Embryogenesis and Development in Stenella attenuata and Other Cetaceans

Thewissen, J. G. M.; Heyning, John E.

doi:10.1201/b11001-12

Cited by 26 publications

(54 citation statements)

References 32 publications

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“…6). The basal Eocene artiodactyl relative of whales (the raoellid Indohyus ) and early cetaceans (represented by Eocene Pakicetus , Remingtonocetus , and a protocetid) retained the basal artiodactyl dental formula of three incisors, one canine, four premolars and three molars per jaw quadrant (Thewissen & Heyning, 2007; Cooper, Thewissen & Hussain, 2009). However, even the first fossil whales (pakicetids) already displayed a loss of molar cusps as compared to their sister group ( Indohyus in Fig.…”

Section: Resultsmentioning

confidence: 99%

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Development and evolution of the unique cetacean dentition

Armfield

Zheng

Bajpai

et al. 2013

PeerJ

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The evolutionary success of mammals is rooted in their high metabolic rate. A high metabolic rate is sustainable thanks to efficient food processing and that in turn is facilitated by precise occlusion of the teeth and the acquisition of rhythmic mastication. These major evolutionary innovations characterize most members of the Class Mammalia. Cetaceans are one of the few groups of mammals in which precise occlusion has been secondarily lost. Most toothed whales have an increased number of simple crowned teeth that are similar along the tooth row. Evolution toward these specializations began immediately after the time cetaceans transitioned from terrestrial-to-marine environments. The fossil record documents the critical aspects of occlusal evolution of cetaceans, and allows us to pinpoint the evolutionary timing of the macroevolutionary events leading to their unusual dental morphology among mammals. The developmental controls of tooth differentiation and tooth number have been studied in a few mammalian clades, but nothing is known about how these controls differ between cetaceans and mammals that retain functional occlusion. Here we show that pigs, a cetacean relative with regionalized tooth morphology and complex tooth crowns, retain the typical mammalian gene expression patterns that control early tooth differentiation, expressing Bmp4 in the rostral (mesial, anterior) domain of the jaw, and Fgf8 caudally (distal, posterior). By contrast, dolphins have lost these regional differences in dental morphology and the Bmp4 domain is extended into the caudal region of the developing jaw. We hypothesize that the functional constraints underlying mammalian occlusion have been released in cetaceans, facilitating changes in the genetic control of early dental development. Such major developmental changes drive morphological evolution and are correlated with major shifts in diet and food processing during cetacean evolution.

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Section: Resultsmentioning

confidence: 99%

“…They were fixed in 10% formalin buffer and stored in 70% ethanol after collection. Prior to use the embryos were aged according to Carnegie stages (Thewissen & Heyning, 2007). Due to the limited supply of dolphin embryos, we were only able to stain one specimen at each stage.…”

Section: Methodsmentioning

confidence: 99%

Development and evolution of the unique cetacean dentition

Armfield

Zheng

Bajpai

et al. 2013

PeerJ

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“…This study allows us to discuss in detail some adaptations that are of general interest in the development of the skull in S. attenuata from stage 20 to stage 23 of Thewissen and Heyning (2007). These adaptations relate to key cranial anatomical elements of the cetacean skull.…”

Section: Discussionmentioning

confidence: 99%

“…1). These fetuses are staged using the adapted and expanded Carnegie system from Thewissen and Heyning (2007). Ages of fetuses are based on Š těrba et al (2000).…”

Section: Methodsmentioning

confidence: 99%

“…The development of the Cetacea skull was studied in embryos (de Burlet, 1913a(de Burlet, , 1913b(de Burlet, , 1914a(de Burlet, , 1914bSchreiber, 1916;Honigmann, 1917;Rauschmann et al, 2006;Thewissen and Heyning, 2007) and fetuses (Schulte, 1916;Ridewood, 1923;Eales, 1950). Cetacean research focused on specific biological systems to understand differences within Mammalia.…”

Section: Introductionmentioning

confidence: 99%

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Development of the Skull of the Pantropical Spotted Dolphin (Stenella attenuata)

Moran

Nummela

Thewissen

2011

The Anatomical Record

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We describe the bony and cartilaginous structures of five fetal skulls of Stenella attenuata (pantropical spotted dolphin) specimens. The specimens represent early fetal life as suggested by the presence of rostral tactile hairs and the beginnings of skin pigmentation. These specimens exhibit the developmental order of ossification of the intramembranous and endochondral elements of the cranium as well as the functional and morphological development of specific cetacean anatomical adaptations. Detailed observations are presented on telescoping, nasal anatomy, and middle ear anatomy. The development of the middle ear ossicles, ectotympanic bone, and median nasal cartilage is of interest because in the adult these structures are morphologically different from those in land mammals. We follow specific cetacean morphological characteristics through fetal development to provide insight into the form and function of the cetacean body plan. Combining these data with fossil evidence, it is possible to overlie ontogenetic patterns and discern evolutionary patterns of the cetacean skull. Anat Rec, 294:1743Rec, 294: -1756Rec, 294: , 2011. V V C 2011 Wiley-Liss, Inc.Key words: cranial development; Stenella attenuata; telescoping; middle ear; CetaceaThe development of the Cetacea skull was studied in embryos (de Burlet, 1913a(de Burlet, , 1913b(de Burlet, , 1914a(de Burlet, , 1914bSchreiber, 1916;Honigmann, 1917;Rauschmann et al., 2006;Thewissen and Heyning, 2007) and fetuses (Schulte, 1916;Ridewood, 1923;Eales, 1950). Cetacean research focused on specific biological systems to understand differences within Mammalia. Comtesse-Weidner (2007), Miller (1923 and Kellogg (1928aKellogg ( , 1928b) studied morphological elements including telescoping. Oelschl-ä ger and Buhl (1985), Klima and van Bree (1990), and Klima (1995 studied nasal anatomy and development. Oelschlä ger (1986, 1990), Solntseva (1990, 2002), and Kinkel et al. (2001 concentrated on hearing reception and sound emission while Mead and Fordyce (2009) focused on general skull anatomy. Although comparative embryological studies on cetaceans were rare, developmental studies were mostly nonexistent. Such studies (e.g., Thewissen et al., 2006, Armfield et al., in press) allow for a deeper understanding of the ontogenetic constraints on the evolution of the cetacean body plan.Habitat changes alter adaptations for specific cetacean body plans. These modifications include those of anatomical function and body plan from land mammals to fully aquatic, air breathing marine mammals. Our study focuses on anatomical structures of five Stenella attenuata (pantropical spotted dolphin) fetuses. Here we describe bony and cartilaginous structures of the

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Anatomy and Age Estimation of an Early Blue Whale (Balaenoptera musculus) Fetus

Roston

Lickorish

Buchholtz

2013

The Anatomical Record

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The external anatomy of a 130-mm blue whale fetus (Balaenoptera musculus) is described, and its internal anatomy is reconstructed noninvasively from microCT scans. The specimen lies developmentally at the junction of the embryonic and fetal periods. Similarly to the embryos of many odontocetes, it lacks a caudal fluke and dorsal fin, but it also exhibits an elongated rostrum, resorbed umbilical hernia, partially exposed cornea, and spatial separation of the anus and genitalia seen in early odontocete fetuses. Dermal ossification of the cranial bones has begun, but the endochondral skeleton is completely cartilaginous. The shape and position of the maxilla suggest that the earliest stages of anterior skull telescoping have begun, but there is no indication of occipital overlap posteriorly. The nasopharynx, larynx, and heart already display the distinctive morphology characteristic of Balaenoptera. This study develops a model of body length changes during blue whale development by integrating the large International Whaling Statistics (IWS) database, historical observations of blue whale migration and reproduction, and descriptions of fetal growth trends in other mammals. The model predicts an age of 65 days postconception for the specimen. The early developmental milestones of Balaenoptera mirror those of the odontocete Stenella to a remarkable extent, but the first appearance of the caudal fluke and dorsal fin are delayed relative to other morphological transitions. The accelerated prenatal growth characteristic of Balaenoptera occurs during fetal, not embryonic, development. Anat Rec, 296:709-722, 2013. V C 2013 Wiley Periodicals, Inc.Key words: blue whale; fetus; mysticete; development; microCT The development of a blue whale (Balaenoptera musculus) from a zygote to a 7.5-m, 2,000-3,000 kg neonate (Reidenberg and Laitman, 2008) is remarkable for both its rapid increase in size and for the reorganization of multiple mammalian anatomical systems for life in the water. Study of the transitions of size and morphology during blue whale development is limited by access to fetal specimens. Many thousands of fetuses were recovered during the decades of active commercial whaling, but very few were preserved for scientific examination. Embryos and small fetuses are particularly rare, with the result that the early ontogeny of the species is largely unknown.

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Embryogenesis and Development in Stenella attenuata and Other Cetaceans

Cited by 26 publications

References 32 publications

Development and evolution of the unique cetacean dentition

Development and evolution of the unique cetacean dentition

Development of the Skull of the Pantropical Spotted Dolphin (Stenella attenuata)

Anatomy and Age Estimation of an Early Blue Whale (Balaenoptera musculus) Fetus

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