Androgen receptor expression could contribute to the honesty of a sexual signal and be the basis of species differences in courtship displays
Year: 2015
Type: article
Abstract: In most species, females choose their mates based on signals that honestly reflect male quality (Searcy & Nowicki 2005). Signal honesty can be imposed by high costs of signal production (Zahavi 1975; Andersson 1994; Searcy & Nowicki 2005) or by mechanistic connections between the quality of a signal and traits that are of importance to females (Byers, Hebets & Podos 2010; Hill 2011). For example, plumage colour in many birds is linked with the amount of food-derived pigments a male obtains, making pigmentation a reliable indicator of foraging ability, nutritional condition and even resistance to oxidative stress (Hill 2011). Research on sexual selection has characterized many of the male ornaments that females prefer and linked ornament quality with male reproductive success for many systems. However, there are relatively few cases in which we understand the specific mechanisms either imposing signalling costs or linking signal quality with variation in the traits for which females are actually selecting. In the current issue of Functional Ecology, Fuxjager et al. identify a molecular mechanism that is tightly associated with variation in the complexity of courtship displays in manakins (Pipridae) and that may therefore help ensure that displays honestly reflect aspects of males’ underlying phenotype. Specifically, the level of androgen receptor transcript in wing muscles varied among the seven species examined and was highest in the species with the most physically demanding and complex courtship dances. Thus, androgen receptor expression may be a molecular mechanism ensuring signal honesty by linking the quality of sexual displays with cellular function. Moreover, changes in androgen receptor gene expression across species could explain the divergence of courtship displays and thus have contributed to the explosive diversification of the manakin clade (Prum 1997). Sexual displays in manakins are not exaggerated sexual ornaments, unlike the exotic plumage and appendages often addressed by sexual selection theory. Rather, manakin dances are physically demanding and intricate performances (Prum 1990). Sexual displays or competitions that depend upon whole-organism motor performance permit females to evaluate males based on integrated aspects of their physiology because displaying relies upon metabolic, immune, hormonal and neural function, among other whole-organism aspects of phenotype (Husak et al. 2009; Byers, Hebets & Podos 2010; Barske et al. 2011). Several recent perspectives have emphasized that the male traits upon which females base their mate choice decisions are often the product of underlying genotype, the developmental environment and a male's current condition, and therefore reflect whole-organism function (Byers, Hebets & Podos 2010; Hill 2011). There are at least two aspects of male motor performance that could reflect holistic aspects of males’ overall phenotype: vigour and skill (Byers, Hebets & Podos 2010). Male behaviours, such as fighting, persistently defending a territory on a lek, repeating vocalizations or physical displays over long periods or defending a harem, may all reflect a male's ‘vigour’, defined as the ability to perform energetically expensive motor acts repeatedly (Byers, Hebets & Podos 2010). Many aspects of manakins’ repetitive, physically demanding and intricate dances within their leks likely reflect males' vigour (Prum 1990; Byers, Hebets & Podos 2010; Barske et al. 2011). Females should attend to motor performances that depend upon vigour because such displays are very energetically costly and thus honest indictors of male's current condition, genetic quality and developmental past (Byers, Hebets & Podos 2010). The skill with which males perform specific motor patterns that are part of a courtship display may be an even better indicator of males’ phenotype than vigour, particularly when motor patterns require activation and coordination of motor units near a physiologically or anatomically imposed limit of production (Podos 1996; Fusani et al. 2007; Byers, Hebets & Podos 2010). Females should pay particular attention to motor skills because such skills rely directly upon musculoskeletal, nervous and sensory system function (Byers, Hebets & Podos 2010). For example, the skill with which male songbirds produce vocal elements with rapidly repeated, high-bandwidth frequency sweeps, termed trills, is limited by bill morphology such that there is a maximal rate of repetition possible for a given bandwidth (Podos 1996; Ballentine 2006). Within species variation in the skill with which males perform trills may be related to male genetic background, developmental history and current condition, and females have been shown to use vocal performance as a basis for mating preferences (Ballentine, Hyman & Nowicki 2004; Ballentine 2006; Caro et al. 2010). Additionally, species differences in bill morphology result in different performance maxima and could lead to variation in song and thus species divergence (Podos 2001; Ballentine 2006). Studies of motor performance across taxa are valuable because performance traits provide an opportunity to examine the microevolutionary process of adaptation (Arnold 1983; Husak et al. 2009). In the case of manakins, individual males differ in the speed and accuracy of their elaborate displays and some movements, such as wing sonation, are proposed to require contraction speeds near the limits of vertebrate muscle (Bostwick & Prum 2003, 2005; Fusani et al. 2007; Byers, Hebets & Podos 2010). Thus, like trill performance in bird song, at least some features of manakin dances are likely constrained by motor performance limits, and variation within species in the speed and accuracy of these display components may be the basis of female mate choice. Additionally, variation between species in their performance maxima could reflect the origins of divergence in displays and thus the physiological basis of speciation. While performance limits can ensure that sexual displays are honest indicators of male condition and quality within species, strong selection on motor performance can drive the evolution of behavioural, physiological and morphological adaptations to move beyond such constraints (Ballentine 2006; Fusani et al. 2014). In manakins, muscle size and the structure of the wing bones may reflect adaptations for courtship displays (Fusani et al. 2014). Further, the elaborate plumage of many dancing birds has been proposed as a secondary adaptation to enhance females’ perception of male motor performance and increase the stimulus value (Byers, Hebets & Podos 2010). The paper by Fuxjager et al. in the current issue of Functional Ecology describes another possible adaptation to enhance motor performance and perhaps shift the performance limit imposed by skeletal muscle contraction speeds: elevated expression of androgen receptor in wing muscle. Androgen receptor expression in the wing and other muscles was already shown to influence fine motor movements and to be expressed at constitutively higher levels in golden-collared manakins compared to nondisplaying species (Feng et al. 2010; Fuxjager et al. 2013). The authors demonstrate that elevated androgen receptor transcript levels in wing muscle are associated with the motor complexity of courtship displays in a comparison of seven avian species, five of which are within the manakin clade. Thus, at least in the manakins, elevated gene expression for androgen receptors could be a mechanism that enhances motor performance. Future work examining the expression of androgen receptor in skeletal muscle of other clades with sexual displays that depend upon motor skill, such as snipes, hummingbirds and birds of paradise, could determine whether this molecular adaptation is widespread among birds (Byers, Hebets & Podos 2010). Additionally, studies within species that examine the relationship between androgen receptor expression, variation in particular motor skills near the limit for the speed of muscle contraction and mating success will determine whether differences in gene expression could also be the basis of individual differences in male performance quality and a mechanism upon which sexual selection acts. Identifying the mechanisms that link sexual displays and ornaments with the traits that actually matter to females for their mate choice decisions informs our understanding of how signal honesty is ensured. In the case of elaborate male displays in manakins and perhaps other birds, the expression of androgen receptor in skeletal muscle may influence the speed of contraction and thus the skill with which males perform their dances. Gene expression, whether for androgen receptor or other proteins important to cellular function, can be influenced by the current and developmental environments, as well as underlying genotype, and therefore represents an aspect of male phenotype that encompasses condition, quality and resilience to environmental perturbation during development (Byers, Hebets & Podos 2010; Hill 2011). In the case of manakins, variation in androgen receptor expression influences the skill with which males perform displays (Fuxjager et al. 2013) and may prove to be the mechanism that links cellular function with the quality of male displays, ensuring signal honesty. Additionally, between species differences in androgen receptor expression could be the origin of divergence in sexual displays, and such change in gene expression may have ultimately contributed to speciation in the manakins and perhaps other avian clades.
Source: Functional Ecology
Author: Kendra B. Sewall
Institution: Virginia Tech
Language: English
Domain: Life Sciences
Open Access status: bronze
OpenAlex ID: W1929920560