Adaptive switch to sexually dimorphic movements by partner-seeking termites

Abstract

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 Coptotermes 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 StatementHow 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 All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/340919 doi: bioRxiv preprint first posted online Jun. 8, 2018; 2 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. IntroductionMoving for survival and reproduction is nearly a defining characteristic of animals (1, 2). Their movement patterns to find targets depend on the availability of sensory information and/or memories about targets (3, 4). When searching for targets with little or no locational information, animal...

Revealing the structure of information flows discriminates similar animal social behaviors

“…Next, we focused on the frequent brief interruptions that give tandem runs a distinctive stop-and-go appearance. During these interruptions, the follower breaks tactile contact with the leader, who then pauses while the follower performs a local random search ( Franks et al, 2010 ; Mizumoto and Dobata, 2019 ). When the follower again touches the leader, the latter resumes motion, and the pair continues on their way.…”

“…Experiments with C. formosanus and R. speratus were performed as part of a study on sexually dimorphic movements of termites during mate search ( Mizumoto and Dobata, 2019 ). Alates from 2 colonies of C. formosanus were collected in Wakayama, Japan, in June 2017; alates from 5 colonies of R. speratus were collected in Kyoto, Japan, in May 2017.…”

“…They use similar signaling mechanisms, in which the leader releases a short-range pheromone that attracts the follower ( Möglich et al, 1974 ; Bordereau and Pasteels, 2010 ), while the follower taps the leader’s body with its antennae to indicate its continued presence ( Möglich et al, 1974 ; Franks and Richardson, 2006 ; Nutting, 1969 ; Vargo and Husseneder, 2009 ). Upon removal of the follower, the leader stops and waits for the follower to resume contact both in ants ( Möglich et al, 1974 ; Franks and Richardson, 2006 ) and in termites ( Mizumoto and Dobata, 2019 ). At long time scales, however, there exist clear functional differences in these seemingly similar behaviors.…”

A guide to area‐restricted search: a foundational foraging behaviour

“…Here, the trigger for local search is the female sex pheromone, which is non‐volatile so preventing the use of chemotaxis as a more direct search strategy. Interestingly, removing the female after pair formation in two termite species leads to ARS behaviour by the male but removing the male does not have the same effect on the female (Mizumoto & Dobata, 2019). Similarly, parasitoids respond to host chemical cues, such as gland secretions, by moving more slowly, turning more frequently, and inspecting the surface with the ovipositor [see Waage (1978) and Strand & Vinson (1982) and references therein].…”

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

“…First, bidirectional feedbacks between females and males enable them to actively regulate movement speed according to partner distance (17). Second, sexually dimorphic movements are expressed upon accidental separation, where females pause and males engage in an intensive search to facilitate reencounter (18).…”