On the Embryonic Development of the Nasal Turbinals and Their Homology in Bats

Ito, Kai; Tú, Vương Tân; Eiting, Thomas P.; Nojiri, Taro; Koyabu, Daisuke

doi:10.3389/fcell.2021.613545

Cited by 27 publications

(32 citation statements)

References 66 publications

(217 reference statements)

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“…The nasopharyngeal ducts are devoid of any portion of turbinals in all echolocating bats examined here. Exceptions are known in Rhinolophus , which projects a freely extended turbinal segment deep into the nasopharyngeal duct (Curtis et al, 2020; also see Ito et al, 2021, who disagreed on the identity of this turbinal). In nonecholocating Cynopterus , the caudal maxilloturbinal is sequestered within the nasopharyngeal duct, as part of a highly vascularized region.…”

Section: Discussionmentioning

confidence: 99%

“…Beyond the vestibule is the main nasal chamber, lined primarily by two epithelial types, respiratory and olfactory (we exclude from discussion a third type, "transitional epithelium," which is lesser in surface area, and of less understood function; Harkema, 2006). The majority of mammals have greater complexity of the nasal fossae than humans by virtue of more complex and prolonged development of turbinals (see below) and accessory compartments called recesses (Ito, Tu, Eiting, Nojiri, & Koyabu, 2021;Smith, Curtis, Bhatnagar, & Santana, 2021). Most mammals have at least three more turbinal outgrowths from the ethmoid bone compared to anthropoid primates (Lundeen and Kirk, 2019); most also have larger recesses, for example, the paranasal recesses found in mammals with laterally positioned eyes (which provide little encroachment on the nasal region; Smith & Rossie, 2008).…”

Section: Comparative Anatomy Of the Nasal And Nasopharyngeal Passagew...mentioning

confidence: 99%

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Venous networks in the upper airways of bats: A histological and diceCT study

Smith

DeLeon

Eiting

et al. 2021

The Anatomical Record

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Our knowledge of nasal cavity anatomy has grown considerably with the advent of micro‐computed tomography (CT). More recently, a technique called diffusible iodine‐based contrast‐enhanced CT (diceCT) has rendered it possible to study nasal soft tissues. Using diceCT and histology, we aim to (a) explore the utility of these techniques for inferring the presence of venous sinuses that typify respiratory mucosa and (b) inquire whether distribution of vascular mucosa may relate to specialization for derived functions of the nasal cavity (i.e., nasal‐emission of echolocation sounds) in bats. Matching histology and diceCT data indicate that diceCT can detect venous sinuses as either darkened, “empty” spaces, or radio‐opaque islands when blood cells are present. Thus, we show that diceCT provides reliable information on vascular distribution in the mucosa of the nasal airways. Among the bats studied, a nonecholocating pteropodid (Cynopterus sphinx) and an oral‐emitter of echolocation sounds (Eptesicus fuscus) possess venous sinus networks that drain into the sphenopalatine vein rostral to the nasopharynx. In contrast, nasopharyngeal passageways of nasal‐emitting hipposiderids are notably packed with venous sinuses. The mucosae of the nasopharyngeal passageways are far less vascular in nasal‐emitting phyllostomids, in which vascular mucosae are more widely distributed in the nasal cavity, and in some nectar‐feeding species, a particularly large venous sinus is adjacent to the vomeronasal organ. Therefore, we do not find a common pattern of venous sinus distribution associated with nasal emission of sounds in phyllostomids and hipposiderids. Instead, vascular mucosa is more likely critical for air‐conditioning and sometimes vomeronasal function in all bats.

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Section: Discussionmentioning

confidence: 99%

Section: Comparative Anatomy Of the Nasal And Nasopharyngeal Passagew...mentioning

confidence: 99%

Venous networks in the upper airways of bats: A histological and diceCT study

Smith

DeLeon

Eiting

et al. 2021

The Anatomical Record

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“…From anterior to posterior with corresponding segmented colors (Fig. 2a), these include the frontoturbinal (pink), ethmoturbinal I (teal), interturbinal II (potentially homologous with ethmoturbinal I [pars posterior] [Ito et al 2021]; orange), ethmoturbinal II (green), and ethmoturbinal III (purple). Residual main olfactory epithelium (yellow) can also be observed on medial parts of the nasal septum and superior portions of the nasal cavity and olfactory recess.…”

Section: Exceptional Variation In Gross Turbinate Morphology Througho...mentioning

confidence: 99%

Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats

et al. 2022

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Although evolvability of genes and traits may promote specialization during species diversification, how ecology subsequently restricts such variation remains unclear. Chemosensation requires animals to decipher a complex chemical background to locate fitness‐related resources, and thus the underlying genomic architecture and morphology must cope with constant exposure to a changing odorant landscape; detecting adaptation amidst extensive chemosensory diversity is an open challenge. In phyllostomid bats, an ecologically diverse clade that evolved plant visiting from a presumed insectivorous ancestor, the evolution of novel food detection mechanisms is suggested to be a key innovation, as plant‐visiting species rely strongly on olfaction, supplementarily using echolocation. If this is true, exceptional variation in underlying olfactory genes and phenotypes may have preceded dietary diversification. We compared olfactory receptor (OR) genes sequenced from olfactory epithelium transcriptomes and olfactory epithelium surface area of bats with differing diets. Surprisingly, although OR evolution rates were quite variable and generally high, they are largely independent of diet. Olfactory epithelial surface area, however, is relatively larger in plant‐visiting bats and there is an inverse relationship between OR evolution rates and surface area. Relatively larger surface areas suggest greater reliance on olfactory detection and stronger constraint on maintaining an already diverse OR repertoire. Instead of the typical case in which specialization and elaboration are coupled with rapid diversification of associated genes, here the relevant genes are already evolving so quickly that increased reliance on smell has led to stabilizing selection, presumably to maintain the ability to consistently discriminate among specific odorants—a potential ecological constraint on sensory evolution.

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“…A similar protocol should be undertaken on bat larynges to provide a better illustration and knowledge of the potential morphotypes described in the literature. Studies focusing on other anatomical features of bats have been performed recently (Yohe et al 2018;Santana 2018;Santana et al 2019;Ito et al 2021;Nojiri et al 2021b;Sohn et al 2021) and some studies used CT and iodine contrastenhanced imaging techniques to answer hypotheses about the evolutionary history of bats, such as recent studies on the hearing apparatus (Nojiri et al 2021a, b;Sulser et al 2022). It will be highly valuable to illustrate the shape and size of the different cartilages, their degree of mineralisation, in addition to the size, shape and position of the different muscles involved in laryngeal echolocation, especially the cricothyroid and the thyrohyoid.…”

Section: Advanced Imagingmentioning

confidence: 99%

The vocal apparatus of bats: an understudied tool to reconstruct the evolutionary history of echolocation?

Brualla¹,

Wilson²,

Doube³

et al. 2022

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Until recently, bat phylogeny separated megabats (laryngeally non-echolocators) and microbats (all laryngeal echolocators) into two distinct clades. This segregation was consistent with the assumption that laryngeal echolocation was acquired by a common ancestor and inherited by all microchiropterans. Thus, laryngeal echolocation was regarded to have evolved once. Recent advances in bat genome sequencing have added insights regarding the origin of bats and their phylogenetic relationships. The megabats previously thought to be phylogenetically isolated are now sharing a common ancestor with the superfamily Rhinolophoidea, which is constituted of laryngeal echolocators. This new relationship brings a counterpoint regarding the hypothesis of single origin of echolocation, which could have appeared several times independently. Concomitantly, recent studies in bat evolutionary developmental biology have illuminated the importance of characters from embryonic development to discussions of how and when echolocation evolved. Here, we describe how comparative chiropteran laryngeal morphology is a novel area of research that could improve the understanding of echolocation and may help resolve the evolutionary history of bats. This review provides morphological descriptions and comparisons of the larynx, bioacoustics interpretations, and newly developed visualisation approaches (i.e., contrast-enhanced computed tomography). We discuss the importance of understanding (1) laryngeal sound production so it may be linked with the evolution of the Chiropteran auditory system and (2) the evolution of laryngeal morphology to understand the ecological and behavioural aspects of bat biology.

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On the Embryonic Development of the Nasal Turbinals and Their Homology in Bats

Cited by 27 publications

References 66 publications

Venous networks in the upper airways of bats: A histological and diceCT study

Venous networks in the upper airways of bats: A histological and diceCT study

Ecological constraints on highly evolvable olfactory receptor genes and morphology in neotropical bats

The vocal apparatus of bats: an understudied tool to reconstruct the evolutionary history of echolocation?

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