The developmental basis of bat wing muscle

Abstract

By acquiring wings, bats are the only mammalian lineage to have achieved flight. To be capable of powered flight, they have unique muscles associated with their wing. However, the developmental origins of bat wing muscles, and the underlying molecular and cellular mechanisms are unknown. Here we report, first, that the wing muscles are derived from multiple myogenic sources with different embryonic origins, and second, that there is a spatiotemporal correlation between the outgrowth of wing membranes and the expansion of wing muscles into them. Together, these findings imply that the wing membrane itself may regulate the patterning of wing muscles. Last, through comparative gene expression analysis, we show Fgf10 signalling is uniquely activated in the primordia of wing membranes. Our results demonstrate how components of Fgf signalling are likely to be involved in the development and evolution of novel complex adaptive traits.

Forelimb Morphology of Bats

“…Musculus occipitopollicalis is specific to chiropterans being probably derived from the m. platysmа as is shown by its innervation by the nervus facialis (Tokita et al 2012); note that the same innervation is found in the propatagial muscle of colugos (Thewissen and Babcock 1993), which we call the m. tensor propatagii. The m. occipitopollicalis of chiropterans originates from the midline of the supraoccipitale or, in Pteropus (Humphry 1869), by four strands: from the occipital crest, lower jaw, throat, and the m. pectoralis.…”

“…In giving this name, Strickler followed Macalister (1872), who had properly defined its homology but described it untenably (in Megaderma, both Macalister and Strickler gave the same name to a slip of the m. latissimus dorsi in spite of its dorsal course relative to the brachial plexus). This muscle is also mentioned as the m. cutaneus maximus in the embryological research of Carollia (Tokita et al 2012). We did not find it in the fruit bats or in horseshoe bats; probably we lost this extremely thin fascicle removing the skin.…”

“…Musculus coracocutaneus shares innervation and embryonic muscular progenitor with the m. cutaneus trunci (Tokita et al 2012). This muscle is found in all chiropterans as a long thin band, which originates from the coracoid process of the scapula and passes inside the plagiopatagium toward digit V, but does not reach it being vanished in the skin.…”

“…Musculus humeropatagialis shares innervation and embryonic muscular progenitor with the m. cutaneus trunci (Tokita et al 2012). It was described in Eumops by Vaughan (1970b), as well as in Noctilio, Nycteridae, Megadermatidae, some species of Phyllostomidae, Mormoopidae, Molossidae, and Emballonuridae by Strickler (1978).…”

Mammalian organogenesis in deep time: tools for teaching and outreach

“…Among the recent descriptions of staging systems or developmental series in mammals are those of some bats (Cretekos et al 2005;Tokita 2006;Wang et al 2010), tenrecs (Werneburg et al 2013a), and the echidna (Werneburg and Sánchez-Villagra 2011). These studies have been stimulated not only by the experimental approaches to understand evolutionary novelties arising in development and involving molecular biology (e.g., Sears 2011;Tokita et al 2012;Montandon et al 2014). The establishment of quantitative methods to compare developmental timing among species (e.g., Smith 2001; Germain and Laurin 2009;Maxwell and Harrison 2009;Goswami et al 2016) has also stimulated analyses of accumulated knowledge, revisions of the anatomy of model species previously undocumented (Hautier et al 2013;Werneburg et al 2013b), and new studies on the comparative embryology and perinatal life of mammals (Bininda-Emonds et al 2003), as in our research which was the basis of the animation presented here (Werneburg et al 2016).…”