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, 466 (7310), 1057-62

The Evolution of Eusociality

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The Evolution of Eusociality

Martin A Nowak et al. Nature.

Abstract

Eusociality, in which some individuals reduce their own lifetime reproductive potential to raise the offspring of others, underlies the most advanced forms of social organization and the ecologically dominant role of social insects and humans. For the past four decades kin selection theory, based on the concept of inclusive fitness, has been the major theoretical attempt to explain the evolution of eusociality. Here we show the limitations of this approach. We argue that standard natural selection theory in the context of precise models of population structure represents a simpler and superior approach, allows the evaluation of multiple competing hypotheses, and provides an exact framework for interpreting empirical observations.

Figures

Figure 1
Figure 1. The ultimate superorganisms
The gigantic queens of the leafcutter ants, one of whom (upper panel) is shown here, attended by some of her millions of daughter workers. Differences in size and labor specialization allows the ants to cut and gather leaf fragments (middle panel), and convert the fragments into gardens to grow fungi (lower panel). The species shown are respectively, top to bottom, Atta vollenweideri, A. sexdens, and A. cephalotes. (Photos by Bert Hölldobler.)
Figure 2
Figure 2. Species on either side of the eusociality threshold
A. A colony of a primitively eusocial Synalpheus snapping shrimp, occupying a cavity excavated in a sponge. The large queen (reproductive member) is supported by her family of workers, one of whom guards the nest entrance (from Duffy). B. A colony of the primitively eusocial halictid bee Lasioglossum duplex, which has excavated a nest in the soil (from Sakagami and Hayashida). C. Adult erotyid beetles of the genus Pselaphacus leading their larvae to fungal food (from Costa); this level of parental care is widespread among insects and other arthropods, but has never been known to give rise to eusociality. These three examples illustrate the principle that the origin of eusociality requires the preadaptation of a constructed and guarded nest site.
Figure 3
Figure 3. The limitation of inclusive fitness
A. The standard approach of evolutionary dynamics takes into account the relevant interactions and then calculates the fitness of each individual. B. The inclusive fitness of an individual is the sum of how the action of that individual affects its own fitness plus that of any other individuals multiplied by relatedness. Inclusive fitness theory is based on the very limiting assumption that the fitness of each individual can be broken down into additive components caused by individual actions. This is not possible in general. C. For calculating inclusive fitness one has to keep track of all competitive interactions that occur in the population. Here A acts on B changing its payoff and fitness. If A or B compete with other individuals, then their fitness values are also affected by A’s action, although no action is directed towards them. Inclusive fitness theory is not a simplification over the standard approach. It is an alternative accounting method, but one that works only in a very limited domain. Whenever inclusive fitness does work, the results are identical to those of the standard approach. Inclusive fitness theory is an unnecessary detour, which does not provide additional insight or information.
Figure 4
Figure 4. Solitary and primitively eusocial waps
A. Progressive provisioning in a solitary wasp. Cutaway view of a nest showing a female Synagris cornuta feeding her larva with a fragment of caterpillar. An ichneumonid wasp and parasite Osprynchotus violator lurks on the outside of the nest (from Cowan) waiting for the right moment to attack the larva. B. A colony of the primitively eusocial wasp Polistes crinitus. Its workers, working together are able simultaneously to guard the nest, forage for food, and attend the larvae sequestered in the nest cells. (Photo by Robert Jeanne.)

Comment in

  • Call for a return to rigour in models.
    van Veelen M, García J, Sabelis MW, Egas M. van Veelen M, et al. Nature. 2010 Oct 7;467(7316):661. doi: 10.1038/467661d. Nature. 2010. PMID: 20930826 No abstract available.
  • Better living through physics.
    Krakauer DC, Flack JC. Krakauer DC, et al. Nature. 2010 Oct 7;467(7316):661. doi: 10.1038/467661a. Nature. 2010. PMID: 20930827 No abstract available.
  • Ground truth is the test that counts.
    Nonacs P. Nonacs P. Nature. 2010 Oct 7;467(7316):661. doi: 10.1038/467661c. Nature. 2010. PMID: 20930828 No abstract available.
  • Inclusive fitness is just bookkeeping.
    Doebeli M. Doebeli M. Nature. 2010 Oct 7;467(7316):661. doi: 10.1038/467661b. Nature. 2010. PMID: 20930829 No abstract available.
  • Inclusive fitness theory and eusociality.
    Abbot P, Abe J, Alcock J, Alizon S, Alpedrinha JA, Andersson M, Andre JB, van Baalen M, Balloux F, Balshine S, Barton N, Beukeboom LW, Biernaskie JM, Bilde T, Borgia G, Breed M, Brown S, Bshary R, Buckling A, Burley NT, Burton-Chellew MN, Cant MA, Chapuisat M, Charnov EL, Clutton-Brock T, Cockburn A, Cole BJ, Colegrave N, Cosmides L, Couzin ID, Coyne JA, Creel S, Crespi B, Curry RL, Dall SR, Day T, Dickinson JL, Dugatkin LA, El Mouden C, Emlen ST, Evans J, Ferriere R, Field J, Foitzik S, Foster K, Foster WA, Fox CW, Gadau J, Gandon S, Gardner A, Gardner MG, Getty T, Goodisman MA, Grafen A, Grosberg R, Grozinger CM, Gouyon PH, Gwynne D, Harvey PH, Hatchwell BJ, Heinze J, Helantera H, Helms KR, Hill K, Jiricny N, Johnstone RA, Kacelnik A, Kiers ET, Kokko H, Komdeur J, Korb J, Kronauer D, Kümmerli R, Lehmann L, Linksvayer TA, Lion S, Lyon B, Marshall JA, McElreath R, Michalakis Y, Michod RE, Mock D, Monnin T, Montgomerie R, Moore AJ, Mueller UG, Noë R, Okasha S, Pamilo P, Parker GA, Pedersen JS, Pen I, Pfennig D, Queller DC, Rankin DJ, Reece SE, Reeve HK, Reuter M, Roberts G, Robson SK, Roze D, Rousset F, Rueppell O, Sachs JL, Santorelli L, Schmid-Hempel P, Schwarz MP, Scott-Phillips T, Shellmann-Sherman J, Sherman PW, Shuker DM, Smith J, Spagna JC, Strassmann B, Suarez AV, Sundström L, Taborsky M, Taylor P, Thompson G, Tooby J, Tsutsui ND, Tsuji K, Turillazzi S, Ubeda F, Vargo EL, Voelkl B, Wenseleers T, West SA, West-Eberhard MJ, Westneat DF, Wiernasz DC, Wild G, Wrangham R, Young AJ, Zeh DW, Zeh JA, Zink A. Abbot P, et al. Nature. 2011 Mar 24;471(7339):E1-4; author reply E9-10. doi: 10.1038/nature09831. Nature. 2011. PMID: 21430721 Free PMC article.
  • Only full-sibling families evolved eusociality.
    Boomsma JJ, Beekman M, Cornwallis CK, Griffin AS, Holman L, Hughes WO, Keller L, Oldroyd BP, Ratnieks FL. Boomsma JJ, et al. Nature. 2011 Mar 24;471(7339):E4-5; author reply E9-10. doi: 10.1038/nature09832. Nature. 2011. PMID: 21430722
  • Kin selection and eusociality.
    Strassmann JE, Page RE Jr, Robinson GE, Seeley TD. Strassmann JE, et al. Nature. 2011 Mar 24;471(7339):E5-6; author reply E9-10. doi: 10.1038/nature09833. Nature. 2011. PMID: 21430723
  • Inclusive fitness in evolution.
    Ferriere R, Michod RE. Ferriere R, et al. Nature. 2011 Mar 24;471(7339):E6-8; author reply E9-10. doi: 10.1038/nature09834. Nature. 2011. PMID: 21430724
  • In defence of inclusive fitness theory.
    Herre EA, Wcislo WT. Herre EA, et al. Nature. 2011 Mar 24;471(7339):E8-9; author reply E9-10. doi: 10.1038/nature09835. Nature. 2011. PMID: 21430725

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