Life history and development ‐ a framework for understanding developmental plasticity in lower termites

Abstract

Termites (Isoptera) are the phylogenetically oldest social insects, but in scientific research they have always stood in the shadow of the social Hymenoptera. Both groups of social insects evolved complex societies independently and hence, their different ancestry provided them with different life-history preadaptations for social evolution. Termites, the 'social cockroaches', have a hemimetabolous mode of development and both sexes are diploid, while the social Hymenoptera belong to the holometabolous insects and have a haplodiploid mode of sex determination. Despite this apparent disparity it is interesting to ask whether termites and social Hymenoptera share common principles in their individual and social ontogenies and how these are related to the evolution of their respective social life histories. Such a comparison has, however, been much hampered by the developmental complexity of the termite caste system, as well as by an idiosyncratic terminology, which makes it difficult for non-termitologists to access the literature. Here, we provide a conceptual guide to termite terminology based on the highly flexible caste system of the "lower termites". We summarise what is known about ultimate causes and underlying proximate mechanisms in the evolution and maintenance of termite sociality, and we try to embed the results and their discussion into general evolutionary theory and developmental biology. Finally, we speculate about fundamental factors that might have facilitated the unique evolution of complex societies in a diploid hemimetabolous insect taxon. This review also aims at a better integration of termites into general discussions on evolutionary and developmental biology, and it shows that the ecology of termites and their astounding phenotypic plasticity have a large yet still little explored potential to provide insights into elementary evo-devo questions.

Hemimetabolous genomes reveal molecular basis of termite eusociality

“…JH is important in caste differentiation in eusocial insects, including termites 12,52 . Haemolymph JH-binding proteins (JHBPs), which transport JH to its target tissues 53 , are reduced within the termites (21 to 33 genes) but significantly expanded in B. germanica (51 copies; P = 0018; Supplementary Table 6).…”

“…Termites and cockroaches are hemimetabolous and so show a direct development, while holometabolous hymenopterans complete the adult body plan during metamorphosis. In termites, workers are immatures and only reproductive castes are adults 12 , while in Hymenoptera, adult workers and queens represent the primary division of labour. Moreover, termites are diploid and their colonies consist of both male and female workers, and usually a queen and king dominate reproduction.…”

“…We analysed the genomes of two lower and one higher termite species and compared them to the genome Hemimetabolous genomes reveal molecular basis of termite eusociality Mark C. Harrison 1,12 , Evelien Jongepier 1,12 , Hugh M. Robertson 2,12 , Nicolas Arning 1 of the German cockroach, Blattella germanica, as a closely related non-eusocial outgroup. Furthermore, differences in expression between nymphs and adults of the cockroach were compared to differences in expression between workers and reproductives of the three termites, to gain insights into how expression patterns changed along with the evolution of castes.…”

“…The former belong to the lower termites and produce simple, small colonies with totipotent workers that can become reproductives. Foraging termites (some lower and all higher termites) form large, complex societies, in which worker castes can be irreversible 12 . For this reason, higher, but not lower, termites can be classed as superorganismal 13 .…”

Brood care and social evolution in termites

“…The degree of social complexity differs greatly among different termite lineages ( figure 1). In wood-dwelling termites, which nest in a single piece of wood that serves both as shelter and food source (also called one-piece-type nesters by Abe [34]) and which form small colonies [35], the workers are totipotent immatures (sometimes also called 'pseudergates') that can explore all caste options [36]. These older instars can function as workers and they can develop into soldiers or two types of reproductives: winged sexuals that found a new nest elsewhere or neotenic reproductives that inherit the natal breeding position when the current reproductives are unhealthy or die.…”