Body Size and Termite Evolution

Abstract

Termites are a monophyletic lineage within the paraphyletic Blattaria, with xylophagous cockroaches in the genus Cryptocercus as sister group. Given this ancestry, termite divergence involved a substantial leap in body plans, as they are pale, fragile, and miniaturized relative to most cockroaches. Here I suggest that the evolutionary transition to an altricial morphotype in termites is grounded in the economics of utilizing a wood diet, and occurred via a series of sequential steps associated with modifications in social behavior. The chief benefit of an altricial morphotype is suggested to be nitrogen made available by decreasing individual body size and by dispensing with a heavy, melanized cuticle. The primary costs lie in increased vulnerability to environment hazards, including predators, pathogens, and desiccation. Termites tipped the evolutionary scale via cooperative behaviors that mitigate the cost or amplify the benefit of a small, fragile morphotype, and were present in rudimentary form in their cockroach relatives. These include building behavior, cooperative feeding, allogrooming, and most notably, trophallaxis. It was the directed circulation of nitrogenous reserves via trophallactic feeding among units of the superorganism rather than their progressive storage in a large, heavily armored body that was the foundation of termite evolutionary success.

‘Cost’ of proctodeal trophallaxis in extant termite individuals has no relevance in analysing the origins of eusociality

“…This behavioural transition and the consequent transfer of costs associated with parental investment from adult parents to juvenile alloparents provides a baseline for the subsequent evolution of life history characteristics specific to extant OP termites, including a sterile soldier caste, small body size, extreme phenotypic plasticity, neotenic reproduction and interdependence of colony members. The hypothesis is also consistent with the reproductive and developmental physiology of cockroaches in a nitrogen‐limited environment (Nalepa, ,b, ).…”

“…It is unlikely they would. Neonate jaws are not sufficiently developed to self‐feed on such a recalcitrant food source, they must establish their gut microbial complex by feeding on the hindgut fluids of a parent or older sibling, their diminutive body and defenceless morphotype renders them vulnerable to physical trauma, pathogens, and predators (Nalepa, ,b; Nalepa, ), and additional somatic systems may be physiologically underdeveloped (e.g. they lack nephrocytes ‐ Costa‐Leonardo et al , ).…”

Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae)

“…The generality of decreased MB investment with the evolution of insect sociality should be tested in other insect taxa, including solitary and social species such as bees and termites/roaches [47,48], to act as important checks on the generality of our findings. Elaborations of social structure that occurred after sociality evolved were not associated with directional changes in MB calyx investment.…”

Ecology shapes metabolic and life history scalings in termites

“…This has been attributed, at least in part, to an observed positive scaling of individual mass with colony mass; this, coupled to the negative allometry typical of individual‐level metabolic scaling, is sufficient to cause larger colonies to have relatively lower metabolic rates (Shik, ; Shik et al , ; Waters, ). In contrast, sociobiological models typically assume a trade‐off in social resource allocation, where societies invest in either many small individuals or fewer, larger ones (Jaffe & Deneubourg, ; Karsai & Wenzel, ; Bourke, ; Nalepa, ; van Oudenhove et al , ; Feinerman & Traniello, ). Thus, there is considerable uncertainty on the scalings among metabolic rate, individual mass and colony mass, as well as on the extent to which they are shaped by ecological differentiation.…”

“…Negative allometry has also been found in termite colony‐level metabolic scaling, although comprehensive data are only available for a single species (Jaffe, ). However, while at coarse taxonomic levels there is a general increase in colony size from the termite ancestor to more derived clades (Lepage & Darlington, ), body size seemingly followed the opposite trend (Nalepa, ). This contrasts with the positive scaling between these traits reported for ants (King, ; Shik et al , ; Mason et al , ).…”