Sexual signals reveal males’ oxidative stress defences: Testing this hypothesis in an invertebrate

Abstract

The hypothesis that sexual traits reveal the oxidative stress resistance of their bearers has been widely tested in vertebrates but remains unexplored in invertebrates. Here, Hetaerina americana was used to test whether oxidative stress defences are advertised by male wing spot size and colour (a male sexual trait). To this end, we investigated (1) whether oxidative stress reduced survival, (2) whether wing spot size revealed males’ antioxidant defences and (3) how wing spot size and colour were affected by oxidative stress. We elevated oxidative stress by injecting adult males with paraquat (PQ, a compound that favours the production of free radicals) and then examined how this affected male survival and wing spot size. We then related the expression of wing spot size to indicators of oxidative stress—hydrogen peroxide (H2O2) and total antioxidant capacity (TAC), super oxide dismutase (SOD) and catalase (CAT)—in adult males (whose wing spot is fixed) injected with PQ. In teneral males, whose wing spots are still forming, we compared wing spot size, colour (red and yellow chroma) and brightness in individuals injected with PQ or water as a control. Oxidative stress reduced the survival of adult and teneral males. While the H2O2 and TAC markers of antioxidant defences were positively correlated with wing spot size, there was no correlation with CAT and a negative correlation with SOD. In teneral males, PQ increased the yellow chroma and brightness of wing spots, but did not affect spot size or red chroma. Our results highlight the importance of measuring different markers as indicators of male oxidative stress defences, and that the sexual signals of invertebrates may reveal the oxidative stress status of their bearers. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13051/suppinfo is available for this article.

Interactions between oxidative stress and attractiveness to mates and individual mate choice in the beetle Tenebrio molitor

“…PQ reacts with oxygen and generates ROS, such as the superoxide radical (O2−·) and the hydroxyl radical (•OH), as well as the pro‐oxidant hydrogen peroxide (H2O2) (Adachi et al., 2000; Rzezniczak et al., 2011; Suntres, 2002). Since PQ favors O2−· production in the mitochondria of animals, it is used to experimentally induce oxidative stress in isolated mitochondria, cultured cells, and whole organisms (Sittipunt, 2005; Castello et al., 2007; Cocheme & Murphy, 2008; Hosamani & Muralidhara, 2013; Lazarević et al., 2013; Martínez‐Lendech et al., 2018, 2019; Mehdi et al., 2020). Animals treated with PQ tend to succumb (Bonilla et al., 2006; Martínez‐Lendech et al., 2018; Sittipunt, 2005).…”

“…Since PQ favors O2−· production in the mitochondria of animals, it is used to experimentally induce oxidative stress in isolated mitochondria, cultured cells, and whole organisms (Sittipunt, 2005; Castello et al., 2007; Cocheme & Murphy, 2008; Hosamani & Muralidhara, 2013; Lazarević et al., 2013; Martínez‐Lendech et al., 2018, 2019; Mehdi et al., 2020). Animals treated with PQ tend to succumb (Bonilla et al., 2006; Martínez‐Lendech et al., 2018; Sittipunt, 2005). Antioxidants protect against PQ‐induced oxidative toxicity (Bonilla et al., 2006; Satpute et al., 2017; Thiruchelvam et al., 2005), while PQ affords protection in individuals infected with pathogens that produce antioxidants to avoid the host pro‐oxidant defenses (Medina‐Gómez et al., 2018).…”

“…We induced a state of oxidative stress with paraquat (PQ; SIGMA Chemical Co.). This compound is used to prompt experimentally oxidative stress in animals, including insects (Hosamani & Muralidhara, 2013; Lazarević et al., 2013; Martínez‐Lendech et al., 2018, 2019). Inside a Petri dish (100 mm × 20 mm), 12 ± 1‐day‐old sexually mature virgin males and females (Márquez‐García et al., 2016) were allowed to drink individually either a drop of PQ dissolved in 1 μl of deionized water (20 mM) (paraquat group) or only deionized water (control group).…”

“…Martínez‐Lendech et al. (2018) previously reported that the 3 hr period after the PQ application is sufficient to increase oxidative stress.…”

“…This hypothesis predicts that females would prefer males with elaborate sexual signals, which, in turn, are resistant to oxidative stress, compared with males with underdeveloped sexual signals and confronting oxidative stress. This hypothesis has been tested mainly with vertebrate models (Martínez‐Lendech et al., 2018) and with a focus limited to visually perceived characteristics (Garratt & Brooks, 2012). Hence, it is necessary to determine in invertebrates whether sexual traits other than visual signals could be an indicator of the oxidative stress status of males.…”