Linking gene expression and phenotypic changes in the developmental and evolutionary origins of osteosclerosis in the ribs of bowhead whales (balaena mysticetus).
aging; Cetacea; bone; whales; osteoblasts; hyperostosis
Bowhead whales are among the longest-lived mammals with an extreme lifespan of about 211 years. During the first 25 years of their lives, rib bones increase in mineral density and the medulla transitions from compact to trabecular bone. Molecular drivers associated with these phenotypic changes in bone remain unknown. This study assessed expression levels of osteogenic genes from samples of rib bones of bowheads. Samples were harvested from prenatal to 86-year-old whales, representing the first third of the bowhead lifespan. Fetal to 2-year-old bowheads showed expression levels consistent with the rapid deposition of the bone extracellular matrix. Sexually mature animals showed expression levels associated with low rates of osteogenesis and increased osteoclastogenesis. After the first 25 years of life, declines in osteogenesis corresponded with increased expression of EZH2, an epigenetic regulator of osteogenesis. These findings suggest EZH2 may be at least one epigenetic modifier that contributes to the age-related changes in the rib bone phenotype along with the transition from compact to trabecular bone. Ancient cetaceans and their fossil relatives also display these phenotypes, suggesting EZH2 may have shaped the skeleton of whales in evolutionary history.
Cooper LN; Ball HC; Vinyard CJ; Safadi FF; George JC; Thewissen JGM
Journal of Experimental Zoology. Part B, Molecular and Developmental Evolution
2020
2020-07-29
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
journalArticle
<a href="http://doi.org/10.1002/jez.b.22990" target="_blank" rel="noreferrer noopener">10.1002/jez.b.22990</a>
Evolutionary Changes Of The Importance Of Olfaction In Cetaceans Based On The Olfactory Marker Protein Gene
Aquatic adaptation; deletion causes; Echolocation; Eocene whale; Filter-feeder; Genetics & Heredity; india; marine mammals; neurons; nucleotide; OMP; sea; sequences; whales
Odontocetes and mysticetes are two extant suborders of cetaceans. It is reported that the former have no sense of olfaction, while the latter can smell in air. To explain the ecological reason why mysticetes still retain their sense of smell, two hypotheses have been proposed - the echolocation-priority hypothesis, which assumes that the acquisition of echolocation causes the reduction of the importance of olfaction, and the filter-feeder hypothesis, which assumes that olfactory ability is important for filter-feeders to locate their prey because clouds of plankton give off a peculiar odor. The olfactory marker protein (OMP) is almost exclusively expressed in vertebrate olfactory receptor neurons, and is considered to play important roles in olfactory systems. In this study, full-length open reading frames of OMP genes were identified in 6 cetacean species and we analyzed the nonsynonymous to synonymous substitution rate ratio based on the maximum likelihood method. The evolutionary changes of the selective pressures on OMP genes did fit better to the filter-feeder hypothesis than to the echolocation-priority hypothesis. In addition, no pseudogenization mutations are found in all five odontocetes OMP genes investigated in this study. It may suggest that OMP retains some function even in 'anosmic' odontocetes. (C) 2011 Elsevier B.V. All rights reserved.
Kishida T; Thewissen J G M
Gene
2012
2012-01
Journal Article or Conference Abstract Publication
<a href="http://doi.org/10.1016/j.gene.2011.11.013" target="_blank" rel="noreferrer noopener">10.1016/j.gene.2011.11.013</a>
New Applications For Constrained Ordination: Reconstructing Feeding Behaviors In Fossil Remingtonocetinae (cetacea: Mammalia)
Archaeocetes; components; Constrained ordination; Eocene; eocene cetaceans; evolution; Feeding; india; Mastication; morphology; odontoceti; Reconstruction; regression; suction; transition; whales
Cooper L N; Hieronymus T L; Vinyard C J; Bajpai S; Thewissen J G M
Experimental Approaches to Understanding Fossil Organisms: Lessons from the Living
2014
1905-07
Book Chapter
n/a
Intervertebral and Epiphyseal Fusion in the Postnatal Ontogeny of Cetaceans and Terrestrial Mammals
baleen; Cetacea; Evolutionary Biology; Zoology; India; skeleton; morphology; artiodactyls; Eocene; whales; locomotor evolution; body length; Epiphyseal; fusion; Intervertebral; Vertebra; vertebral osteology
In this paper we studied three related aspects of the ontogeny of the vertebral centrum of cetaceans and terrestrial mammals in an evolutionary context. We determined patterns of ontogenetic fusion of the vertebral epiphyses in bowhead whale (Balaena mysticetus) and beluga whale (Delphinapterus leucas), comparing those to terrestrial mammals and Eocene cetaceans. We found that epiphyseal fusion is initiated in the neck and the sacral region of terrestrial mammals, while in recent aquatic mammals epiphyseal fusion is initiated in the neck and caudal regions, suggesting locomotor pattern and environment affect fusion pattern. We also studied bony fusion of the sacrum and evaluated criteria used to homologize cetacean vertebrae with the fused sacrum of terrestrial mammals. We found that the initial ossification of the vertebral pedicles in the fetus may be a reliable indicator of sacral homology inmodern cetaceans. Finally, we also studied fusion of the centra of cervical vertebrae in B. mysticetus and found that it is not completed until after sexual maturity, and after 20 years of age.
Moran M M; Bajpai S; George J C; Suydam R; Usip S; Thewissen J G M
Journal of Mammalian Evolution
2015
2015-03
Journal Article or Conference Abstract Publication
<a href="http://doi.org/10.1007/s10914-014-9256-7" target="_blank" rel="noreferrer noopener">10.1007/s10914-014-9256-7</a>
The origin and early evolution of whales: macroevolution documented on the Indian Subcontinent
Cetacea; India; evolution; energetics; Life Sciences & Biomedicine - Other Topics; artiodactyls; Eocene; pakistan; whales; cetaceans; Eocene; cetartiodactyla; locomotor evolution; dolphins; middle; semiaquatic mammals; underwater hearing
The origin of whales (order Cetacea) from a four-footed land animal is one of the best understood examples of macroevolutionary change. This evolutionary transition has been substantially elucidated by fossil finds from the Indian subcontinent in the past decade and a half. Here, we review the first steps of whale evolution, i.e. the transition from a land mammal to obligate marine predators, documented by the Eocene cetacean families of the Indian subcontinent: Pakicetidae, Ambulocetidae, Remingtonocetidae, Protocetidae, and Basilosauridae, as well as their artiodactyl sister group, the Raoellidae. We also discuss the influence that the excellent fossil record has on the study of the evolution of organ systems, in particular the locomotor and hearing systems.
Bajpai S; Thewissen J G M; Sahni A
Journal of Biosciences
2009
2009-11
Journal Article or Conference Abstract Publication
<a href="http://doi.org/10.1007/s12038-009-0060-0" target="_blank" rel="noreferrer noopener">10.1007/s12038-009-0060-0</a>
CRANIAL ANATOMY OF MIDDLE EOCENE REMINGTONOCETUS (CETACEA, MAMMALIA) FROM KUTCH, INDIA
hearing; Paleontology; evolution; origin; whales; transition
The family Remingtonocetidae is a basal family of Eocene cetaceans only known from near shore marine environments of India and Pakistan. We describe a new skull for Remingtonocetus harudiensis which elucidates the anatomy and functional morphology of the head and provides new details on cranial cavity and nasopharyngeal region. We suggest that Remingtonocetus was an ambush predator that hunted from a perch on the ocean floor, and that hearing was its most important sense. We speculate that the greatly elongated rostrum is an adaptation for water retention because these are some of the earliest whales living in seawater.
Bajpai S; Thewissen J G M; Conley R W
Journal of Paleontology
2011
2011-07
Journal Article or Conference Abstract Publication
<a href="http://doi.org/10.1666/10-128.1" target="_blank" rel="noreferrer noopener">10.1666/10-128.1</a>
Allometric patterns of fetal head growth in mysticetes and odontocetes: Comparison of Balaena mysticetus and Stenella attenuata
Balaena mysticetus; bowhead whale; dolphins; Marine & Freshwater Biology; mechanism; pan-tropical spotted dolphin; prenatal growth; Stenella attenuata; whales; Zoology
Unlike other mammals, odontocetes and mysticetes have highly derived craniofacial bones. A growth process referred to as "telescoping" is partly responsible for this morphology. Here, we explore how changes in facial morphology during fetal growth relate to differences in telescoping between the adult odontocete Stenella attenuata and the mysticete Balaena mysticetus. We conclude that in both Stenella and Balaena head size increases allometrically. Similarly, odontocete nasal length and mysticete mouth size have strong positive allometry compared to total body length. However, the differences between odontocetes and mysticetes in telescoping are not directly associated with their fetal growth patterns. Our results suggest that cranial changes related to echolocation and feeding between odontocetes and mysticetes, respectively, begin during ontogeny before telescoping is initiated.
Armfield B A; George J C; Vinyard C J; Thewissen J G M
Marine Mammal Science
2011
2011-10
Journal Article or Conference Abstract Publication
<a href="http://doi.org/10.1111/j.1748-7692.2010.00445.x" target="_blank" rel="noreferrer noopener">10.1111/j.1748-7692.2010.00445.x</a>
NEW SKELETAL MATERIAL OF ANDREWSIPHIUS AND KUTCHICETUS, TWO EOCENE CETACEANS FROM INDIA
artiodactyls; gujarat; hearing; kachchh; locomotor evolution; mammalia; Paleontology; whales
The Eocene cetacean genera Andrewsiphius and Kutchicetus are systematically revised, their anatomy described, and their phylogenetic position analyzed. Each genus contains a single species, A. sloani and K. minimus, and both are known only from the middle Eocene of the Indian Subcontinent. Andrewsiphius and Kutchicetus differ in a number of respects, the most important dental difference being that P2, P3, p2, and p3 are double-rooted in Andrewsiphius and single-rooted in Kutchicetus. Lower molars are separated by diastemata in Kutchicetus, but not in Andrewsiphius. Postcranially, Andrewsiphius has caudal vertebrae that are far more robust than those of Kutchicetus. We propose the new clade Andrewsiphiinae for these two genera, based on their unique characters: the extremely slender jaw, fused mandibular symphysis, narrow palate and rostrum, and lower molars that have a low crown with three Cusps lined tip rostro-caudally. A phylogenetic analysis indicates that andrewsiphiines are either a subfamily of Remingtonocetidae or an independent branch on the Eocene cetacean lineage. Interpreting conservatively, we classify them as remingtonocetids. Andrewsiphiines have a long, robust, dorso-ventrally flattened tail and short limbs, Suggesting that they swam using dorsoventral undulation of the tail.
Thewissen J G M; Bajpai S
Journal of Paleontology
2009
2009-09
Journal Article
<a href="http://doi.org/10.1666/08-045.1" target="_blank" rel="noreferrer noopener">10.1666/08-045.1</a>
The early radiations of cetacea (Mammalia): Evolutionary pattern and developmental correlations
archaeocete; artiodactyls; development; Environmental Sciences & Ecology; evolution; Evolutionary Biology; feet; fossil record; India; locomotor evolution; marine mammal; middle eocene; origin; pakistan; Stenella attenuata; time; whales
The origin and early evolution of Cetacea (whales, dolphins, and porpoises) is one of the best examples of macroevolution as documented by fossils. Early whales are divided into six families that differ greatly in their habitats, which varied from land to freshwater, coastal waters, and fully marine. Early cetaceans lived in the Eocene (55-37 million years ago), and they show an enormous morphological diversity. Toward the end of the Eocene the modem cetacean body plan originated, and this body plan remained more or less the same in the subsequent evolution. It is possible that some aspects of this body plan are rooted in constraints that are dictated by cetacean embryologic development and controlled by genes that affect many organ systems at once. It may be possible to use a study of patterns of correlations among morphological traits to test hypotheses of developmental links among organ systems.
Thewissen J G M; Williams E M
Annual Review of Ecology and Systematics
2002
2002
Journal Article
<a href="http://doi.org/10.1146/annurev.ecolysis.33.020602.095426" target="_blank" rel="noreferrer noopener">10.1146/annurev.ecolysis.33.020602.095426</a>
Vestibular evidence for the evolution of aquatic behaviour in early cetaceans
artiodactyls; bony labyrinth; feet; hearing; inner-ear; locomotor evolution; model; origin; petrosal; Science & Technology - Other Topics; whales
Early cetaceans evolved from terrestrial quadrupeds to obligate swimmers, a change that is traditionally studied by functional analysis of the postcranial skeleton(1). Here we assess the evolution of cetacean locomotor behaviour from an independent perspective by looking at the semicircular canal system, one of the main sense organs involved in neural control of locomotion(2). Extant cetaceans are found to be unique in that their canal arc size, corrected for body mass, is approximately three times smaller than in other mammals. This reduces the sensitivity of the canal system, most plausibly to match the fast body rotations that characterize cetacean behaviour. Eocene fossils show that the new sensory regime, incompatible with terrestrial competence, developed quickly and early in cetacean evolution, as soon as the taxa are associated with marine environments. Dedicated agile swimming of cetaceans thus appeared to have originated as a rapid and fundamental shift in locomotion rather than as the gradual transition suggested by postcranial evidence. We hypothesize that the unparalleled modification of the semicircular canal system represented a key 'point of no return' event in early cetacean evolution, leading to full independence from life on land.
Spoor F; Bajpal S; Hussaim S T; Kumar K; Thewissen J G M
Nature
2002
2002-05
Journal Article
<a href="http://doi.org/10.1038/417163a" target="_blank" rel="noreferrer noopener">10.1038/417163a</a>
Cranial anatomy of Pakicetidae (Cetacea, Mammalia)
artiodactyls; eocene; evolution; hearing; origin; pakistan; Paleontology; whales
The skulls and isolated tympanics are described for the earliest whales, pakicetids, from the H-GSP Locality 62 in the Ganda Kas area in Northern Pakistan. Currently three pakicetid genera are known: Pakicetus, Ichthyolestes, and Nalacetus. Ichthyolestes is smaller than the two other genera. Nalacetus and Pakicetus are similar in size, but morphologically different. Pakicetids have a nasal opening at the tip of the rostrum. Their palate retains an incisive foramen. This study reveals three characters of the cranial anatomy useful for systematic analyses. In pakicetids the orbits are orientated dorsally, and there is no supraorbital shield. The dorsal orientation of the orbits is diagnostic for the family, and the lack of supraorbital shield distinguishes pakicetids, ambulocetids, and remingtonocetids from the other Eocene archaeocetes. The intertemporal region of the pakicetid skull is very narrow, a feature that also occurs in many other Eocene cetaceans. The tympanic, which is the most abundant cranial bone (more than 30 specimens) in the pakicetid collections from H-GSP Locality 62, can be used to distinguish the species of pakicetids. In Ichthyolestes, the tympanic bulla is of the same absolute size as in Pakicetus, hence relatively larger, and the tympanic bulla of Nalacetus is larger than either of these. Morphologically, the tympanic bullae differ between the genera, and on the basis of these morphologies it is possible to recognize a fourth species of pakicetid at this locality.
Nummela S; Hussain S T; Thewissen J G M
Journal of Vertebrate Paleontology
2006
2006-09
Journal Article
<a href="http://doi.org/10.1671/0272-4634(2006)26%5B746:caopcm%5D2.0.co;2" target="_blank" rel="noreferrer noopener">10.1671/0272-4634(2006)26%5B746:caopcm%5D2.0.co;2</a>
Thewissen et al. reply.
LETTERS to the editor; WHALES
Replying to: J. H. Geisler & J. M. Theodor 458, 10.1038/nature07776 (2009)The analysis of Geisler and Theodor confirms our main phylogenetic result, that raoellids are, or include, the sister group to cetaceans. Their study expands on our findings by inferring that hippopotamids are the sister group to the combined raoellid–cetacean clade, whereas our paper had explicitly stated that our data could not address the position of the extant artiodactyl families. [ABSTRACT FROM AUTHOR]
Thewissen J G M; Cooper Lisa Noelle; Clementz Mark T; Bajpai Sunil; Tiwari B N
Nature
2009
2009-03-19
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1038/nature07775" target="_blank" rel="noreferrer noopener">10.1038/nature07775</a>
Whales originated from aquatic artiodactyls in the Eocene epoch of India.
*Phylogeny; *Whales/anatomy & histology/classification/physiology; Animals; ARTIODACTYLA; BICUSPIDS; CETACEA; EOCENE stratigraphic geology; India; INDIA; MAMMALOGICAL research; Pakistan; Time Factors; UNGULATES; WHALES
Although the first ten million years of whale evolution are documented by a remarkable series of fossil skeletons, the link to the ancestor of cetaceans has been missing. It was known that whales are related to even-toed ungulates (artiodactyls), but until now no artiodactyls were morphologically close to early whales. Here we show that the Eocene south Asian raoellid artiodactyls are the sister group to whales. The raoellid Indohyus is similar to whales, and unlike other artiodactyls, in the structure of its ears and premolars, in the density of its limb bones and in the stable-oxygen-isotope composition of its teeth. We also show that a major dietary change occurred during the transition from artiodactyls to whales and that raoellids were aquatic waders. This indicates that aquatic life in this lineage occurred before the origin of the order Cetacea.
Thewissen J G M; Cooper Lisa Noelle; Clementz Mark T; Bajpai Sunil; Tiwari B N
Nature
2007
2007-12
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1038/nature06343" target="_blank" rel="noreferrer noopener">10.1038/nature06343</a>
Eocene evolution of whale hearing.
*Biological Evolution; *Fossils; Air; Animals; Ear/*anatomy & histology/*physiology; EVOLUTION (Biology); FOSSILS; HEARING; Hearing/*physiology; MAMMALS; Mammals/anatomy & histology/physiology; Phylogeny; SOUND; Water; WHALES; Whales/*anatomy & histology/*physiology
The origin of whales (order Cetacea) is one of the best-documented examples of macroevolutionary change in vertebrates. As the earliest whales became obligately marine, all of their organ systems adapted to the new environment. The fossil record indicates that this evolutionary transition took less than 15 million years, and that different organ systems followed different evolutionary trajectories. Here we document the evolutionary changes that took place in the sound transmission mechanism of the outer and middle ear in early whales. Sound transmission mechanisms change early on in whale evolution and pass through a stage (in pakicetids) in which hearing in both air and water is unsophisticated. This intermediate stage is soon abandoned and is replaced (in remingtonocetids and protocetids) by a sound transmission mechanism similar to that in modern toothed whales. The mechanism of these fossil whales lacks sophistication, and still retains some of the key elements that land mammals use to hear airborne sound.
Nummela Sirpa; Thewissen J G M; Bajpai Sunil; Hussain S Taseer; Kumar Kishor
Nature
2004
2004-08
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1038/nature02720" target="_blank" rel="noreferrer noopener">10.1038/nature02720</a>