Edited by: Graham J. Thompson, Western University, Canada
Reviewed by: Michael Griesser, University of Zurich, Switzerland; Luke Holman, University of Melbourne, Australia
*Correspondence: Judith Korb
This article was submitted to Social Evolution, a section of the journal Frontiers in Ecology and Evolution
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All social insects are characterized by a reproductive division of labor. Within a colony only a few individuals reproduce (queens and in termites, also a king) while the large majority (workers and soldiers) forgo reproduction, at least temporarily. The evolution of such reproductive altruism can ultimately be explained by inclusive fitness theory. Here, I will review the proximate genetic mechanisms underlying this altruism in termites. As social cockroaches they evolved eusociality independently from the social Hymenoptera, which makes them interesting test cases to look for common underlying mechanisms of eusociality and lineage specific idiosyncrasies. First, I will provide a summary of the genes and their function that have been identified to underlie reproductive division of labor—so called “queen genes,”—in the drywood termite
A major characteristic of social insects is their reproductive division of labor between reproducing (queens, and in termites also kings) and, at least temporally, non-reproducing individuals (workers and soldiers). How such altruistic behavior that reduces an individual's direct fitness can evolve puzzled Darwin when he formulated natural selection theory (Darwin,
In many social insects the caste fate of individuals (i.e., whether they become reproductives or workers/soldiers) is determined early during development, sometimes probably even in the egg (Wilson,
Termites evolved eusociality independently from social Hymenoptera. They are “social cockroaches,” a monophyletic clade (Infraorder Isoptera) nested within the Blattodea, with Cryptocercus woodroaches as sister taxon (Inward et al.,
In termites, primary reproductives develop gradually via several (nymphal) instars and have several conspicuous traits (e.g., wings and eyes), besides those linked to reproduction and maintenance of reproductive division of labor, that distinguish them from workers. This is different for neotenics, which in kalotermitids develop from workers via a single molt and they differ from the latter only in that they are reproducing adults that maintain reproductive monopoly (Hoffmann and Korb,
In the pre-genomic era, five genes have been identified that are highly over-expressed in neotenic females (called
Esterase/lipase | Yes | yes | 1 | no | ? | |
Beta-glucosidase | Yes | yes | 1 | yes | Chem. comm.: volatile? | |
Vitellogenin | Yes | yes | 2 (4) | yes | Fertility and others? | |
P450/CYP4 | Yes | No | 55 (76)/17 (20) | yes | Chem. comm.: CHC | |
unknown | ? | ? | ? | ? | ? |
RNA interference (RNAi) experiments of the most striking Neofem genes,
The genes' identity implied that both may function via chemical communication. Down-regulation of
Currently, we cannot exclude that
Using the same methods as applied to identify the Neofem genes in
Archotermopsidae | One piece nester | Wood-dweller | simple | |
Archotermopsidae | One piece nester | Wood-dweller | simple | |
Kalotermitidae | One piece nester | Wood-dweller | simple | |
Kalotermitidae | One piece nester | Wood-dweller | simple | |
Rhinotermitidae | Separate pieces nester | Foraging | intermediate | |
Rhinotermitidae | Separate pieces nester | Foraging | intermediate | |
Termitidae | Separate pieces nester | Foraging | complex |
The availability of two termite genomes from two further termite families, the dampwood termite
Combining these genomic data with information on other genetic data available for termites and cockroaches, I will draw conclusions and derive hypotheses about the function and evolution of Neofem genes across termites in the remaining text (Table
Orthologs of
A recent phylogeny of termite and cockroach beta-glucosidase genes identified two major clusters, called beta glucosidase I (BGI) and beta glucosidase II (BGII) genes, but
Vgs in termites have mainly been recognized for their role in reproduction and as that in reproductive division of labor. According to results for the rhinotermitid
Whether termite Vgs play a broader social role as observed in social Hymenoptera (see below) is currently unclear. However, the existence of different Vg genes together with their caste-biased expression not only in queens (e.g.,
P450 genes, to which
In other termites, besides a CYP6 gene in
Termites evolved eusociality independent from social Hymenoptera. Hence a comparison between both can reveal insights into common and idiosyncratic mechanisms underlying social evolution. Nothing is known about beta-glucosidases playing an important role in the sociality of social Hymenoptera. However, there are striking commonalities for Vgs and partly for P450s.
Vitellogenins are yolk protein precursors that are crucially linked to fecundity. Hence a caste biased expression is expected to underlie reproductive division of labor. In addition, in social Hymenoptera Vgs have much broader social functions. In the honeybee, Vgs are, for instance, involved in division of labor among workers (forager vs. nurse bees, pollen vs. nectar foragers), in aging or in immune priming (e.g., Seehuus et al.,
Similar to termites, duplications of Vg genes have occurred in ants and different taxa can have different copy numbers (Wurm et al.,
In the honeybee, a single conventional Vg exists. However, it is unusual as high Vg expression is linked to low JH titers in queens. Hence JH seems to have lost its gonadotropin function in honeybee queens, but it regulates, for instance, maturation and division of labor in the worker caste. The bumblebee,
The current results suggest that independently in social Hymenoptera and termites, vitellogenins have been co-opted during social evolution. In the honeybee,
There has been much less research emphasis on P450 genes in social Hymenoptera than in termites. The number of P450 genes vary between social Hymenoptera. In ants between 28 and 84 P450 genes have been found (Oxley et al.,
The author confirms being the sole contributor of this work and approved it for publication.
The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
I thank Graham Thompson and Miriam Richards for inviting me to contribute to this issue. Two reviewers and Graham Thompson gave helpful comments on the manuscript and improved the English. Special thanks go to Michael Rehli without whom the genetic work in