Evolutionary patterns of adaptive acrobatics and physical performance predict expression profiles of androgen receptor - but not oestrogen receptor - in the forelimb musculature

Abstract

1. Superior physical competence is vital to the adaptive behavioral routines of many animals, particularly those that engage in elaborate socio-sexual displays. How such traits evolve across species remains unclear. 2. Recent work suggests that activation of sex steroid receptors in neuromuscular systems is necessary for the fine motor skills needed to execute physically elaborate displays. Thus, using passerine birds as models, we test whether interspecific variation in display complexity predicts species differences in the abundance of androgen and estrogen receptors (AR and ERα) expressed in the forelimb musculature and spinal cord. 3. We find that small-scale evolutionary patterns in physical display complexity positively predict expression of the AR in the main muscles that lift and retract the wings. No such relationship is detected in the spinal cord, and we do not find a correlation between display behavior and neuromuscular expression of ERα. Also, we find that AR expression levels in different androgen targets throughout the body - namely the wing muscles, spinal cord, and testes - are not necessarily correlated, providing evidence that evolutionary forces may drive AR expression in a tissue-specific manner. 4. These results suggest co-evolution between the physical prowess necessary for display performance and levels of AR expression in avian forelimb muscles. Moreover, this relationship appears to be specific to muscle and AR-mediated, but not ERα-mediated, signaling. 5. Given that prior work suggests that activation of muscular AR is a necessary component of physical display performance, our current data support the hypothesis that sexual selection shapes levels of AR expressed in the forelimb skeletal muscles to help drive the evolution of adaptive motor abilities.

Keywords: manakins; neuromuscular physiology; sexual selection; social display; testosterone; tropical birds.

Figure 1

Passerine species included in the current study. At top is our reconstructed phylogenetic tree that depicts the relatedness among species (Jetz et al. 2012). Each species’ image is included under its common and scientific name. Under each image are the species’ scores on the two display complexity indices: the wing movement complexity score and overall motor complexity score (see Table 1 and Methods). At the bottom is a brief description of the bird's display. Species included in the light blue box are suboscine passerines, whereas species in the pink box are oscine passerines. Manakin and flycatcher photographs from Nick Athanas; pin-tailed whydah photograph from Jody de Bruyn; zebra finch photograph from Mat Gilfedder.

Figure 2

Androgen receptor (AR) and estrogen receptor α (ERα) mRNA expression in the different species’ (A and C) wing muscles and (B and D) spinal cords. Both AR (A) and ERα (C) levels in the supracoricoidieus (SC), scapulohumeralis caudalis (SH) and pectoralis (PEC) are collapsed into one group for each species, as we find no effect of muscle on either gene's expression. In the spinal cord, gray bars indicate AR (B) and ERα (D) levels in cervical/thoracic region, whereas white bars indicate these genes’ expression in the lumbar/sacral region. Note that the axes between these two graphs are different, as ERα was abundantly expressed in the blue-crowned manakin lumbar/sacral cord. In all graphs, differences in letters atop error bars depict significant differences between species (Shaffer-Holm correction), whereas asterisks (*) under a species’ respective letter depict species-specific regional differences. Species are indicated on the horizontal axis (GCM=golden-collared manakin; RCM = red-capped manakin; BCM = blue-crowned manakin; LTM = lance-tailed manakin; OBF = ochre-bellied flycatcher; PTW = pin-tailed whydah; and ZF = zebra finch). Data represent means ± 1SEM.

Figure 3

Relationship between species variation in neuromuscular androgen receptor (AR) expression and display complexity. (A) Overall display complexity and (B) wing movement display complex and their relationships to levels of wing muscle AR expression. (C) Overall display complexity and (B) wing movement display complex and their relationships to levels of spinal cord AR expression. Graphic representations do not correct for phylogenetic relatedness, although these corrections are implemented statistically using phylogenetic generalized least-squares (PGLS) models. Best-fit lines represent significant models (p<0.05). GCM=golden-collared manakin; RCM = red-capped manakin; BCM = blue-crowned manakin; LTM = lance-tailed manakin; OBF = ochre-bellied flycatcher; PTW = pin-tailed whydah; and ZF = zebra finch. AR mRNA levels represent each species’ estimated marginal means (EMM) derived from mixed-model analyses.