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

Abstract

Craniofacial morphology is extremely diversified within bat phylogeny, however growth and development of the palate in bats remains unstudied. The formation of both midline and bilateral orofacial clefts in laryngeally echolocating bats, morphologically similar to the syndromic and non-syndromic cleft palate in humans, are not well understood. Developmental series of prenatal samples (n = 128) and adults (n = 10) of eight bat species (two pteropodids, four rhinolophoids, and two yangochiropterans), and two non-bat mammals (Mus musculus and Erinaceus amurensis), were CT-scanned and cranial bones forming the upper jaw complex were three-dimensionally visualised to assess whether differences in palate development can be observed across bat phylogeny. Volumetric data of bones composing the upper jaw complex were measured to quantify palate growth. The premaxilla is relatively reduced in bats compared to other mammals and its shape is heterogeneous depending on the presence and type of orofacial cleft across bat phylogeny. The palatine process of premaxillary bones is lacking in pteropodids and yangochiropterans, whereas the premaxilla is a mobile structure which is only in contact caudally with the maxilla by a fibrous membrane or suture in rhinolophoids. In all bats, maxillary bones progressively extend caudally and palatine bones, in some cases split into three branches, extend caudally so that they are completely fused to another one medially prior to the birth. Ossification of the vomer and fusion of the maxillary and palatine bones occur earlier in rhinolophoids than in pteropodids and yangochiropterans. The vomer ossifies bilaterally from two different ossification centres in yangochiropterans, which is uncommon in other bats and non-bat mammals. Analysis of ontogenetic allometric trajectories of the upper jaw complex revealed faster development of maxillary, vomer, and palatine bones in yangochiropterans compared to other bats, especially rhinolophoids. Ancestral state reconstruction revealed that yangochiropterans have a higher magnitude of change in ossification rate compared to other bats and E. amurensis a lower magnitude compared to M. musculus and bats. This study provides new evidence of heterochronic shifts in craniofacial development and growth across bat phylogeny that can improve understanding of the developmental differences characterising nasal and oral emission strategies.