Nobuaki Mizumoto

Colony-specific architecture of shelter tubes by termites

Social insects build sophisticated and complex architectures such as huge nests and underground galleries based on self-organizing rules. The structures of these architectures vary widely in size and shape within a species. Some studies have revealed that the current environmental and/or social factors can cause differences in the architectures that emerge from collective building. However, little is known about the effect of colony-level variations on the architecture. Here, we demonstrate that termite colonies build colony-specific architecture using shelter-tube construction as a model system. When we divided a colony into multiple groups of individuals, groups drawn from the same colony performed similar patterns of construction, whereas groups from different colonies exhibited different patterns. The colony variations in shelter-tube construction are generally thought to reflect differences in foraging strategy, and this difference can have important fitness consequences depending on the distribution of wood resources in the environment. This is the first demonstration of colony variation in the architecture that emerges from collective behavior. Colony-specific architectural variations provide new insights into our understanding of the self-organization systems, which were previously assumed to provide each species with a species-specific construction mechanism.

Emergence of intercolonial variation in termite shelter tube patterns and prediction of its underlying mechanism

Building behaviours occur in various organisms from bacteria to humans. Social insects build various structures such as large nests and underground galleries, achieved by self-organization. Structures built by social insects have recently been demonstrated to vary widely in size and shape within a species, even under the same environmental conditions. However, little is known about how intraspecific variation in structures emerges from collective behaviours. Here we show that the colony variation of structures can be generated by simply changing two behavioural parameters of group members, even with the same building algorithm. Our laboratory experiment of termite shelter tube construction demonstrated clear intercolonial variation, and a two-dimensional lattice model showed that it can be attributed to the extent of positive feedback and the number of individuals engaged in building. This study contributes to explaining the great diversity of structures emerging from collective building in social insects.

Anomalous diffusion on the servosphere: A potential tool for detecting inherent organismal movement patterns

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.

A Genomic Imprinting Model of Termite Caste Determination: Not Genetic but Epigenetic Inheritance Influences Offspring Caste Fate

Eusocial insects exhibit the most striking example of phenotypic plasticity. There has been a long controversy over the factors determining caste development of individuals in social insects. Here we demonstrate that parental phenotypes influence the social status of offspring not through genetic inheritance but through genomic imprinting in termites. Our extensive field survey and genetic analysis of the termite Reticulitermes speratus show that its breeding system is inconsistent with a genetic caste determination model. We therefore developed a genomic imprinting model, in which queen- and king-specific epigenetic marks antagonistically influence sexual development of offspring. The model accounts for all known empirical data on caste differentiation of R. speratus and other related species. By conducting colony-founding experiments and additively incorporating relevant socio-environmental factors into our genomic imprinting model, we show the relative importance of genomic imprinting and environmental factors in caste determination. The idea of epigenetic inheritance of sexual phenotypes solves the puzzle of why parthenogenetically produced daughters carrying only maternal chromosomes exclusively develop into queens and why parental phenotypes (nymph- or worker-derived reproductives) strongly influence caste differentiation of offspring. According to our model, the worker caste is seen as a “neuter” caste whose sexual development is suppressed due to counterbalanced maternal and paternal imprinting and opens new avenues for understanding the evolution of caste systems in social insects.

Optimizing mating encounters by sexually dimorphic movements

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.

Male same-sex pairing as an adaptive strategy for future reproduction in termites

A wide variety of animals display same-sex behaviours, including courtship, copulation and pairing. However, these behaviours create a paradox, as selection seemingly acts on maladaptive traits, and they have often been regarded as cases of mistaken identity, especially in invertebrates. We show that termite males show nest establishment and pairing formation that usually occur in monogamous colony foundation and demonstrate how this contributes to their fitness. We found that pairs of male dealates stopped searching for females and established nests without females, although single males rarely ceased searching for mates. Males in these male–male pairings had much higher survival than single males. Our colony fusion experiment showed that a male in a surviving same-sex pair can replace a male in an incipient colony and produce offspring. A mathematical model demonstrated that the observed strategy of establishing a male–male pairing instead of searching for females is advantageous when the risk of predation is high, even when colony fusion is very rare. These results indicate that, under certain ecological conditions, a cooperative same-sex pairing with a potential rival for reproduction can be adaptive. Our study implies the existence of various possibilities for explaining the adaptive significance of same-sex sexual behaviours.

Adaptive switch to sexually dimorphic movements by partner-seeking termites

When searching for targets whose location is not known, animals should benefit by adopting movement patterns that promote random encounters. During mate search, theory predicts that the optimal search pattern depends on the expected distance to potential partners. A key question is whether actual males and females update their mate search patterns to increase encounter probability when conditions change. Here we show that two termite species, Reticulitermes speratus and Coptoterines formosanus, adaptively alternate between sexually monomorphic and dimorphic movements during mate search. After leaving their nests in a synchronized manner, termites begin to search for a mate. The resulting pairs perform tandem runs toward potential nest sites. We found that both sexes moved faster and in straight lines before finding partners, which is known to improve encounter rates when targets have completely unpredictable positions. In stark contrast, when pairs were accidentally separated during tandem running, they showed distinct sexually dimorphic movements, where females paused for long periods while males paused only briefly and moved actively. Data-based simulations demonstrated that such sexually dimorphic movements are advantageous when a mate is located nearby but its exact location is unknown. These results emphasize the importance of biological details to evaluate the efficiency of random search in animals. By extending the concept of mutual search beyond the context of mating, the dimorphic movements between partners represent a remarkable convergence between termites and other animals including humans. Significance Statement 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, indicating that the question doesn’t make sense until the searching context is clarified. We demonstrated that termites adaptively switch their search modes depending on the potential distance to their partners. 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. 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 animals.

Loss of males from mixed-sex societies in termites

BackgroundSexual reproduction is the norm in almost all animal species, and in many advanced animal societies, both males and females participate in social activities. To date, the complete loss of males from advanced social animal lineages has been reported only in ants and honey bees (Hymenoptera), whose workers are always female and whose males display no helping behaviors even in normal sexual species. Asexuality has not previously been observed in colonies of another major group of social insects, the termites, where the ubiquitous presence of both male and female workers and soldiers indicate that males play a critical role beyond that of reproduction.ResultsHere, we report asexual societies in a lineage of the termite Glyptotermes nakajimai. We investigated the composition of mature colonies from ten distinct populations in Japan, finding six asexual populations characterized by a lack of any males in the reproductive, soldier, and worker castes of their colonies, an absence of sperm in the spermathecae of their queens, and the development of unfertilized eggs at a level comparable to that for the development of fertilized eggs in sexual populations of this species. Phylogenetic analyses indicated a single evolutionary origin of the asexual populations, with divergence from sampled sexual populations occurring about 14 million years ago. Asexual colonies differ from sexual colonies in having a more uniform head size in their all-female soldier caste, and fewer soldiers in proportion to other individuals, suggesting increased defensive efficiencies arising from uniform soldier morphology. Such efficiencies may have contributed to the persistence and spread of the asexual lineage. Cooperative colony foundation by multiple queens, the single-site nesting life history common to both the asexual and sexual lineages, and the occasional development of eggs without fertilization even in the sexual lineage are traits likely to have been present in the ancestors of the asexual lineage that may have facilitated the transition to asexuality.ConclusionsOur findings demonstrate that completely asexual social lineages can evolve from mixed-sex termite societies, providing evidence that males are dispensable for the maintenance of advanced animal societies in which they previously played an active social role.

Caste-biased movements by termites in isolation

The caste system of termites is an example of phenotypic plasticity. The castes differ not only in morphology and physiology, but also in behavior. As most of their behaviors within colonies involve nestmates, it is difficult to extract innate differences among castes. In this study, we focused on movement patterns of isolated individuals of Hodotermopsis sjostedti . We observed distinct clusters in movement patterns over 30 min, which indicates that termites have multiple innate modes of movement. The use of these modes is biased among castes, among which neotenics had a caste-specific mode and soldiers moved more actively than workers or neotenics. These caste biases may reflect different adaptive responses to social isolation. Our study provides a basis for a deeper understanding of the roles of individual movements in social behaviors.The caste system of termites is an example of phenotypic plasticity. The castes differ not only in morphology and physiology, but also in behavior. As most of their behaviors within colonies involve nestmates, it is difficult to extract innate differences among castes. In this study, we focused on movement patterns of isolated individuals of Hodotermopsis sjostedti. We observed distinct clusters in movement patterns over 30 min, which indicates that termites have multiple innate modes of movement. The use of these modes is biased among castes, among which neotenics had a caste-specific mode and soldiers moved more actively than workers or neotenics. These caste biases may reflect different adaptive responses to social isolation. Our study provides a basis for a deeper understanding of the roles of individual movements in social behaviors. Summary Statement Movement patterns of termites in isolation were described for different castes. We proposed movements as a novel caste-specific characteristics in social insects.

Barricade construction by primitive termites: task allocation and evolutionary perspectives

The collective activities of social insects often result in the formation of complex structures. Previous studies have revealed the building mechanisms of various species, where sophisticated colony-level structures emerge from the interactions among individuals. However, little is known about the building behaviors of primitive species, which would give us an insight into the evolutionary processes that gave rise to collective building of sophisticated structures. Therefore, in this study, I investigated the building behavior of the primitive termite Zootermopsis nevadensis, which constructs simple barricades to plug the openings to its nests. Observation of the time course of barricade construction showed that the building dynamics followed a logistic pattern, suggesting that their collective building involves an amplification phase, which plays an important role in self-organized building activities in social insects. Moreover, this species exhibited highly skewed task allocation during construction. Together, these results suggest that this primitive species possesses building mechanisms similar to species with more sophisticated collective behaviors.