Decreasing worker size diversity does not affect colony performance during laboratory challenges in the ant Temnothorax nylanderi

  • T. Colin
  • C. Doums
  • R. Péronnet
  • M. Molet
Original Article


Within-colony phenotypic diversity can play an essential role in some eusocial insect taxa by increasing the performance of division of labor, thereby increasing colony fitness. Empirical studies of the effect of phenotypic diversity on colony fitness mostly focused on species with discrete castes (workers, soldiers) or with continuously and highly morphologically variable workers, which is not the most common case. Indeed, most species exhibit continuous but limited worker morphological variation. It is still unclear whether this variation impacts colony fitness. To test this, we reduced the worker size diversity in 25 colonies of the ant Temnothorax nylanderi and compared their performances to 25 control colonies. We reared these colonies in the laboratory and measured the effect of treatment (reduced diversity or control) and colony size (number of workers) on colony performance at six challenges, as well as on worker mortality and brood production. The reduction of worker size diversity did not affect colony performance nor mortality and brood production. As expected, colony performance and brood production increased with colony size. These results suggest that worker size diversity may not be under positive selection in this species, but rather the product of a lack of developmental canalization. We propose that social life could decrease the selective pressures maintaining developmental canalization, subsequently leading to higher size diversity without necessarily increasing colony performance.

Significance statement

In social insects, nestmate size diversity is commonly thought to improve division of labour and colony performance. This has been clearly demonstrated in species with high size diversity, either discrete or continuous, but this is unclear in most of the social insects that exhibit low size diversity. We experimentally decreased worker size diversity in the ant Temnothorax nylanderi, a species with low worker size diversity. Reducing worker size diversity had no effect on colony performance, worker mortality, or brood production. Our findings support the hypothesis that low size diversity is merely the product of developmental noise and is not necessarily adaptive. We propose that social life could relax the selective pressures maintaining developmental and social canalizations, subsequently leading to size diversity.


Canalization Division of labor Fitness Phenotypic plasticity Size variation 



This work was funded by Agence Nationale de la Recherche grant ANTEVO ANR-12-JSV7-0003-01. We thank Jeffrey Carbillet-Malherbe, Daphné Cahours, Alexandra Rocland, and Morgane Bequet-Rennes for their help with colony collection, colony rearing, and preliminary experiments and Ian Billick for the information on polyandry and polygyny in Formica neorufibarbis. We thank two anonymous referees for their helpful comments on a previous version of the manuscript.

Authors’ contributions

TC collected colonies, reared them, performed the experiments and statistical analyses, and wrote the manuscript. CD designed the study, contributed to statistical analysis, and wrote the manuscript. RP collected colonies and assisted in rearing and experiments. MM designed the study, wrote the manuscript, and supervised the project. All authors read and approved the final manuscript.

Compliance with ethical standards


This work was funded by Agence Nationale de la Recherche grant ANTEVO ANR-12-JSV7–0003-01.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Data availability statement

The dataset analyzed during the current study is available from the corresponding author on reasonable request.

Supplementary material

265_2017_2322_MOESM1_ESM.docx (33 kb)
Fig. S1 Example of a logistic fit of the workers’ relocation in the colony n°940 during the first challenge. Growth y(t) is the cumulated number of workers in the new nest. μ is the slope of the dashed line i.e. the maximum speed of the emigration process. λ is the lag-phase i.e. the time it took for emigration to start. (DOCX 33 kb).


  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with imageJ. Biophoton Int 11:36–41Google Scholar
  2. Arnan X, Ferrandiz-Rovira M, Pladevall C, Rodrigo A (2011) Worker size-related task partitioning in the foraging strategy of a seed-harvesting ant species. Behav Ecol Sociobiol 65:1881–1890CrossRefGoogle Scholar
  3. Bershers SN, Traniello JFA (1994) The adaptiveness of worker demography in the Attine ant Trachymyrmex septentrionalis. Ecology 75:763–775CrossRefGoogle Scholar
  4. Billick I (2002) The relationship between the distribution of worker sizes and new worker production in the ant Formica neorufibarbis. Oecologia 132:244–249CrossRefPubMedGoogle Scholar
  5. Billick I, Carter C (2007) Testing the importance of the distribution of worker sizes to colony performance in the ant species Formica obscuripes forel. Insect Soc 54:113–117CrossRefGoogle Scholar
  6. Bolnick DI, Amarasekare P, Araujo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  8. Brand N, Chapuisat M (2012) Born to be bee, fed to be worker? The caste system of a primitively eusocial insect. Front Zool 9:35CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brown WD, Keller L (2002) Queen recruitment and split sex ratios in polygynous colonies of the ant Formica exsecta. Ecol Lett 5:102–109CrossRefGoogle Scholar
  10. Buschinger A (1968) Mono-und polygynie bei arten der gattung Leptothorax Mayr (Hymenoptera Formicidae). Insect Soc 15:217–225CrossRefGoogle Scholar
  11. Clémencet J, Rome Q, Fédérici P, Doums C (2008) Aggressions and size-related fecundity of queenless workers in the ant Cataglyphis cursor. Naturwissenschaften 95:133–139CrossRefPubMedGoogle Scholar
  12. Couvillon MJ, Dornhaus A (2010) Small worker bumble bees (Bombus impatiens) are hardier against starvation than their larger sisters. Insect Soc 57:193–197CrossRefGoogle Scholar
  13. Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702CrossRefGoogle Scholar
  14. Debat V, David P, (2001) Mapping phenotypes: canalization, plasticity and developmental stability. Trends Ecol Evol 16 (10):555-561Google Scholar
  15. Dietemann V, Hölldobler B, Peeters C (2002) Caste specialization and differentiation in reproductive potential in the phylogenetically primitive ant Myrmecia gulosa. Insect Soc 49:289–298CrossRefGoogle Scholar
  16. Diez L, Lejeune P, Detrain C (2014) Keep the nest clean: survival advantages of corpse removal in ants. Biol Lett 10:20140306CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dornhaus A, Franks NR (2006) Colony size affects collective decision-making in the ant Temnothorax albipennis. Insect Soc 53:420–427CrossRefGoogle Scholar
  18. Dornhaus A, Franks NR, Hawkins RM, Shere HNS (2004) Ants move to improve: colonies of Leptothorax albipennis emigrate whenever they find a superior nest site. Anim Behav 67:959–963CrossRefGoogle Scholar
  19. Dornhaus A, Holley J, Franks N (2009) Larger colonies do not have more specialized workers in the ant Temnothorax albipennis. Behav Ecol 20:922–929CrossRefGoogle Scholar
  20. Evison SEF, Hughes WOH (2011) Genetic caste polymorphism and the evolution of polyandry in Atta leaf-cutting ants. Naturwissenschaften 98:643–649CrossRefPubMedGoogle Scholar
  21. Evison SEF, Hart AG, Jackson DE (2008) Minor workers have a major role in the maintenance of leafcutter ant pheromone trails. Anim Behav 75:963–969CrossRefGoogle Scholar
  22. Fahrenholz L, Lamprecht I, Schricker B (1989) Thermal investigations of a honey bee colony: thermoregulation of the hive during summer and winter and heat production of members of different bee castes. J Comp Physiol B 159:551–560CrossRefGoogle Scholar
  23. Fjerdingstad EJ, Crozier RH (2006) The evolution of worker caste diversity in social insects. Am Nat 167:390–400CrossRefPubMedGoogle Scholar
  24. Foitzik S, Heinze J (2000) Intraspecific parasitism and split sex ratios in a monogynous and monandrous ant (Leptothorax nylanderi ). Behav Ecol Sociobiol 47:424–431CrossRefGoogle Scholar
  25. Foitzik S, Haberl M, Gadau J, Heinze J (1997) Mating frequency of Leptothorax nylanderi ant queens determined by microsatellite analysis. Insect Soc 44:219–227CrossRefGoogle Scholar
  26. Foster W (1990) Experimental evidence for effective and altruistic colony defence against natural predators by soldiers of the gall-forming aphid Pemphigus spyrothecae (Hemiptera: Pemphigidae). Behav Ecol Sociobiol 27:421–430CrossRefGoogle Scholar
  27. Gobin B, Ito F (2003) Sumo wrestling in ants: major workers fight over male production in Acanthomyrmex ferox. Naturwissenschaften 90:318–321CrossRefPubMedGoogle Scholar
  28. Goulson D, Peat J, Stout JC et al (2002) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Anim Behav 64:123–130CrossRefGoogle Scholar
  29. Grüter C, Menezes C, Imperatriz-Fonseca VL, Ratnieks FLW (2012) A morphologically specialized soldier caste improves colony defense in a neotropical eusocial bee. Proc Natl Acad Sci U S A 109:1182–1186CrossRefPubMedPubMedCentralGoogle Scholar
  30. Harvey JA, Corley LS, Strand MR (2000) Competition induces adaptive shifts in caste ratios of a polyembryonic wasp. Nature 406:183–186CrossRefPubMedGoogle Scholar
  31. Hasegawa E (1993a) Caste specialization in food storage in the dimorphic ant Colobopsis nipponicus (Wheeler). Insect Soc 40:261–271CrossRefGoogle Scholar
  32. Hasegawa E (1993b) Nest defense and early production of the major workers in the dimorphic ant Colobopsis nipponicus (Wheeler) (Hymenoptera: Formicidae). Behav Ecol Sociobiol 33:73–77CrossRefGoogle Scholar
  33. Hasegawa E, Imai S (2012) A trade-off between number and size within the first workers of the ant Camponotus japonicus. J Ethol 30:201–204CrossRefGoogle Scholar
  34. Heinze J, Puchinger W, Hölldobler B (1997) Worker reproduction and social hierarchies in Leptothorax ants. Anim Behav 54:849–864CrossRefPubMedGoogle Scholar
  35. Herbers JM, Cunningham M (1983) Social organization in Leptothorax longispinosus Mayr. Anim Behav 31:759–771CrossRefGoogle Scholar
  36. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeCrossRefGoogle Scholar
  37. Howard KJ (2006) Three queen morphs with alternative nest-founding behaviors in the ant, Temnothorax longispinosus. Insect Soc 53:480–488CrossRefGoogle Scholar
  38. Huang MH, Wheeler DE, Fjerdingstad EJ (2013) Mating system evolution and worker caste diversity in Pheidole ants. Mol Ecol 22:1998–2010CrossRefPubMedGoogle Scholar
  39. Hughes WOH, Sumner S, Van Borm S, Boomsma JJ (2003) Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Natl Acad Sci 100:9394–9397CrossRefPubMedPubMedCentralGoogle Scholar
  40. Hunt BG, Ometto L, Wurm Y et al (2011) Relaxed selection is a precursor to the evolution of phenotypic plasticity. Proc Natl Acad Sci 108:15936–15941CrossRefPubMedPubMedCentralGoogle Scholar
  41. Ispolatov I, Ackermann M, Doebeli M (2012) Division of labour and the evolution of multicellularity. Proc R Soc B Biol Sci 279:1768–1776CrossRefGoogle Scholar
  42. Jaffé R, Kronauer DJC, Kraus FB et al (2007) Worker caste determination in the army ant Eciton burchellii. Biol Lett 3:513–516CrossRefPubMedPubMedCentralGoogle Scholar
  43. Jandt JM, Dornhaus A (2014) Bumblebee response thresholds and body size: does worker diversity increase colony performance? Anim Behav 87:97–106CrossRefGoogle Scholar
  44. Jongepier E, Kleeberg I, Job S, Foitzik S (2014) Collective defence portfolios of ant hosts shift with social parasite pressure. Proc Biol Sci 281:20140225CrossRefPubMedPubMedCentralGoogle Scholar
  45. Kapheim KM, Bernal SP, Smith AR et al (2011) Support for maternal manipulation of developmental nutrition in a facultatively eusocial bee, Megalopta genalis (Halictidae). Behav Ecol Sociobiol 65:1179–1190CrossRefPubMedPubMedCentralGoogle Scholar
  46. Karlik J, Epps MJ, Dunn RR, Penick CA, Foster S (2016) Life inside an acorn: how microclimate and microbes influence nest organization in Temnothorax ants. Ethology 122:790–797CrossRefGoogle Scholar
  47. Karsai I, Hunt JH (2002) Food quantity affects traits of offspring in the paper wasp Polistes metricus (Hymenoptera: Vespidae ). Popul Ecol 31:99–106Google Scholar
  48. Kaspari M (1996) Worker size and seed size selection by harvester ants in a neotropical forest. Oecologia 105:397–404CrossRefPubMedGoogle Scholar
  49. Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694–704CrossRefPubMedGoogle Scholar
  50. Lawson LP, Vander Meer RK, Shoemaker D (2012) Male reproductive fitness and queen polyandry are linked to variation in the supergene Gp-9 in the fire ant Solenopsis invicta. Proc R Soc B Biol Sci 279:3217–3222CrossRefGoogle Scholar
  51. Linksvayer TA, Kaftanoglu O, Akyol E et al (2011) Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen-worker dimorphism. J Evol Biol 24:1939–1948CrossRefPubMedPubMedCentralGoogle Scholar
  52. Luque GM, Giraud T, Courchamp F (2013) Allee effects in ants. J Anim Ecol 82:956–965CrossRefPubMedGoogle Scholar
  53. Macom TE, Porter SD (1996) Comparison of polygyne and monogyne red imported fire ant (Hymenoptera: Formicidae) population densities. Ann Entomol Soc Am 89:535–543CrossRefGoogle Scholar
  54. McGlynn TP (2012) The ecology of nest movement in social insects. Annu Rev Entomol 57:291–308CrossRefPubMedGoogle Scholar
  55. Mehdiabadi NJ, Shultz TR (2009) Natural history and phylogeny of the fungus-farming ants (Hymenoptera: Formicidae: Myrmicinae: Attini). Myrmecological News 13:37–55Google Scholar
  56. Modlmeier AP, Foitzik S (2011) Productivity increases with variation in aggression among group members in Temnothorax ants. Behav Ecol 22:1026–1032CrossRefGoogle Scholar
  57. Modlmeier AP, Liebmann JE, Foitzik S (2012) Diverse societies are more productive: a lesson from ants. Proc R Soc B Biol Sci 279:2142–2150CrossRefGoogle Scholar
  58. Modlmeier AP, Foitzik S, Scharf I (2013) Starvation endurance in the ant Temnothorax nylanderi depends on group size, body size and access to larvae. Physiol Entomol 38:89–94CrossRefGoogle Scholar
  59. Molet M, Wheeler DE, Peeters C (2012) Evolution of novel mosaic castes in ants: modularity, phenotypic plasticity, and colonial buffering. Am Nat 180:328–341CrossRefPubMedGoogle Scholar
  60. O’Shea-Wheller TA, Sendova-Franks AB, Franks NR (2015) Differentiated anti-predation responses in a superorganism. PLoS One 10:1–10Google Scholar
  61. Passera L, Roncin E, Kaufmann B, Keller L (1996) Increased soldier production in ant colonies exposed to intraspecific competition. Nature 379:630–631CrossRefGoogle Scholar
  62. Peat J, Tucker J, Goulson D (2005) Does intraspecific size variation in bumblebees allow colonies to efficiently exploit different flowers? Ecol Entomol 30:176–181CrossRefGoogle Scholar
  63. Peeters C (1997) Morphologically “primitive” ants: comparative review of social characters, and the importance of queen-worker dimorphism. In: the evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 372–391Google Scholar
  64. Perry SP, Chapman TW, Schwarz MP, Crespi BJ (2004) Proclivity and effectiveness in gall defence by soldiers in five species of gall-inducing thrips: benefits of morphological caste dimorphism in two species (Kladothrips intermedius and K. habrus). Behav Ecol Sociobiol 56:602–610CrossRefGoogle Scholar
  65. Pinter-Wollman N, Hubler J, Holley JA, Franks N, Dornhaus A (2012) How is activity distributed among and within tasks in Temnothorax ants? Behav Ecol Sociobiol 66:1407–1420CrossRefGoogle Scholar
  66. Porter SD, Tschinkel WR (1985) Fire ant polymorphism (Hymenoptera: Formicidae): factors affecting worker size. Behav Ecol Sociobiol 16:381–386CrossRefGoogle Scholar
  67. Porter SD, Tschinkel WR (1986) Adaptive value of nanitic workers in newly founded red imported fire ant colonies (Hymenoptera: Formicidae). Ann Entomol Soc Am 79:723–726CrossRefGoogle Scholar
  68. Powell S (2009) How ecology shapes caste evolution: linking resource use, morphology, performance and fitness in a superorganism. J Evol Biol 22:1004–1013CrossRefPubMedGoogle Scholar
  69. Pratt SC, Pierce NE (2001) The cavity-dwelling ant Leptothorax curvispinosus uses nest geometry to discriminate between potential homes. Anim Behav 62:281–287CrossRefGoogle Scholar
  70. Pruitt JNJ, Riechert SSE (2011) How within-group behavioural variation and task efficiency enhance fitness in a social group. Proc R Soc London Ser B-Biological Sci 278:1209–1215CrossRefGoogle Scholar
  71. Pusch K, Heinze J, Foitzik S (2006) The influence of hybridization on colony structure in the ant species Temnothorax nylanderi and T. crassispinus. Insect Soc 53:439–445CrossRefGoogle Scholar
  72. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URLGoogle Scholar
  73. Renucci M, Tirard A, Provost E (2011) Complex undertaking behavior in Temnothorax lichtensteini ant colonies: from corpse-burying behavior to necrophoric behavior. Insect Soc 58:9–16CrossRefGoogle Scholar
  74. Rheindt FE, Strehl CP, Gadau J (2005) A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius. Insect Soc 52:163–168CrossRefGoogle Scholar
  75. Rissing SW (1987) Annual cycles in worker size of the seed-harvester antVeromessor pergandei (Hymenoptera: Formicidae). Behav Ecol Sociobiol 20(2):117–124Google Scholar
  76. Rosengren R, Fortelius W, Lindström K et al (1987) Phenology and causation of nest heating and thermoregulation in red wood ants of the Formica rufa group studied in coniferous forest habitats in southern Finland. Ann Zool Fenn 24:147–155Google Scholar
  77. Schwander T, Rosset H, Chapuisat M (2005) Division of labour and worker size polymorphism in ant colonies: the impact of social and genetic factors. Behav Ecol Sociobiol 59:215–221CrossRefGoogle Scholar
  78. Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25:275–282CrossRefPubMedGoogle Scholar
  79. Sendova-Franks AB, Franks NR (1995) Division-of-labor in a crisis—task allocation during colony emigration in the ant Leptothorax unifasciatus (Latr). Behav Ecol Sociobiol 36:269–282CrossRefGoogle Scholar
  80. Sokal RR, Rohlf FJ (1970) Biometry. The principles and practice of statistics in biological research. Science 167:165CrossRefGoogle Scholar
  81. Spaethe J, Weidenmüller A (2002) Size variation and foraging rate in bumblebees (Bombus terrestris). Insect Soc 49:142–146CrossRefGoogle Scholar
  82. Sumner S, Pereboom JJM, Jordan WC (2006) Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis. Proc R Soc B Biol Sci 273:19–26CrossRefGoogle Scholar
  83. Tóth E, Duffy JE (2008) Influence of sociality on allometric growth and morphological differentiation in sponge-dwelling alpheid shrimp. Biol J Linn Soc 94:527–540CrossRefGoogle Scholar
  84. Westling JN, Harrington K, Bengston S, Dornhaus A (2014) Morphological differences between extranidal and intranidal workers in the ant Temnothorax rugatulus, but no effect of body size on foraging distance. Insect Soc 61:367–369CrossRefGoogle Scholar
  85. Wilson EO (1984) The relation between caste ratios and division of labor in the ant genus Pheidole (Hymenoptera: Formicidae). Behav Ecol Sociobiol 16:89–98CrossRefGoogle Scholar
  86. Wilson EO (1987) Causes of ecological success: the case of the ants. J Anim Ecol 56:1–9CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Institute of Ecology and Environmental Sciences of Paris UMR7618, UPMC Univ Paris 06, CNRSSorbonne UniversitésParisFrance
  2. 2.Institut de Systématique, Évolution, Biodiversité (ISYEB), EPHE, CNRS, UPMC Univ Paris 06, MNHNSorbonne UniversitésParisFrance
  3. 3.EPHEPSL Research UniversityParisFrance

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