that dominants pay costs from having subordinates in communal groups. In all, these findings provide evidence for a mutual tolerance between individuals in communal breeding, which is driven by a tug-of-war competition over resources and reproduction (Eggert et al., 2008; Komdeur et al., 2013; Liu et al., 2020).
In social groups, even though each group member may benefit from active competition for resources, such as increased access to the carcass, a fierce competition, such as eviction or social punishment, may incur more costs for each individual and even total group productivity (Johnstone, 2000; Bradley et al., 2008; Shen and Reeve, 2010; Barker et al., 2012). However, group-living individuals could obtain enhanced fitness benefits, or pay fewer costs, from the suppression of aggression, i.e. a mutual tolerance when there is a tug-of-war competition, while the reciprocity of social service (e.g. nest building and allo-parental care) may be involved in the evolution of social contract between unrelated individuals (Scott, 1998; Reeve et al., 1998; Shen and Reeve, 2010; Liu et al., 2020). Furthermore, such mutual tolerance at some early stages of animal societies, such as communal breeding in some species, may be the semi-social route towards eusociality in animals. Such route is based on aggregation of conspecific individuals over resources and reproduction, and is in parallel with the sub-social route that is associated with a stable familial relationship (Lin and Michener, 1972; Liu et al., 2019).
4|Does communication system favour the complexity of sociality
in animals?
In animal societies, the complexity of communication (e.g. chemical communication systems) is involved in coordinating social interactions between group members, where the conflict of interests over resources and reproduction may be resolved due to a well-organized coordination in behaviour and reproduction (Izzo et al., 2010; Padilla et al., 2016; Funaro et al., 2018). Even though an established dominance could be maintained so as to avoid the escalation of aggression and improve group stability (Clutton-Brock, 1998; Cant and Johnstone, 2000; Komdeur et al., 2013), exchanging social information that encodes sex, personality and fertility become a reliable and effective approach to deal with such social interactions in groups (Howard and Blomquist, 2005; Padilla et al., 2016). Many studies have documented the importance of the chemical communication on social organization in many eusocial insect societies that are highly organized, but how social interactions are mediated via chemical signals/cues at the early stages of societies, such as in communal groups, is limited (Dietemann et al., 2003; d’Ettorre and Lenoir, 2010; Leonhardt et al., 2016). In many insect societies, group cohesion largely relies on sophisticated chemical communication systems, while group members may advertise their fertility, caste and work via chemical signals/cues,
such as cuticular hydrocarbons (CHCs) and volatile pheromones (Keller and Nonacs, 1993; Hannonen et al., 2000; Liebig et al., 2000). It has been suggested that CHCs are associated with an individual’s fertility and reflect a behavioural transition from non-parenting to parenting in burying beetles (Steiger et al., 2007; Scott, 2008). The analyses of CHC profiles from burying beetles that vary in social status and across breeding stages show that each burying beetle individual can convey not only its parenting state but also its dominance status towards its conspecifics via CHCs and methyl geranate (Chapter 6). However, these signals/cues (i.e. CHCs and the emission of methyl geranate) are similar between communally breeding females that are laying eggs. This may be because females change their CHC profiles or the emission of methyl geranate to more closely align with others, thereby adopting a resemblance or mimicry strategy (Eggert and Müller, 2000; Steiger et al., 2011). Such similarity can lead to a reduced error of acceptance towards intraspecific competitors (e.g. subordinates) (Müller et al., 2003; Keppner et al., 2017), and plays a role in mediating group organization due to a low level of aggressive interaction (Maynard Smith, 1982; Cremer et al., 2002; Scott et al., 2007). In our study, dominant females likely exhibit less acceptance towards subordinates with more dissimilar CHCs, compared to subordinates with more similar CHCs. Such change of acceptance error related to CHC similarity may benefit group organization, with a low level of aggression between individuals (Maynard Smith, 1982; Cremer et al., 2002). It has been known that changes in CHCs reflect a sex difference in parenting performance and are elicited by the presence of offspring in burying beetles (Engel et al., 2016). Also, our results show that such changes in CHCs may be associated with a difference in male care. We found that CHCs were similar for dominant males and males that bred as pairs at the egg phase (when individuals bury the carcass together and lay eggs around the carcass), indicating that dominant males, but not subordinate males, likely provide care in carcass preparation and defence. Furthermore, our results suggest that CHCs are involved in the communication of an individual’s parenting and/or dominance status in groups, by which individual could discriminate their group members from other, while such status-specific cues cannot completely maintain a stable interaction between individuals (Peeters et al., 1999; Hannonen et al., 2000; Liebig et al., 2000). In an experiment in which we swapped subordinate individuals with similar CHCs between different groups, we found that dominant individuals responded to the presence of unfamiliar subordinates by decreasing their parental effort to the current broods (i.e. a reduction in time spent on the carcass), despite the fact that CHCs were similar between familiar and unfamiliar subordinates. Overall, our study suggests that there occurs, at least temporarily, behavioural coordination in reproduction and parental care via chemical signals/cues in communal groups of burying beetles, in which each individual could convey its fertility and dominance status towards others.
Here, we offer the idea that the changes in chemical cues/signals may occur in animal societies and may be involved in the regulation of social interaction between individuals, despite that some group members have restricted access to the resources and have limited fertility (‘a behavioural control of dominants over subordinates’ Figure 8-2; Eggert et al., 2008; Pettinger et al., 2011). Such chemical control or signal strategy, i.e. a similarity in smells, might favour the relationship of mutual tolerance in social groups (Scott, 1998; Steiger et al., 2007; Engel et al., 2016; Steiger and Stökl, 2017), which is characterized by several features, such as a reduced risk of infanticide or a behavioural switch to parenting (Eggert and Müller, 2011; Pettinger et al., 2011; Richardson and Smiseth, 2020), a low level of aggression (Scott, 1998; Haberer et al., 2010), and the inhibition of copulation events (Engel et al., 2016; Steiger and Stökl, 2017). Together with the expression analysis of selected genes that are co-opted to influence some behavioural traits, our findings suggest that such improved tolerance interaction has evolved by synchronizing three supportive but interdependent behavioural precursors, including (i) no difference in fertility and parenting behaviour (Smiseth et al., 2005; Cunningham et al., 2016b; Engel et al., 2016), (ii) a low level of aggression between
individuals (Cunningham et al., 2014; Manfredini et al., 2018), and (iii) reduced motivation to remain with the groups (i.e. feed less from the carcass) for individuals (Wu et al., 2003; Cunningham et al., 2016a; Richardson and Smiseth, 2020). Furthermore, these findings demonstrate that the evolution of mutual tolerance may be due to a well-coordinated organization in aggression and parenting behaviour between individuals (Lin and Michener, 1972; Christopher et al., 2016; Manfredini et al., 2018). In communal groups where a scramble for carcasses leads to intense conflicts between individuals over reproduction, each individual likely recognizes its group members using a more intricate communication system that includes information about state- (i.e. breeding state) and class-level (i.e. dominance status). Therefore, our studies on chemical communication in burying beetles support the conflict hypothesis that the communication and recognition processes peak at the intermediate level of sociality and decrease in highly social systems (Steiger et al., 2007; Steiger and Stökl, 2014; O’Donnell et al., 2015). In contrast, some highly eusocial insects rely on a less sophisticated system, i.e. class-level recognition, because social conflict over reproduction is relatively low due to a strict division of labour between queen(s) and other sterile members (‘social complexity hypothesis’ stating social complexity drives the complexity of communication in animals) (Dunbar, 2003; Steiger et al., 2007; Tibbetts and Dale, 2007). We encourage future research to investigate chemical communication systems and their role in coordinating group organization at the different stages of animal societies, which will advance our understanding of how communicative complexity favours the evolution of animal sociality.
Figure 8-2. The schematic of co-evolutionary mechanism underlying social tolerance and the partitioning of reproduction in social groups. In communal groups of burying beetles, some
group members are restricted in resource access and fertility (‘a behavioural control of dominants over subordinates’), while plasticity exists in chemical cues/signals (‘chemical cues/signals strategy’) between individuals. In groups with non-skewed reproduction, there is a high level of social tolerance and less similarity in fertility and dominance signals between individuals. In groups with skewed reproduction, there is a high level of aggression between individuals. However, in groups (e.g. in communal groups), there potentially is a low level of aggression between individuals, with similarity in signals.
5|Understanding eco-evolutionary routes to animal sociality
In this thesis, I use the burying beetle, N. vespilloides, as a studying model to view the eco-evolutionary routes towards animal sociality from three aspects: (i) ecological process favouring group formation, (ii) the establishment of dominance hierarchy and mutual tolerance in groups, and (iii) group organization and the associated communication systems (Figure 8-1). First, we investigate the potential ecological process that determine the formation of social groups and the associated benefits in the beetles. It is known that, for burying beetles, breeding resources (carcasses of small vertebrates) are ephemeral and limited, while ecological constraints explain the formation of such initial groups due to the aggregation of more than two individuals into social units (Wilson and Fudge, 1984; Liu et al., 2020). Due to the fact that there is a fierce competition over resources with other intruders, such as fly maggots, groups are more likely to form if the costs of solitary living are high (Groenewoud et al., 2016; Sun et al., 2014). Thus, it can be expected that such groups are maintained by mutualistic benefits, i.e. the improved defence of carcasses against intruders (Trumbo and Fiore, 1994; Komdeur et al., 2013; Liu et al., 2020). These results highlight the role of ecological process in promoting the formation of social groups (‘ecological constraint hypothesis’; Hatchwell and Komdeur, 2000; Liu et al., 2019). Also, more research about the importance of individual traits (e.g. body size and experience) for the formation of grouping should be encouraged. When there is fierce competition for resources between individuals, the variation in individual traits may lead to a difference in resource-holding potentials (RHPs) for individuals, and this may result in variation in an individual’s inclination to stay with a group (Bergmüller and Taborsky, 2010; Hopwood et al., 2016). More importantly, this variation in individual traits may select for niche specialization in resource use among conspecific individuals (Hopwood et al., 2014; Royle and Hopwood, 2017). Unlike the role of kinship in some eusocial insects (Hamilton, 1964; Lin and Michener, 1972), these findings highlight how ecological factors fundamentally influence group formation, which will advance our understandings of evolutionary transition from solitary living to animal sociality via an ecologically-driven pathway (Hatchwell and Komdeur, 2000; Shen et al., 2017). Second, the establishment of dominance hierarchies as one of the distinctive features of animal sociality plays a role in favouring the evolution of animal sociality (Rowell, 1974). Dominance hierarchy forms and is involved in reducing consistent fighting costs over resources and stabilizing group interactions among individuals. Despite its benefits, dominance status may impose physical and psychological demands on both dominant and subordinate individuals, such as the high risk of disease and chronic stress. In the communally breeding systems of burying beetles, dominant individuals have a monopoly in carcass use and are expected to gain a large proportion of offspring reared in one shared brood, whilst subordinates have restricted access towards the carcass. However, such dominance in access to the carcass is limited, as dominant individuals cannot completely reject others from the carcass, and an equal partitioning of reproduction can even occur, especially on large carcasses. This struggle may be characterized by a tug-of-war competition in resources and reproduction, because no group member can fully control the reproduction of others (Eggert et al., 2008; Komdeur et al., 2013; Liu et al., 2020). Instead of overt competition, there occurs mutual tolerance between dominant and subordinate individuals, while this may be favoured by shared and reciprocal benefits. Moreover, mutual tolerance in groups refers to a fundamental aspect of sociality and can be considered as one of evolutionary transition towards animal societies. Third, group organization largely relies on communication systems in animal societies, while the evolution of animal sociality may be favoured by the complexity of communication (Izzo et al., 2010; Funaro et al., 2018). In burying beetles, individuals can advertise their fertility and social status via chemical signals/cues, while such signals, accompanied with behavioural strategies, are involved in mediating social interactions between group members. In some highly-organized groups (such as some bees and termites), queens have a full control over the
fertility of workers (Keller and Nonacs, 1993; Hoover et al., 2005). However, this scenario is rare across animal societies. Therefore, I propose the idea that at the early stages of societies, such as communal groups of burying beetles and communal nests of paper wasps, social interaction is well organized via behavioural strategies, and also depends on a more intricate communication system. For example, in communal groups of burying beetles, dominants have a limited control over the reproduction of subordinates, while such as control may be via behavioural control/strategies, as well as chemical control/signals. Together, our studies on burying beetles expand our understanding of social evolution in animals, and the communally breeding system of burying beetles potentially offers an ecological and evolutionary model that can be applied to many other animal social systems.
