Compensatory traits can explain concave cost function of purely sexual traits

Abstract

The cost of ornamentation is often measured experimentally to study the relative importance of sexual and viability selection for ornamentation, but these experiments can lead to a misleading conclusion when compensatory trait is ignored. A famous, classic experiment on the outermost tail feathers in the barn swallow Hirundo rustica, explains that the U-shaped aerodynamic performance of the outermost tail feathers would be the evolutionary outcome mainly through viability selection for optimal tail length, but this conclusion depends on the assumption that compensatory traits do not cause reduced performance. Using a simple model experiment, I demonstrated that ornamentation evolved purely though sexual selection can produce a U-shaped cost function under the presence of compensatory traits. Therefore, U-shaped cost function (and the low performance of individuals with reduced ornaments) cannot be used to infer the evolutionary force favoring ornamentation, due to a previously overlooked concept, overcompensation, which can increase, rather than decrease, the apparent cost of ornamentation.

Maneuverable flight evolved with forked tails and opportunities for extrapair mating in swallows and martins (Aves: Hirundininae)

“…In support of these theories, when experimentally manipulating outermost tail feathers in the barn swallow, Evans and colleagues found that estimated peak aerodynamic performance located only around 10 mm shorter from the current outermost tail feathers, suggesting that most forked tails evolved through viability selection for aerodynamic function (e.g., Evans 1998; Buchanan & Evans 2000; Rowe et al 2001). However, their studies, like those of many others that manipulated ornaments, did not take into account the presence of compensatory traits (Hasegawa 2023; also see Oufiero & Garland 2007; Husak & Swallow 2011 for general cautions of ignoring compensatory traits). According to Norberg (1994, p.231), any experimental shortening and lengthening of the outer tail feathers is likely to upset an original co-adapted character set.…”

“…Dotted line is shown as a ridge line. See Hasegawa (2023) for detailed explanation. Illustration was given by Hasegawa (2023).…”

“…In other words, reducing forked tails might deteriorate phenotypic integration with compensatory traits (e.g., wing size and shape; Møller 1996), and thus, impair whole-organism performance (Fig. 1, light blue line; Hasegawa 2023). Therefore, these experiments were not conclusive, and the evolutionary force favoring forked tails remains controversial (e.g., Barbosa 1999; Møller & Barbosa 2001; Matyjyasiak et al 2009 for early disputes; Hasegawa & Arai 2020, 2021, 2022 for recent discussions).…”

Male mate preference against tail‐elongated females in the barn swallow

“…This is because, when tail length is manipulated, aerodynamic ability is impaired because of the reduction in functional integrity associated with compensatory traits (Norberg, 1994, p 231; see fig. 3 in Hasegawa, 2022). Macroevolutionary analysis, i.e., an alternative approach focusing on the evolution of focal traits, provided insight into the evolution of female tail length.…”

“…The barn swallow Hirundo rustica is a socially monogamous bird and model species of sexual selection, in which females have been shown to behaviorally prefer tail-elongated males, explaining their long outermost tail feathers. For example, experimental manipulation of tail length affects acceptance/rejection of extra-pair copulation (Møller, 1988;reviewed in Møller, 1994;Romano et al, 2017;Turner, 2006), which is further reinforced by comparative evidence of the evolution of tail fork depth in relation to opportunities for extrapair paternity in hirundines or the family Hirundinidae (Hasegawa & Arai, 2020a, 2022. Female barn swallows have shorter tails than males, but some studies suggest that female tails are nonetheless costly to produce and maintain (e.g., Cuervo et al, 2003;Cuervo & de Ayala, 2014;Hasegawa et al, 2020;Rowe et al, 2001).…”