The build-up of dominance hierarchies in eusocial insects Shimoji, Hiroyuki; Dobata, Shigeto
Philosophical transactions of the Royal Society of London. Series B. Biological sciences,
02/2022, Volume:
377, Issue:
1845
Journal Article
Peer reviewed
Open access
Reproductive division of labour is a hallmark of eusocial insects. However, its stability can often be hampered by the potential for reproduction by otherwise sterile nest-mates. Dominance hierarchy ...has a crucial role in some species in regulating which individuals reproduce. Compared with those in vertebrates, the dominance hierarchies in eusocial insects tend to involve many more individuals, and should require additional selective forces unique to them. Here, we provide an overview of a series of studies on dominance hierarchies in eusocial insects. Although reported from diverse eusocial taxa, dominance hierarchies have been extensively studied in paper wasps and ponerine ants. Starting from molecular physiological attributes of individuals, we describe how the emergence of dominance hierarchies can be understood as a kind of self-organizing process through individual memory and local behavioural interactions. The resulting global structures can be captured by using network analyses. Lastly, we argue the adaptive significance of dominance hierarchies from the standpoint of sterile subordinates. Kin selection, underpinned by relatedness between nest-mates, is key to the subordinates' acceptance of their positions in the hierarchies. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.
Policing against selfishness is now regarded as the main force maintaining cooperation, by reducing costly conflict in complex social systems. Although policing has been studied extensively in social ...insect colonies, its coevolution against selfishness has not been fully captured by previous theories. In this study, I developed a two-trait quantitative genetic model of the conflict between selfish immature females (usually larvae) and policing workers in eusocial Hymenoptera over the immatures' propensity to develop into new queens. This model allows for the analysis of coevolution between genomes expressed in immatures and workers that collectively determine the immatures' queen caste fate. The main prediction of the model is that a higher level of polyandry leads to a smaller fraction of queens produced among new females through caste fate policing. The other main prediction of the present model is that, as a result of arms race, caste fate policing by workers coevolves with exaggerated selfishness of the immatures achieving maximum potential to develop into queens. Moreover, the model can incorporate genetic correlation between traits, which has been largely unexplored in social evolution theory. This study highlights the importance of understanding social traits as influenced by the coevolution of conflicting genomes.
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We report comprehensive evidence for obligatory thelytokous parthenogenesis in an ant Monomorium triviale. This species is characterized by distinct queen-worker dimorphism with strict reproductive ...division of labor: queens produce both workers and new queens without mating, whereas workers are completely sterile. We collected 333 nests of this species from 14 localities and three laboratory-reared populations in Japan. All wild queens dissected had no sperm in their spermathecae. Laboratory observation confirmed that virgin queens produced workers without mating. Furthermore, microsatellite genotyping showed identical heterozygous genotypes between mothers and their respective daughters, suggesting an extremely low probability of sexual reproduction. Microbial analysis detected no bacterial genera that are known to induce thelytokous parthenogenesis in Hymenoptera. Finally, the lack of variation in partial sequences of mitochondrial DNA among individuals sampled from across Japan suggests recent rapid spread or selective sweep. M. triviale would be a promising model system of superorganism-like adaptation through comparative analysis with well-studied sexual congeners, including the pharaoh ant M. pharaonis.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Cooperation in biological, social, and economic groups is underpinned by public goods that are generated by group members at some personal cost. Theory predicts that public goods will be exploited by ...cheaters who benefit from the goods by not paying for them, thereby leading to the collapse of cooperation. This situation, described as the “public goods dilemma” in game theory, makes the ubiquity of cooperation a major evolutionary puzzle. Despite this generalization, the demonstration of genetic background and fitness effects of the public goods dilemma has been limited to interactions between viruses and between cells, and thus its relevance at higher levels of organismal complexity is still largely unexplored. Here we provide experimental evidence for the public goods dilemma in a social insect, the ant Pristomyrmex punctatus . In this species, all workers are involved in both asexual reproduction and cooperative tasks. Genetic cheaters infiltrate field colonies, reproducing more than the workers but shunning cooperative tasks. In laboratory experiments, cheaters outcompeted coexisting workers in both survival and reproduction, although a group composed only of cheaters failed to produce offspring. The operations of the public goods dilemma in P. punctatus showed a remarkable convergence with those in microbial societies, not only in fitness consequences but also in behavioral mechanisms. Our study reinforces the evolutionary impact of cheaters on diverse cooperative systems in the laboratory and in the field.
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All organisms with sexual reproduction undergo a process of mating, which essentially involves the encounter of two individuals belonging to different sexes. During mate search, both sexes should ...mutually optimize their encounters, thus raising a question of how they achieve this. Here, we show that a population with sexually dimorphic movement patterns achieves the highest individual mating success under a limited lifespan. Extensive simulations found and analytical approximations corroborated the existence of conditions under which sexual dimorphism in the movement patterns (i.e. how diffusively they move) is advantageous over sexual monomorphism. Mutual searchers with limited lifespans need to balance the speed and accuracy of finding their mates, and dimorphic movements can solve this trade-off. We further demonstrate that the sexual dimorphism can evolve from an initial sexually monomorphic population. Our results emphasize the importance of considering mutual optimization in problems of random search.
Evolutionary ecological theory suggests that selection arising from interactions with conspecifics, such as sexual and kin selection, may result in evolution of intraspecific conflicts and ...evolutionary ‘tragedy of the commons’. Here, we propose that such an evolution of conspecific conflicts may affect population dynamics in a way that enhances species coexistence. Empirical evidence and theoretical models suggest that more abundant species is more susceptible to invasion of ‘selfish’ individuals that increase their own reproductive success at the expense of population growth (intraspecific adaptation load). The density-dependent intraspecific adaptation load gives rise to a self-regulation mechanism at the population level, and stabilizes species coexistence at the community level by negative frequency-dependence.
Community ecology has suggested that adaptation to environmental conditions (resources and other species) can affect species coexistence.There has been little discussion on how adaptation to intraspecific interactions (sexual and social conflict) affects community dynamics despite its importance in evolutionary ecology.We propose that adaptation to intraspecific conflicts, which often leads to evolution of selfish traits occurring at the expense of population growth (intraspecific adaptation load), can promote species coexistence.It stems from the density-dependent nature of intraspecific adaptation load; it tends to be larger in a larger population and serves as a self-regulating mechanism, which results in negative frequency-dependent growth in community dynamics.We discuss methods for empirically studying intraspecific adaptation load to better link community and evolutionary ecology.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Tracking animal movements such as walking is an essential task for understanding how and why animals move in an environment and respond to external stimuli. Different methods that implemented image ...analysis and a data logger such as GPS have been used in laboratory experiments and in field studies, respectively. Recently, animal movement patterns without stimuli have attracted an increasing attention in search for common innate characteristics underlying all of their movements. However, it is difficult to track the movements in a vast and homogeneous environment without stimuli because of space constraints in laboratories or environmental heterogeneity in the field, hindering our understanding of inherent movement patterns. Here, we applied an omnidirectional treadmill mechanism, or a servosphere, as a tool for tracking two-dimensional movements of small animals that can provide both a homogenous environment and a virtual infinite space for walking. To validate the use of our tracking system for assessment of the free-walking behavior, we compared walking patterns of individual pillbugs (Armadillidium vulgare) on the servosphere with that in two types of experimental flat arenas. Our results revealed that the walking patterns on the servosphere showed similar diffusive characteristics to those observed in the large arena simulating an open space, and we demonstrated that our mechanism provides more robust measurements of diffusive properties compared to a small arena with enclosure. Moreover, we showed that anomalous diffusion properties, including Lévy walk, can be detected from the free-walking behavior on our tracking system. Thus, our novel tracking system is useful to measure inherent movement patterns, which will contribute to the studies of movement ecology, ethology, and behavioral sciences.
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Eusocial insects are characterized by a well‐developed division of labour among castes. Although the successful division of labour should stem from behavioural differentiation depending on caste ...identity, caste‐specific intrinsic behavioural characteristics might be masked by social interactions within colonies. The present study explores caste‐specific intrinsic locomotive activities of termites by quantifying them in isolation. We track individual movement trajectories of the damp‐wood termite Hodotermopsis sjostedti over 30 min and extract individual locomotion parameters. Multivariate statistical analyses reveal significant differences among castes: soldiers move more actively than workers and neotenic reproductives. The morphometric data of test individuals indicate that locomotor activities reflected caste identity more strongly compared with quantitative morphological variations among individuals. We find that the different locomotor activities of soldiers compared with those of neotenics and workers probably reflect their physiological differentiation. The present study provides a basis for a deeper understanding of the roles of individual locomotor activities in social behaviours.
Termites are characterized by a well‐developed division of labour among physical castes.
We find that different locomotor patterns among castes of the damp‐wood termite, Hodotermopsis sjostedti.
The present study provides a basis for a deeper understanding of the roles of individual locomotor activities in social behaviours.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
How should females and males move to search for partners whose exact location is unknown? Theory predicts that the answer depends on what they know about where targets can be found, raising the ...question of how actual animals update their mate search patterns to increase encounter probability when conditions change. Here, we show that termites adaptively alternate between sexually monomorphic and dimorphic movements during mate search. When the location of potential mates was completely unpredictable, both sexes moved in straight lines to explore widely. In contrast, when the stray partner was at least nearby, males moved while females paused. Data-based simulations confirmed that these movements increase the rate of successful encounters. The context-dependent switch of search modes is a key to enhance random encounters.
In swarm robotics, communication among the robots is essential. Inspired by biological swarms using pheromones, we propose the use of chemical compounds to realize group foraging behavior in robot ...swarms. We designed a fully autonomous robot, and then created a swarm using ethanol as the trail pheromone allowing the robots to communicate with one another indirectly via pheromone trails. Our group recruitment and cooperative transport algorithms provide the robots with the required swarm behavior. We conducted both simulations and experiments with real robot swarms, and analyzed the data statistically to investigate any changes caused by pheromone communication in the performance of the swarm in solving foraging recruitment and cooperative transport tasks. The results show that the robots can communicate using pheromone trails, and that the improvement due to pheromone communication may be non-linear, depending on the size of the robot swarm.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OBVAL, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
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