Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Galindo, Demi; Sweet, Elly M.; DeLeon, Zoey; Wagner, Mitchel; DeLeon, Adrian; Carter, Casey; McMenamin, Sarah K.; Cooper, W. James

doi:10.1101/418483

Cited by 4 publications

(5 citation statements)

References 43 publications

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“…They found abnormal responses in those larvae to T3, and to a lesser degree to T4, resulting in the lower jaw lengthening and projecting beyond the upper jaw, when premetamorphic tadpoles were exposed to high concentration of the hormones. Danioninae fish similarly exhibit taxonomic diversity in protrusible jaws, which correlate with different feeding niches and can be experimentally altered by TH during development (Galindo et al, ). These authors noted that by altering the TH signal they could produce juvenile and adult zebrafish that resembled adults of other genera which normally had less jaw protrusion than the zebrafish.…”

Section: Discussionmentioning

confidence: 99%

Differences in responsiveness and sensitivity to exogenous disruptors of the thyroid gland in three anuran species

2019

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Anuran larval development comprises tissues/organs/systems that are: exclusively of larvae, able to be remodelled, and those of postmetamorphic stages. Also, the anuran larval development is characterized by inter‐related parameters: time, size and shape forming part of growth and differentiation. The anuran metamorphosis starts when growth and differentiation achieve a threshold that differs among species since it is regulated by a number of external (environmental) and internal (hormonal) processes. Here we explore the consequences of exogenous disruptors on the thyroid gland (e.g., methimazole and thyroxine as T4) of three species by immersing premetamorphic tadpoles in predetermined concentrations of the disruptors for short periods (10 or 16 days). The species were Pleurodema borellii, Leptodactylus chaquensis, and Dermatonotus muelleri, which all breed in small temporary ponds during the summer, but differ in their ecomorphology. The experiments were conducted to evaluate the effects of these substances on larval development (based in Gosner larval stages), morphometric variation in body parameters (snout‐vent and total length by larval stages), and thyroid gland histopathology at the end of the assays. In P. borelli and L. chaquensis, methimazole produces significant increment of size measurements (nonparametric Kruskal–Wallis, p < .05) during stages of digit differentiation and induced thyroid gland hypertrophy. In the three species, T4 exposure accelerated limb development and caused atrophy of thyroid gland. Prolonged T4 exposure in L. chaquensis and D. muelleri triggered metamorphic transformation in the gut and skull cartilages. Discussion about interspecific differences in responsiveness and sensitivity elucidates the importance of hormonal signals to morphological evolution.

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Section: Discussionmentioning

confidence: 99%

Differences in responsiveness and sensitivity to exogenous disruptors of the thyroid gland in three anuran species

2019

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“…Danionellas are Danionins relatively closely related to zebrafish (McCluskey and Postlethwait 2014). Members of this miniaturized group are developmentally arrested and resemble larval Danios in several ways: adult Danionellas lack scales, barbels and many typically late-ossifying bones (Britz, Conway et al 2009, Britz andConway 2016), and they retain a larva-like pigment pattern and feeding kinematics (McMenamin, Carter et al 2017, Galindo, Sweet et al 2018. Danionellas are emerging as a novel model for studying behavior, neurobiology and brain function (Penalva, Bedke et al 2018, Schulze, Henninger et al 2018, and a hybrid genome assembly was recently completed (Kadobianskyi, Schulze et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Mauri

Donahue

et al. 2019

Preprint

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BackgroundChanges in post-embryonic developmental trajectories can profoundly alter adult phenotypes and life history transitions. In vertebrate clades with complex, biphasic life cycles, thyroid hormone (TH) regulates metamorphosis, and alterations to TH metabolism underlie famous cases of paedomorphosis. We tested the requirement for TH in multiple post-embryonic developmental processes in the zebrafish, and asked if TH loss was associated with paedomorphosis in miniaturized Danionellas.ResultsWe found that TH regulates the relative growth of different body parts in zebrafish, inhibiting head growth at juvenile stages. The lateral line also showed sensitivity to the hormone: head neuromasts were inhibited by TH, while trunk neuromasts required TH for their proliferation. While several aspects of Danionella morphology resembled that of larval zebrafish, these species did not resemble hypothyroid zebrafish in their shape or lateral line, and these fish showed functional thyroid follicles.ConclusionsAlthough zebrafish do not undergo a discrete ecological transformation, we found that multiple tissues go through a protracted metamorphosis, and that TH ushers in growth patterns and processes typical of juveniles. We found no evidence that compromised TH metabolism is responsible for paedomorphosis in Danionellas. Nonetheless, modulations to TH-sensitive pathways affect evolutionarily-relevant traits, and are likely important targets for adaptation.Bullet PointsThyroid hormone regulates shifts in relative growth trajectories in different zebrafish tissuesThyroid hormone inhibits head growth in juvenile zebrafish, and regulates juvenile growth patternsThyroid hormone stimulates formation of neuromast canals in the head and ‘stitches’ on the trunk of zebrafishDanionella, the miniaturized sister group to Danio morphologically resemble larval zebrafish and do not form neuromast canalsHypothyroidism is not the cause of paedomorphosis in DanionellaGrant SponsorsNIH R00GM105874NIH R03HD091634Burroughs Wellcome Collaborative Research Travel Grant 1017439

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“…The skeletal changes seen in TH-modulated fish likely result in functional consequences. Indeed, TH is required for the onset of mature feeding behaviors, and the failure of elements such as the kinethmoid and premaxilla to properly ossify may help explain the lack of premaxillary protrusion in TH− adults (McMenamin et al, 2017;Galindo et al, 2018). In particular, the kinethmoid is a sesamoid bone and as such is dependent on proper functioning of upper jaw protrusion to properly ossify.…”

Section: Functional Consequencesmentioning

confidence: 99%

Anatomical Assessment of the Adult Skeleton of Zebrafish Reared Under Different Thyroid Hormone Profiles

Keer

Cohen

May

et al. 2019

The Anatomical Record

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Thyroid hormone (TH) directs the growth and maintenance of tissues throughout the body during development and into adulthood, and plays a particularly important role in proper ossification and homeostasis of the skeleton. To better understand the roles of TH in the skeletogenesis of a vertebrate model, and to define areas of the skeleton that are particularly sensitive to developmental TH, we examined the effects of hypo-and hyperthyroidism on skeletal development in zebrafish. Performing a bone-by-bone anatomical assessment on the entire skeleton of adult fish, we found that TH is required for proper ossification, growth, morphogenesis, and fusion of numerous bones. We showed that the pectoral girdle, dermatocranium, Weberian apparatus, and dentary are particularly sensitive to TH, and that TH affects development of skeletal element regardless of bone type and developmental origin. Indeed, the hormone does not universally promote ossification: we found that developmental TH prevents ectopic ossification in multiple thin bones and within connective tissue of the jaw. In all, we found that TH regulates proper morphogenesis and ossification in the majority of zebrafish bones, and that the requirement for the hormone extends across bone types and developmental profiles.

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Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Cited by 4 publications

References 43 publications

Differences in responsiveness and sensitivity to exogenous disruptors of the thyroid gland in three anuran species

Differences in responsiveness and sensitivity to exogenous disruptors of the thyroid gland in three anuran species

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Anatomical Assessment of the Adult Skeleton of Zebrafish Reared Under Different Thyroid Hormone Profiles

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