skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics
Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying the developmental factors that alter protrusion ability will improve our understanding of fish diversification. In the zebrafish protrusion arises postmetamorphosis. Fish metamorphosis typically includes significant changes in trophic morphology, accompanies a shift in feeding niche and coincides with increased thyroid hormone production. We tested whether thyroid hormone affects the development of zebrafish feeding mechanics. We found that it affected all developmental stages examined, but that effects were most pronounced after metamorphosis. Thyroid hormone levels affected the development of jaw morphology, feeding mechanics, shape variation, and cranial ossification. Adult zebrafish utilize protrusile jaws, but an absence of thyroid hormone impaired development of the premaxillary bone, which is critical to jaw protrusion. Premaxillae from early juvenile zebrafish and hypothyroid adult zebrafish resemble those from adults in the generaDanionella, Devario, andMicrodevariothat show little to no jaw protrusion. Our findings suggest that evolutionary changes in how the developing skulls of danionin minnows respond to thyroid hormone may have promoted diversification into different feeding niches.  more » « less
Award ID(s):
1755433
PAR ID:
10114013
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Evolution & Development
Volume:
21
Issue:
5
ISSN:
1520-541X
Page Range / eLocation ID:
p. 231-246
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Synopsis By linking anatomical structure to mechanical performance we can improve our understanding of how selection shapes morphology. Here we examined the functional morphology of feeding in fishes of the subfamily Danioninae (order Cypriniformes) to determine aspects of cranial evolution connected with their trophic diversification. The Danioninae comprise three major lineages and each employs a different feeding strategy. We gathered data on skull form and function from species in each clade, then assessed their evolutionary dynamics using phylogenetic-comparative methods. Differences between clades are strongly associated with differences in jaw protrusion. The paedomorphic Danionella clade does not use jaw protrusion at all, members of the Danio clade use jaw protrusion for suction production and prey capture, and members of the sister clade to Danio (e.g., Devario and Microdevario) use jaw protrusion to retain prey after capture. The shape of the premaxillary bone is a major determinant of protrusion ability, and premaxilla morphology in each of these lineages is consistent with their protrusion strategies. Premaxilla shapes have evolved rapidly, which indicates that they have been subjected to strong selection. We compared premaxilla development in giant danio (Devario aequipinnatus) and zebrafish (Danio rerio) and discuss a developmental mechanism that could shift danionine fishes between the feeding strategies employed by these species and their respective clades. We also identified a highly integrated evolutionary module that has been an important factor in the evolution of trophic mechanics within the Danioninae. 
    more » « less
  2. Abstract BackgroundDifferences in postembryonic developmental trajectories can profoundly alter adult phenotypes and life histories. Thyroid hormone (TH) regulates metamorphosis in many vertebrate taxa with multiphasic ecologies, and alterations to TH metabolism underlie notable cases of paedomorphosis in amphibians. We tested the requirement for TH in multiple postembryonic developmental processes in zebrafish, which has a monophasic ecology, and asked if TH production was compromised in paedomorphicDanionella. ResultsWe showed that TH regulates allometric growth in juvenile zebrafish, and inhibits relative head growth. The lateral line system showed differential requirements for TH: the hormone promotes canal neuromast formation and inhibits neuromast proliferation in the head, but causes expansion of the neuromast population in the trunk. WhileDanionellamorphology resembled that of larval zebrafish, the twoDanionellaspecies analyzed were not similar to hypothyroid zebrafish in their shape or neuromast distribution, and both possessed functional thyroid follicles. ConclusionsAlthough zebrafish do not undergo a discrete ecological transformation, we found that multiple tissues undergo transitions in developmental trajectories that are dependent on TH, suggesting the TH axis and its downstream pathways as likely targets for adaptation. Nonetheless, we found no evidence that evolutionary paedomorphosis inDanionellais the result of compromised TH production. 
    more » « less
  3. Abstract Changing the shape of craniofacial bones can profoundly alter ecological function, and understanding how developmental conditions sculpt skeletal phenotypes can provide insight into evolutionary adaptations. Thyroid hormone (TH) stimulates metamorphosis and regulates skeletal morphogenesis across vertebrates. To assess the roles of this hormone in sculpting the craniofacial skeleton of a non‐metamorphic vertebrate, we tested zebrafish for developmental periods of TH‐induced craniofacial shape change. We analyzed shapes of specific bones that function in prey detection, capture and processing. We quantified these elements from late‐larval through adult stages under three developmental TH profiles. Under wild‐type conditions, each bone progressively grows allometrically into a mature morphology over the course of postembryonic development. In three of the four bones, TH was required to sculpt an adult shape: hypothyroidism inhibited aspects of shape change, and allowed some components of immature shape to be retained into adulthood. Excess developmental TH stimulated aspects of precocious shape change leading to abnormal morphologies in some bones. Skeletal features with functional importance showed high sensitivities to TH, including the transformator process of the tripus, the mandibular symphysis of the lower jaw, the scutiform lamina of the hyomandibula, and the anterior arm of the pharyngeal jaw. In all, we found that TH is necessary for shaping mature morphology of several essential skeletal elements; this requirement is particularly pronounced during larval development. Altered TH titer leads to abnormal morphologies with likely functional consequences, highlighting the potential of TH and downstream pathways as targets for evolutionary change. 
    more » « less
  4. Zebrafish are a valuable model for normal vertebrate skeletogenesis and the study of myriad bone disorders. Bones grow, ossify and change shape throughout the zebrafish lifetime, and 3D technologies allow us to examine skeletogenic processes in detail through late developmental stages. To facilitate analysis of shape, orientation and tissue density of skeletal elements throughout ontogeny and adulthood, we generated a high-resolution skeletal reference dataset of wild-type zebrafish development. Using microCT technology, we produced 3D models of the skeletons of individuals ranging from 12 to 25 mm standard length (SL). We analyzed the dynamics of skeletal density and volume as they increase during juvenile and adult growth. Our resource allows anatomical comparisons between meristic units within an individual—e.g., we show that the vertebral canal width increases posteriorly along the spine. Further, structures may be compared between individuals at different body sizes: we highlight the shape changes that the lower jaw undergoes as fish mature from juvenile to adult. We show that even reproductively mature adult zebrafish (17–25 mm SL) continue to undergo substantial changes in skeletal morphology and composition with continued adult growth. We provide a segmented model of the adult skull and a series of interactive 3D PDFs at a range of key stages. These resources allow changes in the skeleton to be assessed quantitatively and qualitatively through late stages of development, and can serve as anatomical references for both research and education. 
    more » « less
  5. Amphibian metamorphosis represents a dramatic example of post-embryonic development. In the anuran Xenopus laevis frog, this process involves extensive changes to larval tissues, structures, and physiology to produce its adult form. As a long-standing model to study tissue remodeling, both amphibian metamorphosis and mammalian development are under the control of thyroid hormone. Successful remodeling though, also requires precise temporospatial regulation of immune activation. Yet there is much to learn about the immune components linked to metamorphosis. In turn, granulocytes are a class of innate immune cells recently touted for their participation in processes beyond classical immune defenses, including in pathological and non-pathological tissue remodeling. In this manuscript, we explore the roles of granulocytes in perhaps the most conspicuous anuran metamorphic event: tadpole tail reabsorption. We characterize granulocyte infiltration into the tail as metamorphosis progresses. Although some granulocyte subpopulations exist in both Xenopus and mammals, our previous work has identified additional Xenopus-specific populations. Thus, here we further explored subpopulation dynamics through distinct stages of natural metamorphosis, their likely roles during this process, and their relationship with thyroid hormone. As endocrine disruptors continue to threaten species across the animal kingdom, the work described here offers much-needed insight into immune contributions to endocrine-linked development. 
    more » « less