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Social complexity, diet, and brain evolution: modeling the effects of colony size, worker size, brain size, and foraging behavior on colony fitness in ants

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Abstract

Animals may face a tradeoff between enhanced cognitive ability and the cost of maintaining larger and more energetically expensive brains. In social species, this tradeoff could be influenced by energy-reducing benefits of cooperation and collective cognition. Greater social complexity in ants is hypothesized to be associated with smaller brain size, a pattern opposite that found in some social vertebrates. Ants vary in worker and colony size, and worker size-frequency distributions; larger workers have larger, more costly, brains. Colony-level foraging performance and its energetic consequence to fitness depend on individual cognitive capabilities as well as collective behaviors. To explore the impact of diet, behavioral ability, and social organization on brain evolution, we developed a model incorporating food availability, foraging behavior and related energetic gain, colony size, worker size and polymorphism, and brain size. Colonies could increase energy intake through foraging performance by increasing worker size, and by correlation, brain size and expanded task capability, or by increasing colony size and collective foraging. Results show that resource-poor environments favored small colonies of relatively large-bodied and thus large-brained pluripotent workers that had higher energetic costs. In contrast, large colonies of relatively small-bodied and small-brained workers in resource-rich environments harvested food with lower brain investment and hence decreased metabolic costs. Worker size-related behavioral specialization and covarying brain investment also influenced fitness. The energetic advantage of polymorphism depended on the degree of association of the navigational abilities employed during foraging and worker brain size. Our study suggests that diet, colony size, and worker size may influence tradeoffs between individual and collective cognition and the evolution of brain size and division of labor in eusocial insects such as ants.

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References

  • Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199

    Article  Google Scholar 

  • Amador-Vargas S, Gronenberg W, Wcislo WT, Mueller U (2015) Specialization and group size: brain and behavioural correlates of colony size in ants lacking morphological castes. Proc R Soc B 282:20142502

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev Camb Philos 76:211–37

    Article  CAS  Google Scholar 

  • Avarguès-Weber A, Giurfa M (2013) Conceptual learning by miniature brains. Proc R Soc B 280:20131907

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartholomew G, Lighton J, Feener DJ (1988) Energetics of trail running, load carriage, and emigration in the column-raiding army ant Eciton hamatum. Physiol Zool 61:57–68

    Article  Google Scholar 

  • Buehlmann C, Hansson BS, Knaden M (2012) Desert ants learn vibration and magnetic landmarks. PLoS One 7:e33117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burns JG, Foucaud J, Mery F (2011) Costs of memory: lessons from “mini” brains. Proc R Soc Lond B 278:923–929

    Article  Google Scholar 

  • Calabi P, Porter SD (1989) Worker longevity in the fire ant Solenopsis invicta: ergonomic considerations of correlations between temperature, size and metabolic rates. J Insect Physiol 35:643–649

    Article  Google Scholar 

  • Camazine S, Deneubourg JL, Franks NR, Sneyd J, Theraulaz G, Bonabeau E (2003) Self-organization in biological systems. Princeton University Press, Princeton

  • Cao TT, Dornhaus A (2008) Ants under crowded conditions consume more energy. Biol Lett 4:613–615

    Article  PubMed  PubMed Central  Google Scholar 

  • Chittka L, Niven J (2009) Are bigger brains better? Curr Biol 19:R995–R1008

    Article  CAS  PubMed  Google Scholar 

  • Cole BJ (1985) Size and behavior in ants: constraints on complexity. Proc Natl Acad Sci U S A 82:8548–8551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couzin I (2007) Collective minds. Nature 445:715–715

    Article  CAS  PubMed  Google Scholar 

  • Couzin ID (2009) Collective cognition in animal groups. Trends Cogn Sci 13:36–43

    Article  PubMed  Google Scholar 

  • Delgado J, Solé RV (1997) Collective-induced computation. Phys Rev E 55:2338–2344

    Article  CAS  Google Scholar 

  • Donaldson-Matasci MC, DeGrandi-Hoffman G, Dornhaus A (2013) Bigger is better: honeybee colonies as distributed information-gathering systems. Anim Behav 85:585–592

    Article  PubMed  PubMed Central  Google Scholar 

  • Dornhaus A, Powell S, Bengston S (2012) Group size and its effects on collective organization. Annu Rev Entomol 57:123–141

    Article  CAS  PubMed  Google Scholar 

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

  • Eberhard W, Wcislo W (2012) Plenty of room at the bottom. Am Sci 100:226–233

    Article  Google Scholar 

  • Feinerman O, Korman A (2012) Memory lower bounds for randomized collaborative search and implications for biology. In: Proceedings of International Symposium on Distributed Computing (DISC). Salvador, pp 61–75

  • Feinerman O, Korman A, Lotker Z, Sereni J-S (2012) Collaborative search on the plane without communication. In: PODC ’12 Proceedings of the 2012 ACM symposium on principles of distributed computing. New York, pp 77–86

  • Fonseca-Azevedo K, Herculano-Houzel S (2012) Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution. Proc Natl Acad Sci U S A 109:18571–18576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gelblum A, Pinkoviezky I, Fonio E, Ghosh A, Gov FO (2015) Ant groups optimally amplify the effect of transiently informed individuals. Nat Commun 6:7729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giraldo YM, Patel E, Gronenberg W, Traniello JFA (2013) Division of labor and structural plasticity in an extrinsic serotonergic mushroom body neuron in the ant Pheidole dentata. Neurosci Lett 534:107–111

    Article  CAS  PubMed  Google Scholar 

  • Gronenberg W (2008) Structure and function of ant (Hymenoptera: Formicidae) brains: strength in numbers. Myrmecol News 11:25–36

    Google Scholar 

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

    Google Scholar 

  • Harrison JF, Fewell JH, Stiller TM, Breed MD (1989) Effects of experience on use of orientation cues in the giant tropical ant. Anim Behav 37:869–871

    Article  Google Scholar 

  • Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc R Soc Lond B 274:453–464

    Article  Google Scholar 

  • Healy SD, Rowe C (2013) Costs and benefits of evolving a larger brain: doubts over the evidence that large brains lead to better cognition. Anim Behav 86:e1–e3

    Article  Google Scholar 

  • Holbrook CT, Barden PM, Fewell JH (2011) Division of labor increases with colony size in the harvester ant Pogonomyrmex californicus. Behav Ecol 22:960–966

    Article  Google Scholar 

  • Holldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge

    Book  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 

  • Isler K, van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2:557–560

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamhi JF, Traniello JFA (2013) Biogenic amines and collective organization in a superorganism: neuromodulation of social behavior in ants. Brain Behav Evol 82:220–236

    Article  PubMed  Google Scholar 

  • Kamhi JF, Nunn K, Robson SKA, Traniello JFA (2015) Polymorphism and division of labour in a socially complex ant: neuromodulation of aggression in the Australian weaver ant, Oecophylla smaragdina. Proc R Soc B 282:20150704

    Article  PubMed Central  Google Scholar 

  • Korman A, Greenwald E, Feinerman O (2014) Confidence sharing: an economic strategy for efficient information flows in animal groups. PLoS Comput Biol 10:e1003862

    Article  PubMed  PubMed Central  Google Scholar 

  • Kotrschal A, Rogell B, Bundsen A, Svensson B, Zajitschek S, Brännström I, Immler S, Maklakov AA, Kolm N (2013) Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Curr Biol 23:168–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krause J, Ruxton GD, Krause S (2010) Swarm intelligence in animals and humans. Trends Ecol Evol 25:28–34

    Article  PubMed  Google Scholar 

  • Laughlin SB, de Ruyter van Steveninck RR, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41

    Article  CAS  PubMed  Google Scholar 

  • Lighton J, Bartholomew G, Feener DJ (1987) Energetics of locomotion and load carriage and a model of the energy cost of foraging in the leaf-cutter ant Atta colombica Guer. Physiol Zool 60:524–537

    Article  Google Scholar 

  • Lihoreau M, Latty T, Chittka L (2012) An exploration of the social brain hypothesis in insects. Front Physiol 3:1–7

    Article  Google Scholar 

  • Marshall JAR, Bogacz R, Dornhaus A, Planqué R, Kovacs T, Franks NR (2009) On optimal decision-making in brains and social insect colonies. J R Soc Interface 6:1065–1074

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller N, Garnier S, Hartnett AT, Couzin ID (2013) Both information and social cohesion determine collective decisions in animal groups. Proc Natl Acad Sci U S A 110:5263–5268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moll K, Federle W, Roces F (2012) The energetics of running stability: costs of transport in grass-cutting ants depend on fragment shape. J Exp Biol 215:161–168

    Article  PubMed  Google Scholar 

  • Moreau CS (2006) Phylogeny of the ants: diversification in the age of angiosperms. Science 312:101–104

    Article  CAS  PubMed  Google Scholar 

  • Morgan DE (2009) Trail pheromones of ants. Physiol Entomol 34:1–17

    Article  CAS  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 

  • Muscedere ML, Gronenberg W, Moreau CS, Traniello JFA (2014) Investment in higher order central processing regions is not constrained by brain size in social insects. Proc R Soc B 281:20140217

    Article  PubMed  PubMed Central  Google Scholar 

  • Naug D, Wenzel J (2006) Constraints on foraging success due to resource ecology limit colony productivity in social insects. Behav Ecol Sociobiol 60:62–68

    Article  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, 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  PubMed Central  Google Scholar 

  • Ott SR, Rogers SM (2010) Gregarious desert locusts have substantially larger brains with altered proportions compared with the solitarious phase. Proc R Soc Lond B 277:3087–3096

    Article  Google Scholar 

  • Razin N, Eckmann J, Feinerman O (2013) Desert ants achieve reliable recruitment across noisy interactions. J R Soc Interface 10:20130079

    Article  PubMed  PubMed Central  Google Scholar 

  • Riveros A, Seid M, Wcislo W (2012) Evolution of brain size in class-based societies of fungus-growing ants (Attini). Anim Behav 83:1043–1049

    Article  Google Scholar 

  • Robinson EJH, Franks NR, Ellis S et al (2011) A simple threshold rule is sufficient to explain sophisticated collective decision-making. PLoS One 6:e19981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson EJH, Feinerman O, Franks NR (2014) How collective comparisons emerge without individual comparisons of the options. Proc R Soc B 281:20140737

    Article  PubMed  PubMed Central  Google Scholar 

  • Sasaki T, Pratt SC (2011) Emergence of group rationality from irrational individuals. Behav Ecol 22:276–281

    Article  Google Scholar 

  • Sasaki T, Pratt SC (2012) Groups have a larger cognitive capacity than individuals. Curr Biol

  • Seeley T (2010) Honeybee democracy. Princeton University Press, Princeton

    Google Scholar 

  • Seid MA, Traniello JFA (2006) Age-related repertoire expansion and division of labor in Pheidole dentata (Hymenoptera: Formicidae): a new perspective on temporal polyethism and behavioral plasticity in ants. Behav Ecol and Sociobiol 60:631–644

  • Seid MA, Harris KM, Traniello JFA (2005) Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. J Comp Neurol 488:269–277

    Article  PubMed  Google Scholar 

  • Seid MA, Goode K, Li C, Traniello JFA (2008) Age- and subcaste-related patterns of serotonergic immunoreactivity in the optic lobes of the ant Pheidole dentata. Dev Neurobiol 68:1325–1333

    Article  PubMed  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 

  • Shultz S, Dunbar R (2010) Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc Natl Acad Sci U S A 107:21582–21586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steck K, Hansson BS, Knaden M (2009) Smells like home: desert ants, Cataglyphis fortis, use olfactory landmarks to pinpoint the nest. Front Zool 6:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Sumpter DJT (2010) Collective animal behavior. Princeton University Press, Princeton

    Book  Google Scholar 

  • Thomas ML, Elgar MA (2003) Colony size affects division of labour in the ponerine ant Rhytidoponera metallica. Naturwissenschaften 90:88–92

    CAS  PubMed  Google Scholar 

  • Wehner R (2003) Desert ant navigation: how miniature brains solve complex tasks. J Comp Physiol A 189:579–588

    Article  CAS  Google Scholar 

  • Wehner R, Fukushi T, Isler K (2007) On being small: brain allometry in ants. Brain Behav Evol 69:220–228

    Article  PubMed  Google Scholar 

  • Weier JA, Feener DH (1995) Foraging in the seed-harvester ant genus Pogonomyrmex: are energy costs important? Behav Ecol Sociobiol 36:291–300

    Article  Google Scholar 

  • Weitz S, Blanco S, Fournier R et al (2012) Modeling collective animal behavior with a cognitive perspective: a methodological framework. PLoS One 7:e38588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson EO (1980) Caste and division of labor in leaf-cutter ants (Hymenoptera: Formicidae: Atta). Behav Ecol Sociobiol 7:143–156

    Article  Google Scholar 

  • Wilson EO, Hölldobler B (2009) The superorganism: the beauty, elegance, and strangeness of insect societies. W. W Norton & Company, New York

    Google Scholar 

  • Wittlinger M, Wehner R, Wolf H (2006) The ant odometer: stepping on stilts and stumps. Science 312:1965–1967

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Drs. Asaf Gal, Sara Arganda Carreras, Dhruba Naug, and Stephen Pratt for critically reading and commenting on the manuscript and Dr. Corrie Moreau for her insights. This work was supported by National Science Foundation grant IOS‐1354291 (JFT sponsor) and by European Research Council (648032), the Israel Science Foundation (712166), the Minerva Foundation, and the Clore Foundation (OF sponsor). OF is the incumbent of the Louis and Ida Rich career development chair.

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Correspondence to Ofer Feinerman.

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Communicated by D. Naug

This manuscript is a contribution to the special issue Integrative Analysis of Division of Labor—Guest Editors: Simon K. Robson, James F.A. Traniello

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Feinerman, O., Traniello, J.F.A. Social complexity, diet, and brain evolution: modeling the effects of colony size, worker size, brain size, and foraging behavior on colony fitness in ants. Behav Ecol Sociobiol 70, 1063–1074 (2016). https://doi.org/10.1007/s00265-015-2035-5

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