Adaptive evolution of a derived radius morphology in manakins (Aves, Pipridae) to support acrobatic display behavior

Abstract

The morphology of the avian skeleton is often studied in the context of adaptations for powered flight. The effects of other evolutionary forces, such as sexual selection, on avian skeletal design are unclear, even though birds produce diverse behaviors that undoubtedly require a variety of osteological modifications. Here, we investigate this issue in a family of passerine birds called manakins (Pipridae), which have evolved physically unusual and elaborate courtship displays. We report that, in species within the genus Manacus, the shaft of the radius is heavily flattened and shows substantial solidification. Past work anecdotally notes this morphology and attributes it to the species' ability to hit their wings together above their heads to produce loud mechanical sonations. Our results show that this feature is unique to Manacus compared to the other species in our study, including a variety of taxa that produce other sonations through alternate wing mechanisms. At the same time, our data reveal striking similarities across species in total radius volume and solidification. Together, this suggests that supposedly adaptive alterations in radial morphology occur within a conserved framework of a set radius volume and solidness, which in turn is likely determined by natural selection. Further allometric analyses imply that the radius is less constrained by body size and the structural demands that underlie powered flight, compared to other forelimb bones that are mostly unmodified across taxa. These results are consistent with the idea that the radius is more susceptible to selective modification by sexual selection. Overall, this study provides some of the first insight into the osteological evolution of passerine birds, as well as the way in which opposing selective forces can shape skeletal design in these species. J. Morphol. 277:766-775, 2016. © 2016 Wiley Periodicals, Inc.

Physiological constraint on acrobatic courtship behavior underlies rapid sympatric speciation in bearded manakins

“…This is indicative of evolutionary discordance between different facets of the muscle’s contractile machinery, which ultimately put the brakes on sexual selection for a rapid display. Further evolutionary elaboration of the roll-snap speed would likely require modifications to the calcium handling properties, alongside other adaptations for the performance of this signal in bearded manakins ( Friscia et al, 2016 ; Fuxjager et al, 2016b ; Fuxjager et al, 2016c ). Notably, limitations to muscular calcium handling are not typically associated with the speed-endurance trade-off, which is often considered to result from muscle fiber type composition ( Rivero et al, 1993 ; Komi, 1984 ; Esbjörnsson et al, 1993 ).…”

Determination of the wingsnap sonation mechanism of the Golden-collared manakin (Manacus vitellinus)

“…Analysis of other wing-bone characteristics, such as those of the carpals, revealed nothing unique. A detailed description of other manakin skeletal characteristics is forthcoming (Friscia et al, 2016).…”

Neuromuscular mechanisms of an elaborate wing display in the golden-collared manakin (Manacus vitellinus)

“…Rather, decades of research show that numerous species incorporate extraordinary physicality into the social displays used for courtship and competition (Amézquita and Hödl, 2004;Frith and Beehler, 1998;Garrick and Lang, 1977;Girard et al, 2011;Grafe et al, 2012;Hogg and Forbes, 1997;Masonjones and Lewis, 1996;Miles et al, 2017;Ord et al, 2001Ord et al, , 2002Pelletier et al, 2004;Prum, 1990;Voigt et al, 2001;Walls and Semlitsch, 1991). Underlying many of these athletic courtship displays are remarkable anatomical and physiological specializations that have evolved to support behavioral output (Bostwick et al, 2012;Clifton et al, 2015;Friscia et al, 2016;Fuxjager et al, 2016a;Lindsay et al, 2015;Mangiamele et al, 2016). However, one of the biggest challenges to studying adaptations for behavioral display centers around assessing the neuromuscular mechanisms that control complex and unusual physical movements.…”