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Rediscovering the Axolotl As a Model for Thyroid Hormone Dependent Development Anne Crowner University of Kentucky, [email protected]

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Rediscovering the Axolotl As a Model for Thyroid Hormone Dependent Development Anne Crowner University of Kentucky, Anne.Crowner@Uky.Edu University of Kentucky UKnowledge Neuroscience Faculty Publications Neuroscience 4-12-2019 Rediscovering the Axolotl as a Model for Thyroid Hormone Dependent Development Anne Crowner University of Kentucky, [email protected] Shivam Khatri University of Kentucky, [email protected] Dana Blichmann University of Kentucky, [email protected] S. Randal Voss University of Kentucky, [email protected] Right click to open a feedback form in a new tab to let us know how this document benefits oy u. Follow this and additional works at: https://uknowledge.uky.edu/neurobio_facpub Part of the Anatomy Commons, Comparative and Evolutionary Physiology Commons, Endocrinology Commons, Genetics and Genomics Commons, and the Neuroscience and Neurobiology Commons Repository Citation Crowner, Anne; Khatri, Shivam; Blichmann, Dana; and Voss, S. Randal, "Rediscovering the Axolotl as a Model for Thyroid Hormone Dependent Development" (2019). Neuroscience Faculty Publications. 60. https://uknowledge.uky.edu/neurobio_facpub/60 This Article is brought to you for free and open access by the Neuroscience at UKnowledge. It has been accepted for inclusion in Neuroscience Faculty Publications by an authorized administrator of UKnowledge. For more information, please contact [email protected]. Rediscovering the Axolotl as a Model for Thyroid Hormone Dependent Development Notes/Citation Information Published in Frontiers in Endocrinology, v. 10, 237, p. 1-6. © 2019 Crowner, Khatri, Blichmann and Voss. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Digital Object Identifier (DOI) https://doi.org/10.3389/fendo.2019.00237 This article is available at UKnowledge: https://uknowledge.uky.edu/neurobio_facpub/60 PERSPECTIVE published: 12 April 2019 doi: 10.3389/fendo.2019.00237 Rediscovering the Axolotl as a Model for Thyroid Hormone Dependent Development Anne Crowner, Shivam Khatri, Dana Blichmann and S. Randal Voss* Department of Neuroscience, Spinal Cord and Brain Injury Research Center, and Ambystoma Genetic Stock Center, University of Kentucky, Lexington, KY, United States The Mexican axolotl (Ambystoma mexicanum) is an important model organism in biomedical research. Much current attention is focused on the axolotl’s amazing ability to regenerate tissues and whole organs after injury. However, not forgotten is the axolotl’s equally amazing ability to thwart aspects of tissue maturation and retain juvenile morphology into the adult phase of life. Unlike close tiger salamander relatives that undergo a thyroid hormone regulated metamorphosis, the axolotl does not typically undergo a metamorphosis. Instead, the axolotl exhibits a paedomorphic mode of development that enables a completely aquatic life cycle. The evolution of paedomorphosis allowed axolotls to exploit relatively permanent habitats in Mexico, Edited by: and preadapted axolotls for domestication and laboratory study. In this perspective, Marco António Campinho, we first introduce the axolotl and the various meanings of paedomorphosis, and then Centro de Ciências do Mar (CCMAR), stress the need to move beyond endocrinology-guided approaches to understand the Portugal axolotl’s hypothyroid state. With the recent completion of the axolotl genome assembly Reviewed by: Veerle M. Darras, and established methods to manipulate gene functions, the axolotl is poised to provide KU Leuven, Belgium new insights about paedomorphosis and the role of thyroid hormone in development Paul Webb, California Institute for Regenerative and evolution. Medicine, United States Keywords: axolotl, paedomorphosis, metamorphosis, thyroid hormone, ambystoma *Correspondence: S. Randal Voss [email protected] INTRODUCTION Specialty section: Mexican axolotls (Ambystoma mexicanum) have been studied in laboratories throughout the world This article was submitted to for over two-hundred years (1). Beginning in the early nineteenth century, French expeditions to Thyroid Endocrinology, Mexico brought preserved adult specimens back to Paris for examination by curators at the Jardin a section of the journal des Plantes. Esteemed zoologist Georges Cuvier originally classified these specimens as larvae of an Frontiers in Endocrinology unknown species (2). It was not until decades later, when living axolotls were brought to Paris and Received: 20 January 2019 a laboratory population was established by Auguste Duméril, that these presumptive larval forms Accepted: 25 March 2019 were found to be reproductively mature and capable of metamorphosis. From the same axolotl Published: 12 April 2019 spawn, Duméril (3) observed that most sibs reached an adult state and some reproduced while Citation: retaining larval characteristics including external gills, while a few individuals metamorphosed Crowner A, Khatri S, Blichmann D and into forms typical of terrestrial salamanders (4). The observation of both metamorphic and non- Voss SR (2019) Rediscovering the Axolotl as a Model for Thyroid metamorphic forms arising from a single spawn inspired theories and experiments to explain the Hormone Dependent Development. axolotl’s unusual mode of paedomorphic development (5). While much has been learned from Front. Endocrinol. 10:237. studies of the axolotl and other salamanders, the mechanistic basis of paedomorphosis remains doi: 10.3389/fendo.2019.00237 largely unknown. Frontiers in Endocrinology | www.frontiersin.org 1 April 2019 | Volume 10 | Article 237 Crowner et al. Axolotl and Thyroid Hormone Paedomorphosis non-adaptive variation in the expression of paedomorphosis Paedomorphosis is a somewhat confusing term because it is known (9). The mechanisms that allow for such plasticity has been used to explain variation at evolutionary, ecological, are presumably influenced by an individual’s genetic makeup, and genetic levels of inquiry. At an evolutionary level, health status, and environmental cues. For example, studies paedomorphosis is used to describe a specific pattern of of salamanders that express paedomorphosis facultatively have developmental variation among ancestral and descendant species shown clear ecological correlates. Paedomorphosis is more (6). The ancestral mode of development in salamanders is frequent in permanent aquatic habitats that do not undergo generally thought to include a single, obligate metamorphosis seasonal drying (10, 11). It has been argued that ecological which partitions the life cycle between an early aquatic phase conditions largely dictate the expression of metamorphosis and a more terrestrial adult phase. Indeed, close tiger salamander or paedomorphosis in facultative species to increase fitness- (A. tigrinum) relatives of the axolotl are known to invariably associated traits, such as body size (bigger is generally better) undergo a metamorphosis (Figure 1). In contrast, the axolotl and the probability of earlier and more frequent reproduction typically does not undergo a metamorphosis; axolotls are (12). It is important to point out that genetics also plays a paedomorphic because they express ancestral juvenile traits role. Evidence for a population genetic component of variation in the adult stage of life. Paedomorphosis thus provides an has been shown in experiments that altered the heritability of evolutionary explanation for how new patterns of variation paedomorphosis in A. talpoideum over several generations of arise among species; the biphasic life cycle of an ancestral selection (10). However, such studies do not provide resolution of species was truncated somehow during evolution to yield a genetic factors that regulate the expression of paedomorphosis. paedomorphic species. Within the lexicon of heterochrony, a Paedomorphosis has also been used to describe developmental theory that associates changes in developmental timing to the variation among siblings within genetic crosses. Taking origin of new forms, Gould (6) proposed that paedomorphic advantage of the recent evolution of paedomorphosis among salamanders arose during evolution as a result of changes in tiger salamander complex species, interspecific genetic crosses mechanisms that regulate metamorphic timing. While such have been performed in the laboratory to segregate metamorphic description is useful for describing evolutionary patterns of and paedomorphic modes of development and map the genomic developmental variation, what we ultimately seek is proximate- location of genetic factors (13–18). These crosses have identified level understanding of timing mechanisms that regulate the major effect quantitative trait loci (QTL) that regulate the expression of paedomorphosis. timing of metamorphosis and expression of paedomorphosis. In ecological studies, paedomorphosis is used to describe For example, second generation backcross individuals of A. patterns of developmental variation among individuals within mexicanum x A. tigrinum hybrid crosses that inherit axolotl species and populations. At this level, paedomorphosis is thought alleles at the met1 QTL delay metamorphosis or express to be an adaptive developmental strategy for exploiting favorable paedomorphosis. It is not clear if genetic factors identified from larval habitats for growth and reproduction
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