Early Development and Orientation of the Acoustic Funnel Provides Insight into the Evolution of Sound Reception Pathways in Cetaceans

Abstract

Whales receive underwater sounds through a fundamentally different mechanism than their close terrestrial relatives. Instead of hearing through the ear canal, cetaceans hear through specialized fatty tissues leading to an evolutionarily novel feature: an acoustic funnel located anterior to the tympanic aperture. We traced the ontogenetic development of this feature in 56 fetal specimens from 10 different families of toothed (odontocete) and baleen (mysticete) whales, using X-ray computed tomography. We also charted ear ossification patterns through ontogeny to understand the impact of heterochronic developmental processes. We determined that the acoustic funnel arises from a prominent V-shaped structure established early in ontogeny, formed by the malleus and the goniale. In odontocetes, this V-formation develops into a cone-shaped funnel facing anteriorly, directly into intramandibular acoustic fats, which is likely functionally linked to the anterior orientation of sound reception in echolocation. In contrast, the acoustic funnel in balaenopterids rotates laterally, later in fetal development, consistent with a lateral sound reception pathway. Balaenids and several fossil mysticetes retain a somewhat anteriorly oriented acoustic funnel in the mature condition, indicating that a lateral sound reception pathway in balaenopterids may be a recent evolutionary innovation linked to specialized feeding modes, such as lunge-feeding.

Cetacean Skull Telescoping Brings Evolution of Cranial Sutures into Focus

“…Recently, computed tomography has allowed the internal morphology of rare and irreplaceable prenatal cetacean specimens to be examined noninvasively (Roston et al, 2013;Hampe et al, 2015). This has allowed researchers to assemble larger data sets of fetal series to compare development across species (Yamato and Pyenson, 2015). Apart from Moran et al (2011), most descriptions of embryonic and fetal skulls provided in the literature do not explicitly discuss the origin of telescoped skull morphologies, but some make mention of the presence or absence of bone overlap (e.g., Ridewood, 1923).…”

Decoupling Tooth Loss from the Evolution of Baleen in Whales

“…Their broad habitat ranges and large body size imposes serious logistical and methodological constraints (Pyenson, 2011), while their conservation status and the legal framework protecting them depends on geopolitical context, making it extremely difficult to collect fresh vouchers for specimen-based research, especially from fetal material crucial to understanding embryonic tooth development. Examination of the Yamato and Pyenson (2015) dataset failed to identify tooth buds in mysticete embryos between 16 and 500 cm in total length, suggesting they are too small to appear in conventional medical computed tomography (CT) scanning techniques, though potentially could be visible with enhancement (e.g., iodine-based contrast-enhanced methods).…”

Inner ear development in cetaceans

“…Our samples for three‐dimensional analysis included 20 odontocetes and nine mysticetes. We measured total length as the circumferential (rather than straight) distance between the tip of the rostrum to the tail fluke notch, similar to Yamato & Pyenson (), and followed Yamato & Pyenson () in dividing each specimen's total length by previously reported newborn total length measurements (see Table ). We also analysed four unique, unsexed S. scrofa specimens, including an adult skull, a postnatal skull, and two whole foetuses of 23–24 cm crown–rump length (CRL), measured from the top of the head to the tail base.…”

“…Solntseva () examines peripheral auditory system development in cetaceans and pinnipeds. Yamato & Pyenson () and Kinkel et al. () provide insight into cetacean middle ear ontogeny, and Solntseva () documents how auditory structures form in terrestrial, semi‐aquatic and aquatic species.…”

“…) – relatively few have examined foetal specimens as well (see Dunkin et al. ; Tsai & Fordyce, ; Yamato & Pyenson, ). There is relatively little information on how cetacean cranial morphology changes during foetal growth, though the studies on the topic that exist (for example, Klima, ; Rauschmann et al.…”