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Eusocial Insects As Superorganisms Insights from Metabolic Theory

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Eusocial Insects As Superorganisms Insights from Metabolic Theory ARTICLE ADDENDUM Communicative & Integrative Biology 3:4, 360-362; July/August 2010; © 2010 Landes Bioscience Eusocial insects as superorganisms Insights from metabolic theory James F. Gillooly,1,* Chen Hou2 and Michael Kaspari3,4 1Department of Biology; University of Florida; Gainesville, FL USA; 2Department of Systems and Computational Biology; Albert Einstein College of Medicine; Bronx, NY USA; 3Ecology and Evolutionary Biology Graduate Program; Department of Zoology; University of Oklahoma; Norman, OK USA; 4Smithsonian Tropical Research Institute; Balboa, Republic of Panama e recently published a paper titled selection as a single entity at a level above W“Energetic Basis of Colonial that of gene and individual.1,2,7,9,10 While Living in Social Insects” showing that there remain calls for synthesis, based on basic features of whole colony physiol- bridging selfish genes with self-organiza- ogy and life history follow virtually the tion,11 there also exists a need for predic- same size-dependencies as unitary organ- tions allowing one to differentiate colonies isms when a colony’s mass is the summed structured by relatedness versus those mass of individuals. We now suggest that structured by ergonomic efficiency.12 these results are evidence, not only for Here we suggest that one way to test the the superorganism hypothesis, but also utility of the superorganism hypothesis is for colony level selection. In addition, to test its predictions about the size scal- we further examine the implications ing of life history traits. A basic prediction of these results for the metabolism and of the “gene-individual selection hypoth- lifetime reproductive success of eusocial esis” is that the reproductive behavior, insect colonies. We conclude by discuss- growth rate, indeed all life history traits ing the mechanisms which may underlie of a colony should arise from the summed the observed mass-dependence of sur- behavior of a colony’s genes and individu- vival, growth and reproduction in these als. For example, as long as an individual’s colonies. optimal metabolic rate fails to vary with colony mass this hypothesis predicts iso- Social insects occupy a central front in metric scaling of colony metabolism. [We the long-standing battle regarding units are unaware of any theory that predicts of selection in the evolution of biologi- how tactics maximizing individual fit- 1-6 7 Key words: allometry, metabolic rate, cal diversity. Ever since W.M. Wheeler ness in a eusocial insect colony should scaling, colony, multi-level selection coined the term “superorganism” there vary with colony size, and thus ultimately has been an historic dialectic among two result in colony level metabolic allometries Submitted: 03/24/10 camps over the ability for populations of like those we discuss here]. Accepted: 03/25/10 eusocial insects to evolve based on adapta- In contrast, the “superorganism tions, not of individual workers, but of the hypothesis” posits that selection acts on Previously published online: colonies in which they are a part. To skep- eusocial colonies just as it does on uni- www.landesbioscience.com/journals/cib/ tics the simplest explanation remains that tary organisms.1 If so, the same ecologi- article/11887 selection acts solely on the inclusive fitness cal challenges should generate convergent *Correspondence to: of a colony’s many individuals (or their phenotypic solutions regardless of the James F. Gillooly; Email: [email protected] genes).5,6,8 In the other camp are those level of selection. Consider, for example, that posit that “superorganism” is more colonies of leaf cutter ants competing Addendum to: Hou C, Kaspari M, Vander Zanden HB, Gillooly JF. Energetic basis of colonial living than a heuristic metaphor (e.g., queens with cattle for the grass of an Argentine in social insects. Proc Natl Acad Sci USA 2010; are the colony’s ovaries and workers its savannah. Both populations would tend 107:3634–8; PMID: 20133582; DOI: 10.1073/ soma) but that colonies indeed are organ- to accumulate organisms effective at con- pnas.0908071107. isms comprised of organisms that undergo suming grass, maintaining their microbial 360 Communicative & Integrative Biology Volume 3 Issue 4 ARTICLE ADDENDUM ARTICLE ADDENDUM Social Insects”,13 we show that basic fea- tures of whole colony physiology and life history follow virtually the same size- dependencies as unitary organisms when a colony’s mass is the summed mass of indi- viduals. Given the above reasoning, and in the absence of any similar theory arising from individual level selection, we suggest that this is evidence for the superorganism hypothesis, and hence colony level selec- tion. Here we further develop the impli- cations of these findings by making three points related to the size dependence of whole-colony metabolic rate, growth rate, reproductive rate and lifespan. First, in Hou et al. 2010 we observed that whole colony metabolic rate scales sublinearly with whole colony mass where M is mass. Thus, whole colony metabolic rate is not simply the sum of individual metabolic rates but is proportional to about M0.75, similar to the scaling found in unitary insects. This allometry implies that the per-capita metabolic rate of an individual worker is independent of col- ony mass when outside the colony, but that on average, metabolic rates of work- ers in a colony decrease with increasing colony mass c. M-1/4. Here we provide some support for this hypothesis by show- ing that this appears to be the case in at least one species, the honey bee (Fig. 1A). Note that this observation is remarkably similar to the metabolic rates of cells in a mammal: in vivo they scale to the -1/4 power of organism mass; in vitro and sep- arated from the organism from which they derive, cellular metabolic rate is indepen- dent of organism mass (Fig. 1B). Next we showed that egg produc- tion rates also scaled as approximately M¾, again mirroring the allometry of unitary organisms. Put another way, egg production is a constant fraction of the Figure 1. (A) Mass-specific metabolic rate of honey bees as function of colony mass (data of colony’s overall energy budget. One impli- 13 colonies from; data of individual bee is averaged from ref. 30 and 31). (B) Metabolic rate of single cation, consistent with the superorganism mammalian cells as function of body mass (reviewed in refs. 32 and 33). hypothesis, is that the metabolic rate of a colony governs the metabolic rate and egg symbionts, and producing viable off- chemistry and evolutionary history, one production rate of its queen. As such, a spring. Likewise, the savannah’s 100 or so would expect that the mass-specific allom- queen’s often prolific egg production13 is social insect species and innumerable uni- etries of growth and reproduction—the only an outlier in the diversity of life when tary animal species face the same evolu- basic patterns of metabolic ecology— the queen is viewed as an individual. tionary challenge—consume biomass and would converge, regardless of whether the Finally, we showed in Hou et al. 2010 convert it into efficiently into growth and organism was a colony or quadruped. that colony lifespan, as approximated reproduction. If there are a limited num- In our recently published paper titled by queen lifespan, scales with colony ber of effective solutions set by physics, “Energetic Basis of Colonial Living in mass in the same way as lifespan scales www.landesbioscience.com Communicative & Integrative Biology 361 12. Hammond RL, Keller L. Conflict over male parent- with body mass in unitary insects (i.e., (reviewed in ref. 27); each may thus con- age in social insects. PLoS Biol 2004; 2:1472-82. ∼M0.25). Again, the famously exceptional tribute to sub-linear metabolic scaling. 13. Hou C, Kaspari M, Vander Zanden HB, Gillooly JF. Energetic basis of colonial living in social insects. nature of social insect biology, this time Other candidates exist. Nest archi- Proc Natl Acad Sci USA 2010; 107:3634-8. 14-16 the lifespans of queens, may disap- tecture, variable with age and across spe- 14. Jemielity S, Chapuisat M, Parker JD, Keller L. Long pear in the context of the superorganism cies (reviewed in ref. 28), may constrain live the queen: studying aging in social insects. Age 2005; 27:241-8. hypothesis which views queens as the ova- metabolism in a variety of ways including 15. Keller L. Queen lifespan and colony characteristics in ries of a larger organism. Furthermore, gas exchange. Similarly, gas/heat exchange ants and termites. Insectes Soc 1998; 45:235-46. these results present interesting questions may scale allometrically if the way indi- 16. Keller L, Genoud M. Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 1997; regarding the relationship between colony viduals “clump” in the nest varies with 389:958-60. metabolism, queen metabolism, and the colony size, in turn shaping the colony’s 17. McCoy MW, Gillooly JF. Predicting natural mor- lifespan of queens/colonies, because they collective surface area to volume ratio. tality rates of plants and animals. Ecol Lett 2008; 11:710-6. suggest queen lifespan is inversely pro- Finally, at least one model has shown that 18. Tschinkel WR. Sociometry and sociogenesis of colo- portional to mass-specific colony meta- fractal-like foraging trails of some ants can nies of the harvester ant, Pogonomyrmex badius: bolic rate. On the one hand, from the generate something close to the observed worker characteristics in relation to colony size and seasons. Insectes Soc 1998; 45:385-410. 29 superorganism perspective, these results scaling of colony metabolic rate under 19. Brian MV, Elmes GW. Production by ant Tetramorium suggests that so long as queens are not the assumption that selection is acting on caespitum in a Southern english heath.
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