Skip to main content
Log in

Intergenerational effect of juvenile hormone on offspring in Pogonomyrmex harvester ants

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Parents can influence the phenotypes of their offspring via a number of mechanisms. In harvester ants, whether female progeny develop into workers or daughter queens is strongly influenced by the age and temperature conditions experienced by their mother, which is associated with variation in maternal ecdysteroid deposition in fertilized eggs. In many insects, juvenile hormone (JH) is antagonistic to ecdysteroid release, suggesting that seasonal and age-based variation in maternal JH titers may explain maternal effects on offspring size and reproductive caste. To test this hypothesis, we artificially increased maternal JH titers with methoprene, a JH analog, in laboratory colonies of two Pogonomyrmex populations exhibiting genetic caste determination. Increasing maternal JH resulted in a 50% increase in worker body size, as well as a sharp reduction in total number of progeny reared, but did not alter the genotype of progeny reared to adulthood. The intergenerational effect of JH manipulation was not mediated by a reduction in ecdysteroid deposition into eggs; instead, changes in egg size, trophic egg availability or brood/worker ratio may have altered the nutritional environment of developing larvae. Egg ecdysteroid content was significantly negatively correlated with natural variation in worker body size, however, suggesting that there are multiple independent routes by which queens can modify offspring phenotypes.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Brent CS, Dolezal AG (2009) Ant ecdysteroid extraction and radioimmunoassay. Cold Spring Harb Protoc 4. doi:10.1101/pdb.prot5247

  • Brent CS, Vargo EL (2003) Changes in juvenile hormone biosynthetic rate and whole body content in maturing virgin queens of Solenopsis invicta. J Insect Physiol 49:967–974

    Article  PubMed  CAS  Google Scholar 

  • Brent CS, Peeters C, Dietemann V, Crewe R, Vargo EL (2006) Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi. J Comp Physiol A 192:315–320

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Brian MV (1980) Social control over sex and caste in bees, wasps and ants. Biol Rev 55:379–415

    Article  Google Scholar 

  • Bullière D, Bullière F, de Reggi M (1979) Ecdysteroid titres during ovarian and embryonic development in Blaberus craniifer. Develop Genes Evol 186:103–114

    Google Scholar 

  • Burns SN, Vander Meer RK, Teal PEA (2007) Juvenile hormone III concentrations in female reproductives of Solenopsis invicta Buren. J Entomol Sci 42:206–309

    Google Scholar 

  • Clark RM, Anderson KE, Gadau J, Fewell JH (2006) Behavioral regulation of genetic caste determination in a Pogonomyrmex population with dependent lineages. Ecology 87:2201–2206

    Article  PubMed  Google Scholar 

  • Cruz J, Martin D, Pascual N, Maestro JL, Piulachs MD, Belles X (2003) Quantity does matter. Juvenile hormone and the onset of vitellogenesis in the German cockroach. Insect Biochem Mol Bio 33:1219–1225

    Article  CAS  Google Scholar 

  • de Menten L, Fournier D, Brent C, Passera L, Vargo EL, Aron S (2005) Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula. Behav Ecol Sociobiol 58:527–533

    Article  Google Scholar 

  • Dolezal AG, Brent CS, Gadau J, Hölldobler B, Amdam GV (2009) Endocrine physiology of the division of labour in Pogonomyrmex californicus founding queens. Ann Behav 77:1005–1010

    Article  Google Scholar 

  • Dubrovsky EB, Dubrovskaya VA, Berger EM (2002) Juvenile hormone signaling during oogenesis in Drosophila melanogaster. Insect Biochem Mol Biol 32:1555–1565

    Article  PubMed  CAS  Google Scholar 

  • Farley BM, Ryder SP (2008) Regulation of maternal mRNAs in early development. Crit Rev Biochem Mol Biol 43:135–162

    Article  PubMed  CAS  Google Scholar 

  • Giray T, Givanetti M, West-Eberhard MJ (2005) Juvenile hormone, reproduction and worker behavior in the neotropical social wasp Polistes canadensis. Proc Nat Acad Sci USA 102:3330–3335

    Article  PubMed  CAS  Google Scholar 

  • Glinka AV, Wyatt GR (1996) Juvenile hormone activation of gene transcription in locust fat body. Insect Biochem Mol Biol 26:13–18

    Article  CAS  Google Scholar 

  • Goetsch W (1938) Kolonie-Gründung und Kasten-Bildung im Ameisenstaat. Forsch Fortschr 14:223–224

    Google Scholar 

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

    Article  Google Scholar 

  • Gösswald K, Bier K (1953) Untersuchungen zur Kastendetermination in der Gattung Formica. 2. Die Aufzucht von Geschlechtstieren bei Formica rufa pratensis. Zool Anzieger 151:126–134

    Google Scholar 

  • Greenberg L, Fletcher DJC, Vinson SB (1985) Differences in worker size and mound distribution in monogynous and polygynous colonies of the fire ant Solenopsis invicta Buren. J Kansas Entomol Soc 58:9–18

    Google Scholar 

  • Gregg PC, Roberts B, Wentworth SL (1987) Levels of ecdysteroids in diapause and non-diapause eggs of the Australian plague locust Chortoicetes terminifera (Walker). J Insect Physiol 33:237–242

    Article  CAS  Google Scholar 

  • Hardie J (1987) The corpus allatum, neurosecretion and photoperiodically controlled polymorphism in an aphid. J Insect Physiol 33:201–205

    Article  Google Scholar 

  • Hartfelder K, Emlen DJ (2005) Endocrine control of insect polyphenism. In: Gilbert LI (ed) Comprehensive molecular insect science. Endocrinology, vol 3. Elsevier, New York, pp 651–703

  • Helms Cahan S, Julian GE (2010) Shift in frequency-dependent selection across the life-cycle in obligately interbreeding harvester ant lineages. Evol Ecol 24:359–374

    Article  Google Scholar 

  • Helms Cahan S, Keller L (2003) Complex hybrid origin of genetic caste determination in harvester ants. Nature 424:306–309

    Article  PubMed  CAS  Google Scholar 

  • Helms Cahan S, Julian GE, Rissing SW, Schwander T, Parker JD, Keller L (2004) Loss of phenotypic plasticity explains genotype-caste association in harvester ants. Curr Biol 14:2277–2282

    Article  Google Scholar 

  • Henrick CA, Willy WE, Staal GB (1976) Insect juvenile hormone activity of alkyl (2E, 4E)-3, 7, 11-trimethyl-2,-4-dodecadienoates. Variations in the ester function and in the carbon chain. J Agri Food Chem 24:207–218

    Article  CAS  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The Ants. The Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Hughes WOH, Boomsma JJ (2007) Genetic polymorphism in leaf-cutting ants is phenotypically plastic. Proc R Soc Lond B 274:1625–1630

    Article  CAS  Google Scholar 

  • Hughes WOH, Boomsma JJ (2008) Genetic royal cheats in leaf-cutting ant societies. Proc Nat Acad Sci USA 105:5150–5153

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 100:9394–9397

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Yasuda A, Sonobe H (2008) Synthesis and phosphorylation of ecdysteroids during ovarian development in the silkworm Bombyx mori. Zool Sci 25:727–732

    Article  Google Scholar 

  • Lagueux M, Hirn M, Hoffman JA (1977) Ecdysone during ovarian development in Locusta migratoria. J Insect Physiol 23:109–119

    Article  PubMed  CAS  Google Scholar 

  • Legay JM, Calvez B, Hirn M, De Reggi ML (1976) Ecdysone and oocyte morphogenesis in Bombyx mori. Nature 262:489–490

    Article  CAS  Google Scholar 

  • Lengyel F, Westerlund SA, Kaib M (2007) Juvenile hormone III influences task-specific cuticular hydrocarbon profile changes in the ant Myrmicaria eumenoides. J Chem Ecol 33:167–181

    Article  PubMed  CAS  Google Scholar 

  • Lim SP, Lee CY (2005) Effects of juvenile hormone analogs on new reproductives and colony growth of Pharaoh ant (Hymenoptera : Formicidae). J Econ Entomol 98:2169–2175

    Article  PubMed  CAS  Google Scholar 

  • MacKay WP (1981) A comparison of the nest phonologies of three species of Pogonomyrmex harvester ants. Psyche 88:25–74

    Article  Google Scholar 

  • Matsuura K, Kobayashi N (2010) Termite queens adjust egg size according to colony development. Behav Ecol 21:1018–1023

    Article  Google Scholar 

  • Meunier J, Chapuisat M (2009) The determinants of queen size in a socially polymorphic ant. J Evol Biol 22:1906–1913

    Article  PubMed  CAS  Google Scholar 

  • Mousseau TA, Dingle H (1991) Maternal effects in insect life histories. Ann Rev Entomol 36:511–534

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  PubMed  CAS  Google Scholar 

  • Nijhout HF (1994) Insect Hormones. Princeton University Press, Princeton

    Google Scholar 

  • Nijhout HF (2003) The control of body size in insects. Develop Biol 261:1–9

    Article  PubMed  CAS  Google Scholar 

  • Nijhout HF, Wheeler DE (1982) Juvenile hormone and the physiological basis of insect polymorphisms. Quart Rev Biol 57:109–133

    Article  CAS  Google Scholar 

  • Parthasarathy R, Sun ZY, Bai H, Palli SR (2010) Juvenile hormone regulation of vitellogenin synthesis in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 40:405–414

    Article  PubMed  CAS  Google Scholar 

  • Passera L, Suzzoni J-P (1978) Traitement des reines par l’hormone juvenile et sexualisation du couvain chez Pheidole pallidula (Nyl.) (Hymenoptera, Formicidae). C R Acad Sci Ser Gen Vie Sci 287:1231–1233

    CAS  Google Scholar 

  • Passera L, Suzzoni J-P (1979) Le role de la reine de Pheidole pallidula (Nyl.) (Hymenoptera, Formicidae) dans la sexualisation du couvain après traitement par l’hormone juvenile. Insectes Sociaux 26:343–353

    Article  Google Scholar 

  • Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Ann Rev Entomol 51:581–608

    Article  CAS  Google Scholar 

  • Robeau RM, Vinson SB (1976) Effects of juvenile hormone analogues on caste differentiation in the imported fire ant, Solenopsis invicta. J Ga Entomol Soc 11:198–203

    CAS  Google Scholar 

  • Robinson GE, Vargo EL (1997) Juvenile hormone in adult eusocial hymenoptera: gonadotropin and behavioral pacemaker. Arch Insect Biochem Physiol 35:559–583

    Article  PubMed  CAS  Google Scholar 

  • Sano-Fujii I (1979) Effect of parental age and development rate on the production of active form of Callosobruchus maculates (F.) (Coleoptera: Bruchidae). Mech Age Dev 10:283–293

    Article  CAS  Google Scholar 

  • Schrempf A, Heinze J (2006) Proximate mechanisms of male morph determination in the ant Cardiocondyla obscurior. Evol Dev 8:266–272

    Article  PubMed  Google Scholar 

  • 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 and Sociobiol 59:215–221

    Article  Google Scholar 

  • Schwander T, Helms Cahan S, Keller L (2007) Characterization and distribution of Pogonomyrmex harvester ant lineages with genetic caste determination. Mol Ecol 16:367–387

    Article  PubMed  CAS  Google Scholar 

  • Schwander T, Humbert J-Y, Brent CS, Helms Cahan S, 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 

  • Smith CR, Schoenick C, Anderson KE, Gadau J, Suarez AV (2007) Potential and realized reproduction by different worker castes in queen-less and queen-right colonies of Pogonomyrmex badius. Insectes Sociaux 54:260–267

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Steel CGH, Lees AD (1977) The role of neurosecretion in the photoperiodic control of polymorphism in the aphid Megoura viciae. J Exp Biol 67:117–135

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tadros W, Lipshitz HD (2009) The maternal-to-zygotic transition: a play in two acts. Development 136:3033–3042

    Article  PubMed  CAS  Google Scholar 

  • Vargo EL, Laurel M (1994) Studies on the mode of action of a queen primer pheromone of the fire ant Solenopsis invicta. J Insect Physiol 40:601–610

    Article  CAS  Google Scholar 

  • Via S, Gomulkiewicz R, De Jong G, Scheiner SM, Schlichting CD, Van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol Evol 10:212–217

    Article  PubMed  CAS  Google Scholar 

  • Volny VP, Greene MJ, Gordon DM (2006) Brood production and lineage discrimination in the red harvester ant (Pogonomyrmex barbatus). Ecology 87:2194–2200

    Article  PubMed  Google Scholar 

  • Warren JT, Gilbert LI (1986) Ecdysone metabolism and distribution during the pupal adult development of Manduca sexta. Insect Biochem 16:65–82

    Article  CAS  Google Scholar 

  • Warren JT, Smith W, Gilbert LI (1984) Simplification of the ecdysteroid radioimmunoassay by the use of protein-A from Staphylococcus aureus. Experientia 40:393–394

    Article  CAS  Google Scholar 

  • Wheeler DE, Nijhout HF (1981) Soldier determination in ants: new role for Juvenile Hormone. Science 213:361–363

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to acknowledge the help of Todd Clason for providing access and training in microscopy techniques, and Matthew Rand for sharing techniques to distinguish trophic eggs. This work was funded by research grants awarded to C.J. Graves from the Beta Beta Beta National Biology Honors Society and from the HELiX (Hughes Endeavor for Life Science Excellence) program at the University of Vermont.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sara Helms Cahan.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cahan, S.H., Graves, C.J. & Brent, C.S. Intergenerational effect of juvenile hormone on offspring in Pogonomyrmex harvester ants. J Comp Physiol B 181, 991–999 (2011). https://doi.org/10.1007/s00360-011-0587-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-011-0587-x

Keywords