Parasite‐mediated sexual selection in a damselfly

Abstract

Sexual selection can improve population fitness and purge deleterious mutation from the gene pool by promoting condition‐dependent mate selection. One ecological factor that reduces individual condition is parasitism. Parasitism tends to increase hosts' mutation load and likely indicates inferior host genetic quality. Parasite‐mediated selection, therefore, should favour the mating success of parasite‐resistant individuals over parasitised individuals. We tested this hypothesis in male Agriocnemis pygmaea damselflies, which are parasitised by Arrenurus water mites. We calculated frequency (i.e. the proportion of parasitism) and intensity (i.e. the number of parasites per parasitised individual) of parasitism in free‐flying males and males in copula in seven natural populations. We predicted that males observed mating will be less likely to be parasitised than expected based on the frequency of parasitism in the population. We further predicted that parasite intensity would be lower in males caught in copula than single males. We found that parasitised males were significantly less likely to be found in copula than non‐parasitised males, independent of their occurrence frequency. However, there was no difference in the average parasite load between males captured in copula or free‐flying males. Our study shows that in addition to natural selection, sexual selection is a strong agent against parasitism and implies that it could promote local adaptation to counteract parasite driven extinction risks.

Environmental variation shapes and links parasitism to sexual selection

“…Points and error bars show the selection gradients (and +/-1 standard errors) on parasite prevalence and load per population. Lines show predicted selection coefficient for a particular measure of parasitism in relation to environmental variables and 95% confidence interval with coloured lines depicting statistically significant effects 2020; Khan and Herberstein 2022). This heterogeneity in parasitism was partially explained by environmental factors.…”

“…In both species, only one population showed directional selection, yet in opposite directions, favouring parasitized individuals in E. ebrium and against parasitized individuals in E. geminatum. In general, research on the effect of parasitism on damselfly male mating success is also somewhat mixed: selection against parasitized males has been found in some studies (Forbes 1991;Honkavaara et al 2009;Gómez-Llano et al 2020) and not in others (Rolff et al 2000;Khan and Herberstein 2022), or found in some years but not in others (Andres and Cordero 1998). Environmental variables can increase or decrease selection against parasitized individuals if they affect the costs of defences against parasites (Sandland and Minchella 2003;Mitchell et al 2005;Lazzaro and Little 2009;Wolinska and King 2009;Hughes et al 2016) and drive parasite-host coevolution (Paplauskas et al 2021).…”

“…The causes of sexual selection can vary among populations, as female mate choice, male signalling, male competition, and the expression of secondary sexual traits often depend on environmental context (Andersson 1994;Badyaev and Qvarnström 2002;Kokko et al 2002;Chaine and Lyon 2008;Cornwallis and Uller 2010;Siepielski et al 2022). Parasitism is a key interaction that can affect the strength and direction of sexual selection because infection can decrease host condition, the expression of secondary sexual traits, and mating success (Hamilton and Zuk 1982;Åbro 1982;Forbes and Baker 1991;Vergara et al 2012;Gómez-Llano et al 2020;Dougherty 2021).…”

Gut parasites infection increases mate rejection in a species with indirect sperm transfer

“…In the fruit fly Drosophila melanogaster , a species with a nonsex role reversed system, both healthy males and females prefer uninfected mates (Wittman & Fedorka, 2014). Male infection also alters their intrasexual competition abilities, diminishing their reproductive success in the damselfly Agriocnemis pygmaea (Khan & Herberstein, 2022). Interestingly, if we evaluate mating success concerning parasitism status in mutual choice scenarios, it is influenced not only by partner condition, but also by the chooser's condition (Gao et al, 2021; Reyes‐Ramírez et al, 2020).…”

Parasitism shapes selection by drastically reducing host fitness and increasing host fitness variation

“…Despite considerable interest in parasites as selective agents generating fitness costs for hosts [3,[5][6][7][8][9], we have no general, quantitative understanding of the extent to which parasitism may differentially affect host reproductive fitness components and their variance. Identifying which fitness components are most strongly affected by parasites will allow for predicting when parasite-mediated selection is likely to be strong or weak.…”