Sex-specific immunocompetence: resistance and tolerance can both be futile but not under the same circumstances

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Abstract Immunocompetence evolution can involve a “resistance is futile” scenario if parasite encounter rates are so high that high investment in resistance only marginally delays infection. Here, we investigate two understudied aspects of “futility”: the mode of immunocompetence and sexual selection. First, immunocompetence is usefully categorized as reducing the rate of becoming infected (resistance) or reducing the negative fitness consequences of infection once it happened (tolerance). We compare the prospects of futility for resistance, tolerance, and their joint occurrence, showing that resistance futility arises with respect to parasite encounter rates, while tolerance futility arises with respect to parasite virulence. However, if the same host trait improves pleiotropically both resistance and tolerance, futility disappears altogether and immunity investment remains profitable when increasing parasite encounter rates, virulence, or both. Second, we examine how sexual selection strength impacts these findings. If one sex (typically males) is near the faster end of a fast-slow continuum of life histories, then life history patterns reflecting futility can evolve sex-specificity. The solutions often feature sexual dimorphism in immunocompetence, but not always in the direction of strong sexual selection yielding low immunity: sexual selection can select for faster and “sicker” lives, but if sexual selection also favors traits that impact parasite encounter rates, the results are strongly dependent on whether futility (along any axis) plays a role.