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Negative genetic correlation between male sexual attractiveness and survival

Abstract

Indirect selection of female mating preferences may result from a genetic association between male attractiveness and offspring fitness1,2. The offspring of attractive males may have enhanced growth3,4,5, fecundity3,4, viability5,6,7,8 or attractiveness4,9,10,11. However, the extent to which attractive males bear genes that reduce other fitness components has remained unexplored. Here I show that sexual attractiveness in male guppies (Poecilia reticulata) is heritable and genetically correlated with ornamentation. Like ornamentation12,13,14, attractiveness may be substantially Y-linked. The benefit of mating with attractive males, and thus having attractive sons, is opposed by strong negative genetic correlation between attractiveness and both offspring survival and the number of sons maturing. Such correlations suggest either antagonistic pleiotropy between attractiveness and survival or linkage disequilibrium between attractive and deleterious alleles. The presence of many colour pattern genes on or near the non-recombining section of the Y chromosome may facilitate the accumulation of deleterious mutations by genetic hitch-hiking15,16. These findings show that genes enhancing sexual attractiveness may be associated with pleiotropic costs or heavy mutational loads.

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Figure 1: Approximate multiple genetic correlation28 between ornamentation and male attractiveness.
Figure 2: The relationship between male survival and attractive ornamentation (ornamentation in Fig. 1).
Figure 3: Scale plan of the choice tank used in measuring attractiveness, with eight enclosures.

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Acknowledgements

I thank E. Bolitho and Y. Williams for assistance, and M. W. Blows, M. J. Caley, L. Day, J. A. Endler, K. Hughes, M. D. Jennions, M. Petrie, J. D. Reynolds, F. H. Rodd and B. Walsh for discussion, encouragement, advice and comments on the manuscript. I am supported by a fellowship and grant from the ARC.

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Brooks, R. Negative genetic correlation between male sexual attractiveness and survival . Nature 406, 67–70 (2000). https://doi.org/10.1038/35017552

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