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

Abstract

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 latestage 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

Embryonic staging of bats with special reference to Vespertilio sinensis and its cochlear development

“…lucifugus 21 ; My. myotis 17,27 ; Pipistrellus abramus 24 ; Rhinolophus ferrumequinum 20 ; Ro. aegyptiacus 19 ; Rousettus amplexicaudatus 23 ; and Scotophilus kuhlii 16 …”

“…Embryonic staging tables have been established for various bat species to understand their overall embryogenesis 16‐28 . The first detailed embryonic staging table was established for Carollia perspicillata , 22 although older embryonic descriptions also exist 16,21 .…”

“…This staging was in principle based on the Carnegie system of human development 29,30 by arranging the timed laboratory matings. Later research on the embryonic staging system of bats have built on the C. perspicillata system 20,24,26 . Comparisons of embryonic staging tables have led to the claim of potential heterochronic shifts in the tail, 24 forelimb and hind limb, 25 and nose‐leaves 20,26 among bat species.…”

“…Later research on the embryonic staging system of bats have built on the C. perspicillata system 20,24,26 . Comparisons of embryonic staging tables have led to the claim of potential heterochronic shifts in the tail, 24 forelimb and hind limb, 25 and nose‐leaves 20,26 among bat species. However, these descriptive studies did not incorporate their data into a quantitative framework.…”

Fissures, folds, and scrolls: The ontogenetic basis for complexity of the nasal cavity in a fruit bat (Rousettus leschenaultii)

“…There are two overarching goals for this study. First, since pteropodids studied to date have a relatively unspecialized internal nasal morphology (Allen, 1882; Giannini et al, 2012; Starck, 1943), nasal capsule ontogeny in Rousettus may offer context to recognize developmental distinctions with more specialized bats, few of which have been studied ontogenetically to date (e.g., Myotis— Frick, 1954, as discussed in Zeller, 1987; Rhinolophus— Usui & Tikita, 2019). Second, in light of recent studies indicating postnatal plasticity of certain turbinals or parts of turbinals (Coppola, Craven, Seeger, & Weiler, 2014; Pang et al, 2016; Smith et al, 2007; Smith, Martell, Rossie, Bonar, & DeLeon, 2016; Van Valkenburgh et al, 2014), it may be possible to infer predominant mechanisms influencing internal nasal morphology that are specific to a certain life stage or contiguous stages.…”