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Behavior, brain, and morphology in a complex insect society: trait integration and social evolution in the exceptionally polymorphic ant Pheidole rhea

  • Darcy G. Gordon
  • Iulian Ilieş
  • James F. A. Traniello
Original Article

Abstract

Polyphenisms in social insects arise from flexible developmental mechanisms that may produce behaviorally and morphologically specialized workers. The ant genus Pheidole is typically characterized by small minor worker and large soldier subcastes, but larger supersoldiers have evolved in several species, including the exceptionally polymorphic Pheidole rhea. To examine worker phenotype evolution in this socially complex ant, we tested the hypotheses that behavior, brain structure, and morphology are integrated within worker size classes due to selection for specialized social roles and that traits have been discretized among these groups. Our analyses revealed significant differences in brain structure and body shape between minor workers and the two soldier size classes. Behavioral repertoires of minors, soldiers, and supersoldiers were similar, but minors performed important tasks at higher frequencies than soldiers and supersoldiers. The extensive overlap in behavioral repertoire between soldier and supersoldier groups correlated with shared neuroanatomical and morphological traits. Although head and body size vary allometrically among P. rhea size classes, scaling analyses revealed little allometry in brain substructure. The covariation of behavior and brain organization between soldier size classes suggests that their functionality may be due to differences in task performance rate or efficiency rather than task repertoire. The early branching position of P. rhea in the phylogeny of Pheidole and patterns of worker phenotypic plasticity suggest this species exhibits an ancestral state of sociobiological and neurobiological organization that served as a ground plan for diversification in this ecologically dominant ant genus. Selection for divergent social roles may impact the degree to which behavioral, neuroanatomical, and morphological phenotypes are integrated within individuals and between specialized groups. Behavioral repertoire, neuroanatomy, and worker body shape in the strongly polymorphic P. rhea, a species of the hyperdiverse ant genus Pheidole that branched early in the phylogeny of the clade appear to show a relatively low degree of integration with worker head-body size. The putatively ancestral and developmentally plastic condition in which larger-bodied soldier groups are not distinguishable in behavior, brain scaling relationships, and body shape suggests the advantage of worker head-body allometry may derive from variation in quantitative aspects of behavioral performance rather than specialization on qualitatively different tasks. This appears to be significant to social evolution in the genus.

Keywords

Division of labor Caste development Social brain evolution Neuroethology Developmental plasticity Trait integration 

Notes

Acknowledgments

We thank S. Cover for access to museum specimens and valuable insights from his extensive field experience. We are grateful to Dr. M. Huang for access to colonies used in the neuroanatomical and behavioral studies and to Dr. W. Gronenberg for sharing his expertise in histology and comments on the manuscript. We thank Drs. M.L. Muscedere, S. Arganda, J.F. Kamhi, and Y.M. Giraldo, as well as A.P. Hoadley for their comments and technical support, and Dr. E. Abouheif and one anonymous reviewer for their constructive insights on the manuscript. This research was supported by National Science Foundation grant IOS 1354291 to JFAT and a Grant-in-Aid-of-Research from the Society of Integrative and Comparative Biology to DGG.

Data availability

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

Compliance with ethical standard

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2017_2396_MOESM1_ESM.pdf (256 kb)
ESM 1 (PDF 256 kb)
265_2017_2396_MOESM2_ESM.pdf (251 kb)
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265_2017_2396_MOESM3_ESM.pdf (248 kb)
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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Darcy G. Gordon
    • 1
  • Iulian Ilieş
    • 2
  • James F. A. Traniello
    • 1
    • 3
  1. 1.Department of BiologyBoston UniversityBostonUSA
  2. 2.Healthcare Systems Engineering Institute, College of EngineeringNortheastern UniversityBostonUSA
  3. 3.Graduate Program for NeuroscienceBoston UniversityBostonUSA

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