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The evolution of ant worker polymorphism correlates with multiple social traits

Abstract

In eusocial insects, worker polymorphism is shaped by several factors, including colony size, queen mating frequency, and the timing of queen-worker differentiation during larval development. In a comparative study of 18 species of Cataglyphis desert ants representing a wide range of worker sizes, we used phylogenetically controlled analyses to examine correlations between worker head width variation (i.e., worker polymorphism) and multiple social traits, namely, mature colony size, mean worker head width, queen head width, queen-worker head width dimorphism, and within-colony genetic relatedness, resulting from multiple mating by queens. We found that worker polymorphism was positively correlated with mature colony size, mean worker head width, and queen head width. In contrast, worker polymorphism was not correlated with queen-worker dimorphism and within-colony genetic relatedness. These results underscore that evolution of worker polymorphism and social traits are correlated. They also illustrate that additional research using multivariate approaches is needed to further clarify the evolution of insect societies.

Significance statement

In eusocial insects, worker morphological variation (i.e., worker polymorphism) is tightly linked to division of labor. Multiple factors are supposed to shape the evolution of worker polymorphism. Using phylogenetically controlled analyses of worker head width variation from 18 species of Cataglyphis desert ants, we show that worker polymorphism positively correlates with mature colony size, mean worker head width, and queen size. These results highlight that the evolution of worker polymorphism and social traits are correlated. Identifying the mechanisms underlying these relationships could provide major insights into the development and evolution of insect societies.

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References

  1. Agosti D (1990) Review and reclassification of Cataglyphis (Hymenoptera, Formicidae). J Nat Hist 24:1457–1505

    Article  Google Scholar 

  2. Amor F, Ortega P (2014) Cataglyphis tartessica sp.n., a new ant species (Hymenoptera: Formicidae) in south- western Spain. Myrmecol News 19:125–132

    Google Scholar 

  3. Amor F, Ortega P, Boulay R, Cerdá X (2017) Frequent colony orphaning triggers the production of replacement queens via worker thelytoky in a desert-dwelling ant. Insect Soc 64:373–378

    Article  Google Scholar 

  4. Amor F, Villalta I, Doums C, Angulo E, Caut S, Castro S, Jowers MJ, Cerdá X, Boulay R (2016) Nutritional versus genetic correlates of caste differentiation in a desert ant: caste differentiation in ants. Ecol Entomol 41:660–667

    Article  Google Scholar 

  5. Anderson C, McShea DW (2001) Individual versus social complexity, with particular reference to ant colonies. Biol Rev 76:211–237

    CAS  PubMed  Article  Google Scholar 

  6. Aron S, Darras H, Eyer PA, Leniaud L, Pearcy M (2013) Structure génétique des sociétés et systèmes d’accouplement chez la fourmi Cataglyphis viatica (Fabricius 1787). Bulletin De L’institut Scientifique De Rabat 35:103–109

    Google Scholar 

  7. Aron S, Mardulyn P, Leniaud L (2016) Evolution of reproductive traits in Cataglyphis desert ants: mating frequency, queen number, and thelytoky. Behav Ecol Sociobiol 70:1367–1379

    Article  Google Scholar 

  8. Blanchard BD, Moreau CS (2017) Defensive traits exhibit an evolutionary trade-off and drive diversification in ants. Evolution 71:315–328

    PubMed  Article  Google Scholar 

  9. Boomsma JJ, Ratnieks FL (1996) Paternity in eusocial Hymenoptera. Phil Trans R Soc B 351:947–975

    Article  Google Scholar 

  10. Boulay R, Aron S, Cerdá X, Doums C, Graham P, Hefetz A, Monnin T (2017) Social life in arid environments: the case study of Cataglyphis ants. Annu Rev Entomol 62:305–321

    CAS  PubMed  Article  Google Scholar 

  11. Bourke AF (1999) Colony size, social complexity and reproductive conflict in social insects. J Evol Biol 12:245–257

    Article  Google Scholar 

  12. Clémencet J, Doums C (2007) Habitat-related microgeographic variation of worker size and colony size in the ant Cataglyphis cursor. Oecologia 152:211–218

    PubMed  Article  Google Scholar 

  13. Cole BJ (1983) Multiple mating and the evolution of social behavior in the Hymenoptera. Behav Ecol Sociobiol 12:191–201

    Article  Google Scholar 

  14. Cronin AL, Chifflet-Belle P, Fédérici P, Doums C (2016a) High inter-colonial variation in worker nestmate relatedness and diverse social structure in a desert ant from Mongolia. Insect Soc 63:87–98

    Article  Google Scholar 

  15. Cronin AL, Monnin T, Sillam-Dusses D, Aubrun F, Fédérici P, Doums C (2016b) Qualitative bias in offspring investment in a superorganism is linked to dispersal and nest inheritance. Anim Behav 119:1–9

    Article  Google Scholar 

  16. Darras H (2010) Analyse comparative des stratégies de reproduction au sein du genre Cataglyphis (Hyménoptères, Formicidae): structure des populations, multifécondation et compétition spermatique. Master thesis, Brussels: Université Libre de Bruxelles

  17. Darras H, Kuhn A, Aron S (2019) Evolution of hybridogenetic lineages in Cataglyphis ants. Mol Ecol 28:3073–3088

    PubMed  Article  Google Scholar 

  18. den Boer SP, Baer B, Dreier S, Aron S, Nash DR, Boomsma JJ (2009) Prudent sperm use by leaf-cutter ant queens. Proc Royal Soc B 276:3945–3953

    Article  Google Scholar 

  19. Evison SEF, Hughes WO (2011) Genetic caste polymorphism and the evolution of polyandry in Atta leaf-cutting ants. Naturwissenschaften 98:643–649

    CAS  PubMed  Article  Google Scholar 

  20. Eyer PA (2014) Mode de reproduction et diversité génétique chez les fourmis du genre Cataglyphis. PhD thesis, Brussels: Université Libre de Bruxelles, p 145

  21. Eyer PA, Freyer J, Aron S (2013a) Genetic polyethism in the polyandrous desert ant Cataglyphis cursor. Behav Ecol 24:144–151

    Article  Google Scholar 

  22. Eyer PA, Leniaud L, Darras H, Aron S (2013b) Hybridogenesis through thelytokous parthenogenesis in two Cataglyphis desert ants. Mol Ecol 22:947–955

    CAS  PubMed  Article  Google Scholar 

  23. Ferguson-Gow H, Sumner S, Bourke AFG, Jones KE (2014) Colony size predicts division of labour in attine ants. Proc Royal Soc B 281:20141411

    Article  Google Scholar 

  24. Fjerdingstad EJ, Boomsma JJ (1998) Multiple mating increases the sperm stores of Atta colombica leafcutter ant queens. Behav Ecol Sociobiol 42:257–261

    Article  Google Scholar 

  25. Fjerdingstad EJ, Crozier RH (2006) The evolution of worker caste diversity in social insects. Am Nat 167:390–400

    PubMed  Article  Google Scholar 

  26. Fournier D, Battaille G, Timmermans I, Aron S (2008) Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor. Anim Behav 75:151–158

    Article  Google Scholar 

  27. Frumhoff PC, Ward PS (1992) Individual-level selection, colony-level selection, and the association between polygyny and worker monomorphism in ants. Am Nat 139:559–590

    Article  Google Scholar 

  28. Gernhard T (2008) The conditioned reconstructed process. J Theor Biol 253:769–778

    PubMed  Article  Google Scholar 

  29. Goodisman MAD, Ross KG (1996) Relationship of queen number and worker size in polygyne colonies of the fire ant Solenopsis invicta. Insect Soc 43:303–307

    Article  Google Scholar 

  30. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  31. Jaffé R, Kronauer DJ, Bernhard Kraus F, Boomsma JJ, Moritz RF (2007) Worker caste determination in the army ant Eciton burchellii. Biol Lett 3:513–516

    PubMed  PubMed Central  Article  Google Scholar 

  32. Jowers MJ, Leniaud L, Cerdá X, Alasaad S, Caut S, Amor F, Aron S, Boulay R (2013) Social and population structure in the ant Cataglyphis emmae. PLoS ONE 8:e72941

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Karlsson B, Wickman PO (1990) Increase in reproductive effort as explained by body size and resource allocation in the speckled wood butterfly, Pararge aegeria (L.). Funct Ecol 4:609–617

    Article  Google Scholar 

  34. Karsai I, Wenzel JW (1998) Productivity, individual-level and colony-level flexibility, and organization of work as consequences of colony size. PNAS 95:8665–8669

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Kaspari M, Vargo EL (1995) Colony size as a buffer against seasonality: Bergmann’s rule in social insects. Am Nat 145:610–632

    Article  Google Scholar 

  36. Kraus FB, Neumann P, Van Praagh J, Moritz RFA (2004) Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 55:494–501

    Article  Google Scholar 

  37. Kuhn A (2013) Hybridogenèse sociale chez les fourmis désertiques Cataglyphis. Master thesis, Brussels: Université Libre de Bruxelles

  38. Kuhn A, Darras H, Paknia O, Aron S (2019) Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants. Mol Ecol 29:549–564

    PubMed  Article  Google Scholar 

  39. Lemey P, Rambaut A, Welch JJ, Suchard MA (2010) Phylogeography takes a relaxed random walk in continuous space and time. Mol Biol Evol 27:1877–1885

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Leniaud L, Heftez A, Grumiau L, Aron S (2011) Multiple mating and supercoloniality in Cataglyphis desert ants. Biol J Linn Soc Lond 104:866–876

    Article  Google Scholar 

  41. Leniaud L, Pearcy M, Aron S (2013) Sociogenetic organisation of two desert ants. Insect Soc 60:337–344

    Article  Google Scholar 

  42. Leniaud L, Pearcy M, Taheri A, Aron S (2015) Testing the genetic determination of the soldier caste in the silver ant. Insect Soc 62:517–524

    Article  Google Scholar 

  43. Lillico-Ouachour A, Abouheif E (2017) Regulation, development, and evolution of caste ratios in the hyperdiverse ant genus Pheidole. Curr Opin Insect Sci 19:43–51

    PubMed  Article  Google Scholar 

  44. Marmolejo-Ramos F, Ospina R (2019) Performance of some estimators of relative variability. Front Appl Math Stat 5:43

    Article  Google Scholar 

  45. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364

    CAS  PubMed  Article  Google Scholar 

  46. Monjane AL, Dellicour S, Hartnady P et al (2020) Symptom evolution following the emergence of maize streak virus. Elife 9:e51984

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22:408–413

    PubMed  Article  Google Scholar 

  48. Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton

    Google Scholar 

  49. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    CAS  PubMed  Article  Google Scholar 

  50. Pearcy M, Aron S (2006) Local resource competition and sex ratio in the ant Cataglyphis cursor. Behav Ecol 17:569–574

    Article  Google Scholar 

  51. Pearcy M, Hardy O, Aron S (2006) Thelytokous parthenogenesis and its consequences on inbreeding in an ant. Heredity 96:377–382

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  52. Peeters C, Aron S (2017) Evolutionary reduction of female dispersal in Cataglyphis desert ants. Biol J Linn Soc Lond 122:58–70

    Article  Google Scholar 

  53. Pincheira-Donoso D, Hunt J (2017) Fecundity selection theory: concepts and evidence. Biol Rev 92:341–356

    PubMed  Article  Google Scholar 

  54. Pincheira-Donoso D, Tregenza T (2011) Fecundity selection and the evolution of reproductive output and sex-specific body size in the Liolaemus lizard adaptive radiation. Evol Biol 38:197–207

    Article  Google Scholar 

  55. Powell S (2008) Ecological specialization and the evolution of a specialized caste in Cephalotes ants. Funct Ecol 22:902–911

    Article  Google Scholar 

  56. Powell S (2016) A comparative perspective on the ecology of morphological diversification in complex societies: nesting ecology and soldier evolution in the turtle ants. Behav Ecol Sociobiol 70:1075–1085

    Article  Google Scholar 

  57. Powell S, Franks NR (2005) Caste evolution and ecology: a special worker for novel prey. Proc Royal Soc B 272:2173–2180

    Article  Google Scholar 

  58. Powell S, Franks NR (2006) Ecology and the evolution of worker morphological diversity: a comparative analysis with Eciton army ants. Funct Ecol 20:1105–1114

  59. Powell S, Price SL, Kronauer DJ (2020) Trait evolution is reversible, repeatable, and decoupled in the soldier caste of turtle ants. PNAS 117:6608–6615

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  60. Pybus OG, Suchard MA, Lemey P et al (2012) Unifying the spatial epidemiology and molecular evolution of emerging epidemics. PNAS 109:15066–15071

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  61. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    PubMed  Article  PubMed Central  Google Scholar 

  62. R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  63. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. Ratnieks FL (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236

    Article  Google Scholar 

  65. Reiner Brodetzki T, Hefetz A (2018) Determining social and population structures requires multiple approaches: a case study of the desert ant Cataglyphis israelensis. Ecol Evol 8:12365–12374

    PubMed  PubMed Central  Article  Google Scholar 

  66. 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 52:163–168

    Article  Google Scholar 

  67. Roff DA (2002) Life history evolution. Sinauer Associates Inc, Sunderland, Massachusetts, USA

    Google Scholar 

  68. Schmid-Hempel P (1998) Parasites in social insects (Vol 60). Princeton University Press, Princeton

    Google Scholar 

  69. Schöning C, Kinuthia W, Franks NR (2005) Evolution of allometries in the worker caste of Dorylus army ants. Oikos 110:231–240

    Article  Google Scholar 

  70. Smith CR, Anderson KE, Tillberg CV, Gadau J, Suarez AV (2008) Caste determination in a polymorphic social insect: nutritional, social, and genetic factors. Am Nat 172:497–507

    CAS  PubMed  Article  Google Scholar 

  71. Smith CR, Tschinkel WR (2006) The sociometry and sociogenesis of reproduction in the Florida harvester ant. Pogonomyrmex Badius. J Insect Sci 6:32

    PubMed Central  Article  PubMed  Google Scholar 

  72. Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol 4:vey016

  73. Timmermans I, Grumiau L, Hefetz A, Aron S (2010) Mating system and population structure in the desert ant Cataglyphis livida. Insect Soc 57:39–46

    Article  Google Scholar 

  74. Timmermans I, Hefetz A, Fournier D, Aron S (2008) Population genetic structure, worker reproduction and thelytokous parthenogenesis in the desert ant Cataglyphis sabulosa. Heredity 101:490–498

    CAS  PubMed  Article  Google Scholar 

  75. Traniello JF, Rosengaus RB (1997) Ecology, evolution and division of labour in social insects. Anim Behav 53:209–213

    Article  Google Scholar 

  76. Tschinkel WR (1998) Sociometry and sociogenesis of colonies of the harvester ant, Pogonomyrmex badius: worker characteristics in relation to colony size and season. Insect Soc 45:385–410

    Article  Google Scholar 

  77. Vrancken B, Lemey P, Rambaut A, Bedford T, Longdon B, Günthard HF, Suchard MA (2015) Simultaneously estimating evolutionary history and repeated traits phylogenetic signal: applications to viral and host phenotypic evolution. Methods Ecol Evol 6:67–82

    PubMed  Article  Google Scholar 

  78. Wenseleers T, Helanterä H, Hart A, Ratnieks FL (2004) Worker reproduction and policing in insect societies: an ESS analysis. J Evol Biol 17:1035–1047

    CAS  PubMed  Article  Google Scholar 

  79. Wetterer JK (1999) The ecology and evolution of worker size-distribution in leaf-cutting ants (Hymenoptera: Formicidae). Sociobiology 34:119–144

    Google Scholar 

  80. Wheeler DE (1986) Developmental and physiological determinants of caste in social Hymenoptera: evolutionary implications. Am Nat 128:13–34

    Article  Google Scholar 

  81. Wheeler DE (1991) The developmental basis of worker caste polymorphism in ants. Am Nat 138:1218–1238

    Article  Google Scholar 

  82. Wickman PO, Karlsson B (1989) Abdomen size, body size and the reproductive effort of insects. Oikos 56:209–214

    Article  Google Scholar 

  83. Wiernasz DC, Cole BJ (2003) Queen size mediates queen survival and colony fitness in harvester ants. Evolution 57:2179–2183

    PubMed  Article  Google Scholar 

  84. Wills BD, Powell S, Rivera MD, Suarez AV (2018) Correlates and consequences of worker polymorphism in ants. Annu Rev Entomol 63:575–598

    CAS  PubMed  Article  Google Scholar 

  85. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

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Acknowledgements

We thank Xim Cerdá, Hugo Darras, Abraham Hefetz, Alexandre Kuhn, Laurianne Leniaud, Rémy Perez, and Quentin Willot for their help on the field; ICTS-RBD for providing us fieldwork facilities; Claudie Doums for kindly providing us with samples of C. aenescens; J. Pearce-Duvet for her language editing services; and two reviewers for their constructive comments on the manuscript.

Funding

NL, SD, and SA are supported by the Belgian Fonds National pour la Recherche Scientifique (FRS-FNRS) (Grant No. J.0063.14, J.0151.16, and T.0140.18 to SA).

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NL and SA conceived the study; NL and SA collected field data; NL carried out the lab work; NL and SD performed the data analysis; NL and SA drafted the manuscript. All authors gave final approval for publication and agree to be held accountable for the work performed therein.

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Correspondence to Nathan Lecocq de Pletincx.

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Lecocq de Pletincx, N., Dellicour, S. & Aron, S. The evolution of ant worker polymorphism correlates with multiple social traits. Behav Ecol Sociobiol 75, 113 (2021). https://doi.org/10.1007/s00265-021-03049-6

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Keywords

  • Worker polymorphism
  • Head width
  • Colony size
  • Polyandry
  • Queen-worker dimorphism
  • Evolution