Adult sex ratio and male body condition affect alternative reproductive tactics in a spider

Abstract

Biases in adult sex ratios can alter the intensity of sexual selection by enhancing competition for mates. Under intense competition males increase their investment in behaviors to outcompete rivals (e.g., fighting). Yet, given that in male-biased environments mating opportunities are rare males may alternatively reduce costly courtship and/or adopt alternative reproductive tactics (ARTs). Males of the spider Pisaura mirabilis adopt different mating tactics, offering females genuine nuptial gifts (prey), nutritionally worthless gifts (prey leftovers), or no gifts. To test whether behavioral shifts between gift tactics are triggered by changes in the competitive environment, we established replicate spider populations under natural conditions at varying adult sex ratios (male-biased, female-biased and equal) and sampled gift tactics repeatedly over time. We additionally explored how male individual traits, such as body size and condition, affect the expression of ARTs. In male-biased populations males produced more gifts but of low quality, suggesting competition to trigger increased mating effort to ensure mate acquisition and fertilizations, but through a worthless gift tactic. Production of gifts and of genuine gifts was favored by high body condition, pointing to energetic limitations as being central for male reproductive capacity. We hence highlight two co-existing mechanisms at play to explain ARTs in this system, the competitive social environment where expression of gift tactics is based on optimal-decision making to overcome competition, and a conditional strategy linked to the individual’s energetic state.

Sex roles and sex ratios in animals

“…Most empirical work has been conducted in the laboratory (Gao & Kang, 2006; Head, Lindholm & Brooks, 2008; de Jong et al ., 2009; Edward, Fricke & Chapman, 2010; Weir, 2013; Jehan et al ., 2020), under semi‐natural conditions (e.g. outdoor pools; Mills & Reynolds, 2003), or in fenced natural areas (Le Galliard et al ., 2005; Rosa et al ., 2017; Heimerl et al ., 2022). Fewer experiments have been conducted in the field (Cox et al ., 2019).…”

“…Fewer experiments have been conducted in the field (Cox et al ., 2019). These studies have focused on a broad range of taxa, including fish (Mills & Reynolds, 2003; Head et al ., 2008; de Jong et al ., 2009; Wacker et al ., 2013; Weir, 2013; Liao et al ., 2014), birds (Cox et al ., 2019), lizards (Le Galliard et al ., 2005; Fitze & Le Galliard, 2008), snakes (Shine, Langkilde & Mason, 2003), insects (Gao & Kang, 2006; Edward et al ., 2010; Kelly, 2015; Fritzsche et al ., 2016; Godwin et al ., 2017; Rosa et al ., 2017; McNamara et al ., 2019; Jehan et al ., 2020) and spiders (Heimerl et al ., 2022).…”

“…Studies applying manipulations during an individual's lifetime (within one or multiple breeding seasons) have demonstrated responses to changes in ASR across a broad range of traits. Male‐biased ASR triggers increased male contest behaviour (common lizard, Lacerta vivipara ; Le Galliard et al ., 2005), courtship (garter snake, Thamnophis sirtalis parietalis (Shine et al ., 2003); two‐spotted goby (de Jong et al ., 2009)], nuptial gift production (nursery web spider, Pisaura mirabilis ; Heimerl et al ., 2022), sperm investment (Chinese bushcricket, Gampsocleis gratiosa ; Gao & Kang, 2006), post‐mating guarding behaviour (New Zealand stick insect, Micrarchus hystriculeus ; Kelly, 2015), parental care (i.e. nest attendance) (beetle Lethrus apterus ; Rosa et al ., 2017), and changes in cooperative breeding behaviours (brown headed nuthatch, Sitta pusilla ; Cox et al ., 2019).…”

“…Studies applying manipulations during an individual's lifetime (within one or multiple breeding seasons) have demonstrated responses to changes in ASR across a broad range of traits. Male-biased ASR triggers increased male contest behaviour(common lizard, Lacerta vivipara;Le Galliard et al, 2005), courtship (garter snake, Thamnophis sirtalis parietalis(Shine et al, 2003); twospotted goby(de Jong et al, 2009)], nuptial gift production (nursery web spider, Pisaura mirabilis;Heimerl et al, 2022), sperm investment (Chinese bushcricket, Gampsocleis gratiosa;…”

“…Weir, 2013;Liao et al, 2014), birds(Cox et al, 2019), lizards(Le Galliard et al, 2005;Fitze & Le Galliard, 2008), snakes(Shine, Langkilde & Mason, 2003), insects(Gao & Kang, 2006;Edward et al, 2010;Kelly, 2015;Fritzsche et al, 2016;Godwin et al, 2017;Rosa et al, 2017;McNamara et al, 2019;Jehan et al, 2020) and spiders(Heimerl et al, 2022).…”