Little is known about the operation of male mate choice in systems with perceived high costs to male choosiness, like Rana sylvatica; matings with preferred females produced fewer and lower-quality offspring

Fitness costs of mating with preferred females in a scramble mating system. Lindsey Swierk, Tracy Langkilde. Behavioral Ecology, arz001, https://doi.org/10.1093/beheco/arz001

Abstract: Little is known about the operation of male mate choice in systems with perceived high costs to male choosiness. Scramble mating systems are one type of system in which male choice is often considered too costly to be selected. However, in many scramble mating systems, there are also potentially high rewards of male choosiness, as females vary dramatically in reproductive output and males typically mate once per season and/or per lifetime. Using scramble mating wood frogs (Rana sylvatica), we tested whether males gain fitness benefits by mating with preferred females. We conducted choice trials (1 male presented simultaneously with 2 females) and permitted males to mate with their preferred or nonpreferred female. Offspring of preferred and nonpreferred females were reared in the laboratory and field, and we quantified various fitness-relevant parameters, including survivorship and growth rates. Across multiple parameters measured, matings with preferred females produced fewer and lower-quality offspring than did those with nonpreferred females. Our results are inconsistent with the idea that mate choice confers benefits on the choosing sex. We instead propose that, in scramble systems, males will be more likely to amplex females that are easier to capture, which may correlate with lower quality but increases male likelihood of successfully mating. Such male choice may not favor increased fitness when the operational sex ratio is less biased toward males in scramble mating systems but is, instead, a bet-hedging tactic benefitting males when available females are limited.

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Our data suggest that an untested parameter of male wood frog mate choice may also play a role in determining its rela-tive costs and benefits. In recent decades, mate choice based on genetic compatibility has been demonstrated to be an important and widely observed component of mate choice (see Brown 1997; Tregenza and Wedell 2000; Mays and Hill 2004). In particular, mate choice based on dissimilarity of major histocompatibility complex (MHC) genes has been observed in humans (Wedekind et al. 1995) and other species (e.g., Gowaty et al. 2003; Agbali et al. 2010; Rymešová et al. 2017; for review see Kamiya et al. 2014); benefits of choosing a mate with dissimilar MHC genes include provisioning offspring with a greater variety of cell-surface proteins that enable the immune system to identify and fight pathogens and parasites (Bernatchez and Landry 2003; Piertney and Oliver 2006; Ruff et al. 2012). If male mate choice in wood frogs also has an MHC-compatibility component (or similar), then it could be pre-dicted that, when faced with challenges to the immune system, offspring of preferred females would have a fitness advantage over the offspring of nonpreferred females. When taken as a whole, our data support this idea. In the lab, in the absence of immune chal-lenges, offspring of preferred females had lower survivorship than the offspring of nonpreferred females (Figure 3a), possibly due to reasons associated with female catchability, as proposed above. However, in the presence of numerous immune challenges in the field, this difference in offspring survivorship disappears (Figure 4a). A MHC-related fitness cost to mating with nonpreferred mates could be responsible for closing the gap between preferred and nonpreferred offspring field survivorship. While admittedly far from conclusive, these results imply that multiple types of mate choice may exist in this scramble system and could warrant future study.