Parameter tuning facilitates the evolution of diverse tunneling patterns in termites

Abstract

9The nest structures built by social insects are complex group-level patterns that emerge from 10 interactions among individuals following simple behavioral rules. The theory of complex systems 11 predicts that there is no simple one-to-one relationship between variations in collective patterns and 12 variation in individual behaviors; therefore, it is essential to know how actual behavior evolves to 13 change pattern formation. Here we demonstrate that the evolutionary divergence of termite tunneling 14 patterns is achieved by quantitative tuning of shared behavioral rules, rather than the acquisition of 15 novel behaviors. We compared tunnel formation between two closely related species, Reticulitermes 16 tibialis and Heterotermes aureus, and found that H. aureus builds more highly branched tunnels than 17 R. tibialis. Our behavioral analysis and data-based modeling revealed that these species share the same 18 behavioral repertoire, but a quantitative difference in the probability of sidewall excavation leads to 19 diverse tunneling patterns. In contrast, we also found that Paraneotermes simplicicornis, which 20 evolved tunneling independently, possesses a distinct behavioral repertoire, but shows convergence of 21 branching patterns with R. tibialis. These results elucidate the complex relationship between individual 22 behavior and group-level patterns; in some cases, distinct behavioral rules can produce similar group-23 level patterns, but in others, a common rule set can yield distinct patterns via parameter tuning. The 24 evolutionary process of collective behavior is flexible and much more complex than we can infer from 25 group-level patterns alone. 26 27 29 Among these, nest structures built by social insects play an important role in their ecological success 30 by providing shelter and favorable microenvironments [2,3]. A wide variety of structures has evolved, 31 adapted to each species' typical environment [4,5]. This leads to the fundamental question of what is 32 the behavioral mechanism underlying the evolution of diverse nest structures? In collective building, 33 group-level structures emerge from local interactions among individuals following simple behavioral 34 rules [1,6]. Thus, different collective outcomes may be obtained either by differentiated behavioral 35 rules or by regulation of a common set of rules to modify the interactions [7]. Theoretical studies have 36 supported the latter model; they predict that diverse nest structures can be explained by parameter 37tuning, which is the quantitative modification of a single set of behavioral rules shared among species, 38 in ants [8,9], termites [10-12] and paper wasps [13,14]. However, because of the lack of comparative 39 studies, there is no empirical evidence for the sharing of behavioral rules across species, and thus the 40 key factor creating interspecific variation in patterns remains unknown. 41Because evolutionary changes of nest structures occur through the modification of building 42 processes, it is essential to clarify the ...

Modern termites inherited the potential of collective construction from their common ancestor

“…These observations suggest that the common ancestor of modern termites was a multiple‐piece nester able to build shelter tubes and tunnel through soil. However, in disagreement with this hypothesis, a recent comparative study found that the behavioral rules for collective excavation of tunnels shared by Reticulitermes tibialis and Heterotermes aureus (Rhinotermitidae) are not shared by Paraneotermes simplicicornis (Kalotermitidae) (Mizumoto, Bardunias, et al, 2019), possibly indicating an independent origin of tunneling in P. simplicicornis following the secondary loss of shelter tubes in Kalotermitidae. These results indicate that the comparison of a limited set of species is insufficient to determine the evolutionary processes at the origin of tunneling.…”

“…We did not consider belowground tunnels, which have the same function as shelter tubes and may experience similar evolutionary processes (Mizumoto, Bardunias, & Pratt, 2019). Yet, these two structures can be distinguished in terms of their complexity; tunneling is mainly performed by excavation and can be considered as an extension of feeding activities (Emerson, 1938), while shelter tube construction requires specific deposition patterns to form tube‐like structures.…”

“…However, it is not excluded that some species, especially those diverging early on in the Kalotermitidae tree of life, retain the potential to build shelter tubes. One example is Paraneotermes simplicicornis , the only definite multiple‐piece nesting species in the Kalotermitidae, which can dig galleries through the soil (Abe, 1987; Light, 1937; Mizumoto, Bardunias, et al, 2019). In addition, some populations of Neotermes rainbowi are known to be multiple‐piece nesters, and construct tunnel‐like structures made of bark chips on the surface of palm tree trunks; however, this behavior is absent in other species of Neotermes (Waterhouse & Norris, 1993).…”

Colony expansions underlie the evolution of army ant mass raiding

“…One possibility is that natural selection acts on the neural substrate that encodes the underlying behavioral rules. Across species of social insects, for example, workers may respond differently to local cues during nest construction, which could translate into different nest architectures (Mizumoto et al, 2019;Theraulaz and Bonabeau, 1995). Such behavioral rules can evolve rapidly, as has been demonstrated via artificial selection experiments on collective movement in guppies (Kotrschal et al, 2020).…”