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Social insect symbionts: evolution in homeostatic fortresses

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The massive environmentally buffered nests of some social insects can contain millions of individuals and a wide variety of parasites, commensals and mutualists. We suggest that the ways in which these homeostatic fortress environments affect the evolution of social insect symbionts are relevant for epidemiology, evolutionary biology and macroecology. We contend that specialized parasites will tend to become less virulent and mutualists less cooperative, compared to those associated with solitary or small-colony hosts. These processes are expected to contribute to the very high symbiont diversity observed in these nests. We hypothesize that biodiversity gradients in these hotspots might be less affected by abiotic latitudinal clines than gradients in neighboring ‘control’ habitats. We suggest several research lines to test these ideas.

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Social insects and the homeostatic fortresses they create

An ant colony of any size is always an impressive sight, but one containing five million sisters certainly qualifies as one of the ‘great achievements of organic evolution’ [1]. Insect societies (ants, termites, some wasps and bees; Box 1) have developed multiple forms of division of labor, efficient ways of communication and spectacular feats of engineering in nest building and trail construction. The major milestones of insect social evolution and self-organized collective behavior have been

Why parasites of long-lived insect societies are expected to be nonvirulent

Parasites, by definition, negatively affect hosts and this is termed virulence. Our understanding of virulence evolution and epidemiology (Box 2) has been greatly informed by mathematical modeling. Although this body of theory has started to include populations that are structured by group living [9], we will argue that the unique factors inside homeostatic nest patches will require more complex models to explain the evolution of virulence in parasites of advanced insect societies [10]. To help

Benign ectosymbiont diversity begets further diversity

The unique conditions inside large homeostatic fortresses that we have argued affect parasite virulence might also be important when considering mutualists. In particular, the stable environment of homeostatic fortresses facilitates the formation of complex communities where mutualists can themselves be targets for parasites leading to a reduction in mutualist performance for the social insect host. Among the numerous mutualisms involving insect societies, the farming practices that

Do insect society symbionts have shallow latitudinal biodiversity gradients?

We have suggested that the unique conditions in nests of large insect societies are expected to produce highly diverse communities of relatively avirulent pathogens and moderately benign mutualists. The modest information available indicates that symbiont diversity is indeed very high: at least 111 families of arthropods in 17 orders are known to be associated with ant colonies alone 6, 7. Even some commensals that do not interact directly with ants prefer colony life, as up to seven times as

Perspectives

We have entered a new era in understanding the complexity and diversity of Darwin’s tangled bank, with symbionts claiming an increasingly important position in biodiversity assessments 47, 53, 54, 55. Despite concerns about emerging diseases and possible pandemics (e.g. [56]), it has also become clear that many potentially virulent pathogens are fairly harmless as long as they are imbedded in a rich natural community of other symbionts associated with the same host [47]. Insect societies

Acknowledgements

This essay has benefited from discussion with and comments from several colleagues including Troy Day, Dieter Ebert, Corrie Moreau, Pekka Pamilo, Carsten Rahbek, Andrew Read, Jake Russell, Doug Schemske, Steve Stearns, Lotta Sundstrom and Stu West. We are very grateful to three anonymous reviewers for insightful comments. D.P.H. is supported by an EU FP6 Marie Curie Individual Intra-European Fellowship (MEIF-CT-2006–041613) and a WWF-Novozymes Biodiversity grant. D.P.H. and J.J.B. are further

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