Review and experimental evaluation of the embryonic development and evolutionary history of flipper development and hyperphalangy in dolphins (Cetacea: Mammalia)

Cooper, Lisa Noelle; Sears, Karen E.; Armfield, Brooke A.; Kala, B; Hubler, Merla J.; Thewissen, J. G. M.

doi:10.1002/dvg.23076

Cited by 24 publications

(39 citation statements)

References 89 publications

(142 reference statements)

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“…A most illustrative example of this fact are the varieties in the pattern of interdigital cell death according to the pattern of digit webbing in species adapted to live in distinct habits. Thus, among the differences in humans, mice or chickens, interdigital cell death is absent or reduced in the developing bat wings (Weatherbee et al, 2006), in the developing flippers of aquatic mammalias (Cooper et al, 2018) and in the feet of swimming aquatic birds (Tokita et al, 2020). The discovery of "cell death genes" directly related to the physiological elimination of specific cells in the worm C. elegans (Ellis and Horvitz, 1986) and their evolutionary conservation in mammals (Peter et al, 1997) provided strong support for this idea.…”

Section: Introductionmentioning

confidence: 99%

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

Montero

Lorda‐Diez

Hurlé

2020

Front. Cell Dev. Biol.

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Digits develop in the distal part of the embryonic limb primordium as radial prechondrogenic condensations separated by undifferentiated mesoderm. In a short time interval the interdigital mesoderm undergoes massive degeneration to determine the formation of free digits. This fascinating process has often been considered as an altruistic cell suicide that is evolutionarily-regulated in species with different degrees of digit webbing. Initial descriptions of interdigit remodeling considered lysosomes as the primary cause of the degenerative process. However, the functional significance of lysosomes lost interest among researcher and was displaced to a secondary role because the introduction of the term apoptosis. Accumulating evidence in recent decades has revealed that, far from being a unique method of embryonic cell death, apoptosis is only one among several redundant dying mechanisms accounting for the elimination of tissues during embryonic development. Developmental cell senescence has emerged in the last decade as a primary factor implicated in interdigit remodeling. Our review proposes that cell senescence is the biological process identified by vital staining in embryonic models and implicates lysosomes in programmed cell death. We review major structural changes associated with interdigit remodeling that may be driven by cell senescence. Furthermore, the identification of cell senescence lacking tissue degeneration, associated with the maturation of the digit tendons at the same stages of interdigital remodeling, allowed us to distinguish between two functionally distinct types of embryonic cell senescence, "constructive" and "destructive."

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Section: Introductionmentioning

confidence: 99%

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

Montero

Lorda‐Diez

Hurlé

2020

Front. Cell Dev. Biol.

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“…The appearance of these repeated joint patterns in the fossil record marks the emergence of tetrapod limb morphology, exemplified in the polydactylous Acanthostega (Coates and Clack, 1990). In extant tetrapods, joint patterns show significant variation, ranging from the widely spaced joints enabling flight of the bat wing (Sears et al, 2006), to the hyperphalangeal flippers of whales and dolphins (Cooper et al, 2007(Cooper et al, , 2018.…”

Section: Introductionmentioning

confidence: 99%

A dot-stripe Turing model of joint patterning in the tetrapod limb

Cornwall-Scoones

Hiscock

2020

Development

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Iterative joints are a hallmark of the tetrapod limb, and their positioning is a key step during limb development. Although the molecular regulation of joint formation is well studied, it remains unclear what controls the location, number and orientation (i.e. the pattern) of joints within each digit. Here, we propose the dot-stripe mechanism for joint patterning, comprising two coupled Turing systems inspired by published gene expression patterns. Our model can explain normal joint morphology in wild-type limbs, hyperphalangy in cetacean flippers, mutant phenotypes with misoriented joints and suggests a reinterpretation of the polydactylous Ichthyosaur fins as a polygonal joint lattice. By formulating a generic dot-stripe model, describing joint patterns rather than molecular joint markers, we demonstrate that the insights from the model should apply regardless of the biological specifics of the underlying mechanism, thus providing a unifying framework to interrogate joint patterning in the tetrapod limb.

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“…Embryos of dolphins develop hyperphalangy in utero under the influence of extended FGFs and WNT signals (Cooper et al, 2018).…”

mentioning

confidence: 99%

“…These FGFs also coordinate with gremlin signals within the tissues between the digits to prevent apoptosis of these interdigital tissues and lay a foundation for the formation of a flipper (Cooper et al, 2018).…”

mentioning

confidence: 99%

Linking gene expression and phenotypic changes in the developmental and evolutionary origins of osteosclerosis in the ribs of bowhead whales (Balaena mysticetus)

et al. 2020

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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.

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Review and experimental evaluation of the embryonic development and evolutionary history of flipper development and hyperphalangy in dolphins (Cetacea: Mammalia)

Cited by 24 publications

References 89 publications

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

Confluence of Cellular Degradation Pathways During Interdigital Tissue Remodeling in Embryonic Tetrapods

A dot-stripe Turing model of joint patterning in the tetrapod limb

Linking gene expression and phenotypic changes in the developmental and evolutionary origins of osteosclerosis in the ribs of bowhead whales (Balaena mysticetus)

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