Animal Behaviour: Feeding the Superorganism - Cell Press

and Komdeur, J. (2009). ... J. Anim. Ecol. 70, 730–738. 12. Lindströ m, J. (1999). Early development and .... Ants. (Cambridge: Harvard University Press). 2.
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Alternatively, the observed effect is due to intense male–male competition, whereby an extra-pair male really is a ‘winner that takes it all’. He gains extra offspring, positions them such that they are more likely to survive, and such that the other male is even more likely to care for them. Game, set and match. Can the world be this simple? And if these ‘super extra-pair males’ indeed exist, would their status not be partly due to additive genetic effects, which females would then obtain when mating with these males and produce super sexy sons [20]? No doubt, the discussion about the genetic benefits of mate choice will continue. References 1. Jennions, M., and Petrie, M. (2000). Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75, 21–64. 2. Kempenaers, B. (2007). Mate choice and genetic quality: a review of the heterozygosity theory. Adv. Study Behav. 37, 189–278. 3. Arnqvist, G., and Kirkpatrick, M. (2005). The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females. Am. Nat. 165, 26–37.

4. Akc¸ay, E., and Roughgarden, J. (2007). Extrapair paternity in birds: review of the genetic benefits. Evol. Ecol. Res. 9, 855–868. 5. Griffith, S. (2007). The evolution of infidelity in socially monogamous passerines: neglected components of direct and indirect selection. Am. Nat. 169, 274–281. 6. Eliassen, S., and Kokko, H. (2008). Current analyses do not resolve whether extra-pair paternity is male or female driven. Behav. Ecol. Sociobiol. 62, 1795–1804. 7. Sheldon, B.C., Merila¨, J., Qvarnstro¨m, A., Gustafsson, L., and Ellegren, H. (1997). Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc. R. Soc. Lond. B 264, 297–302. 8. Magrath, M.J.L., Vedder, O., van der Velde, M., and Komdeur, J. (2009). Maternal effects contribute to the superior performance of extra-pair offspring. Curr. Biol. 19, 792–797. 9. Lemel, J. (1989). Body-mass dependent fledging order in the great tit. Auk 106, 490–492. 10. Both, C., Visser, M.E., and Verboven, N. (1999). Density-dependent recruitment rates in great tits: the importance of being heavier. Proc. R. Soc. Lond. B 266, 465–469. 11. Naef-Daenzer, B., Widmer, F., and Nuber, M. (2001). Differential post-fledging survival of great and coal tits in relation to their condition and fledging date. J. Anim. Ecol. 70, 730–738. 12. Lindstro¨m, J. (1999). Early development and fitness in birds and mammals. Trends Ecol. Evol. 14, 343–348. 13. Metcalfe, N.B., and Monaghan, P. (2001). Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 254–260.

Animal Behaviour: Feeding the Superorganism Insect societies are often described as superorganisms, and there are many functional parallels between organisms and superorganisms. Elegant work using ants shows that nutrient regulation, which occurs in many non-social animals, can also occur at the colony-level. Spencer T. Behmer Bert Ho¨lldobler and E.O. Wilson, two of the most renowned biologists in the world, recently followed their Pulitzer Prize-winning book The Ants [1] with a new book entitled Superorganism [2]. This book, which focuses on ants to take a fresh look at social evolution, defines a superorganism as: ‘‘A society, such as a eusocial insect colony, that possesses features of organization analogous to the physiological properties of single organisms. The eusocial colony, for example, is divided into reproductive castes (analogous to gonads) and worker castes (analogous to somatic tissue); its members may, for example, exchange nutrients and pheromones by trophallaxis and grooming

(analogous to the circulatory system). Among the thousand of known social insect species, we can find almost every conceivable grade in the division of labor, from little more than competition among nestmates for reproductive status to highly complex systems for specialized subcastes.’’

Key to the survival and growth of the superorganism, and also true for any non-social organism, is obtaining nutrients in the correct amounts and balance. Most animals require the same suite of about 30 nutrients — for example, a range of amino acids, sugars, fatty acids, vitamins, and in the case of insects, sterols — but the amounts and ratios that are needed to optimize growth differs among species, and can differ within a species depending on developmental

14. Krist, M., Na´dvornı´k, P., Uvı´rova´, L., and Buresˇ, S. (2005). Paternity covaries with laying and hatching order in the collared flycatcher Ficedula hypoleuca. Behav. Ecol. Sociobiol. 59, 6–11. 15. Arnold, K., and Owens, I.P.F. (2002). Extra-pair paternity and egg dumping in birds: life history, parental care and the risk of retaliation. Proc. R. Soc. Lond. B 269, 1263–1269. 16. Sheldon, B. (2002). Relating paternity to paternal care. Phil. Trans. Roy. Soc. B 357, 341–350. 17. Kempenaers, B., and Sheldon, B. (1996). Why do male birds not discriminate between their own and extra-pair offspring? Anim. Behav. 51, 1165–1173. 18. Lessells, C.M. (2002). Parentally biased favouritism: why should parents specialize in caring for different offspring? Phil. Trans. R. Soc. Lond. B 357, 381–403. 19. Slagsvold, T. (1997). Brood division in birds in relation to offspring size: sibling rivalry and parental control. Anim. Behav. 54, 1357–1368. 20. Kokko, H., Brooks, R., Jennions, M.D., and Morley, J. (2003). The evolution of mate choice and mating biases. Proc. R. Soc. Lond. B 270, 653–664.

Max Planck Institute for Ornithology, Department Behavioural Ecology & Evolutionary Genetics, E. Gwinnerstr., 82305 Starnberg (Seewiesen), Germany. E-mail: [email protected]

DOI: 10.1016/j.cub.2009.03.028

or reproductive status [3]. In this issue of Current Biology, Dussutour and Simpson [4] report, for the first time, that a superorganism can simultaneously regulate the intake of multiple nutrients to optimize colony growth. Equally important, they show the amounts of nutrients consumed, and the ratios in which they are consumed, are determined by the composition of the colony. For any non-social organism feeding decisions with respect to specific nutrients are made based on that individual’s current needs [5,6]. In contrast, a superorganism’s feeding decisions are more complex because foraging is restricted to a subset of a colony’s members. Thus, the challenge for individuals tasked with foraging is to address their own nutritional needs, while also responding to the needs of the queen, larvae, nurse ants and other workers. So what are the nutritional needs of the different members of an ant colony? Vinson and colleagues [7,8], studying red imported fire ants (Solenopsis invicta), found that

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foragers, nurses and workers primarily require energy, while larvae and queens require significant quantities of protein for growth and egg production, respectively. Adult ants are poor digesters of protein, so nurse ants generally take protein to the larvae first, where it can be digested extra-orally. Nurse ants then collect the digested protein and feed it to the queen, but nurses may also retain some for themselves, as a reserve. All members of the colony also require oils, with queens requiring greater proportions than either workers or larvae. In a series of starvation experiments, Vinson and colleagues [9] also demonstrated that fire ant foragers respond appropriately to nutritional deficits. When the colony was starved for sugar, more sugar was returned, with foragers retaining most of it. When colonies were starved for oil, foragers brought more oil back. It was distributed across the colony, but more of it went to nurses. Finally, when colonies were starved for protein, foragers returned with more protein, with much of it being retained by nurses. But how did foragers know what to collect? Ants exchange food with one another via trophallaxis, and a typical chain of exchange between members of a colony is shown in Figure 1. Reserve workers collect food from foragers, and pass it on to nurses, which in turn share it with the larvae. Foragers and larvae are thus linked by reserve and nurse ants, and nurse ants are likely to play a critical role in terms of providing information to the foragers about the current nutritional needs of the larvae in the colony [10]. The acceptance or rejection of food returned to the colony by foragers should heavily influence a forager’s decision to return with a similar food type. For instance, a steady supply of protein-rich insect material would be of little value to colonies with a small relative population of larvae. In the real world, though, organisms must simultaneously regulate multiple nutrients if they are to optimize performance. Protein and carbohydrates are the two key macronutrients that strongly influence ant colony growth and survival [11], and Dussutour and Simpson [4] used the experimental approach of the ‘Geometric Framework’ [12,13] to

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Figure 1. Food transfer between different members of a typical ant colony. Foragers, shown in black, give food to reserve ants, shown in blue. Reserve ants pass the food to nurse ants, shown in orange. Nurse ants then pass the food to the larvae, shown in yellow. As food is transferred between workers and nurse ants, sugars and oils can be extracted, but generally little protein is consumed by the workers. Larvae are the main consumers of protein and are also responsible for digesting the protein that eventually is fed to the queen by nurse ants. (Figure courtesy of Brad Vinson.)

study protein and carbohydrate regulation in an evolutionarily primitive omnivorous and opportunistic ant (Rhytidoponera sp.) which includes in its diet arthropods, dead insects, seeds and honeydew from sap-feeding hemipterans [14]. The Geometric Framework was originally developed to explore nutrient regulation in solitary insect herbivores, namely locusts and caterpillars, but over recent years it has also successfully been applied to study nutrient regulation in other animals, including chickens [15], rats [16], mice [17], fish [18], and humans [19]. The strength of the Geometric Framework is two-fold. First, it identifies the extent to which an organism, or superorganism, regulates, or ‘defends’, a specific nutrient ‘intake target’. For example, Figure 2A shows two foods, each containing fixed ratios of protein and carbohydrate, represented as trajectories, or ‘rails’, extending outwards from the origin. An organism can reach its protein–carbohydrate intake target, defined as the blend of protein and carbohydrate that

results in optimal growth, by switching back and forth between these two food rails. Dussutour and Simpson [4] found that their ants are strong protein–carbohydrate regulators across a range of nutritional scenarios, but that the protein:carbohydrate ratio a colony defends shifts depending on the presence of larvae. It is protein-biased when larvae are present, but carbohydrate-biased when larvae are absent. This shift could reflect changes in the nutritional needs of the colony, because larvae fail to grow when protein intake is low. Nurse ants were likely mediating this shift by rejecting offerings of protein-rich foods when larvae were absent. The second strength of the Geometric Framework is that it can reveal the extent to which an organism, or superorganism, prioritizes one nutrient over the other when confined to nutritionally imbalanced foods. In the case of protein–carbohydrate regulation, this response can be measured experimentally by placing an organism on a range of diets with various protein:carbohydrate ratios,

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Figure 2. How does the Geometric Framework work? (A) All animals grow best on a particular mixture of protein and carbohydrate. In the Geometric Framework this mixture is called the ‘intake target’ (represented by the red bulls-eye). Foods in the Geometric Framework are represented as trajectories, or ‘rails’, extending outward from the origin. Here two foods are represented. The pink line is a food with a fixed protein:carbohydrate ratio of 3:1, while the gold line is a food with a fixed protein:carbohydrate ratio of 1:4. An animal can reach its intake target by mixing the two foods (feeding is indicated by the small arrows running parallel to the food rails). The grey dotted line represents the protein:carbohydrate ratio that would be obtained if feeding on the two foods was random. Thus, the example shown demonstrates active nutrient regulation. (B) Regulatory rules with respect to each class of nutrient can be established by restricting animals to a range of foods with fixed protein:carbohydrate ratios (the five thin grey lines), measuring the intake point for each diet (the closed circles), and then constructing an ‘intake array’ (the colored lines) by connecting the observed intake points. The red bulls-eye represents the hypothetical intake target from (A), and the three colored lines represent three different regulatory responses. The orange line demonstrates strong carbohydrate regulation, while the blue line shows strong protein regulation. The green line represents a compromise. Here the nutrient in excess, relative to the intake target, is moderately over-eaten, while the nutrient in deficit, relative to the intake target, is moderately under-eaten.

measuring protein–carbohydrate intake for each diet, and then constructing an ‘intake array’ using the observed intake points for each diet. As shown in Figure 2B, a nearly vertical intake array demonstrates strong protein-regulation, while a horizontal intake array demonstrates strong carbohydrate-regulation. A third outcome, a more curved intake array, represents a compromise between over-eating the nutrient which is in excess of requirements, while under-eaten the nutrient that is in deficit. Dussutour and Simpson’s [4] work shows that ants, in the absence of larvae, place a premium on carbohydrate regulation. In contrast, when larvae are present, colonies restricted to carbohydrate-rich foods abandon carbohydrate regulation in order to increase their intake of protein, which is essential for larval development. When ants are restricted to protein-rich diets, however, they fail to overcome the carbohydrate deficit. High worker mortality was observed on the protein-rich foods both in the presence and absence of larvae, despite the fact that ants were able to manipulate the collected diet. They were very efficient at extracting carbohydrate, and processing and rejecting large quantities of protein, but clearly there was a cost associated with performing this task, particularly in the absence of the larvae. Additionally, larval survival and development was also extremely poor on protein-rich diets. This finding is consistent with work showing that larval and colony growth is greatly enhanced when both protein and carbohydrates are in adequate supply [11,20]. Ants have clearly proven to be premier organisms for research in behavioral ecology and sociobiology, and have been used to greatly further our understanding of a number of biological phenomena [1]. Dussutour and Simpson’s [4] paper helps shed further light on the nature of physiological and behavioral regulatory processes in social organizations, and the hierarchy in control processes, particularly in relation to nutrition. This paper also demonstrates that for organisms and superorganisms alike, optimal performance is all about getting their nutritional balance right.

References 1. Ho¨lldobler, B., and Wilson, E.O. (1990). The Ants. (Cambridge: Harvard University Press). 2. Ho¨lldobler, B., and Wilson, E.O. (2009). The Superorganism: The Beauty, Elegance, and Strangeness of Insect Societies. (New York: W.W. Norton). 3. Behmer, S.T. (2009). Insect herbivore nutrient regulation. Annu. Rev. Entomol. 54, 165–187. 4. Dussutour, A., and Simpson, S.J. (2009). Communal nutrition in ants. Curr. Biol. 19, 740–744. 5. Simpson, S.J., and Raubenheimer, D. (2000). The hungry locust. Adv. Anim. Behav. 29, 1–44. 6. Simpson, S.J., Sibly, R.M., Lee, K.P., Behmer, S.T., and Raubenheimer, D. (2004). Optimal foraging when regulating intake of multiple nutrients. Anim. Behav. 68, 1299–1311. 7. Sorensen, A.A., and Vinson, S.B. (1981). Quantitative food distribution studies within laboratory colonies of the imported fire ant, Solenopsis invicta Buren. Insect Socio. 28, 129–160. 8. Sorensen, A.A., Mirenda, J.T., and Vinson, S.B. (1981). Food exchange and distribution by functional subcastes of the imported fire ant, Solenopsis invicta Buren. Insect Socio. 28, 383–394. 9. Sorensen, A.A., Busch, T.M., and Vinson, S.B. (1985). Control of food influx by temporal subcastes in the fire ant, Solenopsis invicta. Behav. Ecol. Sociobiol. 17, 191–198. 10. Casill, D.L., and Tschinkel, W.R. (1999). Regulation of diet in the fire ant, Solenopsis invicta. J. Insect Behav. 12, 307–328. 11. Macom, T.E., and Porter, S.D. (1995). Food and energy requirements of laboratory fire ant colonies (Hymenoptera: Formicidae). Environ. Entomol. 24, 387–391. 12. Raubenheimer, D., and Simpson, S.J. (1999). Integrating nutrition: a geometrical approach. Entomol. Exp. Appl. 91, 67–82. 13. Simpson, S.J., and Raubenheimer, D. (1999). Assuaging nutritional complexity: a geometrical approach. Proc. Nutr. Soc. 58, 779–789. 14. Ward, P.S. (1981). Ecology and life history of the Rhytidoponera impressa group (Hymenoptera: Formicidae). I. Habitats, nest sites, and foraging behavior. Psyche 88, 89–108. 15. Raubenheimer, D., and Simpson, S.J. (1997). Integrative models of nutrient balancing: application to insects and vertebrates. Nutr. Res. Rev. 10, 151–179. 16. Simpson, S.J., and Raubenheimer, D. (1997). The geometric analysis of feeding and nutrition in the rat. Appetite 28, 201–213. 17. Sørensen, A., Mayntz, D., Raubenheimer, D., and Simpson, S.J. (2008). Protein leverage in mice: geometry of macronutrient balancing and consequences for fat deposition. Obesity 16, 566–571. 18. Ruohonen, K., Simpson, S.J., and Raubenheimer, R. (2007). A new approach to diet optimization: a re-analysis using European whitefish (Coregonus lavaretus). Aquaculture 267, 147–156. 19. Simpson, S.J., Batley, R.B., and Raubenheimer, D. (2003). Geometric analysis of macronutrient intake in humans: the power of protein? Appetite 41, 123–140. 20. Tschinkel, W.R. (2006). The Fire Ants. (Cambridge: Harvard University Press.)

Department of Entomology, Texas A&M University, College Station, TX 77843-2475, USA. E-mail: [email protected]

DOI: 10.1016/j.cub.2009.03.033