Patterns of orofacial clefting in the facial morphology of bats: a possible naturally occurring model of cleft palate

Abstract

A normal feature of the facial anatomy of many species of bat is the presence of bony discontinuities or clefts, which bear a remarkable similarity to orofacial clefts that occur in humans as a congenital pathology. These clefts occur in two forms: a midline cleft between the two premaxillae (analogous to the rare midline craniofacial clefts in humans) and bilateral paramedian clefts between the premaxilla and the maxillae (analogous to the typical cleft lip and palate in humans). Here, we describe the distribution of orofacial clefting across major bat clades, exploring the relationship of the different patterns of clefting to feeding mode, development of the vomeronasal organ, development of the nasolacrimal duct and mode of emission of the echolocation call in different bat groups. We also present the results of detailed radiographic and soft tissue dissections of representative examples of the two types of cleft. The midline cleft has arisen independently multiple times in bat phylogeny, whereas the paramedian cleft has arisen once and is a synapomorphy uniting the Rhinolophidae and Hipposideridae. In all cases examined, the bony cleft is filled in by a robust fibrous membrane, continuous with the periosteum of the margins of the cleft. In the paramedian clefts, this membrane splits to enclose the premaxilla but forms a loose fold laterally between the premaxilla and maxilla, allowing the premaxilla and nose-leaf to pivot dorsoventrally in the sagittal plane under the action of facial muscles attached to the nasal cartilages. It is possible that this is a specific adaptation for echolocation and/or aerial insectivory. Given the shared embryological location of orofacial clefts in bats and humans, it is likely that aspects of the developmental control networks that produce cleft lip and palate in humans may also be implicated in the formation of these clefts as a normal feature in some bats. A better understanding of craniofacial development in bats with and without clefts may therefore suggest avenues for research into abnormal craniofacial development in humans.

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

“…The bilateral cleft evolved only once in the common ancestor of Rhinolophidae and Hipposideridae. Character mapping was based on Orr et al [ 88 ] …”

“…Bats have a unique morphological feature in the rostral part of the upper jaw, an orofacial cleft on the premaxilla and maxilla bones that is anatomically similar to that observed in humans with congenital anomalies [ 87 , 88 ]. There are two types of chiropteran orofacial cleft, midline and bilateral clefts.…”

“…There are two types of chiropteran orofacial cleft, midline and bilateral clefts. The midline cleft is observed in nine families of bats: Megadermatidae, Emballonuridae, Molossidae, Miniopteridae, Vespertilliionidae, Cistugidae, Myzopodidae, Thyropteridae, Furipteridae [ 88 ] (Fig. 3 ).…”

“…The inner space of the cleft is occupied with a robust, translucent, fibrous membrane. The bilateral cleft is only seen in Rhinolophidae and Hipposideridae [ 88 ] (Fig. 3 ).…”

Contrasting patterns of RUNX2 repeat variations are associated with palate shape in phyllostomid bats and New World primates

“…An understanding of the genetic basis associated with craniofacial variability in animal natural populations is a major focus of modern evolutionary and developmental studies 1 – 5 . Until recently, broad phenotypic differences were thought to be the result of several gene mutations, each one with relatively small effects 6 .…”