Facial muscle modification associated with chiropteran noseleaf development: Insights into the developmental basis of a movable rostral appendage in mammals

Abstract

Background: Mammal evolution has generated diverse craniofacial morphologies, including remarkable movable rostral appendages. However, the muscular and skeletal architecture providing the mobility of these appendages remains largely unexplored. Here, we focus on chiropteran noseleaves and compare the three-dimensional internal morphology of late-stage embryos between the greater horseshoe bat Rhinolophus ferrumequinum, which possesses a noseleaf, and the Asian bent-winged bat Miniopterus fuliginosus and Egyptian fruit bat Rousettus aegyptiacus, which do not. We also assess earlier stage cell proliferation within the rostrum to elucidate cellular mechanisms underlying noseleaf-associated morphological modifications. Results: The musculus maxillolabialis inserted into proximal vibrissae follicles in M fuliginosus and R aegyptiacus embryos but instead inserted into the horseshoe plate in R ferrumequinum. This modification suggests that the M maxillolabialis has adapted to controlling the noseleaf rather than vibrissae in rhinolophid bats. Our cellular analysis showed higher cell proliferation within the maxillary and frontonasal processes of St. 14 embryos in R ferrumequinum compared to M fuliginosus and R aegyptiacus, suggesting that the spatial alteration of noseleaf-associated muscle is derived from changes in facial morphogenesis that occur by St. 14. Conclusion: This is the first study clarifying the morphological and cellular bases underlying the development of mammalian rostral appendages.