Skip to main content
SpringerLink
Log in

Into the black and back: the ecology of brain investment in Neotropical army ants (Formicidae: Dorylinae)

  • Original Paper
  • Published:
The Science of Nature Aims and scope Submit manuscript

Abstract

Shifts to new ecological settings can drive evolutionary changes in animal sensory systems and in the brain structures that process sensory information. We took advantage of the diverse habitat ecology of Neotropical army ants to test whether evolutionary transitions from below- to above-ground activity were associated with changes in brain structure. Our estimates of genus-typical frequencies of above-ground activity suggested a high degree of evolutionary plasticity in habitat use among Neotropical army ants. Brain structure consistently corresponded to degree of above-ground activity among genera and among species within genera. The most above-ground genera (and species) invested relatively more in visual processing brain tissues; the most subterranean species invested relatively less in central processing higher-brain centers (mushroom body calyces). These patterns suggest a strong role of sensory ecology (e.g., light levels) in selecting for army ant brain investment evolution and further suggest that the subterranean environment poses reduced cognitive challenges to workers. The highly above-ground active genus Eciton was exceptional in having relatively large brains and particularly large and structurally complex optic lobes. These patterns suggest that the transition to above-ground activity from ancestors that were largely subterranean for approximately 60 million years was followed by re-emergence of enhanced visual function in workers.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Allman JM (2000) Evolving brains. Scientific American Library, New York

    Google Scholar 

  • Barton RA, Harvey PH (2000) Mosaic evolution of brain structure in mammals. Nature 405:1055–1058

    Article  CAS  PubMed  Google Scholar 

  • Barton RA, Purvis AA, Harvey PH (1995) Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores. Philos Trans R Soc Lond B 348:381–392

    Article  CAS  Google Scholar 

  • Baudier KM, Mudd AE, Erickson SC, O’Donnell S (2015) Microhabitat and body size effects on heat tolerance: implications for responses to climate change (army ants: Formicidae, Ecitoninae). J Anim Ecol 84:1322–1330

    Article  PubMed  Google Scholar 

  • Berghoff SM, Franks NR (2007) First record of the army ant Cheliomyrmex morosus in Panama and its high associate diversity. Biotropica 39:771–773

    Article  Google Scholar 

  • Brady SG (2003) Evolution of the army ant syndrome: the origin and long-term evolutionary stasis of a complex of behavioral and reproductive adaptations. Proc Natl Acad Sci U S A 100:6575–6579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci U S A 103:18172–18177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brady SG, Fisher BK, Schultz TR, Ward PS (2014) The rise of army ants and their relatives: diversification of specialized predatory doryline ants. BMC Evol Biol 14:1–14

    Article  Google Scholar 

  • Catania KC (2005) Evolution of sensory specializations in insectivores. Anat Rec A 287:1038–1050

    Article  Google Scholar 

  • Coody CJ, Watkins JF II (1986) The correlation of eye size with circadian flight periodicity of Nearctic army ant males of the genus Neivamyrmex (Hymenoptera; Formicidae; Ecitoninae). Tex J Sci 38

  • Dunn R (2003) Imposter in the nest. Nat Hist 112:22–26

    Google Scholar 

  • Eberhard WG, Wcislo WT (2011) Grade changes in brain–body allometry: morphological and behavioural correlates of brain size in miniature spiders, insects and other invertebrates. Adv Insect Physiol 40:155–214

    Article  Google Scholar 

  • Fahrbach SE (2006) Structure of the mushroom bodies of the insect brain. Annu Rev Entomol 51:209–232

    Article  CAS  PubMed  Google Scholar 

  • Farris SM (2008) Evolutionary convergence of higher order brain centers spanning the protostome deuterostome boundary. Brain Behav Evol 72:106–122

    Article  PubMed  Google Scholar 

  • Farris SM, Robinson GE, Fahrbach SE (2001) Experience and age-related outgrowth of intrinsic neurons in the mushroom bodies of the adult worker honeybee. J Neurosci 21:6395–6404

    CAS  PubMed  Google Scholar 

  • Gotwald WH Jr (1995) Army ants: the biology of social predation. Cornell University Press, Ithaca

    Google Scholar 

  • Gronenberg W (1999) Modality-specific segregation of input to ant mushroom bodies. Brain Behav Evol 54:85–95

    Article  CAS  PubMed  Google Scholar 

  • Gronenberg W (2001) Subdivisions of Hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 436:474–489

    Article  Google Scholar 

  • Gronenberg W, Hölldobler B (1999) Morphologic representation of visual and antennal information in the ant brain. J Comp Neurol 412:229–240

    Article  CAS  PubMed  Google Scholar 

  • Gronenberg W, Liebig J (1999) Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–345

    Article  CAS  Google Scholar 

  • Gronenberg W, Riveros AJ (2009) Social brains and behavior: past and present. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Cambridge, pp 377–401

    Google Scholar 

  • Gronenberg W, Heeren S, Hölldobler B (1996) Age dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011–2019

    PubMed  Google Scholar 

  • Hodos W, Butler AB (1997) Evolution of sensory pathways in vertebrates. Brain Behav Evol 50:189–197

    Article  CAS  PubMed  Google Scholar 

  • Ilies I, Muscedere ML, Traniello JFA (2015) Neuroanatomical and morphological trait clusters in the ant genus Pheidole: evidence for modularity and integration in brain structure. Brain Behav Evol 85:63–76

    Article  PubMed  Google Scholar 

  • Jeffery WR (2001) Cavefish as a model system in evolutionary developmental biology. Dev Biol 231:1–12

    Article  CAS  PubMed  Google Scholar 

  • Jones TA, Donlan NA, O’Donnell S (2009) Growth and pruning of mushroom body Kenyon cell dendrites during worker behavioral development in the paper wasp, Polybia aequatorialis (Hymenoptera: Vespidae). Neurobiol Learn Mem 92:485–495

    Article  PubMed  Google Scholar 

  • Kaspari M, Powell S, Lattke J, O’Donnell S (2011) Predation and patchiness in the tropical litter: do swarm‐raiding army ants skim the cream or drain the bottle? J Anim Ecol 80:818–823

    Article  PubMed  Google Scholar 

  • Kuebler LS, Kelber C, Kleineidam CJ (2010) Distinct antennal lobe phenotypes in the leaf‐cutting ant (Atta vollenweideri). J Comp Neurol 518:352–365

    Article  CAS  PubMed  Google Scholar 

  • Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480

    Article  CAS  PubMed  Google Scholar 

  • Lefebvre L, Sol D (2008) Brains, lifestyles and cognition: are there general trends? Brain Behav Evol 72:135–144

    Article  PubMed  Google Scholar 

  • Mace GM, Eisenberg JF (1982) Competition, niche specialization and the evolution of brain size in the genus Peromyscus. Biol J Linn Soc 17:243–257

    Article  Google Scholar 

  • Moller AP, Erritzoe J, Garamszegi LZ (2005) Covariation between brain size and immunity in birds: implications for brain size evolution. J Evol Biol 18:223–237

    Article  CAS  PubMed  Google Scholar 

  • Moreau CS, Bell CD, Vila R, Archibald SB, Pierce NE (2006) Phylogeny of the ants: diversification in the age of angiosperms. Science 312:101–104

    Article  CAS  PubMed  Google Scholar 

  • Moser JC, Reeve JD, Bento JMS, Della Lucia TMC, Cameron RS, Heck NM (2004) Eye size and behaviour of day- and night-flying leafcutting ant alates. J Zool Lond 264:69–75

    Article  Google Scholar 

  • Mota T, Yamagata N, Giurfa M, Gronenberg W, Sandoz J-C (2011) Neural organization and visual processing in the anterior optic tubercle of the honeybee brain. J Neurosci 31:11443–11456

    Article  CAS  PubMed  Google Scholar 

  • Muscedere ML, Traniello JFA (2012) Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste- and age-related patterns of worker brain organization. PLoS One 7, e31618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narendra A, Reid SF, Greiner B, Peters RA, Hemmi JM, Ribi WA, Zeil J (2011) Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants. Proc R Soc B 278:1141–1149

    Article  PubMed  PubMed Central  Google Scholar 

  • Navarrete A, van Schaik CP, Isler K (2011) Energetics and the evolution of human brain size. Nature 480:91–93

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa M, Watanabe H, Yokohari F (2012) Higher brain centers for social tasks in worker ants, Camponotus japonicas. J Comp Neurol 520:1584–1598

    Article  PubMed  Google Scholar 

  • Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804

    Article  CAS  PubMed  Google Scholar 

  • O’Donnell S, Lattke J, Powell S, Kaspari M (2005) Extraordinary predation by the Neotropical army ant Cheliomyrmex andicola: implications for the evolution of the army ant syndrome. Biotropica 37:706–709

    Article  Google Scholar 

  • O’Donnell S, Lattke J, Powell S, Kaspari M (2007) Army ants in four forests: geographic variation in raid rates and species composition. J Anim Ecol 76:580–589

    Article  PubMed  Google Scholar 

  • O’Donnell S, Lattke J, Powell S, Kaspari M (2009) Species and site differences in Neotropical army ant emigration behavior. Ecol Entomol 34:476–482

    Article  Google Scholar 

  • O’Donnell S, Kumar A, Logan C (2010) Army ant raid attendance and bivouac-checking behavior by Neotropical montane forest birds. Wilson J Ornithol 122:503–512

    Article  Google Scholar 

  • O’Donnell S, Clifford MR, DeLeon S, Papa C, Zahedi N, Bulova SJ (2013) Brain size and visual environment predict species differences in paperwasp sensory processing brain regions (Hymenoptera: Vespidae, Polistinae). Brain Behav Evol 82:177–184

    Article  PubMed  Google Scholar 

  • O’Donnell S, Bulova SJ, DeLeon S, Khodak P, Miller S, Sulger E (2015) Distributed cognition and social brains: reductions in mushroom body investment accompanied the origins of sociality in wasps (Hymenoptera: Vespidae). Proc R Soc B 282:20150791

    Article  PubMed  Google Scholar 

  • Perfecto I (1992) Observations of a Labidus coecus (Latreille) underground raid in the central highlands of Costa Rica. Psyche 99:214–220

    Article  Google Scholar 

  • Rabeling C, Brown JM, Verhaagh M (2008) Newly discovered sister lineage sheds light on early ant evolution. Proc Natl Acad Sci U S A 105:14913–14917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rehan SM, Bulova SJ, O’Donnell S (2015) Cumulative effects of foraging behavior and social dominance on brain development in a facultatively social bee (Ceratina australensis). Brain Behav Evol 85:117–124

    Article  PubMed  Google Scholar 

  • Rettenmeyer CW (1963) Behavioral studies of army ants. Univ Kans Sci Bull 44:281–465

    Google Scholar 

  • Schneirla TC (1971) Army ants: a study in social organization. W. H. Freeman, Oxford, England

    Google Scholar 

  • Seid MA, Castillo A, Wcislo WT (2011) The allometry of brain miniaturization in ants. Brain Behav Evol 77:5–13

    Article  PubMed  Google Scholar 

  • Sherry DF (2006) Neuroecology. Annu Rev Psychol 57:167–197

    Article  PubMed  Google Scholar 

  • Smaers JB, Soligo C (2013) Brain reorganization, not relative brain size, primarily characterizes anthropoid brain evolution. Proc Biol Sci 280:20130269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthoprod Struct Dev 34:235–256

    Article  Google Scholar 

  • Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11–37

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sulger E, Mcaloon N, Bulova SJ, Sapp J, O’Donnell S (2014) Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca). Biol J Linn Soc 113:415–422

    Article  Google Scholar 

  • Villareal DG, MacKay WP, Manriguez AR, Vinson SB (1995) New records for the ant Cheliomyrmex morosus in Mexico (Hymenoptera: Formicidae). J New York Ent Soc 103:219–220

    Google Scholar 

  • Ward PS (2007) Phylogeny, classification, and species-level taxonomy of ants (Hymenoptera: Formicidae). Zootaxa 1668:549–563

    Google Scholar 

  • Weber NA (1941) The rediscovery of the queen of Eciton (Labidus) coecum Latr. (Hym.: Formicidae). Am Midl Nat 26:325–329

    Article  Google Scholar 

  • Weiser MD, Kaspari M (2006) Ecological morphospace of New World ants. Ecol Entomol 31:131–142

    Article  Google Scholar 

  • Werringloer A (1932) Die Sehorgane und Sehzentren der Dorylinen nebst Untersuchungen über die Facettenaugen der Formiciden. Akad Verlag 131:432–524

    Google Scholar 

  • Wheeler WM (1921) Observations on army ants in British Guiana. Proc Am Acad Art Sci 56:291–328

    Article  Google Scholar 

  • Wilkie KTR, Mertl AL, Traniello JFA (2007) Biodiversity below ground: probing the subterranean ant fauna of Amazonia. Naturwissenschaften 94:725–731

    Article  Google Scholar 

  • Yamagata N, Nishino H, Mizunami M (2006) Pheromone-sensitive glomeruli in the primary olfactory centre of ants. Proc R Soc B 273:2219–2225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Phil Ward and Sean Brady shared insights into the evolutionary history of doryline army ants. Thanks to three anonymous reviewers for making valuable comments particularly related to statistical analyses. Thanks to Michael Kaspari and David Donoso for providing C. andicola specimens. Kaitlin Baudier, Marie Clifford, Yamile Molina, Karina O’Donnell, Siobhan O’Donnell, Tom Soare, Sean Tully, and William Wood assisted with specimen collections and field research. Ants were collected in Costa Rica and Ecuador under research permits from those countries. Research was funded by NSF grant IOS 1209072 and Drexel University startup funds to S.O’D.

Author information

Authors and Affiliations

  1. Biodiversity, Earth & Environmental Science, Drexel University, Philadelphia, PA, 19104, USA

    S. Bulova, K. Purce, P. Khodak, E. Sulger & S. O’Donnell

Authors
  1. S. Bulova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Purce
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. P. Khodak
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. E. Sulger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. O’Donnell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. O’Donnell.

Additional information

Communicated by: Alain Dejean

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bulova, S., Purce, K., Khodak, P. et al. Into the black and back: the ecology of brain investment in Neotropical army ants (Formicidae: Dorylinae). Sci Nat 103, 31 (2016). https://doi.org/10.1007/s00114-016-1353-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00114-016-1353-4

Keywords

Search

Navigation