Skip to main content
SpringerLink
Log in

Early developmental processes limit socially mediated phenotypic plasticity in an ant

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Caste determination in social insects has long been considered to exemplify socially mediated phenotypic plasticity: young larvae can develop into queens or workers depending on the social environment. However, recent studies have challenged this view by showing that, in some species, larval development can be biased early by factors such as larval genotype. We analyzed this issue in the ant species Aphaenogaster senilis. First, we found that the probability that a larva develops into a queen or a worker varies consistently among colonies. Next, we conducted a cross-fostering experiment in which larvae from colonies with relatively low queen production were transferred to colonies with relatively high queen production and vice versa. The results show a strong significant interaction between early determination and worker control of larval caste fate. Therefore, our study shows that socially mediated phenotypic plasticity is limited by processes occurring at an early developmental stage that possibly include direct or indirect genetic effects or non-genetic maternal effects.

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

Similar content being viewed by others

References

  • Alaux C, Jaisson P, Hefetz A (2005) Reproductive decision-making in semelparous colonies of the bumblebee bombus terrestris. Behav Ecol Sociobiol 59:270–277

    Article  Google Scholar 

  • Amor F, Ortega P, Jowers MJ, Cerdá X, Billen J, Lenoir A, Boulay R (2011) The evolution of worker–queen polymorphism in Cataglyphis ants: interplay between individual-and colony-level selections. Behav Ecol Sociobiol 65:1473–1482

    Article  Google Scholar 

  • Anscombe F (1948) The transformation of Poisson, binomial and negative binomial data. Biometrical 35:246–254

    Article  Google Scholar 

  • Bartlett M (1947) The use of transformations. Biometrics 3:39–52

    Article  PubMed  CAS  Google Scholar 

  • Blight O, Albet Díaz-Mariblanca G, Cerdá X, Boulay R (2015) Ecological implications of consistent colony-level behavioural differences in a social insect. Behav Ecol. doi:10.1093/beheco/arv127

  • Boulay R, Hefetz A, Cerdá X, Devers S, Francke W, Twele R, Lenoir A (2007) Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size. Behav Ecol Sociobiol 61:1531–1541

    Article  Google Scholar 

  • Boulay R, Cerdá X, Fertin A, Ichinose K, Lenoir A (2009) Brood development into sexual females depends on the presence of a queen but not on temperature in an ant dispersing by colony fission, Aphaenogaster senilis. Ecol Entomol 34:595–602

    Article  Google Scholar 

  • Brian MV (1957) Caste determination in social insects. Annu Rev Entomol 2:107–120

    Article  Google Scholar 

  • Caut S, Jowers MJ, Arnan X, Pearce-Duvet J, Rodrigo A, Cerdá X, Boulay R (2014) The effects of fire on ant trophic assemblage and sex allocation. Ecol Evol 4:35–49

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapman BB, Thain H, Coughlin J, Hughes WO (2011) Behavioural syndromes at multiple scales in Myrmica ants. Anim Behav 82:391–397

    Article  Google Scholar 

  • Chéron B, Doums C, Federici P, Monnin T (2009) Queen replacement in the monogynous ant Aphaenogaster senilis: supernumerary queens as life insurance. Anim Behav 78:1317–1325

    Article  Google Scholar 

  • Chéron B, Cronin AL, Doums C, Fédérici P, Haussy C, Tirard C, Monnin T (2011) Unequal resource allocation among colonies produced by fission in the ant Cataglyphis cursor. Ecology 92:1448–58

    Article  PubMed  Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, Chichester

    Book  Google Scholar 

  • Crozier RH (1973) Apparent differential selection at an isozyme locus between queens and workers of the ant Aphaenogaster rudis. Genetics 73:313–318

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dingemanse NJ, Araya-Ajoy YG (2015) Interacting personalities: behavioural ecology meets quantitative genetics. Trends Ecol Evol 30:88–97

    Article  PubMed  Google Scholar 

  • Gamer M, Lemon J, Fellows I, Singh P (2012) irr: various coefficients of interrater reliability and agreement. R package version 0.84. http://www.CRANR-projectorg/package=irr

  • Goulson D (2003) Bumblebees: their behaviour and ecology. Oxford University Press, Oxford

    Google Scholar 

  • Hughes WO, Boomsma JJ (2008) Genetic royal cheats in leaf-cutting ant societies. Proc Natl Acad Sci U S A 105:5150–5153

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Iwanishi S, Shin S, Ohkawara K (2007) Biasing mechanisms for the sex investment ratio in the monogynous and monandrous ant Aphaenogaster smythiesi japonica Forel. Ethol Ecol Evol 19:275–289

  • Jandt JM, Bengston S, Pinter-Wollman N, Pruitt JN, Raine NE, Dornhaus A, Sih A (2014) Behavioural syndromes and social insects: personality at multiple levels. Biol Rev Camb Philos Soc 89:48–67

    Article  PubMed  Google Scholar 

  • Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci U S A 99:8157–8160

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kamakura M (2011) Royalactin induces queen differentiation in honeybees. Nature 473:478–483

    Article  PubMed  CAS  Google Scholar 

  • Ledoux A (1976) Inhibition exercée sur l’apparition de nouvelles femelles ailées, par la femelle reine pondeuse chez Aphaenogaster senilis (Hyméoptère Formicoidea). CR Acad Sci D Nat 283:1197–1200

    Google Scholar 

  • Ledoux A (1981) Conséquences de l’orphelinage sur la biologie des colonies d’Aphaenogaster senilis (Mayr.) (Hymenoptera Formicoidea). CR Acad Sci III-vie 293:237–240

    Google Scholar 

  • Leniaud L, Darras H, Boulay R, Aron S (2012) Social hybridogenesis in the clonal ant Cataglyphis hispanica. Curr Biol 22:1188–1193

    Article  PubMed  CAS  Google Scholar 

  • Libbrecht R, Schwander T, Keller L (2011) Genetic component to caste allocation in a multiple-queen ant species. Evolution 65:2907–2915

    Article  PubMed  Google Scholar 

  • Libbrecht R, Corona M, Wende F, Azevedo DO, Serrão JE, Keller L (2013) Interplay between insulin signaling, juvenile hormone, and vitellogenin regulates maternal effects on polyphenism in ants. Proc Natl Acad Sci U S A 110:11050–11055

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Linksvayer TA (2006) Direct, maternal, and sibsocial genetic effects on individual and colony traits in an ant. Evolution 60:2552–2561

    Article  PubMed  Google Scholar 

  • Linksvayer TA (2007) Ant species size differences are determined by epistasis between brood and worker genomes. PLoS One 2:e994

    Article  PubMed  PubMed Central  Google Scholar 

  • Linksvayer TA, Kaftanoglu O, Akyol E, Blatch S, Amdam G, Page R Jr (2011) Larval and nurse worker control of developmental plasticity and the evolution of honey bee queen-worker dimorphism. J Evol Biol 24:1939–1948

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Modlmeier AP, Liebmann JE, Foitzik S (2012) Diverse societies are more productive: a lesson from ants. Proc R Soc B 279:2142–2150

    Article  PubMed  PubMed Central  Google Scholar 

  • Passera L (1980) La ponte d’oeufs préorientés chez la fourmi Pheidole pallidula (Nyl.) (Hymenoptera-Formicidae). Insect Soc 27:79–95

    Article  Google Scholar 

  • Pereboom J, Velthuis H, Duchateau M (2003) The organisation of larval feeding in bumblebees (Hymenoptera, Apidae) and its significance to caste differentiation. Insect Soc 50:127–133

    Article  Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing

  • Ramm SA, Stockley P (2009) Adaptive plasticity of mammalian sperm production in response to social experience. Proc R Soc B 276:745–751

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodd FH, Reznick DN, Sokolowski MB (1997) Phenotypic plasticity in the life history traits of guppies: responses to social environment. Ecology 78:419–433

    Article  Google Scholar 

  • Ruel C, Cerdá X, Boulay R (2012) Behaviour-mediated group size effect constrains reproductive decisions in a social insect. Anim Behav 84:853–860

    Article  Google Scholar 

  • Ruel C, Cerdá X, Boulay R (2013) Surface lipids of queen-laid eggs do not regulate queen production in a fission-performing ant. Naturwissenschaften 100:91–100

    Article  PubMed  CAS  Google Scholar 

  • Schwander T, Keller L (2008) Genetic compatibility affects queen and worker caste determination Science 322: 552

  • Schwander T, Keller L (2012) Evolution: sociality as a driver of unorthodox reproduction. Curr Biol 22:R525–R527

    Article  PubMed  CAS  Google Scholar 

  • Schwander T, Humbert J-Y, Brent CS, Cahan SH, Chapuis L, Renai E, Keller L (2008) Maternal effect on female caste determination in a social insect. Curr Biol 18:265–269

    Article  PubMed  CAS  Google Scholar 

  • Schwander T, Lo N, Beekman M, Oldroyd BP, Keller L (2010) Nature versus nurture in social insect caste differentiation. Trends Ecol Evol 25:275–282

    Article  PubMed  Google Scholar 

  • Seeley TD (2009) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Harvard

    Google Scholar 

  • Smith CR, Suarez AV (2010) The trophic ecology of castes in harvester ant colonies. Funct Ecol 24:122–130

    Article  Google Scholar 

  • Suzzoni JP, Passera L, Strambi A (1980) Ecdysteroid titre and caste determination in the ant, Pheidole pallidula (Nyl.) (Hymenoptera: Formicidae). Experientia 36:1228–1229

    Article  CAS  Google Scholar 

  • Teseo S, Châline N, Jaisson P, Kronauer D (2014) Epistasis between adults and larvae underlies caste fate and fitness in a clonal ant. Nat Commun 5:3363

    Article  PubMed  Google Scholar 

  • Torossian C (1958) L’aliment proctodéale chez la fourmi Dolichoderus quadripunctatus (Dolichoderidae). CR Acad Sci D Nat 246:3524–3526

    Google Scholar 

  • Tschinkel WR (1993) Sociometry and sociogenesis of colonies of the fire ant Solenopsis invicta during one annual cycle. Ecol Monogr 63:425–457

    Article  Google Scholar 

  • 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 

  • Villalta I, Angulo E, Devers S, Cerdá X, Boulay R (2015) Regulation of worker egg-laying by larvae in a fission-performing ant. Anim Behav 106:149–156

    Article  Google Scholar 

  • West-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Ann Rev Ecol Syst 20:249–278

    Article  Google Scholar 

  • Zar J (1999) Biostatistical analysis, 4th edn. Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank Ines Ocon Santamaria and Séverine Devers for their help with the experiments and Jessica Pearce for her English editing services. We thank Claudie Doums and three anonymous referees for their comments on an early version of this manuscript.

Author information

Authors and Affiliations

  1. Estación Biológica de Doñana – CSIC, Av. Americo Vespucio, 41092, Sevilla, Spain

    Irene Villalta, Olivier Blight, Elena Angulo, Xim Cerdá & Raphaël Boulay

  2. Institut de Recherches sur la Biologie de l’Insecte, CNRS UMR 7261, Université François Rabelais de Tours, Tours, France

    Irene Villalta & Raphaël Boulay

  3. Institut Méditerranéen de Biodiversité et d’Ecologie, Université d’Avignon et des Pays de Vaucluse, UMR CNRS IRD Aix Marseille Université, Avignon, France

    Olivier Blight

Authors
  1. Irene Villalta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Olivier Blight
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elena Angulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xim Cerdá
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raphaël Boulay
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Irene Villalta.

Ethics declarations

This study was funded by the Spanish Ministry of Economy and Competitiveness and the FEDER (CGL2012-36181).

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

Additional information

Communicated by W. Hughes

Significance statement

Colonies of ants are composed of two castes of females with different morphologies and tasks. The queens specialize in reproduction whereas the workers are sterile and contribute to domestic tasks such as food gathering and colony defense. For decades, the difference between workers and queens has been thought to stem from nutritional and other environmental differences during the larval stage. We indeed show marked differences between colonies in the capacity of workers to rear new queens. However, worker control on the destiny of diploid larvae is constrained by precocious larval pre-determination. These precocious effects possibly include direct or indirect genetic effects or non-genetic maternal effects. Overall, our study shows that colony-level resource allocation to the production of new queens is the result of complex interactions between adults and larvae.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Figure S1

Proportion of queens produced among the female pupae in function of the colony size (original number of workers in the colony). Red and black triangles are HWinter and LWinter, respectively: colonies with relatively high and low queen production in winter. Blue and green circles are HSpring and LSpring, respectively: colonies with relatively high and low queen production in spring. (DOCX 36 kb)

Table S1

Results of the experiment 1 showing the total production of females (=FEM) and the proportion of queens among the females (P(Q)) in different colonies collected in winter and spring as a function of the colony size (initial number of workers), queen weight (in mg), and the number of surviving workers. (DOCX 23 kb)

Table S2

Results of the experiment 2 showing the total production of females (=FEM) and the proportion of queens among the females (P(Q)) in six different experimental conditions (treatment). H colonies with high queen production in experiment 1, L colonies with low queen production in experiment 1, Control larvae of the same colony as the workers. (DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Villalta, I., Blight, O., Angulo, E. et al. Early developmental processes limit socially mediated phenotypic plasticity in an ant. Behav Ecol Sociobiol 70, 285–291 (2016). https://doi.org/10.1007/s00265-015-2052-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-2052-4

Keywords

Search

Navigation