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Short independent lives and selection for maximal sperm survival make investment in immune defences unprofitable for leaf-cutting ant males

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Abstract

The short-lived males of ants and other highly eusocial Hymenoptera are essentially ejaculates with compound eyes, brains and wings to vector sperm to its destination. Males compete for lifetime ejaculate storage by females to produce the equivalent of somatic cells (sterile workers) and new seed-propagules (gynes; males are haploid and have no father) after the colony has become sexually mature. Hymenopteran queens never re-mate later in life, which makes partner commitment between queen and male-ejaculate analogous to a sperm and egg committing when forming a zygote that subsequently sequesters a germ line and produces somatic tissues. This semelparous commitment remains unchanged when queens store ejaculates from multiple males, and colonies become chimeras of patrilines. The soma of eusocial hymenopteran males may thus not be under selection for more than minimal independent life, but eusocial male ejaculates are unusually long-lived, and sperm cells may not be used until years after storage. Somatic repair and immune defence in males should thus be minimal, particularly in response to challenges late in adult life. We tested this idea using males of Atta and Acromyrmex leaf-cutting ants and show that lethal infections with the fungal pathogen Metarhizium brunneum affect male sperm quality, but fail to induce an encapsulation immune response. This result is consistent with expectation because fungal infections are highly unlikely to ever reach immature ant males while they are nursed by their sister workers and because males will die natural deaths after leaving their colonies to mate before new infections can kill them.

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Acknowledgments

We thank Louise Lee Munk, Nicolai Vitt Meyling and Jørgen Eilenberg for making the Metarhizium brunneum plates available, David Nash for statistical help, Susanne den Boer and Gaspar Bruner for helping to collect ants in the field, the Smithsonian Tropical Research Institute for facilitating our fieldwork and the Autoridad Nacional de Ambiente (ANAM) for issuing collection and export permits. The work was supported by a grant from the Danish National Research Foundation to JJB (DNRF57) and a Future Fellowship and Linkage Grant from the Australian Research Council to B.B.

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Correspondence to M. Stürup.

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Communicated by W. O. H. Hughes

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Stürup, M., Baer, B. & Boomsma, J.J. Short independent lives and selection for maximal sperm survival make investment in immune defences unprofitable for leaf-cutting ant males. Behav Ecol Sociobiol 68, 947–955 (2014). https://doi.org/10.1007/s00265-014-1707-x

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