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.

Bioinspiration from bats and new paradigms for autonomy in natural environments

“…Certain bat species with sophisticated biosonar systems that allow the animals to navigate and hunt their prey in dense vegetation, in particular, horseshoe bats (family Rhinolophidae) and Old-World leaf-nosed bats (family Hipposideridae), have highly dynamic baffle on the emission and reception interfaces. These bats emit their biosonar pulses through nostrils that are surrounded by megaphonelike baffles that are actuated by a musculature that consists of 14 muscles [60]. The noseleaf actuations can take place while the biosonar pulse is being emitted [21] and result in changes to the acoustic characteristics of the pinna.…”

Soft tissues influence nasal airflow in diapsids: Implications for dinosaurs

“…Although not as mobile, nasal passage reconstructions suffer from a similar lack of resolution in extinct animals. Many aspects of the nasal passage are comprised solely of soft tissues, such as the cartilaginous conchae of birds (Bang, 1971; Danner et al, 2017), the muscular hydrostats of elephant trunks (Marchant & Shoshani, 2007; Miall & Greenwood, 1878), and the elaborate nostrils of many bat species (Brokaw and Smotherman, 2020; Usui et al, 2022). These aspects of extinct animal anatomy and physiology are often lost to the vagaries of fossilization, wherein bones, teeth, and other hard parts are often all that remains.…”