Abstract
Caste differentiation and division of labour are the hallmarks of insect societies1 and at the root of their ecological success2. Kin selection predicts that caste determination should result from environmentally induced differences in gene expression3,4, a prediction largely supported by empirical data5. However, two exceptional cases of genetically determined caste differentiation have recently been found in harvester ants6,7,8. Here we show that genetic caste determination evolved in these populations after complex hybridization events. We identified four distinct genetic lineages, each consisting of unique blends of the genomes of the parental species, presumably Pogonomyrmex barbatus and P. rugosus. Crosses between lineages H1 and H2 and between J1 and J2 give rise to workers, whereas queens develop from within-lineage matings. Although historical gene flow is evident, genetic exchange among lineages and between lineages and the parental species no longer occurs. This unusual system of caste determination seems to be evolutionarily stable.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 51 print issues and online access
$199.00 per year
only $3.90 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Wilson, E. O. The Insect Societies (Belknap, Cambridge, 1971)
Oster, G. F. & Wilson, E. O. Caste and Ecology in the Social Insects (Princeton Univ. Press, 1978)
Crozier, R. H. & Pamilo, P. Evolution of Social Insect Colonies: Sex Allocation and Kin Selection (Oxford Univ. Press, 1996)
Seger, J. Kinship and covariance. J. Theor. Biol. 91, 191–213 (1981)
Wheeler, D. E. Developmental and physiological determinants of caste in social Hymenoptera—evolutionary implications. Am. Nat. 128, 13–34 (1986)
Helms Cahan, S. et al. Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc. R. Soc. Lond. B 269, 1871–1877 (2002)
Volny, V. P. & Gordon, D. M. Genetic basis for queen–worker dimorphism in a social insect. Proc. Natl Acad. Sci. USA 99, 6108–6111 (2002)
Julian, G. E., Fewell, J. H., Gadau, J., Johnson, R. A. & Larrabee, D. Genetic determination of the queen caste in an ant hybrid zone. Proc. Natl Acad. Sci. USA 99, 8157–8160 (2002)
Cole, A. C. Pogonomyrmex Harvester Ants; a Study of the Genus in North America (Univ. of Tennessee Press, Knoxville, 1968)
Buschinger, A. in Social Insects—an Evolutionary Approach to Castes and Reproduction (ed. Engels, W.) 37–57 (Springer, New York, 1990)
Jones, T. R., Routman, E. J., Begun, D. J. & Collins, J. P. Ancestry of an isolated subspecies of salamander, Ambystoma tigrinum stebbinsi Lowe: The evolutionary significance of hybridization. Mol. Phylogenet. Evol. 4, 194–202 (1995)
Welch, M. E. & Rieseberg, L. H. Patterns of genetic variation suggest a single, ancient origin for the diploid hybrid species Helianthus paradoxus. Evolution 56, 2126–2137 (2002)
Xu, S. Phylogenetic analysis under reticulate evolution. Mol. Biol. Evol. 17, 897–907 (2000)
Volny, V. P. & Gordon, D. M. Characterization of polymorphic microsatellite loci in the red harvester ant, Pogonomyrmex barbatus. Mol. Ecol. Notes 2, 302–303 (2002)
Bourke, A. F. G., Green, H. A. A. & Bruford, M. W. Parentage, reproductive skew and queen turnover in a multiple-queen ant analysed with microsatellites. Proc. R. Soc. Lond. B 264, 277–283 (1997)
Foitzik, S., Haberl, M., Gadau, J. & Heinze, J. Mating frequency of Leptothorax nylanderi ant queens determined by microsatellite analysis. Insectes Soc. 44, 219–227 (1997)
Taber, S. W. The World of the Harvester Ants (Texas A&M Univ. Press, College Station, 1998)
Parker, J. D. & Rissing, S. W. Molecular evidence for the origin of workerless social parasites in the ant genus Pogonomyrmex. Evolution 56, 2017–2028 (2002)
Simon, C. et al. Evolution, weighting and phylogenetic utility of mitochondrial gene-sequences and a compilation of conserved polymerase chain-reaction primers. Ann. Entomol. Soc. Am. 87, 651–701 (1994)
Cavalli-Sforza, L. L. & Edwards, A. W. F. Phylogenetic analysis: Models and estimation procedures. Evolution 21, 550–570 (1967)
Acknowledgements
We thank J. Seger for proposing the model presented here; K. Helms, G. Julian and the Student Challenge Awards Project research teams for assistance with field collections; J. Gadau and V. Volny for primer information; and M. Chapuisat, P. Christe, R. Hammond, J. Goudet and J. Parker for feedback on the manuscript. Financial support was provided by grants from the Swiss National Science Foundation to L.K. and the Durfee Foundation to S.H.C.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no competing financial interests.
Supplementary information
Rights and permissions
About this article
Cite this article
Helms Cahan, S., Keller, L. Complex hybrid origin of genetic caste determination in harvester ants. Nature 424, 306–309 (2003). https://doi.org/10.1038/nature01744
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1038/nature01744
This article is cited by
-
Ecological and genetic distinctiveness of socially hybridogenetic lineages of Pogonomyrmex harvester ants at regional and local scales
Evolutionary Ecology (2023)
-
Division of labor in work shifts by leaf-cutting ants
Scientific Reports (2021)
-
Brood recognition and discrimination in ants
Insectes Sociaux (2020)
-
Sex-biased dispersal creates spatial genetic structure in a parthenogenetic ant with a dependent-lineage reproductive system
Heredity (2017)
-
Climate-driven range shift prompts species replacement
Insectes Sociaux (2016)
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.