Prenatal growth patterns of the upper jaw complex with implications for laryngeal echolocation in bats

Abstract

Craniofacial morphology is extremely diversified within bat phylogeny, howevergrowth and development of the palate in bats remains unstudied. The formation ofboth midline and bilateral orofacial clefts in laryngeally echolocating bats, morpholog-ically similar to the syndromic and non-syndromic cleft palate in humans, are not wellunderstood. Developmental series of prenatal samples (n = 128) and adults (n = 10) ofeight bat species (two pteropodids, four rhinolophoids, and two yangochiropterans),and two non-bat mammals (Mus musculus and Erinaceus amurensis), were CT-scannedand cranial bones forming the upper jaw complex were three-dimensionally visualisedto assess whether differences in palate development can be observed across bat phy-logeny. Volumetric data of bones composing the upper jaw complex were measuredto quantify palate growth. The premaxilla is relatively reduced in bats compared toother mammals and its shape is heterogeneous depending on the presence and typeof orofacial cleft across bat phylogeny. The palatine process of premaxillary bonesis lacking in pteropodids and yangochiropterans, whereas the premaxilla is a mobilestructure which is only in contact caudally with the maxilla by a fibrous membrane orsuture in rhinolophoids. In all bats, maxillary bones progressively extend caudally andpalatine bones, in some cases split into three branches, extend caudally so that theyare completely fused to another one medially prior to the birth. Ossification of thevomer and fusion of the maxillary and palatine bones occur earlier in rhinolophoidsthan in pteropodids and yangochiropterans. The vomer ossifies bilaterally from twodifferent ossification centres in yangochiropterans, which is uncommon in other batsand non-bat mammals. Analysis of ontogenetic allometric trajectories of the upperjaw complex revealed faster development of maxillary, vomer, and palatine bones inyangochiropterans compared to other bats, especially rhinolophoids. Ancestral statereconstruction revealed that yangochiropterans have a higher magnitude of changein ossification rate compared to other bats and E. amurensis a lower magnitude com-pared to M. musculus and bats. This study provides new evidence of heterochronicshifts in craniofacial development and growth across bat phylogeny that can improve understanding of the developmental differences characterising nasal and oral emis-sion strategies.

Yannick Pommery, Daisuke Koyabu, Fumiya Meguro, Vuong Tan Tu, Thongchai Ngamprasertwong, Thanakul Wannaprasert, Taro Nojiri, Laura A.B. Wilson
Journal of Anatomy (2024)