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Complex hybrid origin of genetic caste determination in harvester ants

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.

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Figure 1: Linearized neighbour-joining tree of a 433-base-pair portion of the cox1 mitochondrial gene in the two pairs of interbreeding lineages and populations of Pogonomyrmex barbatus and P. rugosus.
Figure 2: Maximum-likelihood consensus tree from the use of chord genetic distances20 calculated from nuclear markers (six allozymes and four microsatellites).

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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.

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Correspondence to Sara Helms Cahan.

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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

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