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      Neurovascular evidence for a co-occurrence of teeth and baleen in an Oligocene mysticete and the transition to filter-feeding in baleen whales

      1 , 2 , 2
      Zoological Journal of the Linnean Society
      Oxford University Press (OUP)

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          Abstract

          Extant baleen whales (Mysticeti) have a deciduous foetal dentition, but are edentulous at birth. Fossils reveal that the earliest mysticetes possessed an adult dentition. Aetiocetids, a diverse clade of Oligocene toothed mysticetes, have a series of small palatal foramina and associated sulci medial to the postcanine dentition. The openings have been homologized with lateral palatal foramina that transmit neurovascular structures to baleen in extant mysticetes, thereby implying a co-occurrence of teeth and baleen in aetiocetids. However, homology of the foramina and sulci have been questioned. Using CT-imaging, we report that the lateral palatal foramina of Aetiocetus weltoni are connected internally to the superior alveolar canal, which transmits neurovascular structures to baleen in extant mysticetes and to teeth in extant odontocetes. Furthermore, the lateral palatal foramina of Aetiocetus are separate from the more medially positioned canals for the greater palatine arterial system. These results provide critical evidence to support the hypothesis that the superior alveolar neurovasculature was co-opted in aetiocetids and later diverging mysticetes to serve a new function associated with baleen. We evaluate competing hypotheses for the transition from teeth to baleen, and explore the transition from raptorial feeding in early mysticetes to filter-feeding in extant species.

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          Baleen boom and bust: a synthesis of mysticete phylogeny, diversity and disparity

          A new, fully dated total-evidence phylogeny of baleen whales (Mysticeti) shows that evolutionary phases correlate strongly with Caenozoic modernization of the oceans and climates, implying a major role for bottom-up physical drivers. The phylogeny of 90 modern and dated fossil species suggests three major phases in baleen whale history: an early adaptive radiation (36–30 Ma), a shift towards bulk filter-feeding (30–23 Ma) and a climate-driven diversity loss around 3 Ma. Evolutionary rates and disparity were high following the origin of mysticetes around 38 Ma, coincident with global cooling, abrupt Southern Ocean eutrophication and the development of the Antarctic Circumpolar Current (ACC). Subsequently, evolutionary rates and disparity fell, becoming nearly constant after approximately 23 Ma as the ACC reached its full strength. By contrast, species diversity rose until 15 Ma and then remained stable, before dropping sharply with the onset of Northern Hemisphere glaciation. This decline coincided with the final establishment of modern mysticete gigantism and may be linked to glacially driven variability in the distribution of shallow habitats or an increased need for long-distance migration related to iron-mediated changes in glacial marine productivity.
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            Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales.

            The origin of baleen in mysticete whales represents a major transition in the phylogenetic history of Cetacea. This key specialization, a keratinous sieve that enables filter-feeding, permitted exploitation of a new ecological niche and heralded the evolution of modern baleen-bearing whales, the largest animals on Earth. To date, all formally described mysticete fossils conform to two types: toothed species from Oligocene-age rocks ( approximately 24 to 34 million years old) and toothless species that presumably utilized baleen to feed (Recent to approximately 30 million years old). Here, we show that several Oligocene toothed mysticetes have nutrient foramina and associated sulci on the lateral portions of their palates, homologous structures in extant mysticetes house vessels that nourish baleen. The simultaneous occurrence of teeth and nutrient foramina implies that both teeth and baleen were present in these early mysticetes. Phylogenetic analyses of a supermatrix that includes extinct taxa and new data for 11 nuclear genes consistently resolve relationships at the base of Mysticeti. The combined data set of 27,340 characters supports a stepwise transition from a toothed ancestor, to a mosaic intermediate with both teeth and baleen, to modern baleen whales that lack an adult dentition but retain developmental and genetic evidence of their ancestral toothed heritage. Comparative sequence data for ENAM (enamelin) and AMBN (ameloblastin) indicate that enamel-specific loci are present in Mysticeti but have degraded to pseudogenes in this group. The dramatic transformation in mysticete feeding anatomy documents an apparently rare, stepwise mode of evolution in which a composite phenotype bridged the gap between primitive and derived morphologies; a combination of fossil and molecular evidence provides a multifaceted record of this macroevolutionary pattern.
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              Development and evolutionary origin of feathers.

              Avian feathers are a complex evolutionary novelty characterized by structural diversity and hierarchical development. Here, I propose a functionally neutral model of the origin and evolutionary diversification of bird feathers based on the hierarchical details of feather development. I propose that feathers originated with the evolution of the first feather follicle-a cylindrical epidermal invagination around the base of a dermal papilla. A transition series of follicle and feather morphologies is hypothesized to have evolved through a series of stages of increasing complexity in follicle structure and follicular developmental mechanisms. Follicular evolution proceeded with the origin of the undifferentiated collar (stage I), barb ridges (stage II), helical displacement of barb ridges, barbule plates, and the new barb locus (stage III), differentiation of pennulae of distal and proximal barbules (stage IV), and diversification of barbule structure and the new barb locus position (stage V). The model predicts that the first feather was an undifferentiated cylinder (stage I), which was followed by a tuft of unbranched barbs (stage II). Subsequently, with the origin of the rachis and barbules, the bipinnate feather evolved (stage III), followed then by the pennaceous feather with a closed vane (stage IV) and other structural diversity (stages Va-f). The model is used to evaluate the developmental plausibility of proposed functional theories of the origin of feathers. Early feathers (stages I, II) could have functioned in communication, defense, thermal insulation, or water repellency. Feathers could not have had an aerodynamic function until after bipinnate, closed pennaceous feathers (stage IV) had evolved. The morphology of the integumental structures of the coelurisaurian theropod dinosaurs Sinosauropteryx and Beipiaosaurus are congruent with the model's predictions of the form of early feathers (stage I or II). Additional research is required to examine whether these fossil integumental structures developed from follicles and are homologous with avian feathers. J. Exp. Zool. (Mol. Dev. Evol.) 285:291-306, 1999. Copyright 1999 Wiley-Liss, Inc.
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                Author and article information

                Journal
                Zoological Journal of the Linnean Society
                Oxford University Press (OUP)
                0024-4082
                1096-3642
                May 24 2021
                May 24 2021
                Affiliations
                [1 ]Department of Biology, San Diego State University, Campanile Drive, San Diego, CA  USA
                [2 ]Department of Paleontology, San Diego Natural History Museum, El Prado, San Diego, CA, USA
                Article
                10.1093/zoolinnean/zlab017
                7c12f08f-0c86-4338-9926-65ebe37f626e
                © 2021

                http://creativecommons.org/licenses/by-nc/4.0/

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