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1.
Dev Biol ; 2024 Jul 17.
Article in English | MEDLINE | ID: mdl-39029570

ABSTRACT

Regenerating tissues must remember or interpret their spatial position, using this information to restore original size and patterning. The external skeleton of the zebrafish caudal fin is composed of 18 rays; after any portion of the fin is amputated, position-dependent regenerative growth restores each ray to its original length. We tested for transcriptional differences during regeneration of proximal versus distal tissues and identified 489 genes that differed in proximodistal expression. Thyroid hormone directs multiple aspects of ray patterning along the proximodistal axis, and we identified 364 transcripts showing a proximodistal expression pattern that was dependent on thyroid hormone context. To test what aspects of ray positional identity are directed by extrinsic cues versus remembered identity autonomous to the tissue itself, we transplanted distal portions of rays to proximal environments and evaluated regeneration within the new location. While neighboring proximal tissue showed robust expression of scpp7, a transcript with thyroid-regulated proximal enrichment, regenerating rays originating from transplanted distal tissue showed reduced (distal-like) expression during outgrowth. These distal-to-proximal transplants regenerated far beyond the length of the graft itself, indicating that cues from the proximal environment promoted additional growth. Nonetheless, these transplants initially regenerated at a much slower rate compared to controls, suggesting memory of distal identity was retained by the transplanted tissue. This early growth retardation caused rays that originated from transplants to become noticeably shorter than their native neighboring rays. While several aspects of fin ray morphology (bifurcation, segment length) were found to be determined by the environment, regeneration speed and ray length are remembered autonomously by tissues, persisting across multiple rounds of amputation and regeneration.

2.
bioRxiv ; 2024 Apr 27.
Article in English | MEDLINE | ID: mdl-38712299

ABSTRACT

Recent adaptive radiations provide evolutionary case studies, which provide the context to parse the relationship between genomic variation and the origins of distinct phenotypes. Sympatric radiations of the charr complex (genus Salvelinus) present a trove for phylogenetics as charrs have repeatedly diversified into multiple morphs with distinct feeding specializations. However, species flocks normally comprise only two to three lineages. Dolly Varden charr inhabiting Lake Kronotske represent the most extensive radiation described for the charr genus, containing at least seven lineages, each with defining morphological and ecological traits. Here, we perform the first genome-wide analysis of this species flock to parse the foundations of adaptive change. Our data support distinct, reproductively isolated lineages with little evidence of hybridization. We also find that specific selection on thyroid signaling and craniofacial genes forms a genomic basis for the radiation. Thyroid hormone is further implicated in subsequent lineage partitioning events. These results delineate a clear genetic basis for the diversification of specialized lineages, and highlight the role of developmental mechanisms in shaping the forms generated during adaptive radiation.

3.
bioRxiv ; 2024 Jul 11.
Article in English | MEDLINE | ID: mdl-38585773

ABSTRACT

Regenerating tissues must remember or interpret their spatial position, using this information to restore original size and patterning. The external skeleton of the zebrafish caudal fin is composed of 18 rays; after any portion of the fin is amputated, position-dependent regenerative growth restores each ray to its original length. We tested for transcriptional differences during regeneration of proximal versus distal tissues and identified 489 genes that differed in proximodistal expression. Thyroid hormone directs multiple aspects of ray patterning along the proximodistal axis, and we identified 364 transcripts showing a proximodistal expression pattern that was dependent on thyroid hormone context. To test what aspects of ray positional identity are directed by extrinsic cues versus remembered identity autonomous to the tissue itself, we transplanted distal portions of rays to proximal environments and evaluated regeneration within the new location. While neighboring proximal tissue showed robust expression of scpp7 , a transcript with thyroid-regulated proximal enrichment, regenerating rays originating from transplanted distal tissue showed reduced (distal-like) expression during outgrowth. These distal-to-proximal transplants regenerated far beyond the length of the graft itself, indicating that cues from the proximal environment promoted additional growth. Nonetheless, these transplants initially regenerated at a much slower rate compared to controls, suggesting memory of distal identity was retained by the transplanted tissue. This early growth retardation caused rays that originated from transplants to become noticeably shorter than their native neighboring rays. While several aspects of fin ray morphology (bifurcation, segment length) were found to be determined by the environment, regeneration speed and ray length are remembered autonomously by tissues, persisting across multiple rounds of amputation and regeneration.

4.
bioRxiv ; 2023 Aug 10.
Article in English | MEDLINE | ID: mdl-37609193

ABSTRACT

The model zebrafish ( Danio rerio ) belongs to the Danioninae subfamily with a range of informative phenotypes. However, the craniofacial diversity across the subfamily is not fully described. To better understand craniofacial phenotypes across Danioninae we used microCT and 3D geometric morphometrics to capture skull shapes from nine species. The Danio species examined showed largely similar skull shapes, although D. aesculapii , the sister species to D. rerio showed a unique morphology. Two non- Danio species examined, Chela dadiburjori and Devario aequipinnatus showed distinct skull morphologies unique from those of other species examined. Thyroid hormone regulates skeletal development and remodeling, and we asked if changes in developmental thyroid hormone metabolism could underlie some of the craniofacial diversity across Danioninae. We reared two Danio species under altered thyroid profiles, finding that hypothyroid individuals from both species showed corresponding morphological shifts in skull shape. Hypothyroid Danios showed skull morphologies closer to that of Chela and unlike any of the examined wild-type Danio species. We provide an examination of the evolved craniofacial diversity across Danioninae, and demonstrate that alterations to thyroid hormone have the capacity to create unique skull phenotypes.

5.
Proc Natl Acad Sci U S A ; 120(21): e2219770120, 2023 05 23.
Article in English | MEDLINE | ID: mdl-37186843

ABSTRACT

Processes that regulate size and patterning along an axis must be highly integrated to generate robust shapes; relative changes in these processes underlie both congenital disease and evolutionary change. Fin length mutants in zebrafish have provided considerable insight into the pathways regulating fin size, yet signals underlying patterning have remained less clear. The bony rays of the fins possess distinct patterning along the proximodistal axis, reflected in the location of ray bifurcations and the lengths of ray segments, which show progressive shortening along the axis. Here, we show that thyroid hormone (TH) regulates aspects of proximodistal patterning of the caudal fin rays, regardless of fin size. TH promotes distal gene expression patterns, coordinating ray bifurcations and segment shortening with skeletal outgrowth along the proximodistal axis. This distalizing role for TH is conserved between development and regeneration, in all fins (paired and medial), and between Danio species as well as distantly related medaka. During regenerative outgrowth, TH acutely induces Shh-mediated skeletal bifurcation. Zebrafish have multiple nuclear TH receptors, and we found that unliganded Thrab-but not Thraa or Thrb-inhibits the formation of distal features. Broadly, these results demonstrate that proximodistal morphology is regulated independently from size-instructive signals. Modulating proximodistal patterning relative to size-either through changes to TH metabolism or other hormone-independent pathways-can shift skeletal patterning in ways that recapitulate aspects of fin ray diversity found in nature.


Subject(s)
Zebrafish Proteins , Zebrafish , Animals , Zebrafish/physiology , Zebrafish Proteins/genetics , Zebrafish Proteins/metabolism , Thyroid Hormones/genetics , Animal Fins/physiology , Regeneration/physiology
6.
Front Physiol ; 13: 875866, 2022.
Article in English | MEDLINE | ID: mdl-35721557

ABSTRACT

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.

7.
Evol Dev ; 24(1-2): 61-76, 2022 03.
Article in English | MEDLINE | ID: mdl-35334153

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.


Subject(s)
Thyroid Hormones , Zebrafish , Animals , Bone and Bones , Jaw/physiology , Larva/metabolism , Thyroid Hormones/metabolism
8.
Elife ; 92020 01 29.
Article in English | MEDLINE | ID: mdl-31995030

ABSTRACT

The vertebral column or spine assembles around the notochord rod which contains a core made of large vacuolated cells. Each vacuolated cell possesses a single fluid-filled vacuole, and loss or fragmentation of these vacuoles in zebrafish leads to spine kinking. Here, we identified a mutation in the kinase gene dstyk that causes fragmentation of notochord vacuoles and a severe congenital scoliosis-like phenotype in zebrafish. Live imaging revealed that Dstyk regulates fusion of membranes with the vacuole. We find that localized disruption of notochord vacuoles causes vertebral malformation and curving of the spine axis at those sites. Accordingly, in dstyk mutants the spine curves increasingly over time as vertebral bone formation compresses the notochord asymmetrically, causing vertebral malformations and kinking of the axis. Together, our data show that notochord vacuoles function as a hydrostatic scaffold that guides symmetrical growth of vertebrae and spine formation.


Subject(s)
Notochord/metabolism , Spine/growth & development , Vacuoles/metabolism , Zebrafish/embryology , Animals , Gene Expression Regulation, Developmental , Mutation , Receptor-Interacting Protein Serine-Threonine Kinases/genetics , Zebrafish Proteins/genetics
9.
Evol Dev ; 21(5): 231-246, 2019 09.
Article in English | MEDLINE | ID: mdl-31374588

ABSTRACT

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 genera Danionella, Devario, and Microdevario that 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.


Subject(s)
Jaw/physiology , Thyroid Hormones/metabolism , Zebrafish/physiology , Animals , Biological Evolution , Biomechanical Phenomena , Feeding Behavior , Maxillofacial Development/physiology , Zebrafish/growth & development
10.
Dev Dyn ; 248(11): 1144-1154, 2019 11.
Article in English | MEDLINE | ID: mdl-31228301

ABSTRACT

BACKGROUND: Differences 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 paedomorphic Danionella. RESULTS: We 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. While Danionella morphology resembled that of larval zebrafish, the two Danionella species analyzed were not similar to hypothyroid zebrafish in their shape or neuromast distribution, and both possessed functional thyroid follicles. CONCLUSIONS: Although 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 in Danionella is the result of compromised TH production.


Subject(s)
Lateral Line System/embryology , Thyroid Gland/embryology , Thyroid Hormones/metabolism , Zebrafish/embryology , Animals
11.
Anat Rec (Hoboken) ; 302(10): 1754-1769, 2019 10.
Article in English | MEDLINE | ID: mdl-30989809

ABSTRACT

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. Anat Rec, 302:1754-1769, 2019. © 2019 American Association for Anatomy.


Subject(s)
Osteogenesis/physiology , Skeleton/growth & development , Thyroid Hormones/metabolism , Zebrafish/growth & development , Animals , Animals, Genetically Modified , Models, Animal , Thyroid Hormones/genetics
13.
Zebrafish ; 14(6): 517-525, 2017 12.
Article in English | MEDLINE | ID: mdl-28933679

ABSTRACT

The physical demands for swimming and feeding change dramatically over the course of development for many aquatic animals. Indeed, in teleosts, the transition from larva to adult involves major shifts in both trophic morphology and feeding behavior. A spike in thyroid hormone (TH) coordinates many developmental processes that occur during this adult transition in numerous vertebrate species. Using mutant and transgenic zebrafish, we tested the hypothesis that TH is essential for the transition from larval to adult feeding kinematic profiles. We found that every measured kinematic variable that distinguished larvae from adults also differentiated hypothyroid from wild-type (WT) euthyroid adults, suggesting that TH is indeed necessary for the onset of mature feeding behaviors. In contrast, feeding kinematics in hyperthyroid adults were extremely similar to those measured in euthyroid adults. Altered TH signaling underlies pedomorphosis in some amphibian species, and Danionella is a pedomorphic danionin genus. We therefore tested whether feeding kinematics of adult Danionella would more closely match larval zebrafish (and hypothyroid adults) than WT adult zebrafish. We found Danionella feeding kinematics resemble those of larval (and hypothyroid) zebrafish in multiple respects. Overall, we conclude that TH is essential in stimulating the onset of adult feeding kinematics in zebrafish, and that some of the underlying developmental pathways may have been lost in Danionella.


Subject(s)
Feeding Behavior , Thyroid Hormones/metabolism , Zebrafish/physiology , Animals , Animals, Genetically Modified , Biomechanical Phenomena , Feeding Behavior/drug effects , Larva/metabolism , Signal Transduction/drug effects , Zebrafish/growth & development
14.
Elife ; 62017 09 08.
Article in English | MEDLINE | ID: mdl-28884682

ABSTRACT

Phenomics, which ideally involves in-depth phenotyping at the whole-organism scale, may enhance our functional understanding of genetic variation. Here, we demonstrate methods to profile hundreds of phenotypic measures comprised of morphological and densitometric traits at a large number of sites within the axial skeleton of adult zebrafish. We show the potential for vertebral patterns to confer heightened sensitivity, with similar specificity, in discriminating mutant populations compared to analyzing individual vertebrae in isolation. We identify phenotypes associated with human brittle bone disease and thyroid stimulating hormone receptor hyperactivity. Finally, we develop allometric models and show their potential to aid in the discrimination of mutant phenotypes masked by alterations in growth. Our studies demonstrate virtues of deep phenotyping in a spatially distributed organ system. Analyzing phenotypic patterns may increase productivity in genetic screens, and facilitate the study of genetic variants associated with smaller effect sizes, such as those that underlie complex diseases.


Subject(s)
Biological Variation, Population , Skeleton/anatomy & histology , Skeleton/diagnostic imaging , X-Ray Microtomography/methods , Zebrafish/anatomy & histology , Animals , Humans , Sensitivity and Specificity
15.
Science ; 345(6202): 1358-61, 2014 Sep 12.
Article in English | MEDLINE | ID: mdl-25170046

ABSTRACT

Pigment patterns are useful for elucidating fundamental mechanisms of pattern formation and how these mechanisms evolve. In zebrafish, several pigment cell classes interact to generate stripes, yet the developmental requirements and origins of these cells remain poorly understood. Using zebrafish and a related species, we identified roles for thyroid hormone (TH) in pigment cell development and patterning, and in postembryonic development more generally. We show that adult pigment cells arise from distinct lineages having distinct requirements for TH and that differential TH dependence can evolve within lineages. Our findings demonstrate critical functions for TH in determining pigment pattern phenotype and highlight the potential for evolutionary diversification at the intersection of developmental and endocrine mechanisms.


Subject(s)
Body Patterning , Cell Differentiation , Cell Lineage , Melanophores/physiology , Skin Pigmentation/physiology , Thyroid Hormones/physiology , Zebrafish/embryology , Animals , Embryo, Nonmammalian/cytology , Melanophores/cytology , Melanophores/drug effects , Skin Pigmentation/genetics , Thyroid Hormones/genetics , Thyroid Hormones/pharmacology
16.
Endocrinology ; 154(4): 1476-87, 2013 Apr.
Article in English | MEDLINE | ID: mdl-23456361

ABSTRACT

Somatic growth and adipogenesis are closely associated with the development of obesity in humans. In this study, we identify a zebrafish mutant, vizzini, that exhibits both a severe defect in somatic growth and increased accumulation of adipose tissue. Positional cloning of vizzini revealed a premature stop codon in gh1. Although the effects of GH are largely through igfs in mammals, we found no decrease in the expression of igf transcripts in gh1 mutants during larval development. As development progressed, however, we found overall growth to be progressively retarded and the attainment of specific developmental stages to occur at abnormally small body sizes relative to wild type. Moreover, both subcutaneous (sc) and visceral adipose tissues underwent precocious development in vizzini mutants, and at maturity, the sizes of different fat deposits were greatly expanded relative to wild type. In vivo confocal imaging of sc adipose tissue (SAT) expansion revealed that vizzini mutants exhibit extreme enlargement of adipocyte lipid droplets without a corresponding increase in lipid droplet number. These findings suggest that GH1 signaling restricts SAT hypertrophy in zebrafish. Finally, nutrient deprivation of vizzini mutants revealed that SAT mobilization was greatly diminished during caloric restriction, further implicating GH1 signaling in adipose tissue homeostasis. Overall, the zebrafish gh1 mutant, vizzini, exhibits decreased somatic growth, increased adipose tissue accumulation, and disrupted adipose plasticity after nutrient deprivation and represents a novel model to investigate the in vivo dynamics of vertebrate obesity.


Subject(s)
Adipocytes/pathology , Adipogenesis/genetics , Adiposity/genetics , Dwarfism/genetics , Growth Hormone/genetics , Obesity/genetics , Zebrafish/genetics , Animals , Codon, Nonsense , Hypertrophy
17.
Curr Top Dev Biol ; 103: 127-65, 2013.
Article in English | MEDLINE | ID: mdl-23347518

ABSTRACT

Teleosts are the largest and most diverse group of vertebrates, and many species undergo morphological, physiological, and behavioral transitions, "metamorphoses," as they progress between morphologically divergent life stages. The larval metamorphosis that generally occurs as teleosts mature from larva to juvenile involves the loss of embryo-specific features, the development of new adult features, major remodeling of different organ systems, and changes in physical proportions and overall phenotype. Yet, in contrast to anuran amphibians, for example, teleost metamorphosis can entail morphological change that is either sudden and profound, or relatively gradual and subtle. Here, we review the definition of metamorphosis in teleosts, the diversity of teleost metamorphic strategies and the transitions they involve, and what is known of their underlying endocrine and genetic bases. We suggest that teleost metamorphosis offers an outstanding opportunity for integrating our understanding of endocrine mechanisms, cellular processes of morphogenesis and differentiation, and the evolution of diverse morphologies and life histories.


Subject(s)
Fishes/growth & development , Metamorphosis, Biological , Animals , Biodiversity , Endocrine System/growth & development , Morphogenesis
18.
PLoS One ; 7(3): e32763, 2012.
Article in English | MEDLINE | ID: mdl-22427878

ABSTRACT

Recent data indicates that blotched tiger salamanders (Ambystoma tigrinum melanostictum) in northern regions of Yellowstone National Park are declining due to climate-related habitat changes. In this study, we used ancient and modern mitochondrial haplotype diversity to model the effective size of this amphibian population through recent geological time and to assess past responses to climatic changes in the region. Using subfossils collected from a cave in northern Yellowstone, we analyzed >700 base pairs of mitochondrial sequence from 16 samples ranging in age from 100 to 3300 years old and found that all shared an identical haplotype. Although mitochondrial diversity was extremely low within the living population, we still were able to detect geographic subdivision within the local area. Using serial coalescent modelling with Bayesian priors from both modern and ancient genetic data we simulated a range of probable population sizes and mutation rates through time. Our simulations suggest that regional mitochondrial diversity has remained relatively constant even through climatic fluctuations of recent millennia.


Subject(s)
Ambystoma/genetics , DNA, Mitochondrial/genetics , Fossils , Genetic Variation , Analysis of Variance , Animals , Base Sequence , Bayes Theorem , Computer Simulation , DNA Primers/genetics , Evolution, Molecular , Haplotypes/genetics , Models, Genetic , Molecular Sequence Data , Mutation Rate , Population Density , Sequence Analysis, DNA , Wyoming
19.
BMC Ecol ; 10: 10, 2010 Apr 03.
Article in English | MEDLINE | ID: mdl-20361876

ABSTRACT

BACKGROUND: Loss of pond habitat is catastrophic to aquatic larval amphibians, but even reduction in the amount of time a breeding site holds water (hydroperiod) can influence amphibian development and limit reproductive success. Using the landscape variation of a glacial valley in the Greater Yellowstone Ecosystem as the context for a natural experiment, we examined variation in growth pattern and life history of the salamander Ambystoma tigrinum melanostictum and determined how these developmental characteristics varied with hydroperiod over several summers. RESULTS: In ponds that dried early in the season, maximum larval size was reduced relative to the sizes achieved in permanent ponds. Ephemeral ponds were associated with early metamorphosis at small body sizes, while permanent ponds facilitated longer larval periods and later metamorphosis. Paedomorphosis resulted from indefinite metamorphic postponement, and was identified only in the most permanent environments. Patterns of growth and allometry were similar between ponds with different hydroperiods, but considerable life history variation was derived from modulating the timing of and size at metamorphosis. Considering maximum rates of growth and inferring the minimum size at metamorphosis across 25 ponds over the course of three years, we calculated that hydroperiods longer than three months are necessary to support these populations through metamorphosis and/or reproductive maturity. CONCLUSIONS: Landscape heterogeneity fosters life history variation in this natural population. Modulation of the complex ambystomatid life cycle allows this species to survive in unpredictable environments, but current trends towards rapid pond drying will promote metamorphosis at smaller sizes and could eliminate the paedomorphic phenotype from this region. Metamorphosis at small size is has been linked to altered fitness traits, including reduced survival and fecundity. Thus, widespread environmental truncation of larval periods may lead to decreased population persistence. We found that the hydroperiods of many ponds in this region are now shorter than the developmental period required for larvae to reach the minimum size for metamorphosis; these locations serve as reproductive sinks that may be detrimental for persistence of the species in the region.


Subject(s)
Ambystoma/growth & development , Ecosystem , Metamorphosis, Biological , Animals , Body Size , Fresh Water , Larva/growth & development , Models, Biological
20.
Proc Natl Acad Sci U S A ; 105(44): 16988-93, 2008 Nov 04.
Article in English | MEDLINE | ID: mdl-18955700

ABSTRACT

Amphibians are a bellwether for environmental degradation, even in natural ecosystems such as Yellowstone National Park in the western United States, where species have been actively protected longer than anywhere else on Earth. We document that recent climatic warming and resultant wetland desiccation are causing severe declines in 4 once-common amphibian species native to Yellowstone. Climate monitoring over 6 decades, remote sensing, and repeated surveys of 49 ponds indicate that decreasing annual precipitation and increasing temperatures during the warmest months of the year have significantly altered the landscape and the local biological communities. Drought is now more common and more severe than at any time in the past century. Compared with 16 years ago, the number of permanently dry ponds in northern Yellowstone has increased 4-fold. Of the ponds that remain, the proportion supporting amphibians has declined significantly, as has the number of species found in each location. Our results indicate that climatic warming already has disrupted one of the best-protected ecosystems on our planet and that current assessments of species' vulnerability do not adequately consider such impacts.


Subject(s)
Amphibians/physiology , Climate , Extinction, Biological , Wetlands , Animals , Biodiversity , Ecosystem , Population Density , Population Dynamics , United States
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