Prenatal developmental sequence of the skull of minke whales and its implications for the evolution of mysticetes and the teeth‐to‐baleen transition

Abstract

Baleen whales (Mysticeti) have an extraordinary fossil record documenting the transition from toothed raptorial taxa to modern species that bear baleen plates, keratinous bristles employed in filter-feeding. Remnants of their toothed ancestry can be found in their ontogeny, as they still develop tooth germs in utero. Understanding the developmental transition from teeth to baleen and the associated skull modifications in prenatal specimens of extant species can enhance our understanding of the evolutionary history of this lineage by using ontogeny as a relative proxy of the evolutionary changes observed in the fossil record. Although at present very little information is available on prenatal development of baleen whales, especially regarding tooth resorption and baleen formation, due to a lack of specimens. Here I present the first detailed description of prenatal specimens of minke whales (Balaenoptera acutorostrata and Balaenoptera bonaerensis), focusing on the skull anatomy and tooth germ development, resorption, and baleen growth. The ontogenetic sequence described consists of 10 specimens of both minke whale species, from the earliest fetal stages to full term. The internal skull anatomy of the specimens was visualized using traditional and iodine-enhanced computed tomography scanning. These highquality data allow detailed description of skull development both qualitatively and quantitatively using threedimensional landmark analysis. I report distinctive external anatomical changes and the presence of a denser tissue medial to the tooth germs in specimens from the final portion of gestation, which can be interpreted as the first signs of baleen formation (baleen rudiments). Tooth germs are only completely resorbed just before the eruption of the baleen from the gums, and they are still present for a brief period with baleen rudiments. Skull shape development is characterized by progressive elongation of the rostrum relative to the braincase and by the relative anterior movement of the supraoccipital shield, contributing to a defining feature of cetaceans, telescoping. These data aid the interpretation of fossil morphologies, especially of those extinct taxa where there is no direct evidence of presence of baleen, even if caution is needed when comparing prenatal extant specimens with adult fossils. The ontogeny of other mysticete species needs to be analyzed before drawing definitive conclusions about the influence of development on the evolution of this group. Nonetheless, this work is the first step towards a deeper understanding of the most distinctive patterns in prenatal skull development of baleen whales, and of the anatomical changes that accompany the transition from tooth germs to baleen. It also presents comprehensive hypotheses to explain the influence of developmental processes on the evolution of skull morphology and feeding adaptations of mysticetes.

Enhancing CT imaging: A safe protocol to stain and de‐stain rare fetal museum specimens using diffusible iodine‐based staining (diceCT)

“…Subsequent to the pilot study described here, we stained, CT scanned and successfully de‐stained four additional ethanol‐preserved and two formalin‐preserved pre‐natal mysticete specimens. These specimens greatly varied in volume, from about 200 cm 3 to over 20,000 cm 3 (Table – see also Lanzetti, 2019, Lanzetti et al, 2020). The largest specimen is at the upper size limit for applying this protocol.…”

“…As with the pig specimens, the humpback whale was CT scanned both prior to and after the stain. Following this trial, the protocol was also applied to other six prenatal specimens of various baleen whale species preserved in 70% ethanol, including two preserved in a water-based formalin solution (Table S1; Lanzetti, 2019;Lanzetti et al, 2020).…”

“…Although we did not perform dissection or CT scans after the stain was removed, the external appearance of the specimen was overall similar as before the staining process (Figure 3). This specimen, as many cetacean fetal specimens in museum fluid collections, present a yellow coloration likely due to the fixatives used initially on them and long term storage in ethanol (see Lanzetti, 2019 andLanzetti et al, 2020 for additional examples). We noticed the precipitation of 2-3 mm long sodium thiosulfate crystals in small patches on the skin.…”

Morphological variation of the relictual alveolar structures in the mandibles of baleen whales

“…Unfortunately, dental counts for embryonic mysticetes are rare, making it difficult to test this prediction. Recent work by Lanzetti (2019) andThewissen et al (2017), which builds on that of Ishikawa & Amasaki (1995) and Ishikawa et al (1999), expands the histological datasets of early ontogenetic variability in mysticete dentition, especially across a taxonomic breadth that may elucidate an evolutionary framework to test the relationship between alveoli and tooth identity. Additionally, many 19th and early 20th century anatomists report tooth counts for foetal mysticetes, though this work is scattered across many languages and difficult to verify (see Peredo, Pyenson & Boersma (2017a) for a review of embryological and histological data pertaining to mysticete tooth buds).…”

“…Baleen whales are born entirely edentulous, although fossil relatives have mineralized teeth as adults. Embryological evidence demonstrates extant mysticetes briefly develop teeth in utero before resorbing them prior to birth (Lanzetti, 2019;Lanzetti, Berta & Ekdale, 2018;Peredo, Pyenson & Boersma, 2017a).…”