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Genetic diversity, paternal origin and pathogen resistance in Cataglyphis desert ants

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Abstract

Group genetic diversity is usually associated with a reduced risk of disease outbreak and a slower rate of pathogen transmission. In social insects, multiple mating by queens (polyandry) evolved several times albeit reducing worker’s inclusive fitness. One major hypothesis suggests that polyandry has been selected for to mitigate the risk of outbreak thanks to increased genetic diversity within colonies. We investigated this hypothesis in the ant Cataglyphis mauritanica, in which nestmate workers are produced by several clonal, single-mated queens. Using natural colonies, we correlated genetic diversity with worker survival to a fungal entomopathogen. We further tested whether workers from different paternal lineages (but a common maternal genome) show differential resistance in experimentally single- or multiple-patriline groups, and whether an increased number of patrilines in a group improved disease resistance. We show that workers from distinct patrilines vary in their resistance to a pathogen in single-patriline colonies, but the difference among patrilines disappears when they are mixed in multiple-patriline colonies. Furthermore, pathogen resistance was affected by the number of patrilines in a group, with two- and three-patriline groups being more resistant than single-patriline groups. However, resistance did not differ between groups made of two and three patrilines; similarly, it was not associated with genetic diversity in natural colonies. Overall, our results suggest that collective disease defenses might homogenize workers’ resistance from different patrilines and, thereby, stabilize colony resistance.

Significance Statement

The occurrence of multiple breeders in insect societies has been hypothesized to be selected for because increased within-colony genetic diversity reduces the risk of severe outbreaks. We show that nestmate workers from distinct paternal lineages vary in their resistance to pathogens when reared in single-patriline groups. However, this difference disappears when workers are mixed in multiple-patriline groups. These results suggest that multiple mating by queens dilutes the deleterious consequences of a single patriline producing only susceptible offspring, rather than directly enhancing pathogen resistance.

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Data availability

Data generated in this study have been made publicly available on the Open Science Framework depository(https://osf.io/4tu5r/). https://doi.org/10.17605/OSF.IO/4TU5R

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Acknowledgements

Thanks to M. Avet for her help with experiments. Thanks to D. Gàlvez and M. Chapuisat for providing fungus samples, their helpful experimental expertise, and their comments on previous versions of the manuscript. We are grateful to B. Gassner for English improvement of the manuscript, as well as to the Morocco’s High Commission for Water, Forests and Combating Desertification (HCEFLCD—Decision 277/2012) for granting us collection permits. This work was supported by a PhD fellowship from the FRIA (Fonds pour l’Encouragement de la Recherche Scientifique dans l’Industrie et l’Agriculture) (PAE), as well as grants from the Belgian FRS-FNRS (Fonds National pour la Recherche Scientifique; grants # T.0140.18 and J.0063.14) and the Université Libre de Bruxelles (Actions Blanches) (SA).

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  1. Department of Entomology, Texas A&M University, College Station, TX, 77843, USA

    P. A. Eyer

  2. Evolutionary Biology & Ecology, Université Libre de Bruxelles, 50 Av. F.D. Roosevelt, B-1050, Brussels, Belgium

    P. A. Guery & S. Aron

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Eyer, P.A., Guery, P.A. & Aron, S. Genetic diversity, paternal origin and pathogen resistance in Cataglyphis desert ants. Behav Ecol Sociobiol 77, 81 (2023). https://doi.org/10.1007/s00265-023-03358-y

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