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

Abstract

Laryngeal echolocation in bats could have evolved following two scenarios: a single origin from a common ancestor or an independent acquisition inside the two clades Yinpterochiroptera and Yangochiroptera. Later, some members of Yinpterochiroptera possibly lost their ability to echolocate. In bats, the larynx produces vocalizations for communication and, in most species, for echolocation. 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 bat larynx and bioacoustics interpretations. 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. We find that a strong phylogenetic signal is potentially the main source explaining macroevolutionary variation in laryngeal form among bats. We predict that the three parameters of sound production in echolocation (frequency, intensity, and rate of calls) are independently modulated by different laryngeal components, but this hypothesis remains understudied in terms of species diversity.

Development of the hyolaryngeal architecture in horseshoe bats: Insights into the evolution of the pulse generation for laryngeal echolocation

“…Characteristics ( 2), (3), and ( 5) are consistent with the descriptions of Rhinolophus hipposideros [43] and Hipposideros caffer [26]. As reported in other laryngeally echolocating bats [19,49], the intrinsic laryngeal muscles of horseshoe bats are hypertrophied compared to those of mice, and the laryngeal cartilage is drastically modified to provide attachment sites for these muscles. The overall pattern of innervation of the intrinsic laryngeal muscles of horseshoe bats was identical to that of mice, except for a novel branch of the cranial laryngeal nerve and the absence of the foramen thyroideum (Fig.…”

“…Abduction of the glottis to vibrate the vocal fold involves contraction of the dorsal cricoarytenoid muscle. It has been suggested that tracheal chambers contribute to sound intensity [26,27,49,72]. Given that the ventral part of the cricothyroid muscle is attached to the lateral tracheal chambers, mineralization of the tracheal chambers can be promoted by superfast contraction of this muscle.…”

“…Concerning the sound-producing organs of bats, a few studies have reported the musculoskeletal morphology of the hyolaryngeal apparatus in adults [26,40,[42][43][44][45][46][47][48]. Laryngeally echolocating bats possess hypertrophied intrinsic laryngeal muscles supported by reinforced cricoid, thyroid, and arytenoid cartilage [26,43,49]. In particular, the cricothyroid muscle is a superfast muscle essential for the generation of high-frequency sounds in yangochiropterans [19].…”

Musculoskeletal morphogenesis supports the convergent evolution of bat laryngeal echolocation

“…Our work established foundation for further studies of bat larynx to reveal not only bat laryngeal echolocation origin but also their unique evolutionary history. In the future, functional morphological analyses should be done to understand the relationship between laryngeal anatomy and acoustic properties of the ultrasonic sounds produced in bats [30]. Moreover, new insights into evolutionary history of the bat laryngeal echolocation should be obtained from observation of innervation pattern of the laryngeal muscles [30,37] and studies of molecular mechanisms that regulate the laryngeal morphogenesis and SFM formation in the echolocating bat lineages.…”

“…In addition, the cricothyroid muscle, whose contraction produces high-frequency sound in mammals (figure 1b and electronic supplementary material, figure S1), is enlarged and specialized into superfast muscle (SFM) in yangochiropteran bats, allowing them to emit several dozens of ultrasonic pulses per second [27][28][29]. Morphological and molecular comparisons of the larynx between echolocating and non-echolocating linages, and within echolocating linages, may shed light on the origin of chiropteran laryngeal echolocation [30].…”