Disease resistance: A benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera: Termopsidae)

Department of Biology, Boston University, Boston, Massachusetts, United States
Behavioral Ecology and Sociobiology (Impact Factor: 2.35). 01/1998; 44(2):125-134. DOI: 10.1007/s002650050523


The benefit of sociality in relation to disease susceptibility was studied in the dampwood termite Zootermopsis angusticollis. Although contact with high concentrations of fungal conidia is lethal, the survivorship of nymphs exposed to spore suspensions
ranging from 6 × 106 to 2 × 108 spores/ml of the fungus Metarhizium anisopliae increased with group size. The survivorship (measured as LT50) of isolated individuals ranged from 3.0 to 4.8 days, but infected nymphs living in groups of 10 and 25 individuals survived
significantly longer (5.6–8.3 and 5.6–9.1 days, respectively). In most cases, there were no significant differences in the
survival distributions of the 10- and 25-termite groups. When nymphs were infected with concentrations of 7 × 101–7 × 104 spores/ml and allowed to interact with healthy nestmates, fungal infections were not contracted by the unexposed termites.
Moreover, infected termites benefitted from social contact with unexposed nestmates: their survival rates were significantly
higher than those of infected termites living with similarly infected nestmates. Allogrooming, which increased in frequency
during and after exposure to conidia, appeared to remove potentially infectious spores from the cuticle, thus increasing termite
survivorship. These results suggest that allogrooming plays a crucial role in the control of disease and its death hazard
in termites. The infection-reducing advantage of group living may have been significant in the evolution of social behavior
in the Isoptera.

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Available from: Rebeca B Rosengaus
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    • "However, in addition to individual-level immune defenses, social organisms are able to employ social defenses that have been termed " social immunity " in the broad sense (Dunbar 1991; Cremer et al. 2007; Wisenden et al. 2009; Otti et al. 2014). This can include behavioral defenses such as grooming, and the production and transfer of antimicrobial compounds (Rosengaus et al. 1998, 2004; Fern andez- Mar ın et al. 2006; Yanagawa et al. 2008; Hamilton et al. 2011; Baracchi et al. 2012; Turnbull et al. 2012), which can mitigate or even outweigh the fitness cost from parasites for group-living animals (Rosengaus et al. 1998; Hughes et al. 2002; Ugelvig and Cremer 2007; Reber et al. 2011). The threat of disease has led the most diverse group of social insects, the ants, to evolve a unique exocrine structure, the metapleural gland (MG), which varies in size between species and phenotypes, and in many taxa, produces an antimicrobial secretion that is spread over the cuticle either passively or, in some species, actively by grooming (H€ olldobler and Wilson 1990; Bot and Boomsma 1996; Sumner et al. 2003; Fern andez-Mar ın et al. 2006; Poulsen et al. 2006; Hughes et al. 2008, 2010; Yek and Mueller 2011). "
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    ABSTRACT: Parasites are a major force in evolution, and understanding how host life history affects parasite pressure and investment in disease resistance is a general problem in evolutionary biology. The threat of disease may be especially strong in social animals, and ants have evolved the unique metapleural gland (MG), which in many taxa produce antimicrobial compounds that have been argued to have been a key to their ecological success. However, the importance of the MG in the disease resistance of individual ants across ant taxa has not been examined directly. We investigate experimentally the importance of the MG for disease resistance in the fungus-growing ants, a group in which there is interspecific variation in MG size and which has distinct transitions in life history. We find that more derived taxa rely more on the MG for disease resistance than more basal taxa and that there are a series of evolutionary transitions in the quality, quantity, and usage of the MG secretions, which correlate with transitions in life history. These shifts show how even small clades can exhibit substantial transitions in disease resistance investment, demonstrating that host-parasite relationships can be very dynamic and that targeted experimental, as well as large-scale, comparative studies can be valuable for identifying evolutionary transitions.
    Full-text · Article · Nov 2015 · Ecology and Evolution
    • "independent of an exact assessment). Here, we may only expect deviations from theory if expression of such behaviours may be restricted or have little effect, as seems to be the case of self-grooming in termites [21,51,52] . Yet, testing these predictions is complicated by the fact that pathogen transmission not always reflects disease transmission. "
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    ABSTRACT: To prevent epidemics, insect societies have evolved collective disease defences that are highly effective at curing exposed individuals and limiting disease transmission to healthy group members. Grooming is an important sanitary behaviour-either performed towards oneself (self-grooming) or towards others (allogrooming)-to remove infectious agents from the body surface of exposed individuals, but at the risk of disease contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal pathogen Metarhizium as a model system to study how pathogen presence affects self-grooming and allogrooming between exposed and healthy individuals. We develop an epidemiological SIS model to explore how experimentally observed grooming patterns affect disease spread within the colony, thereby providing a direct link between the expression and direction of sanitary behaviours, and their effects on colony-level epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously decreasing allogrooming. This behavioural modulation seems universally adaptive and is predicted to contain disease spread in a great variety of host-pathogen systems. In contrast, allogrooming directed towards pathogen-exposed individuals might both increase and decrease disease risk. Our model reveals that the effect of allogrooming depends on the balance between pathogen infectiousness and efficiency of social host defences, which are likely to vary across host-pathogen systems. © 2015 The Author(s) Published by the Royal Society. All rights reserved.
    No preview · Article · May 2015 · Philosophical Transactions of The Royal Society B Biological Sciences
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    • "A faecal pellet can be a source of microbial protein, but is also a mechanism for transmitting the resistant stages of prokaryotes, as well as semiochemicals and metabolites originating with the excretor and all its gut mutualists (Nalepa et al., 2001; Bell et al., 2007). Faecal pellets play a role in sanitising the nest (Rosengaus et al., 1998b, 2013) and also serve as bricks and mortar to plug holes and gaps, to build pillars and walls to partition galleries, and to erect barriers when galleries approach those of conspecifics adjacent in the log (Bell et al., 2007: fig. 9.4). "
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    ABSTRACT: 1. Numerous cladistic analyses have converged: termites are a monophyletic clade embedded within the paraphyletic cockroaches, and sister group to the biparental, wood-feeding cockroach Cryptocercus. The latter is therefore an appropriate model for testing assumptions regarding early termite evolution. 2. The ground plan of the termite ancestor is reviewed based on shared characters of ecology, life history and behavior in Cryptocercus and incipient termite colonies, and includes two levels of dependence: a reliance of all individuals on gut microbiota, and dependence of early instars on parental care. Both these conditions co-evolved with parent-to-offspring proctodeal trophallaxis. 3. The termite ancestor lived in a single log serving as food and nest. This ‘one-piece’ nesting ecology prioritizes nitrogen conservation and strongly influences interacting social, nutritional, and microbial environments. Each of these environments individually and in combination profoundly affect cockroach development. 4. Proctodeal trophallaxis integrates the social, nutritional, and microbial environments. A change in trophallactic behavior, from parental to alloparental, can, therefore, shift developmental trajectories, ultimately adding a third level of dependence. The death of gut protists during the host molting period and consequent interdependence of family members shifted the hierarchical level at which selection acted; fixation of eusociality quickly followed. 5. The basic nesting ecology did not change when termites evolved eusociality, the change occurred in the allocation and use of existing resources within the social group, driven by nitrogen scarcity, mediated by trophallaxis and made possible by a strongly lineage specific set of life history characteristics.
    Full-text · Article · Mar 2015 · Ecological Entomology
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