University of Groningen
Eco-evolutionary routes towards animal sociality
Ma, Long
DOI:
10.33612/diss.160350920
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Publication date: 2021
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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
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Summary
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The evolution of animal sociality is a biological mystery that has puzzled ecologists and biologists for centuries. To understand social evolution it is necessary to address how ecological, social and genetic forces jointly determine the biological process of animal societies and the mechanism of sociality (e.g. group living and reproducing) in animals. In communally or cooperatively breeding systems, individuals permanently or temporarily live and reproduce together. Fitness benefits of group living are influenced by kinship, ecological constraints and other aspects associated with grouping. Compared with some highly advanced societies (e.g. Hymenoptera societies), communal or cooperative breeding systems may refer to the early stages of animal societies. Unravelling the ecology and behaviour of communal or cooperative breeding systems will advance our knowledge of social evolution in animals and humans. In this thesis, using the European burying beetle, Nicrophorus vespilloides, I addressed three main evolutionary issues: (i) the ecological process that determines the formation of groups and the underlying factors influencing individual behaviour in this process, (ii) the associated benefits and costs of group living and reproduction and the evolutionary mechanism, of group living and reproduction and (iii) how group interactions are organized and how group members communicate with each other. Burying beetles utilise carcasses as breeding resources that are needed for their offspring and themselves, and provide extended care towards developing offspring on the buried carcasses. These beetles always breed as pairs and can also form groups by sharing a single carcass with other pairs (communal breeding). These biological and behavioural features make these beetles a classic model for studying the evolution of animal sociality.
In animals, conspecific individuals may form groups by sharing nests or communal resources, which can evolutionarily be maintained both by benefits of group living in terms of reproduction and defence and by costs associated with not living in a group. In Chapter 2, I explored the underlying ecological processes that shape the formation of groups in the burying beetle, by experimentally studying the impact of several ecological and intrinsic factors on the formation of groups and the precise fitness benefits of these factors for groups and their group members. I found that group living occurred more frequently on larger carcasses. During the process of group formation, the likelihood that an individual stayed in a group was positively influenced both by carcass size and the presence of fly maggots, and was negatively influenced by an individual’s own size and relative size. Breeding in groups had higher reproductive output at larval dispersal (larger and heavier broods) compared to non-group breeding (including solitary and pair breeding), while other aspects of reproductive success were similar. However, the per capita number of larvae produced was lower for individuals that lived in groups than individuals that bred as pairs or solitarily, suggesting a reproductive cost associated with group reproduction. These results demonstrate that large-sized carcasses promote the occurrence of group living through resource sharing, whereas group living may not provide enhanced reproductive benefits. These results highlight the ecological processes that promote group formation and the importance of considering both ecological and intrinsic factors influencing group membership decisions for the evolution of social behaviour. Furthermore, these results provide insights towards the understanding of the ecologically-driven processes of group living and the evolution of social behaviour in animals.
Gaining a range of social experiences, such as prior breeding experience, may enable individuals to better keep up with social interactions. To test the impact of individual intrinsic conditions (e.g. breeding experience and dominance status) on benefits and costs of grouping, I studied in Chapter 3 whether and how individuals adjust their behaviour and reproductive performance depending on the prior breeding experience and dominance status of themselves and other group members in communal groups of burying beetles. In such groups, a large (dominant) pair of individuals always has a monopoly in carcass use, whereas smaller (subordinate) individuals may have restricted access towards the carcass. I found that for both
carcass. In contrast, both experienced dominants and subordinates lost more weight during breeding compared to inexperienced individuals. Furthermore, irrespective of their own breeding experience, dominants that shared a group with subordinates with prior breeding experience sustained fewer injuries and gained less weight than when they shared a group with inexperienced subordinates, although this did not affect their survival and time spent on the carcass. Conversely, for subordinates there was no effect of the dominants’ breeding experience on their number of injuries. Communal groups with experienced subordinates produced larger broods at larval dispersal compared to groups with inexperienced subordinates. These results suggest that experienced individuals may be better able to avoid the escalation of aggressive interaction by reducing their access to the carcass. Moreover, in groups where individuals compete for breeding resources, dominants may obtain more benefits, or pay fewer costs, from having experienced subordinates. These results highlight the role of an individual’s own breeding experience and that of other group members in mediating social interactions in groups.
Assessing the short- and long-term fitness benefits of group living and for individuals that reproduce in groups contributes towards our understanding of the mechanism of group formation in animals. In Chapter 4, I conducted an experiment to examine the implications of communal breeding on immediate fitness benefits (e.g. reproductive success and reproductive outcome during communal breeding compared to pair breeding), as well as its carry-over effects on future fitness. My results suggest that not only immediate benefits promote communal breeding, but that also carry-over effects on fitness play a role. Furthermore, sex differences in carry-over effects of communal breeding on fitness may generate sexual conflict over parental investment in social animals. In this study, individuals that reproduced in communal groups did not have higher reproductive benefits than individuals that bred as pairs. This result indicates that communal breeding still incurred costs for each individual in reproduction, despite that there occurred mutualistic benefits of communal breeding, such as the improved joint defence of a large carcass against interspecific intruders. Also, I found experimental evidence that the carry-over effects of communal breeding were more pronounced for males than for females, suggesting that these may be associated with sex differences in the allocation of parental investment between current and future reproduction. Overall, this study on burying beetles offers a novel perspective for our understanding of communal breeding and shows evidence for carry-over effects of communal breeding on fitness and a sex difference in these carry-over effects. Future research should investigate the importance of the carry-over effects of cooperative and communal breeding, and the sex-differences in these carry-over effects, to improve our understanding of the evolution of social behaviour in animals.
In some social groups, there occurs a tug-of-war competition over resources and reproduction as none of the group members is able to fully control the others, for example in communal groups of burying beetles. Subsequently, both dominants and subordinates that are able to reproduce often have enhanced fitness benefits from a supposed tolerance interaction. To understand the underlying mechanism of such mutual tolerance between individuals in such tug-of-war competition, I examined in Chapter 5 two key questions: whether individuals (i.e. subordinates) pay by helping in order to stay in groups and therefore increase their reproductive shares (‘pay-to-stay’), and whether individuals (i.e. dominants) pay costs because of other group members staying (‘pay-from-staying’), in communal groups of burying beetles. My findings supported the pay-to-stay hypothesis and showed that cooperative subordinates paid by helping dominant breeders in carcass burial to be tolerated on the carcass, but they did not gain increased reproductive shares by helping. When their partners
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were present, dominants could effectively control subordinate’s access towards the resources, while this cannot fully compensate the costs of having subordinates. Moreover, a single remaining dominant individual in the absence of its dominant partner paid more cost from having subordinates, partly due to its worse ability to control subordinates and a sex difference in response to the loss of mates. Overall, these results demonstrate that subordinates pay by helping to stay in groups, while dominants pay cost from having subordinates in communal groups. Furthermore, a mutual tolerance occurring in a tug-of-war competition is involved in the resolution of conflicts in animal societies.
Social organization is associated with and largely relies on sophisticated communication systems, for example chemical signals/cues. A well-coordinated organization in behaviour of individuals has been suggested to benefit the resolution of conflicts over resources and reproduction in groups. In Chapter 6, I comprehensively analysed chemical signals/cues and tested their potential roles in determining an individual’s aggression and parenting behaviour, using burying beetles. Also, by profiling gene expression associated with behaviour, I examined the underlying mechanism of the mediation of group interactions, potentially through mutual tolerance between individuals. My results showed that in case of breeding in communal groups, individuals could advertise not only their breeding status but also their dominance status towards each other via chemical cues/signals, e.g. cuticular hydrocarbons (CHCs) and methyl geranate. Also, I found that, at the egg phase, similar CHCs and the emission of methyl geranate were present in individuals and this may be involved in mediating the level of aggression between dominants and subordinates, thereby promoting mutual tolerance in such groups. Together with the expression analysis of genes that are co-opted to influence some behavioural traits, these results suggest that such enhanced tolerance interactions have evolved by synchronizing some behavioural/reproductive precursors, including individuals showing no difference in fertility, reduced level of aggression, and reduced motivations to remain within the carcass (i.e. save more resources for offspring). Thus, this study underlying the mediation of social interactions via chemical signals contributes to a better understanding of the evolution of the complexity of communication in animal societies.
In the current era, organisms are increasingly facing fast and unpredictable climate and environmental changes. To cope with such conditions they may require a degree of flexibility that may be unattainable through phenotypic plasticity. Sociality is likely to be a key, yet largely overlooked factor that shapes rather than limits the potential for phenotypic plasticity. In Chapter 7, I reviewed current advances of studies on cooperative breeders to elucidate how ecology and sociality together shape the adjustment of animals to rapid and extreme environmental change. Observed adjustments in social behaviour and life history decisions may be strategic and ultimately enhance long term survival and fitness. To translate individual and group results to adaptive ability of the group, population and species, it is important to also investigate the long-term effects on demography and population viability. We are confident that future research into the ecology and social dynamics will reveal new avenues for the adaptive ability of cooperative breeders and other social species.
The evolution of animal sociality is regarded as a fundamental and core issue of evolutionary biology. In this thesis, using the communal breeding system of burying beetles as one of the studying models, I studied the ecological processes that shaped the formation of groups and the associated benefits and costs in terms of reproduction and other aspects. Also, I addressed how group individuals are well coordinated in behaviour and reproduction and the role of intricate chemical communication systems in influencing such group organization. My studies on burying beetle societies investigated how group-living individuals adapted to changing environments and social interactions, which will expand our understanding of the
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