University of Groningen Eco-evolutionary routes towards animal sociality Ma, Long

Eco-evolutionary routes towards animal sociality

Ma, Long

DOI:

10.33612/diss.160350920

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Publication date: 2021

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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

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Chapter 1

General introduction

1|Cooperation and the evolution of sociality

Man is by nature a social creature: an individual who is unsocial naturally and not

accidentally is either beneath our notice or more than human. Society is something in

nature that precedes the individual. Anyone who either cannot lead the common life or

is so self-sufficient as not to need to and therefore does not partake of society is either

a beast or a god. (Aristotle, 328 B.C.)

As Aristotle appreciated, animal societies naturally arise when each individual

accidentally or not accidentally interacts with others in the common life, while these

societies may be due to simple aggregation, common goals in benefits, and even

cooperation (Lin and Michener, 1972; Parrish and Edelstein-Keshet, 1999). In animal

and human societies, each group member may obtain direct or indirect (i.e.

kin-selected) fitness benefits, for example in survival and reproduction, either by

receiving assistance from others or by giving assistance to others (Hamilton, 1963;

Clutton-Brock, 1998; Parrish and Edelstein-Keshet, 1999). Such cooperative behaviour,

namely actions to assist recipients at the cost of helpers’ fitness benefits,

fundamentally drives the evolution of animal sociality (Hamilton, 1964; Trivers et al.,

1971; Clutton-Brock, 1998). How cooperative behaviour has evolved and how animal

societies are maintained have long been core issues in the subject of evolutionary

biology.

Most theoretical and empirical studies highlight kin selection as the mechanism

leading to the evolution of social behaviour and cooperation in animals. According to

Hamilton’s theory of kin selection (Hamilton, 1963; 1964), an individual that helps

kin-related individuals can spread the gene better than by its own reproduction. This

could be mathematically simplified as ‘Hamilton’s rule’,

rb - c > 0, where c is the cost

to the actor that helps (e.g. the average number of own offspring the helper could

have produced instead of helping),

b is the benefit to the recipient of help (e.g. the

number of the recipient’s offspring produced because of the helper’s assistance), and

r

is the relatedness between the helper and recipient (Hamilton, 1963; 1964). Hamilton

introduced the concept of ‘inclusive fitness’ for explaining cooperation between kin.

This inclusive fitness consists of the ‘direct’ fitness that individuals derive from

producing their own progeny and the ‘indirect’ fitness that they derive from helping

non-descendant relatives minus any benefits received from them (Grafen, 1982;

Brown, 1987). In some species with parental care, altruistic behaviour arises and an

individual’s genes can be transferred to its own progeny, e.g. when a mother provision

her developing young or defend her young against predation. However, cooperative

behaviour concerns those altruistic traits that improve the fitness benefits of relatives

at the expense of the individual’s fitness, for example, an individual that stays in its

natal nest and assists its parents in parental care (Komdeur, 1994; Hatchwell and

Komdeur, 2000). The societies of Hymenoptera and Isoptera provide a remarkable

example of kin selection as one of the mechanisms explaining the evolution of

cooperation and social behaviour (Lin and Michener, 1972; Toth and Rehan, 2017). For

instance, in some eusocial Hymenoptera insects, where females are more closely

related to their sisters than to their sons or daughters due to haplodiploidy, females

can gain indirect fitness benefits from helping their queens to rear female sisters (Lin

and Michener, 1972).

Even though kin selection is a satisfactory theory that can explain the evolution of

cooperation among relatives, many examples of cooperation between unrelated

individuals exist in insects, birds and mammals (Clutton-Brock, 1998; Dugatkin, 2002;

Stevens and Gilby, 2004; Hamilton and Taborsky, 2005). In animal societies, a large

number of empirical and theoretical studies explain the maintenance of cooperation

between non-kin by either reciprocity (Watts, 2002; Hamilton and Taborsky, 2005;

Clutton-Brock, 2009) or mutualism (Creel and Creel, 2001; Dugatkin, 2002). According

to Triver’s concept of reciprocal altruism (Trivers et al., 1971), these cooperative

interactions between unrelated individuals are usually referred to as reciprocal

exchanges of resources or services. In some cases, there arises ‘direct reciprocity’

between the donor and the recipient when individuals directly receive benefits from

individuals that they have previously helped (Dugatkin, 2002; Nowak, 2006), for

example, allo-grooming in primates (Schino and Aureli, 2009), the exchange of blood

meals in vampire bats,

Desmodus rotundusa (Wilkinson, 1984), and alarm calling

against predators in birds and deer (Taylor et al., 1990). Direct reciprocity largely relies

on repeated interactions between the same two individuals who are able to provide

help, while this case is difficult to study in animals. Besides, models of ‘indirect and

generalized reciprocity’ have developed the theory of reciprocal altruism. These

models show that cooperation stably arises between third parties, and even between

inter-group members, and generate social reputation or generalized commodities in

exchanging resources and services between individuals (Boyd and Richerson, 1989;

Dugatkin, 2002; Hamilton and Taborsky, 2005; Nowak, 2006; Rutte and Taborsky,

2007). Alternatively, more recent studies provide empirical evidence of the importance

of shared, mutualistic benefits in maintaining cooperative behaviour in animal societies

(Hamilton, 1963; 1964; Clutton-Brock, 2009). For example, individuals who live in

groups have enhanced defence of food against intruders and higher hunting success,

compared to solitary ones (Grinnell et al., 1995). Moreover, in some species that rear

the young communally, group breeders may suffer reduced costs of raising young

from having helpers that assist the breeders in raising young (Creel and Creel, 2001).

Also, in some animal species, mutualistic coalitions, such as cooperation in offspring

care and mutual grooming, may allow individuals to form long-term social relationships

between individuals (Silk et al., 2003).

The evolutionary routes to animal societies and how these societies are

maintained by cooperation between individuals have long puzzled biologists and

ecologists. However, with the current advance of cooperation theory, insect societies

and their associated benefits have proven highly suitable models for studying the

evolution of animal sociality (Lin and Michener, 1972). Owing to complexity in habitats

and species, diverse patterns of sociality are found across insect taxa (Figure 1-1; Lin

and Michener, 1972; Tarnita et al., 2013; Toth and Rehan, 2017), ranging from solitary

to subsocial (that is, parent-offspring association; Lin and Michener, 1972; Scott,

1998), to communal colonies (Bourke and Heinze, 1994; Paxton et al., 1996), to highly

eusocial societies (e.g. in Hymenoptera and Isoptera insects; Lin and Michener, 1972;

Dinchin et al., 2008; Linksvayer, 2010). Although most studies on insect societies have

primarily focused on highly or primitively eusocial societies (Dinchin et al., 2008), early

stages of social evolution, such as parental care, group living and communal rearing in

insects, are also important for understanding the origins of sociality and the

evolutionary transition from solitary to sociality (Scott, 1998; Heg et al., 2004; Smiseth

et al., 2012; Wong et al., 2013; Liu et al., 2019). Parental care is a complex

behavioural feature in animals, in which sexually-mature parents provide extended

and intricate care for their young so as to enhance young’s survival (Székely et al.,

1996; Scott, 1998; Smiseth et al., 2012), including nest attendance, offspring

provisioning and protection against abiotic and biotic stress (Trumbo, 1995; 2012;

Wong et al., 2013). Furthermore, parental care is commonly manifested as a biological

feature of subsociality and has been deeply studied (Smiseth and Moore, 2004; Ohba

et al., 2006; Mas et al., 2009). Also, as one of the evolutionary adaptation to the

surroundings/environment, group living or communal breeding systems always appear

when individuals may live and breed together by sharing a single nest or common

resources (Trumbo and Wilson, 1994; Gilchrist et al., 2004; Eggert et al., 2008). In this

thesis, I will systematically study and discuss such early evolutionary stages of sociality,

including group living and communally breeding systems, in the social burying beetles,

Nicrophorus vespilloides, which breed as pairs or communally, and provide extended

care for their offspring (Trumbo, 1995; Scott, 1998). Conceivably, our studies will

advance our understandings of cooperation and the evolutionary routes to sociality in

animals.

Figure 1-1. The diversity of insect sociality. In insects, there are five social patterns, including solitary, subsocial, communal, quaisocial, semisocial, and eusocial patterns. Examples of species are shown: praying mantis,Iris oratoria(Mantodea); burying beetles,Nicrophorus vespilloides(Coleoptera); eastern caterpillar, Malacosoma americanum (Lepidoptera); orchid bee, Euglossa hyacinthina (Hymenoptera); paper wasp,Polistes dominula(Hymenoptera); and termite,Reticulitermes bonyulensis (Isoptera) (Lin and Michener, 1972; Tarnita et al., 2013; Wong et al., 2013; Leonhardt et al., 2016).

2|Behaviour, ecology and evolution in burying beetles

2.1|Study species and life cycle of burying beetles

Burying beetles, belonging to Nicrophorus (Coleoptera: Silphidae), are saprophagous insects and are widely distributed in America, Asia, and Europe (Trumbo, 1992; Scott, 1998). In these beetles, sexually-mature adults search for small vertebrate carcasses (e.g. birds, mice, and rodents), bury the carcasses as shelters and food resources for their developing offspring and themselves. Then, intricate and extended care is provided until offspring independence, including carcass maintenance, carcass defence against intruders, and offspring provisioning on the buried carcass (Scott, 1998; Smiseth and Moore, 2004; Cotter and Kilner, 2009). Due to such intriguing behaviour, numerous ethologists and ecologists pay attention to burying beetles, and use them as model systems to investigate the underlying mechanism of parental care and the evolutionary process that shapes social behaviour in social animals (Scott, 1998; Parker et al., 2015). Until now, many aspects of burying beetles behaviour have been studied, including ecological and social drivers of parental care and associated behaviour (Trumbo, 2012; Sun et al., 2014), behavioural strategy and plasticity (i.e. social conflict and cooperation; Hopwood et al., 2015; Takata et al., 2016), communication and recognition system (Steiger et al., 2015; Engel et al., 2016), and molecular mechanism of social behaviour (Rauter and Moore, 2004; Dachin et al., 2008; Takata et al., 2016).

In the bi-parental care system of burying beetles, female and male parents always cooperate in carcass preparation and provisioning the developing larvae on the carcass, and brood defence against other intruders, as well as the primary division of labour in the breeding systems (Scott, 1998; Smiseth and Moore, 2004; Cotter and Kilner, 2009). For burying beetles, reproductive success is largely dependent on carcass availability and carcass size as such resources are limited and needed by both offspring and parents (Scott, 1998; Parker et al., 2015). Such competition over resources may influence an individual’s allocation of parental investment between indirect (that is, maintenance and guard of brood) and direct care (that is, direct provisioning of young) (Smiseth and Moore, 2004; Parker et al., 2015), and between current and future reproduction (Richardson et al., 2020; Richardson and Smiseth, 2020). Furthermore, there occurs a partial division of labour in parental care between breeding partners, which is different from the strict features in many eusocial insect societies (Linksvayer, 2010; Trumbo, 2012; Wong et al., 2013). In particular, females are found to provide care in carcass preparation and offspring provisioning, whereas males primarily engage in carcass preparation and brood defence (Scott, 1998; Cotter and Kilner, 2009; Steiger, 2015).

2.2|Proximate and ultimate causes of parental care in burying

beetles

Ecological factors influencing parental care

Ecological factors, with the concurrent effects of genetic bases, are proposed to shape an individual’s genotypes and phenotypes in animals, such as morphological traits and behaviour (Figure 1-2a; Wilson, 1984; Filippi-Tsukamoto et al., 1995). These factors could be categorized in three aspects: environments (i.e. climate, ambient temperature and habitats) (Wilson et al., 1984; Scott, 1998), resources (i.e. nest and food resources) (Royle et al., 2012; Wong et al., 2013), and predators and/or parasites (Wilson, 1984; Smiseth et al., 2012). Until now, theoretical and empirical studies have provided some correlative evidence for the implications of ecological factors and associated network they form for the evolution of

parental behaviour in animal species (Scott, 1998; Klug and Bonsall, 2010; Wong et al., 2013). Nevertheless, it is interesting and unclear how these ecological factors drive the evolutionary process of parenting behaviour (Bonsall and Klug, 2011; Wong et al., 2013). Until now, a large number of studies across animals species, including mammals, birds, fishes and invertebrates, provide classic models for understanding the ecology of behaviour (Gilchrist et al., 2004; Clutton-Brock, 2008; Smiseth et al., 2012; Wong et al., 2013). Here, I use burying beetles as one of models, and summarize the current advances about the ecological factors shaping behaviour in these beetles.

In natural conditions, ambient temperature has a direct influence on an individual’s behaviour in animals, including burying beetles (Meierhofer et al., 1999; Nisimura et al., 2005). For example, in N.quadripunctatus, each individual’s crepuscular behaviour is more active under cooler conditions, whereas in N.vespillo, low temperature in spring prolongs the duration of parental care partly because a prolonged developmental period is required by larvae (Meierhofer et al., 1999; Nisimura et al., 2005). Moreover, such activity that is dependent on temperature may alleviate the extent of congeneric competition across burying beetles (Wilson et al., 1984). Also, ambient temperature is found to mediate an individual’s thermal-regulatory ability and antimicrobial activity (Merrick and Smith, 2004; Jacques et al., 2009). In addition, thermal tolerance, combined with reproductive photoperiodism, shapes breeding phenology and the level of cooperation in burying beetles, where cooperative groups with large size are found to be successful at colonizing and expanding their living environment in more extreme temperatures, while non-cooperative groups are only found to have high reproductive successes at intermediate temperatures (Scott, 1998; Sun et al., 2014; Tsai et al., 2020).

Figure 1-2. (a) The proximate pathways linking between ecological environments and social interactions and animal behaviour. In animals, the five proximate pathways from three

levels are found to influence how animal individuals adjust their behaviour in response to ecological and social factors, involving in (i) nervous-hormonal processes (including neural system and hormonal regulation); (ii) gene expression and epigenetic regulation; and (iii) genetic basis-genome. In the aspect of ecological factors, there mainly exist ecological (i.e. physical environments, food, and competitors) and social factors (i.e. the complex relationship among parents, offspring, and even siblings). Accordingly, from the evolutionary perspective, ecological and social factors jointly drive the evolution of animal behaviour, ranging from courtship and mating, parental care, group living, division of labour, and hierarchy (that is, dominance and rank in highly-advanced societies)(Wilson, 1984; Filippi-Tsukamoto et al., 1995). (b) The schematic of trade-offs among life-history traits, physiology, and molecular mechanism. The trade-offs of cost-benefit are present at the different levels, involving in life-history traits, physiology, and molecular mechanisms in animals (Stearns, 1989; 2000; Wilkins, 2005; Roff, 2007; Gilbert and Manica, 2010).

For burying beetles, carcasses of small vertebrates are ephemeral and are required as food resources for their developing offspring and themselves (Eggert, 1992; Scott, 1998). After occupying the carcasses, parents first remove hair or feather of carcasses and then roll the carcasses as balls with secretions of antimicrobial substances (Eggert, 1992; Scott, 1998; Schnell et al., 2008). Because burying carcasses is costly for both parents, they may offset the costs by feeding on the carcass (Scott, 1998; Richardson et al., 2020). Burying beetle individuals who have had carcasses available for energetic and reproductive reservoir may have a high probability of overwinter survival (Schnell et al., 2008). When carcasses are large parents could reproduce a large size of broods, while parents may reduce the size of broods and even selectively kill a subset of brood on small carcasses (that is, a shift from parenting to cannibalistic behaviour) or when carcasses are occupied by other intruders (Scott, 1998). Thus, it is suggested that carcass availability (e.g. the size of carcass) is beneficial for offspring (Trumbo and Xhihani, 2015), as well as parents (Schnell et al., 2008; Richardson et al., 2020). Because carcasses are not only needed by carrion beetles, but also by other scavengers, there always occurs a fierce competition over limited carcasses among different species (Scott, 1990; 1998; Trumbo, 1994a; 1994b; Komdeur et al., 2013). Inter- and intra-specific intruders that are attracted by the carcass may feed on the carcass, kill young of residents and even breed their own offspring if carcasses are usurped by them (Trumbo, 1994a; 1994b; 2006). Such competition has a fatal impact on the survival and reproduction of burying beetle offspring and parents (Trumbo, 1994a; Richardson et al., 2o20).

Life-history traits, trade-off between benefits and costs of parental care

In animals, individuals behave in response to the surroundings they encounter based on trade-offs between ‘what they would make’ and ‘what they can get’ (Stearns, 1989; Zrea and Harshman, 2001). Central in life-history theory are trade-offs between survival and reproduction, and between current and future reproduction (Figure 1-2b; Taborsky, 2006; Gilbert and Manica, 2010; Hopwood et al., 2013). In general, the trade-offs of cost-benefit are present at the different levels, including life-history traits, physiology, and molecular mechanisms in animals. (i) In the life-history traits, the trade-off between survival and reproduction is involved, whereas the trade-offs of feeding-fight and reproduction in the current and future are shown in survival and reproduction, respectively (Stearns, 1989; 2000; Gilbert and Manica, 2010); (ii) At the level of physiology, the three main aspects, including nervous-hormonal systems, chemical signals, and immune response, are thought to engage in trade-offs of cost-benefits to adapt to surroundings (Zrea and Harshman, 2001; Angilletta et al., 2003); (iii) As the basis of genetic structure and genome, the trade-offs of cost-benefits are also primarily in gene regulation, protein synthesis (i.e. enzymes and transcription factors, TFs), and epi-(genetic) modification (Wilkins, 2005; Roff, 2007). In other words, the entire trade-offs among life-history traits, physiology, and genome are performed as an adaptive consequence for natural and social environments via an evolutionary approach.

At an individual’s level, the allocation of life-history traits between reproduction and self-maintenance (e.g. somatic growth and development) is influenced by ecological factors (Metcalfe and Monaghan, 2001; Taborsky, 2006). Such allocation is significantly present in burying beetles (Williams, 1966; Trumbo and Xhihani, 2015). During breeding, both female and male parents could change their allocation of parental effort between current and future reproduction (Heimpel and Rosenheim, 1995; Rosenheim, 1999), because individuals that provide more cares to their current broods may have smaller body gain, which may lead to more costs in terms of their survival and competitive ability in the future (Williams, 1966; Trumbo and Xhihani, 2015; Richardson et al., 2020). As one of behavioural strategies, either female or male parents or both may directly abandon ‘non-profitable’ current brood, if inter-specific competition with intruders is high, thereby allocating more parental effort to future reproduction (Stearns, 1989; Schrader et al., 2015a; 2015b), which may be associated with the residual reproductive values of parents (Ward et al., 2009). Due to limited resources of a carcass a trade-off occurs between offspring number and offspring size given the size of carcasses (Müller et al., 1990; Trumbo, 1995; Creighton, 2005). The optimization of this trade-off is associated with sibling competition (Smiseth et al., 2007), costs of reproduction (Jenkins et al., 2000; Smiseth et al., 2005a; Schrader et al., 2016), and the intensity of brood parasitism (Trumbo, 1995; Eggert et al., 2008). Parents could change larval density and mass by adjusting the extent of care (e.g. full and no care)(Steiger et al., 2007b; Trumbo, 2009; Cotter et al., 2010; Schrader et al., 2015b), while females may compensate partial losses by reproducing extra clutches when the carrying capacity of carcass exceeds the number of surviving offspring (Scott, 1998; Trumbo, 2012). In the breeding system with bi-parental care, each parent could adjust its own investment to current broods depending on its own condition (e.g. size & sex)(Fetherston et al, 1994; Rauter and Moore, 2004; Smiseth et al., 2005a), as well as its breeding partner (Pilakouta et al., 2015a; 2015b).

2.3|Conflict and cooperation over parental care

In animals, c0mplex social interactions (e.g. parental care) form when individuals associate with others, while conflicts of interests over resource and reproduction are inevitable and are present between sexes (Smiseth and Moore, 2004; Chapman et al., 2003; Houston et al., 2005), between parents and offspring (Trivers, 1974; Godfray, 1995; Mas et al., 2009; Hinde et al., 2010), among relatives (e.g. sibling relationships; Godfray and Parker, 1992; Fox and Reed, 2011; Yun and Agrewal, 2014), and even more complex networks (e.g. eusocial insect community; Ratnieks and Reeve, 1992). As one of the model systems for studying conflicts and cooperation, burying beetles have been deeply studied through many experimental approaches, such as the manipulations of parental efforts, food deprivation and the removals of parents (Lock et al, 2004; Smiseth et al., 2003; 2007; Leigh and Smiseth, 2012).

Sexual conflict and cooperation over parental care

The divergence of fitness between sexes are, in essence, caused by anisogamy, as this difference leads to varying roles of care-giving between sexes in animals (Westneat and Sargent, 1996; Webb et al., 1999; Morales and Velando, 2013). Sexual conflict over parental care widely occurs at different breeding stages, and even among genes or loci, as such conflicts between associated genes may cause differential expressions of biological traits (Chapman et al., 2003; Morales and Velando, 2013). In most species with bi-parental care, females are always found to spend more time on care than males (Trivers, 1972; Kokko and Jennions, 2008), while this scenario may be due to the uncertainty of paternity and enhanced future benefits in reproduction for males (e.g. more mating and reproductive opportunities)(Kvarnemo, 2006; Hopwood et al., 2015; Steiger, 2015). For example, male burying beetles likely desert the developing offspring and disperse from the carcass earlier than females, since they are expected to gain more chances of copulation with other females

and future reproduction (Scott, 1998; Griggio and Pilastro, 2007; Boncoraglio and Kilner, 2012). In some breeding systems, paternal care is usually considered as an advantage for males, whereas Trivers (1972) held the view that a preference of male whether or not to guard the offspring acts as counterparts of female’s mating choice owing to difference on gametes. Moreover, the optimal investment by each individual is largely dependent on the amount of care provided by its partner (Trivers, 1971; Bennett and Owens, 2002; Lessells, 2012). In a breeding attempt, reproductive benefits gained by either females or males are the results of biparental communal efforts in care, whereas each individual’s costs in reproduction are only associated with its own efforts in parental care (Trivers, 1972; Houston et al., 2005; Smiseth et al., 2005a; 2005b). In the game theory (also named as ‘negotiation model’), it is assumed that sexual conflict over parental contributions between breeders is due to the asymmetry in benefits and costs for each sex. However, such asymmetry may promote the co-evolution of sexual antagonism, for example in burying beetles, where each breeder is expected to have reduced efforts to care at the cost of its mates while breeding (Wachtmeister and Enquist, 2000; Chapman et al., 2003). For example, in burying beetles, male parents likely compel females to invest more when males are predominant in the breeding system, whereas females may suffer fewer costs or gain more benefits in reproduction if reproductive chances are controlled by themselves (Bennett and Owens, 2002; Lessells, 2012). It has been known that each parent’s reproductive performance is influenced by both size and status (Chapman et al., 2003; Pilakouta et al., 2015b). In particular, males who are paired with large females show more weight gain compared to those who are paired to small females, while females show different behaviour in response to the mass changes of their partners during parenting (Pilakouta et al., 2016). Some manipulative experiments on burying beetles demonstrate that each parent (female or male) adjusts its care to current brood according to itself and its mates (Fetherston et al., 1994; Trumbo and Fiore, 1994; Jenkins et al., 2000; Rauter and Moore, 2004; Smiseth et al., 2005a; 2005b; Suzuki and Nagano, 2009). For example in experiments with N. vespilloides and N. quandripunctatus where one of the mates is removed, males are found to invest more in their offspring compared with females, in order to compensate the reduced benefits on offspring. Such difference in compensation may be due to the fact that more costs, incurred by the absence of one of the mates, are found in males than in females (Rauter and Moore, 2004; Smiseth et al., 2005b; Suzuki and Nagano, 2009). Sexual conflict over care might be resolved by a counter-adaptation during parental care, in which females that care for offspring alone may benefit more from male’s brood desertion (Boncoraglio and Kilner, 2012).

Parents-offspring conflict and resolution over parental care

In some species, the extent of care provided by parents, at both post-hatching and post-birth, determines the developmental transition of offspring from dependence to independence (Hinde et al., 2010; Leigh and Smiseth, 2012; Rehling et al., 2012). However, the optimal timing of such transition is different for parents and offspring, since parents are favoured to reduce their investment to current broods and allocate more resources for future, whilst offspring attempts to gain more care from their parents (e.g. more food provisioning). Consequently, there occur conflicts over parental care between parents and offspring due to different expectations (Trivers, 1974; Godfray, 1995; Cant, 2006; Mas et al., 2009). Until now, lots of theories and hypotheses have proposed to explain the mechanism of parent-offspring conflict at different levels, ranging from gene to an individual, and to population (Alexander, 1974; Paker and Macnair, 1978; 1979; Godfray, 1995; Cant, 2006). For example, offspring is expected to receive more post-hatching care from their parents by intensely begging, whereas parents promote the self-feeding intensity of offspring (Davis, 1976; Leonard et al., 1991; Kilner and Drummond, 2007; Kilner and Hinde, 2008).

Across burying beetle species, offspring development is influenced by post-hatching care provided by parents, while this is partially and not strictly dependent on the post-hatching care (Scott, 1998; Smiseth et al., 2003; Kilner and Drummond, 2007). Beetle parents can provision food to begging larvae, while these larvae can also gain food by self-feeding from the carcass (Smiseth et al., 2003; Kilner and Drummond, 2007). It is likely that offspring adjust its behaviour in response to the various stimuli, such as food, developmental stage, and their parents, by changing the frequency and intensity of begging behaviour (Smiseth et al., 2003; Leigh and Smiseth, 2012). Some studies suggest that the developmental transition of offspring from dependence to independence, and this is primarily under the control of the offspring itself, partly because offspring may show alterable begging behaviour in response to the presence or absence of parents (Smiseth et al., 2003; 2012). Conversely, some empirical studies demonstrate that the transition to dependence is partly controlled by parents (Smiseth and Morgan, 2009; Leigh and Smiseth, 2012). As we argued above, offspring fitness, such as offspring survival, offspring number, and offspring number per unit volume of carcass, is largely associated with the carrying capacity of food resources (e.g. carcass size), while parents could also adjust offspring number based on the size of carcass (Scott, 1998; Monteith et al., 2012). These enable offspring to adapt to the environments better (Monteith et al., 2012; Trumbo, 2012; Schrader et al., 2015b; 2016). Under harsh natural conditions, such as when resources are limited, parents are likely to allocate the costs of raising young through offspring hatching asynchrony in many birds, despite asynchronous hatching leads to a relatively extended period of caring compared to synchronous hatching (Mock and Schwagmeyer, 1990; Stoleson and Beissinger, 1995). This scenario is also found in burying beetles (Smiseth et al., 2006; Smiseth and Morgan, 2009). Such asynchronous hatching is also correlated with social conflicts among parents, parents and offspring, and siblings, while this is due to the costs of incubation and physiological constraints that influence the onset of incubation (Stoleson and Beissinger, 1995; Takata et al., 2013; 2015; Ford and Smiseth, 2016). Some studies about birds and insects show that offspring that asynchronously hatch may gain more food and care from their parents (Mock and Schwagmeyer, 1990; Müller and Eggert, 1990), while the mechanism of asynchronous hatching is still disputed (Smiseth et al., 2006; Smiseth and Morgan, 2009). For example, in some birds, the onset of incubation is highly variable, while the delaying onset of incubation often results in hatching synchrony (Wang and Beissinger, 2009). Studies on burying beetles provide two explanations for this phenomenon. First, parents have reduced parental workloads during the peak of demands due to asynchronous hatching (‘peak load reduction hypothesis’; Mock and Schwagmeyer, 1990; Smiseth and Morgan, 2009). However, burying beetle studies provide partial support for this hypothesis, as the peak in female food provisioning is not consistent with the level of asynchronous hatching, while a lower offspring survival is observed in highly asynchronous broods compared with in synchronous or asynchronous broods (Smiseth and Morgan, 2009). Second, asynchronous hatching may be associated with the resolution of sexual conflicts over parental efforts, where females may have a reduction in care towards synchronous broods because males invest more in care relative to asynchronous broods (‘exploitation of mate hypothesis’; Slagsvold and Lifjeld, 1989; Ford and Smiseth, 2015; Takata et al., 2015).

Competition and cooperation among siblings

In many altricial birds and mammals, where parents provide their offspring with resources, surplus clutch size exceeds the carrying capacity of limited resources, and this consequently leads to intense competition over resources among siblings (Godfray and Parker, 1992; Wright and Leonard, 2002; Reed et al., 2012). However, in burying beetles the intensity of such competition is associated with the availability (i.e. the size of carcass) and demand for carcasses (i.e. brood size)(Müller et al., 1990). In N.vespilloides, brood size is negatively associated with both the provisioning time of parents and the begging intensity of offspring: A high level of competition among siblings occurs in large broods (Smiseth et al., 2007; Smiseth

and Moore, 2007). To some extents, asynchronous hatching is suggested to aggravate asymmetric competition between senior and junior young in one brood, where younger or newly-hatching larvae may suffer more costs in survival compared to older ones (Wright and Leonard, 2002; Takata et al., 2015). Also, in burying beetles, younger offspring could not gain more food by begging more towards parents compared to seniors as the amount of food that offspring get from their parents is not related to the level of their begging intensity (Smiseth and Moore, 2002; Smiseth et al., 2007). According to Hamilton’s rule, the extent of aggressive and/or cooperative interactions among siblings is related to the relatedness of siblings (Hamilton, 1964; Mock and Parker, 1998; West et al., 2001; Roulin and Dreiss, 2012). In some eusocial insects, cooperative interactions among siblings occur at different levels (Lin and Michener, 1972; Slessor et al., 2005; Mas and Kölliker, 2008; Roulin and Dreiss, 2012; Morales and Velando, 2013), such as elaborate division of labour in a sophisticated Hymenoptera society (Ratnieks et al., 2006). Also, a negotiation in the allocation of resources provided by parents arises among siblings (Roulin et al., 2000; Bulmer et al., 2008; Roulin and Dreiss, 2012), for instance, the exchange of begging signals in the spotless starling, Sturnus unicolor

(Bulmer et al., 2008). In burying beetles, the presence of parents appears to mediate the competitive interaction over resources among siblings (Smiseth et al., 2007; Rebar et al., 2020), where offspring grow faster in the presence of parents than the absence of parents, and offspring grow faster in smaller broods than in larger broods, as offspring in larger broods shifts more from begging towards self-feeding as they grow older compared to offspring in small broods (Smiseth et al., 2002; 2007). Moreover, there occurs a rapid evolutionary switch between sibling rivalry and sibling cooperation, which may be due to a sustained loss of parental care (Rebar et al., 2020). When parents do not provide full care, higher levels of sibling cooperation may compensate for the fitness costs caused by parental absence. Moreover, the close association between parental provisioning of resources and intense sibling competition presents something of a paradox because parental resource provisioning is predicted to evolve by increasing the offspring’s access to critical resources (Clutton-Brock, 1991).

3|Recognition, communication and social evolution

3.1|Recognition and the evolution of social behaviour

In (sub-)social animals, the organization of societies (e.g. family and the larger community) largely relies on kin-recognition (Morales and Velando, 2013). Within families, parents are required to discriminate their breeding partners from intruders, whilst offspring should know their parents so as to obtain more resources from parents (Morales and Velando, 2013; Steiger, 2015). Moreover, kin-recognition systems occur and play a crucial role in maintaining some advanced groups where multiple related and unrelated individuals live and breed together (Haberer et al., 2014; Morales and Velando, 2013). In animals, a variety of signals, including mechanical, chemical, and biological signals, plays a crucial role in mediating (intra-) inter-family interactions (Roulin et al., 2000; Bulmer et al., 2008; Haberer et al., 2010; 2014), while the role of signals is influenced by several factors, such as ecological conditions, life-history traits, and social conflicts (West et al., 2001; Alonzo and Klug, 2012; Wong et al., 2013). Male burying beetles release sex pheromones to attract mates over a long distance, regardless of the presence of carcasses, and these pheromones are different between species (Müller and Eggert, 1987; Haberer et al., 2011). Accordingly, female beetles copulate with males in the absence of carcasses, as they are unable to discriminate carcass-owners from non-owners (Eggert and Müller, 1989). Over a short distance, however, individuals could communicate with each other via either physical contact (Steiger et al., 2008a) or chemical signals, such as cuticular hydrocarbons (CHCs) (Steiger et al., 2007a; 2007b). Like other insects, kin recognition is innate in burying beetles, as receivers can learn to discriminate the

difference in cues/signals emitted by related senders (Royle et al., 2002; Steiger, 2015). Beyond that, the role of non-kinship appears in burying beetles, for example class recognition between previous and new mates (Steiger et al., 2008a). When a breeding partnership is established, each individual is able to discriminate its partner from intruders depending on breeding status (Trumbo and Wilson, 1993; Müller et al., 2003; Steiger et al., 2009), which is associated with chemical cues (Scott et al., 2008; Steiger et al., 2009). Furthermore, beetle individuals can discriminate conspecific intruders from their breeding partners based on a class-specific discrimination (Steiger and Müller, 2010; Steiger, 2015). In particular, they may accept all individuals that are caring for larvae irrespective of their familiarity, but show aggressive behaviour towards all non-breeding beetles. This is due to that the beetles could adjust their acceptance thresholds towards breeding partners depending on the risk of losing broods (Steiger et al., 2008; Steiger, 2015).

Across burying beetle species, there may occur kin-recognition between parents and offspring, by which local breeders can reduce the probability of brood parasitism among intraspecific individuals (Müller et al., 1990; 2007; Eggert et al., 2008). In N.tomentosus, females can increase the number of their own offspring in one communal brood by selectively committing ovicides and/or infanticides by other females, whilst this is associated with egg recognition based on cuticular lipids or other chemicals coated on the surface of eggs (Scott, 1997). However, such specific recognition does not occur across all species of burying beetles (Endler et al. 2006; Eggert et al., 2008). Since adult beetles are unable to directly recognize their own offspring from offspring produced by others, in communal groups local females sometimes kill all larvae before larvae-hatching, and then produce surplus offspring, which is depended on the timing of laying eggs (Bartlett, 1987; Trumbo, 1990b; Eggert and Müller, 2011). When larvae hatch, females will accept all newly-hatching larvae, showing a behavioural shift from infanticide to parenting (Trumbo, 1994a; Oldekop et al., 2007; Eggert and Müller, 2011). Also, parents can allocate food resources towards larvae depending on the signalling of hunger, and then influence their begging behaviour (Smiseth and Moore, 2004; 2008). In this regard, larvae may show different levels of begging towards unfamiliar and familiar beetles, but this mechanism of familiarity recognition is still unclear (Smiseth et al., 2010; Leigh and Smiseth, 2012; Mäenpää et al., 2015). Burying beetle parents provision their young by directly contacting mouthparts, so both mechanical and chemical cues may be involved in such recognition (Mäenpää et al., 2015; Steiger, 2015). Although an individual’s ability to recognize offspring is similar between burying beetles and Tenebrio beetles or Dipteran species (Den Boer and Duchateau, 2006; Mas et al., 2009), it is still unclear whether and how burying beetles can recognize and reject hetero-specific larvae from same or sister genus (Trumbo, 1994a; Trumbo, 2006; Den Boer and Duchateau, 2006).

3.2|Chemical communication and parental care

Between senders and receivers, even bystanders, communication systems play a crucial role in mediating an individual’s behaviour in multiple pathways (Mas and Kölliker, 2008; Bulmer et al., 2008), such as defense signals (Skelhorn and Rowe, 2005), begging behaviour (Smiseth and Moore, 2002; 2007), and kin-recognition (Roulin et al., 2000; Slessor et al., 2005). Moreover, these signalling pathways are involved in the resolution of conflicts between parents, offspring and sibling in burying beetles, where this elaborate recognition system is largely based on chemical cues and other signals (e.g. sounds through stridulation) (Huerta et al., 1992; Steiger et al., 2007a; Haberer et al., 2008; 2010; Steiger, 2015). To date, chemical signalling is commonly regarded as the most ancient and effective pattern of communication in the animal kingdom (Wyatt, 2003; Francke and Dettner, 2005; Haberer et al., 2010), and it has been widely studied in relation to ecology, behaviour, and physiology (Wyatt, 2003; Morales and Velando, 2013). In (sub-)social insects, including burying beetles, chemical substances are

involved in defence against intruders and parasites (Suzuki, 2001; Jacques et al., 2009; Cotter and Kilner, 2010; Degenkolb et al., 2011; Haberer et al., 2014), as well as in the coding of individual and social information (Leigh and Smiseth, 2012; Richard and Hunt, 2013; Chung and Carroll, 2015). During decomposition, corpses of small vertebrates produce a large amount of sulfur-containing compounds, which is attractive for burying beetles and other scavengers and determines aggregation among them (Kalionvá et al., 2009; Podskalská et al., 2009). Moreover, burying beetle individuals can convey social information and communicate with each other via chemical signals, such as cuticular hydrocarbons (CHCs) and volatile pheromones. This communication occurs between sexes, between breeding partners, and even among intraspecific individuals (Müller et al., 2003; Steiger et al., 2008a; 2008b; Haberer et al., 2010; 2014). Despite the importance of acoustic and behavioural cues (Huerta et al., 1992; Smiseth et al., 2010), it is likely that chemical cues play a prominent role in mediating an individual’s behaviour (Huerta et al., 1992; Steiger et al., 2008a; Haberer et al., 2010), for example, the begging behaviour of offspring is primarily triggered by chemical cues from parents (Leigh and Smiseth, 2012). Even though burying beetles can effectively adjust their behaviour via chemical signals in the context of ecological and social environments (Steiger et al., 2012a), how these chemical signals mediate an individual’s behaviour is still little studied. In parallel with the role of androgens in mammals (Tibbetts and Crocker, 2014), juvenile hormone (JH) is found to mediate a variety of biological processes (Scott and Panaitof, 2004; Goodman and Cusson, 2012; Parker et al., 2015). In burying beetles, the role of chemical signals in partner recognition is hormonally mediated, while these similar functions are also found in other social insects (Lengyel et al., 2007; Scott et al., 2008; Tibbetts and Crocker, 2014). In this section, I summarize the potential functions of chemical signals (i.e. CHCs and methyl geranate) in mediating an individual’s aggression and parenting behaviour, aiming to understand how these hormonally-mediated chemical signals influence social behaviour in insects.

Cuticular hydrocarbons (CHCs) and social behaviour

Insect cuticular hydrocarbons (CHCs), coated on the surface of individuals, play a role in maintaining the equilibrium of water in the body, and are involved in many behavioural processes, for example, sexual selection (Chung and Carroll, 2015), parental care (Steiger et al., 2007a; 2008a; Leigh and Smiseth, 2012; Chung and Carroll, 2015). These CHCs change over time and encode a variety of biological information about species, sex and status (Steiger et al., 2009; Chung and Carroll, 2015; Leonhardt et al., 2016). In burying beetles, CHC profiles are comprised of at least 90 different long-chain hydrocarbons, including linear alkanes, methyl-branched alkanes and unsaturated hydrocarbons (Steiger et al., 2007a; 2008b; Haberer et al., 2011). During breeding, CHC profiles are related to individual breeding status, but not with sex (Steiger et al., 2009; Steiger, 2015). In particular, a higher amount of CHCs and volatiles emitted is found in breeding females, but not in non-breeding ones (Steiger et al., 2007a; Haberer et al., 2014), whilst each individual can recognize its breeding partners and show more aggressive behaviour towards intra-specific intruders (Steiger et al., 2008a; Steiger, 2015). Also, it has been suggested that CHCs play a role in mediating social interactions between parents and offspring, for example, offspring begging behaviour (Leigh and Smiseth, 2012; Mäenpää et al., 2015). In all, this sophisticated recognition system based on chemical cues/signals has evolved to shape an individual’s behaviour and mediate complex social interactions in burying beetles (Smiseth et al., 2010; Leigh and Smiseth, 2012; Morales and Velando, 2013). Even though some studies find correlative evidence for the importance of CHCs on recognition and behavioural decision in burying beetles, it is unclear how these CHC cues specifically mediate an individual’s behaviour and social interactions via the regulation of physiological and hormonal changes (e.g. juvenile hormone)(Scott, 1998; Smiseth et al., 2010; Steiger, 2015; Leonhardt et al., 2016).

Juvenile hormone (JH), methyl geranate and parenting behaviour

In insects, juvenile hormone (JH) functions multiply in many biological aspects, such as development (Scott and Panaitof, 2004), fecundity (De Kort, 1981; Scott and Panaitof, 2004), and even polyphenism (Gilbert et al., 2000; Goodman and Cusson, 2012; Jindra et al., 2013). Also, it has been implicated as one of physiological indicators mediating individual behaviour in response to environmental changes, which parallels androgens in vertebrates (Figure 1-3; Trumbo, 1997; Tibbetts and Crocker, 2014; Pandey and Bloch, 2015; Rubenstein and Hofmann, 2015; Yan et al., 2015). For example, in the primitively eusocial wasp Polistes canadensis, there occurs a difference in reproductive and brood-care tasks between queens and workers, as well as the effects of JH titers. The experimental application of the JH analog methoprene accelerates the onset of guarding behaviour and increases the number of foraging females (Giray et al., 2005; Sumner et al., 2006). Furthermore, there is correlative evidence for the role of JH in organizing groups in social insects (Huang and Robinson, 1996; Bloch et al., 2000; Cnaani et al., 2000; Scott and Panaitof, 2004). In burying beetles where adults compete for mates and limited resources that are needed for breeding, JH titers are largely dependent on several non-social and social stimuli (e.g. carcass and mates) (Scott and Panaitof, 2004; Trumbo and Rauter, 2014), and are different for females and males (Panaitof et al., 2004; Rauter and Moore, 2004). After discovering a carcass, changes in JH titers in females, as well as ovarian development, are elicited by the presence of the carcass and offspring, whereas JH titers of males appear to be positively dependent on the presence of their mates (Trumbo, 1995; 1997; Panaitof et al., 2004; Trumbo and Robinson, 2008; Trumbo, 2018). When larvae hatch on the carcass, parents provide direct care that has a positive influence on offspring growth and themselves, such as sexual attractiveness (Eggert et al., 1998; Scott, 1998; Monaghan et al., 2009), in which JH plays a role in influencing various behavioural responses (Fetherston et al., 1994; Suzuki and Nagano, 2009). Within breeding females and males, the presence of a mate and mate status do not influence the initial rise of JH in females, while the absence of a mate significantly depress the JH rise in males (Scott and Panaitof, 2004). Also, such changes in JH are influenced by challenges from intruders of the opposite sex (Scott et al., 2001; Panaitof et al., 2004; Scott, 2006; Trumbo and Rauter, 2014). After the discovery of the carcass, JH titers change rapidly in both sexes (Smiseth et al., 2003; Trumbo and Robinson, 2008), and such as high level of JH can be elicited and prolonged by the presence of larvae who remain at different developing stages (Scott and Panaitof, 2004). In some burying beetles species, parents that provide direct care for offspring (i.e. food provisioning) at the early post-hatching stage suffer a reduction in fitness benefits due to energetic costs which may be associated with the high titers of JH (Fetherston et al., 1990; Monaghan et al., 2009; Trumbo and Rauter, 2014). However, this case is not supported by findings across other burying beetle species (Panaitof et al., 2004; Scott and Panaitof, 2004; Scott, 2006).

Terpenoid methyl generate [(E)-methyl 3,7-dimethyl-2,6-octadienoate], primarily produced by breeding adults, is associated with the mediation of an individual’s behaviour, such as parental care and mating behaviour (Haberer et al., 2008; 2010). The emission of methyl geranate, combined with CHC profiles, forms a complex signalling system that regulates kin-recognition and aggressive interaction in Nicrophorus beetles, and this specific system is different across burying beetles (Steiger et al., 2007a; 2008; Steiger et al., 2011a; Amsalem et al., 2014). Due to a putative shared biosynthetic pathway between methyl geranate and JH, methyl geranate acts as an indicator of JH and is involved in partner recognition by burying beetles (Haberer et al., 2010; Scott et al., 2011). In insects, JH regulates ovarian development by stimulating the synthesis of vitellogenin (Vg) in the fat body and/or by developing oocytes in the ovary (Guidugli et al., 2005; Engel et al., 2016), thereby determining an individual’s behaviour (Paker et al., 2015; Roy-Zokan, 2015). Furthermore, such effects are associated with the division of labour (Amdam et al., 2004; Guidugli et al., 2005; Nelson et al., 2007), and social organization in some eusocial insects (Nelson et al., 2007;

Wurm et al., 2010; Corona et al., 2013). For example, in the colonies of the honey bees, Apis mellifera, JH is involved in the regulation of honey bee age-related division of labour, where young workers have low haemolymph JH titres and rates of JH biosynthesis, while foragers and soldiers have high JH tires and biosynthesis rates (Huang and Robinson, 1996; Jassim et al., 2000). InN.vespilloides, a significant relationship of Vg with parenting behaviour has been reported, with a reduction in the expression of Vg and its receptor, Vgr during the period of parenting (Paker et al., 2015; Roy-Zokan, 2015). For each individual, parenting performance is mediated by JH, with the stimuli of offspring, which is involved in a behavioural shift from copulation to parental care (Scott and Panaitof, 2004; Engel et al., 2014; 2016). As one of gonadotropic hormones, JH is found to regulate Vg production in a concentration-dependent way (Parthasarathy et al., 2010), for example in N.vespilloides, where Vg is down-regulated with an increased level of JH, but up-regulated at a low level of JH (Scott and Panaitof, 2004; Engel et al., 2016). Between breeding partners, methyl geranate functions as an anti-aphrodisiac pheromone to synchronize a coordinated way in providing care to offspring, by mediating female infertility and male sexual abstinence (Müller et al., 2003; Steiger et al., 2009; Engel et al., 2016).

Figure 1-3. Juvenile hormone (JH), methyl geranate and individual behaviour. (a) The biosynthesis of juvenile hormone (JH) and its signalling pathways in insects. (b) The potential roles of JH, combined with the effects of methyl geranate, in responding/determining social environments and individual phenotypes (Tibbetts and Crocker, 2014; Engel et al., 2016).

4|Eco-evolutionary routes to sociality - Ecology and

evolution of communal breeding

4.1|The evolution of communal breeding in animals

Group living and group reproduction (such as communal or cooperative breeding) occurs when multiple individuals of conspecifics may live and reproduce together in a single nest or den and may provide shared parental care to each other’s offspring (Hayes, 2000; Vehrencamp, 2000; Gilchrist et al., 2004). This breeding system is widespread in both vertebrates and insects (Table 1-1; Brown, 1987; Emlen, 1991; Gilchrist et al., 2004). The evolutionary ecology of communal or cooperative breeding across animal species is an important problem of eco-evolution and sociobiology because it helps us to understand the ecological and behavioural features that favour the formation of social groups and social structure in groups, and raises key issues involved in the ecology and evolution of animal sociality (Vehrencamp, 2000; Riehl and Strong, 2015).

Several ecological and biological features make burying beetles an outstanding model to examine the functional basis of group breeding (that is, communal breeding in burying beetles) and the ecological process that drives the evolution of social behaviour in animals. First, burying beetle individuals are found to facultatively form communal groups, where more than two individuals of the same-sex live and breed together and share parental care for a single communal brood (Eggert and Sakaluk, 2000; Eggert et al., 2008). In these breeding groups, each individual may cooperate with others in carcass preparation and carcass defence against intruders (i.e. indirect care), and jointly engage in offspring provisioning in one shared brood (i.e. direct care)(Eggert et al., 2oo8; Richardson and Smiseth, 2020). Second, the formation of communal groups in burying beetles is largely determined by ecological factors, for example, carcass availability (Trumbo, 1995; Eggert and Sakaluk, 2000; Komdeur et al., 2013; Richardson et al., 2020). Specifically, communal breeding is more likely to occur on large carcasses, while the size of carcasses that are occupied by individuals has a significant influence on the reproductive success of groups and reproductive partitioning between individuals (Trumbo, 1995; Müller et al., 2007; Eggert et al., 2008). Third, each individual may deploy different behavioural strategy (e.g. brood parasitism, selective infanticides) in order to maximize its shares in resource and reproduction despite that a dominance hierarchy is always established in groups (Müller et al., 1990; Eggert and Müller, 1992; Steiger et al., 2012; Komdeur et al., 2013; Richardson and Smiseth, 2020). At the initial period of carcass burial, individuals may compete for the carcasses, and the social dominance and the monopolization of carcasses could be established after only several rounds of fights, with larger individuals being more likely to win fights and become dominant (Müller et al., 1990; Komdeur et al., 2013). Even though dominant individuals can largely monopolize the carcass, smaller subordinates have restricted access to the carcass (Müller et al., 1990; Eggert and Müller, 1992). This dominance in carcass use not only determines an individual’s direct reproductive benefits, such as high parentage and energetic savings due to feeding from the carcass (Eggert and Müller, 1992; Eggert et al., 2008; Komdeur et al., 2013) but also influences its future benefits in mating opportunities and reproductive performance (Pilakouta et al., 2016; Chemnitz et al., 2017; Richardson et al., 2020). Individuals losing fights do not abandon the carcass immediately. Instead, losing females may become ‘brood parasites’ and attempt to lay eggs of their own (‘intraspecific brood parasitism’), whilst losing males stealthily mate with females as ‘satellite males’ (Müller et al., 1990). For caring females, such parasitism negatively affects their own reproductive success, especially on small carcasses, while there is a positive correlation between the subordinate female’s duration of stay near the carcass and her chances of parasitizing the dominant female’s brood (Müller et al., 1990; Eggert and Müller,

2011; Richardson and Smiseth, 2020). First, in this situation, females can increase their own reproductive success through reduced competition for its offspring by destroying their co-breeder’s eggs or young (Eggert and Müller, 2011). Such selective infanticide or ovicide requires the perpetrator to discriminate between its own offspring from those of co-breeders, and this is based on temporal cues of oviposition (Eggert and Müller, 2000; 2011). Co-breeding females likely have delayed and highly-synchronous oviposition, which may reduce the risk that an individual’s larvae fall victim to infanticidal acts committed by others (Eggert and Müller, 2000; 2011). Second, co-breeding individuals may respond to the parentage uncertainty by shifting parental allocation, thereby saving more resources to their own offspring, for example, females shift allocation towards egg-laying (lay more and larger eggs and provide less care) in the presence of another female (Müller et al., 1990; Eggert and Müller, 2011; Richardson and Smiseth, 2020).

4.2|Ecological and social factors driving the evolution of

communal breeding

In animals, ecological factors (i.e. food resources & inter-specific competition), as well as the concurrent effects of social factors (i.e. adult sex ratio), have been found to drive the evolution of sociality (Emlen, 1982; Robertson et al., 1998; Hatchwell and Komdeur, 2000; Stacey and Ligon, 1990). In general, limited resources or breeding opportunities are proposed to promote the formation of social groups (‘ecological constraint hypothesis’; Hatchwell and Komdeur, 2000; Heg et al., 2004; Liu et al., 2019), and such scenario may be due to delayed dispersal or high costs of solitary living or breeding (Hatchwell and Komdeur, 2000; Riehl, 2011; Groenewoud et al., 2016), such as high predation risk or fierce competition over resources. Thus, individuals are expected to obtain enhanced benefits by living or breeding in groups, such as reduced costs of nest building and parental care (Vehrencamp et al., 1978; Scott, 1994), or improved defence of nests and resources (Ebensperger et al., 2012; Groenewoud et al., 2016). However, in some cases where there are increased costs or fewer benefits incurred by each individual while living in groups compared to solitary individuals (Gilchrist et al., 2004; Komdeur et al., 2013; Liu et al., 2020), an individual’s decision to remain within groups represents a ‘best-of-a-bad-job’ strategy. For example, in burying beetles individuals are enforced to live in groups due to both the uncertainty of solitary breeding and high costs of evicting other individuals (‘mutual tolerance hypothesis’; Komdeur et al., 2013; Liu et al., 2020). Previous studies on burying beetles suggest that the formation of communal breeding is associated with limited carcass available for breeding and the size of carcasses (Wilson and Fudge, 1984; Eggert and Müller, 1992; Liu et al., 2020). In particular, it has been suggested that individuals have improved defence of a large carcass against fly maggots (Trumbo and Fiore, 1994; Komdeur et al., 2013; Sun et al., 2014). In contrast, a tolerance association is likely to occur when individuals are coerced to share a carcass with others, with the low level of aggression among group members (Eggert and Müller, 1992; Liu et al., 2020). Nevertheless, there is conflicting evidence for the evolutionary mechanism underlying the formation of communal breeding across burying beetle species (Scott, 1994; 1998; Trumbo, 1994; Komdeur et al., 2013; Sun et al., 2014). Studying the ecological and social factors that shape the occurrence of communal breeding will advance our understanding of the evolutionary transition to sociality in animals (Hodge et al., 2011; Ebensperger et al., 2012).

4.3|Group conflict and reproductive skew in communal breeding

In animal groups, there often occurs an unequal partition of reproduction between group members, and such skewed distribution has direct influences in mediating an individual’s behaviour and group conflicts over resources and reproduction (Clutton-Brock, 1998; Reeve et al., 1998; Hamilton et al., 2005). A fundamental feature that influences an individual’s behaviour in a group and the complexity of social groups is the degree to which reproduction is partitioned among group members (Clutton-Brock, 1998; Hamilton, 2013). The reproductive skew theory has been proposed to explain the partitioning of reproduction between individuals who are different in social ranks. The reproductive skew theory consists of two main theoretical models (Clutton-Brock, 1998; Reeve et al., 1998; Shen and Reeve, 2010; Hamilton, 2013). In the ‘transactional’ models (including concession and restraint models), it is assumed that (1) dominant breeders can gain enhanced fitness benefits from having subordinates, (2) subordinates are less likely to challenge the dominant if they are allowed to share a proportion of reproductive benefits (Clutton-Brock, 1998; Reeve et al., 1998; Hamilton, 2013). Moreover, the partitioning of reproductive benefits is completely controlled by some group members (i.e. dominants), whereas such direct benefits of each individual lead to that (1) subordinates attempt to stay in the group (‘staying incentives’) and (2) are less likely to challenge the dominant (‘peace incentives’)(Clutton-Brock, 1998; Reeve et al., 1998). Alternatively, the ‘tug-of-war’ models suggest that no group member has full control over the reproductive attempts of others, whereas the level of subordinate breeding is the result of a fierce struggle over resources and reproduction between dominants and subordinates, which is associated with an individual difference in competitive ability (Clutton-Brock, 1998; Reeve et al., 1998; Shen and Reeve, 2010). Moreover, the reproductive skew models also highlight the importance of several ecological and social parameters, such as the intensity of ecological constraints on the opportunity to disperse and breed independently and relatedness of group members, which determines the degree to which reproduction is skewed within social groups and the inability of dominants to control subordinate’s breeding attempts (Creel and Waser, 1991; Eggert and Müller, 1992; Creel and Waser, 1997; Clutton-Brock, 1998; Shen and Reeve, 2010). To date, the ‘tug-of-war’ hypothesis has been tested in many species (Cant, 2000; Bradley et al., 2005; Hamilton, 2013), where the skewed reproduction among individuals can be mediated by behavioural strategies, such as mate guarding (Cant, 2000; Nichols et al., 2010), egg destruction or infanticide (Eggert and Müller, 1992), and social punishment (Clutton-Brock and Parker, 1995; Cant and Young, 2013). Previous work on burying beetles largely supports that a ‘tug-of-war’ competition occurs in communal groups, where dominant individuals that largely monopolize the limited carcasses are predicted to gain a large proportion of reproductive success in one shared brood, and the degree to which each individual gains benefits in reproduction is associated with resource availability and social structure (Eggert and Müller, 1992; Komdeur et al., 2013; Richardson and Smiseth, 2020). When competing for small carcasses with others, dominant individuals could completely reject rivals from the carcass and even kill them, there occurs a high or extremely-high skew in reproduction for each individual (Trumbo, 1995; Eggert and Sakaluk, 2000). However, on large carcasses reproduction within groups is more likely to be evenly distributed among all adults (i.e. low skew) as none of the individuals has a monopoly in carcass use, and is unable to reject others from the carcass, while both dominant and subordinate females are able to reproduce (Trumbo, 1995; Eggert and Sakaluk, 2000; Eggert et al., 2008; Richardson et al., 2020). Given that dominant individuals exert an incomplete control over subordinate’s reproduction (i.e. restricted access towards the carcass and selective infanticides)(Trumbo and Valletta, 2007; Eggert et al., 2008), it is probable that each individual is coerced to share a single carcass and show tolerance behaviour towards each other due to high costs of aggressive interactions (Komdeur et al., 2013; Liu et al., 2020). However, studies into the mechanism underlying behavioural strategies (e.g. reproductive suppression) and the

resolution of group conflicts in burying beetles, and even in other species are scarce (Trumbo, 2006; Eggert et al., 2008).

5|Thesis outline

In this thesis, I aim to address two main issues, using the burying beetles, Nicrophorus vespilloides: (1) the eco-evolutionary process that drives the evolution of social groups and the associated benefits, and (2) the underlying mechanisms of how conflicts of interests over resources and reproduction are resolved between group members. These beetles are an outstanding model for studying parental care and the evolution of sociality in social animals (Scott, 1998; Eggert and Sakaluk, 2000; Eggert et al., 2oo8; Liu et al., 2019). In Chapter 2, I will explore the ecological processes that shape the formation of social groups, by experimentally investigating the impacts of several ecological (e.g. resource availability, inter-specific competition) and intrinsic factors (e.g. sex & size) on the formation of groups and the associated fitness benefits for groups and their group members. Even though a large number of studies have highlighted the importance of ecological conditions on group living and breeding in social animals (e.g. the ecological constraint theory; Eggert and Müller, 2000; Hatchwell and Komdeur, 2000; Shen et al., 2012), it has not been studied yet how individuals plastically behave in the context of group living depending on their intrinsic conditions (Cant et al., 2006; Willisch and Neuhaus, 2010). In Chapter 3, I will address whether and how individuals adjust their behaviour with respect to aggression and parental care depending on the social status and prior breeding experience of themselves and their group members in communal groups, and the potential influence of individual prior breeding experience on overall group productivity. In many communally or cooperatively breeding species, individuals are expected to obtain immediate non-kin benefits through either reciprocity or mutualism, such as the improved defence of groups against intruders and shared parental care (Gilchrist et al., 2004; Eggert et al., 2008; Clutton-Brock, 2009; Koenig and Dickinson, 2016). Nevertheless, the carry-over effects of communal/cooperative breeding on fitness is less studied. In Chapter 4, I will perform experiments to examine how individuals adjust their parental performance in communal groups compared to pair breeding, and I will study the implications of communal breeding on immediate fitness benefits, as well as its carry-over effects on future fitness (e.g. individual parental investment and fitness benefits). In communal groups, burying beetle individuals may show tolerance behaviour towards each other, as they can gain benefits or pay little costs when there is a fierce tug-of-war competition over resources and reproduction (Eggert et al., 2008; Komdeur et al., 2013; Liu et al., 2019). In Chapter 5, I will explore the underlying mechanism of a tolerance interaction occurring between dominants and subordinates, and test the tug-of-war competition hypothesis in communal breeding. I will address these issues from two perspectives: (i) whether subordinates pay by helping in carcass burial to stay within groups (‘paying-to-stay’), and (ii) whether dominants pay from having subordinates (‘pay-from-staying’). In social groups, social conflicts over resources and reproduction could be resolved due to well-organized coordination in behaviour, while this largely relies on the sophisticated communication systems, such as chemical signals (Ratnieks et al., 2006; Leonhardt et al., 2016). In Box A, I will present a mini-review about cuticular hydrocarbons (CHCs) in insects, which is involved in the biosynthetic process of CHCs and their potential roles in behaviour. In Chapter 6, I will examine whether chemical signals, such as CHCs and methyl geranate, are responsive to an individual’s parenting and/or dominance status, and whether these chemical signals are involved in forming a well-coordinated organization (i.e. mutual tolerance interactions) in communal groups where individuals compete for limited resources and selfishly reproduce. In

Box B, I will summarize the evolutionary relationship of social behaviour with target genes,

and make a mini-review underlying how associated target genes are co-opted to mediate an individual’s behaviour in three selected-model insects. In the current era of rapid and extreme

climate change, organisms, populations and species are increasingly facing environments in which food availability can quickly decline or become highly unpredictable (Barnosky et al., 2011; Butchart et al., 2010; Garcia et al., 2014). To cope with such conditions may require a degree of flexibility that may be unattainable through phenotypic plasticity, for example in cooperative breeders (Cameron et al., 2009; Koenig and Dickinson, 2016; Komdeur et al., 2017; Taborsky et al., 2021). In Chapter 7, I will review the current advances of studies on cooperative breeders to elucidate how ecology and sociality together shape the animal sociality and its adjustment to rapid and extreme environmental change, and address the underlying reasons for our limited knowledge of the mechanisms and functions of group formation. In Chapter 8, I will end the thesis with a synthetic discussion according to previous research chapters.

The image shows one female burying beetle (Nicrophorus vespilloides) caring for its developing larvae (3rd_{-instar) on a mouse carcass. Photo by Long Ma and Sjouke A. Kingma.}