Abstract
Cognitive abilities may be crucial for individuals to respond appropriately to their social and natural environment, thereby increasing fitness. However, the role of cognitive traits in sexual selection has received relatively little attention. Here, we studied 1) whether male secondary sexual traits (colour, courtship, and nest) reflect their cognitive ability, 2) whether females choose mates based on males' and their own cognitive abilities, and 3) how the interplay between secondary sexual traits and cognitive ability determines male attractiveness in the three-spined stickleback (Gasterosteus aculetaus). For this, we first evaluated the cognitive ability of sexually mature males and females in a detour-reaching task. Then, female preference was repeatedly assessed in a dichotomous-choice test, where the female was exposed to two males with contrasting performances (relatively good and bad) in the detour-reaching task. Female preference for better performing males was affected by the female's own cognitive ability. Females with relatively medium-low cognitive ability preferred males with high ability, whereas females with high ability showed no preference. We also found that males with higher cognitive abilities built more elaborated nests, but showed weaker red nuptial colouration. To our knowledge, this is among the first results that illustrate how cognitive traits of both sexes influence female mate preference, which has implications for the strength and direction of sexual selection.
Highlights
Sexual selection, acting through female choice and male competition, is responsible for the evolution and maintenance of secondary sexual displays in males (Darwin 1871; Andersson 1994), such as bright colorations, calls, complex nests/arenas, and elaborated behaviours (Hill and Yasukawa 2014)
In birds, song complexity was linked to the ability to solve different cognitive tasks (Boogert et al 2008; Boogert et al 2011a), suggesting that males can exhibit their cognitive ability through sexual signals (Searcy and Andersson 1986; Catchpole 1987, but see Sewall et al 2013; Templeton et al 2014; Anderson et al 2017)
We selected the final model using Shipley's extension for the Akaike Information Criteria (AIC; Shipley 2013), and evaluated its goodness of fit using the Fisher's C statistic. This statistic can be compared with a χ 2-distribution with k × 2 degrees of freedom, where k is the total number of independence claims specified in the model; P > 0.05 indicating that the model adequately reproduces the hypothesized causal relationships (P > 0.05; Shipley 2009; Lefcheck 2016). Fish improved their performance in the detour-reaching task throughout the repeated trials (LMM, F1, 41 = 25.94, P < 0.001; Figure 1)
Summary
Sexual selection, acting through female choice and male competition, is responsible for the evolution and maintenance of secondary sexual displays in males (Darwin 1871; Andersson 1994), such as bright colorations, calls, complex nests/arenas, and elaborated behaviours (Hill and Yasukawa 2014). An extraordinary example is shown by bowerbirds, where males build and decorate a bower with sticks and brightly coloured objects and perform elaborated courtship displays to attract mates (Doucet and Montgomerie 2003; Keagy et al 2009, 2011; Isden et al 2013). This complex performance of different behaviours in concert requires high cognitive abilities and brain capacity (Madden 2001, but see Day et al 2005). The expression and maintenance of carotenoid-based ornament colouration may divert this resource away from neural and cognitive functions
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