Postnatal ontogeny of the cochlea and flight ability in Jamaican fruit bats (Phyllostomidae) with implications for the evolution of echolocation

Abstract

Recent evidence has shown that the developmental emergence of echolocation calls in young bats follow an independent developmental pathway from other vocalizations and that adult-like echolocation call structure significantly precedes flight ability. These data in combination with new insights into the echolocation ability of some shrews suggest that the evolution of echolocation in bats may involve inheritance of a primitive sonar system that was modified to its current state, rather than the ad hoc evolution of echolocation in the earliest bats. Because the cochlea is crucial in the sensation of echoes returning from sonar pulses, we tracked changes in cochlear morphology during development that included the basilar membrane (BM) and secondary spiral lamina (SSL) along the length of the cochlea in relation to stages of flight ability in young bats. Our data show that the morphological prerequisite for sonar sensitivity of the cochlea significantly precedes the onset of flight in young bats and, in fact, development of this prerequisite is complete before parturition. In addition, there were no discernible changes in cochlear morphology with stages of flight development, demonstrating temporal asymmetry between the development of morphology associated with echo-pulse return sensitivity and volancy. These data further corroborate and support the hypothesis that adaptations for sonar and echolocation evolved before flight in mammals.

Intense natural selection preceded the invasion of new adaptive zones during the radiation of New World leaf-nosed bats

“…The phyllostomid skull provides an excellent model with which to test hypotheses on the evolution of complex morphological phenotypes because of the various functions it performs and its dynamic developmental complexity. Due to its impressive morphological diversity, its ecological importance, and its relevance for the innovation of echolocation by nasal emission, the phyllostomid skull has been extensively studied at a functional, biomechanical, and developmental level 9 – 27 . The remarkable specializations seen in these bats provide a unique opportunity for investigation of the evolutionary forces that have promoted such striking phenotypic diversity and the intensity of these forces.…”

Ontogeny of the hyoid apparatus in Jamaican fruit bats (Chiroptera: Phyllostomidae) in unraveling the evolution of echolocation in bats

“…These data agree with previously published research showing that at birth and well before flight ability, A. jamaicensis exhibits many characteristics of a functioning echolocation system, including production of adult‐like high FM echolocation calls and cochleae that are structurally and apparently functionally adult‐like (Fig. ) (Carter et al ., ; Carter & Adams, ). As A. jamaicensis begins to develop flight abilities, echolocation call rates increase which coincides with calcification of the cricoid cartilage and as we have shown in this study, the ossification of the last bone in the hyoid apparatus that forms a connection between the larynx and the brain.…”

“…In this study, we further investigate the relationship between ontogeny and evolution by incorporating published data on transitional development in A. jamaicensis (Carter & Adams, , ; Carter et al ., ) with novel data on the transitional ontogeny of a highly derived structure (stylohyal tympanic bone articulation) present only in laryngeally echolocating bats to form hypotheses regarding evolutionary transitions from the common ancestor to the highly derived morphology present in extant laryngeal echolocators. Specifically, using both prenatal and postnatal specimens, we hypothesized that the ontogenetic timing and stepwise sequences leading to formation of the stylohyal tympanic bone articulation mimics the evolutionary ancestor–descendants transitions.…”

Anatomía Comparada Del Laberinto Óseo De Los Murciélagos Platalina Genovensium (Phyllostomidae, Lonchophyllinae) Y Tomopeas Ravus (Molossidae, Tomopeatinae)

“…The study of the different aspects of the bony labyrinth in bats is mainly based on histological cross sections, x-ray images, and fossilized petrosals (e.g., Pye, 1966aPye, , b, 1967Pye, , 1970Hinchcliffe & Pye, 1968;Habersetzer & Storch 1992;Simmons et al, 2008;Odendaal & Jacobs, 2011;Carter & Adams, 2015;Czaplewski, 2017). However, the recent availability to researchers of new technology like Computed Tomography (CT) to study the internal morphology of biological structures without damaging the specimens allows the reconstruction of structures that were impossible to observe on their entirety before.…”