Decoupling Tooth Loss from the Evolution of Baleen in Whales

Abstract

Baleen whales, or mysticetes, include the largest vertebrates to have ever evolved. Their gigantism, evolutionary success, and ecological diversity have been linked to filter feeding. Mysticetes filter feed using elaborate keratinous baleen plates, which grow from the palate and allow them to strain large quantities of prey out of the water. While the earliest mysticetes retained the adult, mineralized teeth present in ancestral whales, all species of living baleen whales lack teeth and instead possess baleen. The mechanism by which this evolutionary transformation took place remains unknown. We present four independent, but non-exclusive hypotheses for the origin of baleen. We evaluate the support for these hypotheses based on separate lines of evidence, including paleontological, molecular, and ontogenetic data. We suggest that the origin of baleen is decoupled from the loss of teeth, with a separate morphological and genetic basis. Moreover, we outline how new fossils and phylogenetic analyses may resolve current debates about morphological transformations in tooth loss and baleen origin across the phylogeny of stem and crown Mysticeti. Additional insights will likely arise from more detailed examination of developmental and biomechanical data, with sufficient ontogenetic and phylogenetic sampling.

Tooth Loss Precedes the Origin of Baleen in Whales

“…Previous hypotheses for the origin of baleen [4,5] are inconsistent with the morphology and phylogenetic position of Maiabalaena. The absence of both teeth and baleen in Maiabalaena is consistent with recent evidence that the evolutionary loss of teeth and origin of baleen are decoupled evolutionary transformations, each with a separate morphological and genetic basis [2,6]. Understanding these macroevolutionary patterns in baleen whales is akin to other macroevolutionary transformations in tetrapods such as scales to feathers in birds.…”

“…Our observations may be limited by CT resolution, or it may be attributed to the loss of alveolar bone and subsequent remodeling of the palatal margin. The presence of palatal foramina in stem cetaceans and odontocetes suggests that they supply the gingiva, as suggested by previous authors [2,6,7,14] and as seen in toothed mammals. Therefore, there is no evidence for using palatal foramina to exclusively infer the presence of baleen.…”

“…Whales use baleen, a novel integumentary structure, to filter feed; filter feeding itself evolved at least five times in tetrapod history but demonstrably only once in mammals [1]. Living baleen whales (mysticetes) are born without teeth, but paleontological and embryological evidence demonstrate that they evolved from toothed ancestors that lacked baleen entirely [2]. The mechanisms driving the origin of filter feeding in tetrapods remain obscure.…”

“…In crown mysticetes, deep palatal sulci on the ventral surfaces of the maxillae accommodate structures that innervate and vascularize the tissue overlying the baleen; identical sulci are absent in stem mysticetes, although much smaller foramina in the same area have been proposed as homologs, concurrent with the presence of multicusped, adult teeth on the lateral margins [4]. However, these foramina are not present in all taxa within the relevant clades, and they differ from the sulci of baleen-bearing mysticetes in size, orientation, and overall morphology [2,6,14]. Moreover, similar foramina have been described in the basilosaurid Dorudon atrox [15] (a stem cetacean).…”

Cetacean Skull Telescoping Brings Evolution of Cranial Sutures into Focus

“…Several advances in cetacean biology provide new context for understanding the evolution of telescoped morphologies that was unavailable to Miller (1923) and Kellogg (1928aKellogg ( , 1928b, including recognition that cetaceans are nested within terrestrial artiodactyls (Gingerich, 2001;. A robust and TELESCOPING AND CRANIAL SUTURE EVOLUTION growing fossil record of forms that preceded the telescoped skulls of modern cetaceans (and that may be intermediate between them and their un-telescoped ancestors) permits evolutionary processes to be inferred and hypotheses to be tested (e.g., Hampe and Baszio, 2010;Velez-Juarbe et al, 2015;Churchill et al, 2016;Marx and Fordyce, 2016;Geisler et al, 2017;Peredo et al, 2017;Pyenson, 2017;Churchill et al, 2018). New technology, especially noninvasive 3D imaging, is making rare and fragile specimens more accessible for research and allows telescoped morphologies-especially those of fetal specimens-to be studied for the first time "…a pattern of skull bone position referred to as 'telescoping'…" (Armfield et al, 2011) "…cetacean skulls became more telescoped as the nasal openings migrated dorsally (Miller, 1923)."…”