Social insect symbionts: evolution in homeostatic fortresses David P. Hughes 1, 3, 4 , Naomi E. Pierce 2 and Jacobus J. Boomsma 1 1 Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark 2 Museum of Comparative Zoology Labs, Harvard University, Cambridge, MA 02138-2902, USA 3 Current address: Museum of Comparative Zoology Labs, Harvard University, Cambridge, MA 02138-2902, USA 4 Current address: School of Biosciences, University of Exeter, Exeter EX4 4QD, UK 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, evol- utionary 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 hypoth- esize 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. 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 beha- vior have been intensively studied over recent decades [2], but the evolutionary consequences of insect societies alter- ing their own environments have received less attention. This is surprising, because it is now 40 years since it was first noted that the interior of a large ant colony represents a radically different environment from that encountered beyond its borders, a concept encapsulated in the metaphor of a colony as a ‘factory constructed inside a fortress’ [3]. The nests that large insect societies create provide unique, environmentally buffered patches of habitat for many other organisms. The distinctiveness and quality of such patches are a direct function of the size and longevity of the colonies involved. Societies of ants and termites are remarkably long lived (Box 1). They can achieve this long- evity by recruiting new queens at regular intervals, but also the queens (and kings in termites) themselves can have life spans of decades because the colony interior is a predator-free space where selection will tend to reduce rates of aging [4] (Box 1). Long life span of reproductives, large colony size and a homeostatic nest environment have thus evolved in concert because of positive mutual feed- back [5]. Typical examples in the tropics are the 3 m high termite mounds in dry savannas that employ air-condition- ing chimneys to maintain constant optimal conditions for fungus gardens, leaf-cutting ants that occupy subterra- nean living quarters comparable to the size of an average city apartment and nomadic bands of army ants construct- ing a living nest of worker bodies in temporary bivouacs (Figure 1). Temperate zone equivalents are thermo- regulated honeybee hives and 2 m high nest mounds of boreal wood ants that maintain metabolically heated ‘cel- lars’ to survive À258C winters (Figure 1). The other organisms that have adapted to homeostatic life in insect societies can be collectively referred to as symbionts (symbiosis literally means ‘living together’; Box 2). They are usually considerably smaller than their hosts and can be parasites, commensals, mutualists or a combination of these, depending on context [6,7]. In this essay, we offer several opinions about how long-lived, large, environmentally buffered colony environments can shape the ecology and evolution of symbionts in ways that are quite distinct from the forces acting upon symbionts of solitary and gregarious organisms that normally lack such homeostatic fortress environments. We do so by focusing on the interfaces of evolutionary biology, epidemiology and macroecology. We suggest that parasites of long-lived insect societies might generally be less damaging than those associated with nonsocial hosts, because homeostatic colony life will tend to reduce virulence. In the same vein, mutualists of advanced insect societies could fail to achieve maximal productivity. They are predominantly ectosym- bionts [8], which implies that they are prone to attracting their own parasites and likely to maintain independent and sexual reproductive agendas that are costly for the host. We combine these arguments to infer that advanced insect societies are bound to create biodiversity hotspots that are interesting for comparative macroecological study, because they extend into dry and higher-latitude ecosys- tems that normally lack biodiversity hotspots. 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 evol- Opinion Corresponding author: Hughes, D.P. (d.p.hughes@exeter.ac.uk). 672 0169-5347/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2008.07.011 Available online 23 October 2008