Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior

This study was supported by JSPS Research Fellowships for Young Scientists CPD Grant 20J00660 (to N.M.), Grant-in-Aid for Early-Career Scientists 21K15168 (to N.M.), and Okanawa Institute of Science and Technology core funding. N.W.B. gratefully acknowledges funding from the UK Natural Environment Research Council (NE/T000619/1).Recent attempts to explain the evolutionary prevalence of same-sex sexual behavior (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB may be more complex than simple mistaken identity, instead involving mutual interactions and successful pairing between partners who can detect each other?s sex. Behavioral plasticity is essential for the expression of SSB in such circumstances. To test behavioral plasticity?s role in the evolution of SSB, we used termites to study how females and males modify their behavior in same-sex versus heterosexual pairs. Male termites follow females in paired ?tandems? before mating, and movement patterns are sexually dimorphic. Previous studies observed that adaptive same-sex tandems also occur in both sexes. Here we found that stable same-sex tandems are achieved by behavioral plasticity when one partner adopts the other sex?s movements, resulting in behavioral dimorphism. Simulations based on empirically obtained parameters indicated that this socially cued plasticity contributes to pair maintenance, because dimorphic movements improve reunion success upon accidental separation. A systematic literature survey and phylogenetic comparative analysis suggest that the ancestors of modern termites lack consistent sex roles during pairing, indicating that plasticity is inherited from the ancestor. Socioenvironmental induction of ancestral behavioral potential may be of widespread importance to the expression of SSB. Our findings challenge recent arguments for a prominent role of indiscriminate mating behavior in the evolutionary origin and maintenance of SSB across diverse taxa.Publisher PDFPeer reviewe

The evolution of body size in termites

Termites are social cockroaches. Because non-termite cockroaches are larger than basal termite lineages, which themselves include large termite species, it has been proposed that termites experienced a unidirectional body size reduction since they evolved eusociality. However, the validity of this hypothesis remains untested in a phylogenetic framework. Here, we reconstructed termite body size evolution using head width measurements of 1638 modern and fossil termite species. We found that the unidirectional body size reduction model was only supported by analyses excluding fossil species. Analyses including fossil species suggested that body size diversified along with speciation events and estimated that the size of the common ancestor of modern termites was comparable to that of modern species. Our analyses further revealed that body size variability among species, but not body size reduction, is associated with features attributed to advanced termite societies. Our results suggest that miniaturization took place at the origin of termites, while subsequent complexification of termite societies did not lead to further body size reduction

Complex Relationship between Tunneling Patterns and Individual Behaviors in Termites

The nests built by social insects are complex group-level structures that emerge from interactions among individuals following simple behavioral rules. Nest patterns vary among species, and the theory of complex systems predicts that there is no simple one-to-one relationship between variation in collective patterns and variation in individual behaviors. Therefore, a species-by-species comparison of the actual building process is essential to understand the mechanism producing diverse nest patterns. Here, we compare tunnel formation of three termite species and reveal two mechanisms producing interspecific variation: in one, a common behavioral rule yields distinct patterns via parameter tuning, and in the other, distinct rules produce similar patterns. We found that two related species transport sand in the same way using mandibles but build tunnels with different degrees of branching. The variation arises from different probabilities of choosing between two behavioral options at crowded tunnel faces: excavating the sidewall to make a new branch or waiting for clearance to extend the current tunnel. We further discovered that a third species independently evolved low-branched patterns using different building rules, namely, a bucket brigade that can excavate a crowded tunnel. Our findings emphasize the importance of direct comparative study of collective behaviors at both individual and group levels

Termite males enhance mating encounters by changing speed according to density

1.Search theory predicts that animals evolve efficient movement patterns to enhance encounter rates with specific targets. The optimal movements vary with the surrounding environments, which may explain the observation that animals often switch their movement patterns depending on conditions. However, the effectiveness of behavioural change during search is rarely evaluated because it is difficult to examine the actual encounter dynamics.2.Here we studied how partner‐seeking termites update their search strategies depending on the local densities of potential mates. After a dispersal flight, termites drop their wings and walk to search for a mate; when a female and a male meet, they form a female‐led tandem pair and search for a favourable nesting site. If a pair is separated, they have two search options—reunite with their stray partner, or seek a new partner. We hypothesized that the density of individuals affects separation–reunion dynamics and thus the optimal search strategy.3.We observed the searching process across different densities and found that termite pairs were often separated but obtained a new partner quickly at high mate density. After separation, while females consistently slowed down, males increased their speed according to the density. Under high mate density, separated males obtained a partner earlier than females, who do not change movement with density.4.Our data‐based simulations confirmed that the observed behavioural change by males contributes to enhancing encounters. Males at very low mate densities did best to move slowly and thereby reduce the risk of missing their stray partner, who is the only available mate. On the other hand, males that experienced high mate densities did better in mating encounters by moving fast because the risk of isolation is low, and they must compete with other males to find a partner.5.These results demonstrate that termite males adaptively update their search strategy depending on conditions. Understanding the encounter dynamics experienced by animals is key to connecting the empirical work to the idealized search processes of theoretical studies

Nature of collective decision-making by simple yes/no decision units Eisuke Hasegawa

The study of collective decision-making spans various fields such as brain and behavioural sciences, economics, management sciences, and artificial intelligence. Despite these interdisciplinary applications, little is known regarding how a group of simple 'yes/no' units, such as neurons in the brain, can select the best option among multiple options. One prerequisite for achieving such correct choices by the brain is correct evaluation of relative option quality, which enables a collective decision maker to efficiently choose the best option. Here, we applied a sensory discrimination mechanism using yes/no units with differential thresholds to a model for making a collective choice among multiple options. The performance corresponding to the correct choice was shown to be affected by various parameters. High performance can be achieved by tuning the threshold distribution with the options' quality distribution. The number of yes/no units allocated to each option and its variability profoundly affects performance. When this variability is large, a quorum decision becomes superior to a majority decision under some conditions. The general features of this collective decision-making by a group of simple yes/no units revealed in this study suggest that this mechanism may be useful in applications across various fields

Coordination of movement via complementary interactions of leaders and followers in termite mating pairs

In collective animal motion, coordination is often achieved by feedback between leaders and followers. For stable coordination, a leader\u27s signals and a follower\u27s responses are hypothesized to be attuned to each other. However, their roles are difficult to disentangle in species with highly coordinated movements, hiding potential diversity of behavioural mechanisms for collective behaviour. Here, we show that two Coptotermes termite species achieve a similar level of coordination via distinct sets of complementary leader–follower interactions. Even though C. gestroi females produce less pheromone than C. formosanus, tandem runs of both species were stable. Heterospecific pairs with C. gestroi males were also stable, but not those with C. formosanus males. We attributed this to the males\u27 adaptation to the conspecific females; C. gestroi males have a unique capacity to follow females with small amounts of pheromone, while C. formosanus males reject C. gestroi females as unsuitable but are competitive over females with large amounts of pheromone. An information-theoretic analysis supported this conclusion by detecting information flow from female to male only in stable tandems. Our study highlights cryptic interspecific variation in movement coordination, a source of novelty for the evolution of social interactions

Age-based spatial distribution of workers is resilient to worker loss in a subterranean termite

Elaborate task allocation is key to the ecological success of eusocial insects. Termite colonies are known for exhibiting age polyethism, with older instars more likely to depart the reproductive center to access food. However, it remains unknown how termites retain this spatial structure against external disturbances. Here we show that a subterranean termite Coptotermes formosanus Shiraki combines age polyethism and behavioral flexibility to maintain a constant worker proportion at the food area. Since this termite inhabits multiple wood pieces by connecting them through underground tunnels, disastrous colony splitting events can result in the loss of colony members. We simulated this via weekly removal of all individuals at the food area. Our results showed that termites maintained a worker proportion of ~ 20% at the food area regardless of changes in total colony size and demographic composition, where younger workers replaced food acquisition functions to maintain a constant worker proportion at the food area. Food consumption analysis revealed that the per-capita food consumption rate decreased with younger workers, but the colony did not compensate for the deficiency by increasing the proportion of workers at the feeding site. These results suggest that termite colonies prioritize risk management of colony fragmentation while maintaining suitable food acquisition efficiency with the next available workers in the colony, highlighting the importance of task allocation for colony resiliency under fluctuating environments

Revealing the structure of information flows discriminates similar animal social behaviors

Behavioral correlations stretching over time are an essential but often neglected aspect of interactions among animals. These correlations pose a challenge to current behavioral-analysis methods that lack effective means to analyze complex series of interactions. Here we show that non-invasive information-theoretic tools can be used to reveal communication protocols that guide complex social interactions by measuring simultaneous flows of different types of information between subjects. We demonstrate this approach by showing that the tandem-running behavior of the ant Temnothorax rugatulus and that of the termites Coptotermes formosanus and Reticulitermes speratus are governed by different communication protocols. Our discovery reconciles the diverse ultimate causes of tandem running across these two taxa with their apparently similar signaling mechanisms. We show that bidirectional flow of information is present only in ants and is consistent with the use of acknowledgement signals to regulate the flow of directional information