Elsevier

Animal Behaviour

Volume 83, Issue 4, April 2012, Pages 1043-1049
Animal Behaviour

Evolution of brain size in class-based societies of fungus-growing ants (Attini)

https://doi.org/10.1016/j.anbehav.2012.01.032Get rights and content

A social lifestyle is often assumed to be more complex than a solitary one, due to social demands that may require increased cognitive capabilities. These nested assumptions underlie hypotheses to explain a correlation between brain size and group size in social vertebrates, using group size and accumulation of social traits, as alternative proxies for social complexity. Eusocial insects challenge the generality of the hypothesis that social complexity relies on increased cognitive capabilities of individuals. We used data from previously published studies to test for an association between sociality and brain size across 18 species (nine genera) of fungus-growing ants (Attini), which range from basal taxa with fewer than 100 monomorphic individuals, to derived colonies containing several million polymorphic, highly specialized individuals. Among monomorphic species, increased colony size was associated with decreased relative brain size and increased olfactory lobe size, although the latter result was sensitive to both the exclusion of potential outliers and whether phylogenetically independent contrasts were used. Within leafcutters (Atta), the relative size of the antennal lobes was also associated with group size, but may also reflect ecological foraging specialization, which may be a confounding variable. Comparisons between class- and individual-based societies highlight the general problem of increasing social structure in proportion to group size and show that there are alternative solutions to this problem: one alternative involves increasing behavioural specialization of individuals and evolved rules; the other involves increased diversification of individual behaviour, social norms and ultimately institutions.

Highlights

► We examined sociality and brain size in nine genera of fungus-growing ants (Attini). ► Fungus-growing ants showed broad variation in colony size and social organization. ► Brain size varied among taxa in larger colonies and in more tightly knit societies. ► Larger colony size was associated with differential investment in olfactory brain centres. ► Analyses of social complexity using a scalogram yielded results similar to those using group size as a proxy.

Section snippets

Data Sources and Study Taxa

We obtained data on relative brain mass for 18 species across nine genera in the ant tribe Attini from Seid et al. (2011). The glomeruli of the antennal lobes are the brain regions primarily responsible for processing olfactory inputs. We obtained the relative sizes of the antennal lobes (antennal lobe/optic lobe) and number of glomeruli for 25 species in nine attine genera from Kelber et al. (2009). Since each glomerulus receives projections from neurons expressing a single receptor gene (

Results and discussion

Among attine species there was a significant quadratic association between relative brain size and colony size (R2 = 0.56, N = 18, P = 0.005; after PIC: R2 = 0.52, P = 0.006; Fig. 1a, Table 1), which provided a better fit than a linear equation (R2 = 0.24, N = 18, P = 0.039), but was marginally nonsignificant after PIC correction (R2 = 0.19, P = 0.07). This association was strongly affected by two species, Acromyrmex echinatior and Atta colombica, which are leafcutter species with huge colonies that are commonly

Acknowledgments

We thank Simon Tierney and anonymous referees for helpful comments of earlier versions of this manuscript. A.J.R. was supported by a Latin American Fellowship from the Smithsonian Tropical Research Institute (STRI), and by the Smithsonian Institution’s Scholarly Studies Program (to W. Eberhard, A. J. Riveros and W. Wcislo). We are also grateful for the generous support from the F.H. Levinson Fund to STRI’s Laboratory of Behavior & Evolutionary Biology, and for general research funds from STRI.

References (79)

  • T.J. Bergman et al.

    Hierarchical classification by rank and kinship in baboons

    Science

    (2003)
  • E.A. Bernays et al.

    Sensory capabilities, information processing, and resource specialization

    Quarterly Review of Biology

    (1994)
  • J.T. Bonner

    Dividing the labour in cells and societies

    Current Science

    (1993)
  • J.T. Bonner

    Why Size Matters

    (2006)
  • A.F.G. Bourke

    Colony size, social complexity and reproductive conflict in social insects

    Journal of Evolutionary Biology

    (1999)
  • R.W. Byrne et al.

    Brain evolution: when is a group not a group?

    Current Biology

    (2007)
  • R.W. Byrne et al.

    Neocortex size predicts deception rate in primates

    Proceedings of the Royal Society B

    (2004)
  • R.L. Carneiro

    Scale analysis as an instrument for the study of cultural evolution

    Southwestern Journal of Anthropology

    (1962)
  • R.L. Carneiro

    On the relationship between size of population and complexity of social organization

    Southwestern Journal of Anthropology

    (1967)
  • R.L. Carneiro

    The evolution of complexity in human societies and its mathematical expression

    International Journal of Comparative Sociology

    (1987)
  • R.L. Carneiro

    The transition from quantity to quality: a neglected causal mechanism in accounting for social evolution

    Proceedings of the National Academy of Sciences, U.S.A.

    (2000)
  • R.L. Carneiro et al.

    The application of scale analysis to the study of cultural evolution

    Transactions of the New York Academy of Science

    (1963)
  • R. Condit et al.

    Trees of Panama and Costa Rica

    (2010)
  • F. Dujardin

    Mémoire sur le système nerveux des insects

    Annales des Sciences Naturelles Zoologie et Biologie

    (1850)
  • R.I.M. Dunbar

    The social brain hypothesis

    Evolutionary Anthropology

    (1998)
  • R.I.M. Dunbar

    The social brain: mind, language, and society in evolutionary perspective

    Annual Review of Anthropology

    (2003)
  • R.I.M. Dunbar et al.

    Evolution in the social brain

    Science

    (2007)
  • S.M. Farris et al.

    Coevolution of generalist feeding ecologies and gyrencephalic mushroom bodies in insects

    Proceedings of the National Academy of Sciences, U.S.A.

    (2005)
  • S.M. Farris et al.

    Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects

    Proceedings of the Royal Society B

    (2011)
  • M. Gell-Mann

    Regularities in human affairs

    Cliodynamics

    (2011)
  • W. Gronenberg et al.

    Social brains and behavior: past and present

  • L. Guttman

    A basis for scaling qualitative data

    American Sociological Review

    (1944)
  • M. Heisenberg

    What do mushroom bodies do for the insect brain?

    Learning & Memory

    (1998)
  • K.E. Holekamp

    Questioning the social intelligence hypothesis

    Trends in Cognitive Sciences

    (2006)
  • B. Hölldobler

    The chemistry of social regulation: multicomponent signals in ant societies

    Proceedings of the National Academy of Sciences, U.S.A.

    (1995)
  • B. Hölldobler et al.

    The Ants

    (1990)
  • B. Hölldobler et al.

    The Superorganism

    (2009)
  • B. Hölldobler et al.

    The Leafcutter Ants; Civilization by Instinct

    (2010)
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