Caging, but not air deprivation, slows tadpole growth and development in the amphibian <i>Xenopus laevis</i>

Rose, Christopher

doi:10.1002/jez.1867

Cited by 8 publications

(13 citation statements)

References 60 publications

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“…The CH becomes a little less blocky in larval growth and shrinks into a shorter, much narrower cylindrical shape in metamorphosis. Under optimal growth conditions, these changes occur gradually over 5–6 weeks and 6–8 days for larval growth and metamorphosis respectively (Rose, ; Rose et al. ).…”

Section: Resultsmentioning

confidence: 99%

“…It is also important to consider that larval growth and developmental rates in lab‐raised Xenopus can be extremely variable (Rose, ) and that the durations of TH treatments in this study were determined by two factors beyond the experimenter's ability to control or predict, individual mortality and when the last surviving TH‐treated animal would developmentally arrest. Only in an arrested, but otherwise healthy animal can one assume that a tissue response has proceeded as far as the applied hormone can induce it at the given dose and stage.…”

Section: Resultsmentioning

confidence: 99%

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How thyroid hormones and their inhibitors affect cartilage growth and shape in the frogXenopus laevis

Rose

Cahill

2018

Journal of Anatomy

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Understanding how skeleton changes shape in ontogeny is fundamental to understanding how its shape diversifies in phylogeny. Amphibians pose a special case because their jaw and throat skeleton consists of cartilages that are dramatically reshaped midway through life to support new feeding and breathing styles. Although amphibian metamorphosis is commonly studied by immersing larvae in thyroid hormones (TH), how individual cartilages respond to TH is poorly understood. This study documents the effects of larval stage and TH type (T4 vs. T3), dose and deprivation on the size, shape and morphogenesis of the lower jaw and ceratohyal cartilages in the frog Xenopus laevis. It uses thyroid inhibitors to isolate the effects of each hormone at specific concentrations. It also deconstructs the TH responses into the effects on individual dimensions, and uses measures of percent change to eliminate the effects of body size and growth rate variation. As stage increases, T4 and T3 responses become increasingly similar to each other and to natural remodeling; the differences at low and intermediate stages result largely from abnormal responses to T3. Most notably, the beak-like lower jaw commonly observed at the lowest stage in other studies results largely from arrested growth of cartilage. TH responses are superimposed upon the growth typical for each stage so that cartilages can attain postmetamorphic shapes through dimensional changes that exceed those of natural metamorphosis. Using thyroid inhibitors alters the outcome of TH-induced remodeling, and T4 has almost the same capacity to induce metamorphic shape changes as T3. The results have implications for understanding how the starting shapes of larval elements affect morphogenesis, how chondrocytes behave to change cartilage shape, and how intracellular processing of TH might contribute to interspecific differences in shape change. Also, the data on animal mortality and which stages and doses most closely replicate natural remodeling have practical value for researchers who treat Xenopus tadpoles with TH.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

How thyroid hormones and their inhibitors affect cartilage growth and shape in the frogXenopus laevis

Rose

Cahill

2018

Journal of Anatomy

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“…Unlike the starting body size for tadpole growth, which is relatively uniform among individuals, the starting body size for metamorphosis can vary considerably as a result of variation in tadpole growth and developmental rates ( Fig. 3b; Wilbur & Collins, 1973;Rose, 2005Rose, , 2014. Additionally, as researchers might not appreciate the degree to which body size decreases in frog metamorphosis, they could unwittingly sample larger specimens at later metamorphic stages in an effort to obtain a series of similarly sized specimens.…”

Section: Anatomy and General Observationsmentioning

confidence: 99%

“…Size at the start of metamorphosis in lab-reared Xenopus laevis ranges from 0.70 g to more than 1.71 g (Rose, 2014), and the upper limit is likely greater in wild populations (Wager, 1986). Metamorphosis of the PA skeleton in amphibians involves complex, highly coordinated cellular processes that reshape, rearrange and/or rebuild jaw, hyoid and other elements to articulate with each other in new, precisely integrated feeding motions (Alberch & Gale, 1986;Rose & Reiss, 1993;Rose, 2009).…”

Section: The Developmental and Evolutionary Significance Of Isometricmentioning

confidence: 99%

Deconstructing cartilage shape and size into contributions from embryogenesis, metamorphosis, and tadpole and frog growth

2015

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Understanding skeletal diversification involves knowing not only how skeletal rudiments are shaped embryonically, but also how skeletal shape changes throughout life. The pharyngeal arch (PA) skeleton of metamorphosing amphibians persists largely as cartilage and undergoes two phases of development (embryogenesis and metamorphosis) and two phases of growth (larval and post-metamorphic). Though embryogenesis and metamorphosis produce species-specific features of PA cartilage shape, the extents to which shape and size change during growth and metamorphosis remain unaddressed. This study uses allometric equations and thin-plate spline, relative warp and elliptic Fourier analyses to describe shape and size trajectories for the ventral PA cartilages of the frog Xenopus laevis in tadpole and frog growth and metamorphosis. Cartilage sizes scale negatively with body size in both growth phases and cartilage shapes scale isometrically or close to it. This implies that most species-specific aspects of cartilage shape arise in embryogenesis and metamorphosis. Contributions from growth are limited to minor changes in lower jaw (LJ) curvature that produce relative gape narrowing and widening in tadpoles and frogs, respectively, and most cartilages becoming relatively thinner. Metamorphosis involves previously unreported decreases in cartilage size as well as changes in cartilage shape. The LJ becomes slightly longer, narrower and more curved, and the adult ceratohyal emerges from deep within the resorbing tadpole ceratohyal. This contrast in shape and size changes suggests a fundamental difference in the underlying cellular pathways. The observation that variation in PA cartilage shape decreases with tadpole growth supports the hypothesis that isometric growth is required for the metamorphic remodeling of PA cartilages. It also supports the existence of shape-regulating mechanisms that are specific to PA cartilages and that resist local adaptation and phenotypic plasticity.

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“…That amphibians have exceptionally variable growth and developmental rates could pose a problem in this regard. Rose (2014) lists more than twenty environmental factors that cause variation in one or both rates, and notes that Xenopus tadpoles at the start of metamorphosis exhibit more than a two-fold range in body size. The best way to guard against size-related variation in starting shapes is to stay close to isometric growth and to regulate shape as tightly as possible.…”

Section: G B C D E F Hmentioning

confidence: 99%

The importance of cartilage to amphibian development and evolution

Rose¹

2014

Int. J. Dev. Biol.

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The duality of amphibians is epitomized by their pharyngeal arch skeletons, the larval and adult morphologies of which enable very different feeding and breathing behaviors in aquatic and terrestrial life. To accomplish this duality, amphibian pharyngeal arch skeletons undergo two periods of patterning: embryogenesis and metamorphosis, and two periods of growth: larval and postmetamorphic. Their extreme ontogenetic variation, however, is coupled with relatively limited phylogenetic variation. I propose that amphibians face an evolutionary tradeoff between their ontogenetic and phylogenetic diversification that stems from the need to grow and transform the pharyngeal arch skeleton in cartilage rather than bone. Cartilage differs fundamentally from bone in its histology, function, development and growth. Cartilage is also the first skeletal tissue to form embryonically and provides more cellular pathways for shape change than bone. This article combines morphological, histological and experimental perspectives to explore how pharyngeal arch cartilage shape is controlled in amphibian embryogenesis, growth and metamorphosis, and how amphibian skeletal ontogenies are impacted by using cartilage to evolve a complex life cycle and in evolving away from a complex life cycle.

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Caging, but not air deprivation, slows tadpole growth and development in the amphibian Xenopus laevis

Cited by 8 publications

References 60 publications

How thyroid hormones and their inhibitors affect cartilage growth and shape in the frogXenopus laevis

How thyroid hormones and their inhibitors affect cartilage growth and shape in the frogXenopus laevis

Deconstructing cartilage shape and size into contributions from embryogenesis, metamorphosis, and tadpole and frog growth

The importance of cartilage to amphibian development and evolution

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