Musculoskeletal morphogenesis supports the convergent evolution of bat laryngeal echolocation.

The order Chiroptera (bats) is the second largest group of mammals. One of the essential adaptations that have allowed bats to dominate the night skies is laryngeal echolocation, where bats emit ultrasonic pulses and listen to the returned echo to produce high-resolution 'images' of their surroundings. There are two possible scenarios for the evolutionary origin of laryngeal echolocation in bats: (1) a single origin in a common ancestor followed by the secondary loss in Pteropodidae, or (2) two convergent origins in Rhinolophoidea and Yangochiroptera. Although data from palaeontological, anatomical, developmental and genomic studies of auditory apparatuses exist, they remain inconclusive concerning the evolutionary origin of bat laryngeal echolocation. Here we compared musculoskeletal morphogenesis of the larynx in several chiropteran lineages and found distinct laryngeal modifications in two echolocating lineages, rhinolophoids and yangochiropterans. Our findings support the second scenario that rhinolophoids and yangochiropterans convergently evolved advanced laryngeal echolocation through anatomical modifications of the larynx for ultrasonic sound generation and refinement of the auditory apparatuses for more detailed sound perception.

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

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.

Normal embryonic development of the greater horseshoe bat Rhinolophus ferrumequinum, with special reference to nose leaf formation.

The order Chiroptera (bats) is the second largest group of mammals, composed of more than 1,300 species. Although powered flight and echolocation in bats have attracted many biologists, diversity in bat facial morphology has been almost neglected. Some bat species have a "nose leaf," a leaf-like epithelial appendage around their nostrils. The nose leaf appears to have been acquired at least three times independently in bat evolution, and its morphology is highly diverse among bats species. Internal tissue morphology of nose-leaves has been investigated through histological analyses of late-stage fetuses of some bat species possessing the nose leaf. However, the proximate factors that bring about chiropteran nose-leaves have not been identified. As an initial step to address the question above, we describe the normal embryonic development of the greater horseshoe bat Rhinolophus ferrumequinum, and examine development of the tissues associated with their nose leaf during embryogenesis through histological analyses. We found that the nose leaf of R. ferrumequinum is formed through two phases. First, the primordium of the nose leaf appears as two tissue bulges aligned top and bottom on the face at embryonic stages 15-16. Second, the sub-regions of the nose leaf are differentiated through ingrowth as well as outgrowth of the epithelium at stage 17. In embryogenesis of Carollia perspicillata, a phyllostomid species with a nose leaf, the nose leaf primordium is formed as a small tissue bulge on the nostril at stage 17. This tissue bulge grows into a dorsally projected thin epithelial structure. Such differences in the nose leaf developmental process between chiropteran lineages may suggest that distinct developmental mechanisms have been employed in each lineage's nose leaf evolution.

Creating diversity in mammalian facial morphology: a review of potential developmental mechanisms.

Mammals (class Mammalia) have evolved diverse craniofacial morphology to adapt to a wide range of ecological niches. However, the genetic and developmental mechanisms underlying the diversification of mammalian craniofacial morphology remain largely unknown. In this paper, we focus on the facial length and orofacial clefts of mammals and deduce potential mechanisms that produced diversity in mammalian facial morphology. Small-scale changes in facial morphology from the common ancestor, such as slight changes in facial length and the evolution of the midline cleft in some lineages of bats, could be attributed to heterochrony in facial bone ossification. In contrast, large-scale changes of facial morphology from the common ancestor, such as a truncated, widened face as well as the evolution of the bilateral cleft possessed by some bat species, could be brought about by changes in growth and patterning of the facial primordium (the facial processes) at the early stages of embryogenesis.