188 results on '"Jeffery WR"'
Search Results
2. Hypoxia-sonic hedgehog axis as a driver of primitive hematopoiesis development and evolution in cavefish.
- Author
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van der Weele CM, Hospes KC, Rowe KE, and Jeffery WR
- Abstract
The teleost Astyanax mexicanus consists of surface dwelling (surface fish) and cave dwelling (cavefish) forms. Cavefish have evolved in subterranean habitats characterized by reduced oxygen levels (hypoxia) and exhibit a subset of phenotypic traits controlled by increased Sonic hedgehog (Shh) signaling along the embryonic midline. The enhancement of primitive hematopoietic domains, which are formed bilaterally in the anterior and posterior lateral plate mesoderm, are responsible for the development of more larval erythrocytes in cavefish relative to surface fish. In this study, we determine the role of hypoxia and Shh signaling in the development and evolution of primitive hematopoiesis in cavefish. We show that hypoxia treatment during embryogenesis increases primitive hematopoiesis and erythrocyte development in surface fish. We also demonstrate that upregulation of Shh midline signaling by the Smoothened agonist SAG increases primitive hematopoiesis and erythrocyte development in surface fish, whereas Shh downregulation via treatment with the Smoothened inhibitor cyclopamine decreases these traits in cavefish. Together these results suggest that hematopoietic enhancement is regulated by hypoxia and Shh signaling. Lastly, we demonstrate that hypoxia enhances expression of Shh signaling along the midline of surface fish embryos. We conclude that hypoxia-mediated Shh plasticity may be a driving force for the adaptive evolution of primitive hematopoiesis and erythrocyte development in cavefish., (Copyright © 2024 Elsevier Inc. All rights reserved.)
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- 2024
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3. Natural reversal of cavefish heart asymmetry is controlled by Sonic Hedgehog effects on the left-right organizer.
- Author
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Ng M, Ma L, Shi J, and Jeffery WR
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- Animals, Characidae embryology, Characidae genetics, Gene Expression Regulation, Developmental, Cilia metabolism, Embryo, Nonmammalian metabolism, Hedgehog Proteins metabolism, Hedgehog Proteins genetics, Body Patterning genetics, Heart embryology, Signal Transduction
- Abstract
The direction of left-right visceral asymmetry is conserved in vertebrates. Deviations of the standard asymmetric pattern are rare, and the underlying mechanisms are not understood. Here, we use the teleost Astyanax mexicanus, consisting of surface fish with normal left-oriented heart asymmetry and cavefish with high levels of reversed right-oriented heart asymmetry, to explore natural changes in asymmetry determination. We show that Sonic Hedgehog (Shh) signaling is increased at the posterior midline, Kupffer's vesicle (the teleost left-right organizer) is enlarged and contains longer cilia, and the number of dorsal forerunner cells is increased in cavefish. Furthermore, Shh increase in surface fish embryos induces asymmetric changes resembling the cavefish phenotype. Asymmetric expression of the Nodal antagonist Dand5 is equalized or reversed in cavefish, and Shh increase in surface fish mimics changes in cavefish dand5 asymmetry. Shh decrease reduces the level of right-oriented heart asymmetry in cavefish. Thus, naturally occurring modifications in cavefish heart asymmetry are controlled by the effects of Shh signaling on left-right organizer function., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2024. Published by The Company of Biologists Ltd.)
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- 2024
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4. Cymric , a Maternal and Zygotic HTK-16-Like SHARK Family Tyrosine Kinase Gene, Is Disrupted in Molgula occulta , a Tailless Ascidian.
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Makabe KW, Jensen HI, Fodor ACA, Hsu J, Jeffery WR, Satoh N, and Swalla BJ
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- Animals, Amino Acid Sequence, Zygote, Pseudogenes genetics, Phylogeny, Urochordata genetics, Urochordata enzymology, Protein-Tyrosine Kinases genetics, Protein-Tyrosine Kinases metabolism
- Abstract
AbstractWe describe the cloning and expression of a nonreceptor tyrosine kinase, cymric ( Uro-1 ), a HTK-16-like ( HydraTyrosineKinase-16 ) gene, identified in a subtractive screen for maternal ascidian cDNAs in Molgula oculata , an ascidian species with a tadpole larva. The cymric gene encodes a 4-kb mRNA expressed in gonads, eggs, and embryos in the tailed M. oculata but is not detected in eggs or embryos of the closely related tailless species Molgula occulta . There is a large insertion in cymric in the M. occulta genome, as shown by transcriptome and genome analyses, resulting in it becoming a pseudogene. The cymric amino acid sequence encodes a nonreceptor tyrosine kinase with an N-terminal region containing two SH2 domains and five ankyrin repeats, similar to the HTK-16-like gene found in other ascidians. Thus, the ascidian cymric genes are members of the SHARK (Src-homology ankyrin-repeat containing tyrosine kinase) family of nonreceptor tyrosine kinases, which are found throughout invertebrates and missing from vertebrates. We show that cymric is lacking the tyrosine kinase domain in the tailless M. occulta , although the truncated mRNA is still expressed in transcriptome data. This maternal and zygotic HTK-16-like tyrosine kinase is another described pseudogene from M. occulta and appears not to be necessary for adult development.
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- 2023
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5. Protection and exploration of the scientific potential of Chinese cavefish.
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Ma L, Yang JX, Lei FK, Xu MZ, Zhao YH, and Jeffery WR
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- 2023
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6. Cavefish as biological models in the laboratory and in the wild.
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Jeffery WR, Ma L, and Zhao YH
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- Animals, Caves, Biological Evolution, Models, Biological
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- 2023
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7. Differentially expressed chaperone genes reveal a stress response required for unidirectional regeneration in the basal chordate Ciona.
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Jeffery WR, Li B, Ng M, Li L, Gorički Š, and Ma L
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- Animals, Stem Cells, Chromosome Mapping, Molecular Chaperones genetics, HSP70 Heat-Shock Proteins genetics, Ciona genetics, Ciona intestinalis genetics
- Abstract
Background: Unidirectional regeneration in the basal chordate Ciona intestinalis involves the proliferation of adult stem cells residing in the branchial sac vasculature and the migration of progenitor cells to the site of distal injury. However, after the Ciona body is bisected, regeneration occurs in the proximal but not in the distal fragments, even if the latter include a part of the branchial sac with stem cells. A transcriptome was sequenced and assembled from the isolated branchial sacs of regenerating animals, and the information was used to provide insights into the absence of regeneration in distal body fragments., Results: We identified 1149 differentially expressed genes, which were separated into two major modules by weighted gene correlation network analysis, one consisting of mostly upregulated genes correlated with regeneration and the other consisting of only downregulated genes associated with metabolism and homeostatic processes. The hsp70, dnaJb4, and bag3 genes were among the highest upregulated genes and were predicted to interact in an HSP70 chaperone system. The upregulation of HSP70 chaperone genes was verified and their expression confirmed in BS vasculature cells previously identified as stem and progenitor cells. siRNA-mediated gene knockdown showed that hsp70 and dnaJb4, but not bag3, are required for progenitor cell targeting and distal regeneration. However, neither hsp70 nor dnaJb4 were strongly expressed in the branchial sac vasculature of distal fragments, implying the absence of a stress response. Heat shock treatment of distal body fragments activated hsp70 and dnaJb4 expression indicative of a stress response, induced cell proliferation in branchial sac vasculature cells, and promoted distal regeneration., Conclusions: The chaperone system genes hsp70, dnaJb4, and bag3 are significantly upregulated in the branchial sac vasculature following distal injury, defining a stress response that is essential for regeneration. The stress response is absent from distal fragments, but can be induced by a heat shock, which activates cell division in the branchial sac vasculature and promotes distal regeneration. This study demonstrates the importance of a stress response for stem cell activation and regeneration in a basal chordate, which may have implications for understanding the limited regenerative activities in other animals, including vertebrates., (© 2023. The Author(s).)
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- 2023
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8. Brazilian cave heritage under siege.
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Ferreira RL, Bernard E, da Cruz Júnior FW, Piló LB, Calux A, Souza-Silva M, Barlow J, Pompeu PS, Cardoso P, Mammola S, García AM, Jeffery WR, Shear W, Medellín RA, Wynne JJ, Borges PAV, Kamimura Y, Pipan T, Hajna NZ, Sendra A, Peck S, Onac BP, Culver DC, Hoch H, Flot JF, Stoch F, Pavlek M, Niemiller ML, Manchi S, Deharveng L, Fenolio D, Calaforra JM, Yager J, Griebler C, Nader FH, Humphreys WF, Hughes AC, Fenton B, Forti P, Sauro F, Veni G, Frumkin A, Gavish-Regev E, Fišer C, Trontelj P, Zagmajster M, Delic T, Galassi DMP, Vaccarelli I, Komnenov M, Gainett G, da Cunha Tavares V, Kováč Ľ, Miller AZ, Yoshizawa K, Di Lorenzo T, Moldovan OT, Sánchez-Fernández D, Moutaouakil S, Howarth F, Bilandžija H, Dražina T, Kuharić N, Butorac V, Lienhard C, Cooper SJB, Eme D, Strauss AM, Saccò M, Zhao Y, Williams P, Tian M, Tanalgo K, Woo KS, Barjakovic M, McCracken GF, Simmons NB, Racey PA, Ford D, Labegalini JA, Colzato N, Ramos Pereira MJ, Aguiar LMS, Moratelli R, Du Preez G, Pérez-González A, Reboleira ASPS, Gunn J, Mc Cartney A, Bobrowiec PED, Milko D, Kinuthia W, Fischer E, Meierhofer MB, and Frick WF
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- 2022
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9. Cavefish cope with environmental hypoxia by developing more erythrocytes and overexpression of hypoxia-inducible genes.
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van der Weele CM and Jeffery WR
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- Animals, Biological Evolution, Characidae blood, Characidae immunology, Female, Hypoxia blood, Male, Adaptation, Physiological genetics, Caves, Characidae genetics, Environment, Erythrocytes physiology, Hypoxia genetics
- Abstract
Dark caves lacking primary productivity can expose subterranean animals to hypoxia. We used the surface-dwelling (surface fish) and cave-dwelling (cavefish) morphs of Astyanax mexicanus as a model for understanding the mechanisms of hypoxia tolerance in the cave environment. Primitive hematopoiesis, which is restricted to the posterior lateral mesoderm in other teleosts, also occurs in the anterior lateral mesoderm in Astyanax , potentially pre-adapting surface fish for hypoxic cave colonization. Cavefish have enlarged both hematopoietic domains and develop more erythrocytes than surface fish, which are required for normal development in both morphs. Laboratory-induced hypoxia suppresses growth in surface fish but not in cavefish. Both morphs respond to hypoxia by overexpressing hypoxia-inducible factor 1 ( hif1 ) pathway genes, and some hif1 genes are constitutively upregulated in normoxic cavefish to similar levels as in hypoxic surface fish. We conclude that cavefish cope with hypoxia by increasing erythrocyte development and constitutive hif1 gene overexpression., Competing Interests: Cv, WJ No competing interests declared, (© 2022, van der Weele and Jeffery.)
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- 2022
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10. Publisher Correction: Maternal control of visceral asymmetry evolution in Astyanax cavefish.
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Ma L, Ng M, Shi J, Gore AV, Castranova D, Weinstein BM, and Jeffery WR
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- 2021
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11. Maternal control of visceral asymmetry evolution in Astyanax cavefish.
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Ma L, Ng M, Shi J, Gore AV, Castranova D, Weinstein BM, and Jeffery WR
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- Animals, Biological Evolution, Female, Body Patterning, Characidae embryology
- Abstract
The direction of visceral organ asymmetry is highly conserved during vertebrate evolution with heart development biased to the left and pancreas and liver development restricted to opposing sides of the midline. Here we show that reversals in visceral organ asymmetry have evolved in Astyanax mexicanus, a teleost species with interfertile surface-dwelling (surface fish) and cave-dwelling (cavefish) forms. Visceral organ asymmetry is conventional in surface fish but some cavefish have evolved reversals in heart, liver, and pancreas development. Corresponding changes in the normally left-sided expression of the Nodal-Pitx2/Lefty signaling system are also present in the cavefish lateral plate mesoderm (LPM). The Nodal antagonists lefty1 (lft1) and lefty2 (lft2), which confine Nodal signaling to the left LPM, are expressed in most surface fish, however, lft2, but not lft1, expression is absent during somitogenesis of most cavefish. Despite this difference, multiple lines of evidence suggested that evolutionary changes in L-R patterning are controlled upstream of Nodal-Pitx2/Lefty signaling. Accordingly, reciprocal hybridization of cavefish and surface fish showed that modifications of heart asymmetry are present in hybrids derived from cavefish mothers but not from surface fish mothers. The results indicate that changes in visceral asymmetry during cavefish evolution are influenced by maternal genetic effects.
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- 2021
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12. Apoptosis is a generator of Wnt-dependent regeneration and homeostatic cell renewal in the ascidian Ciona.
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Jeffery WR and Gorički Š
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- Animals, Asymmetric Cell Division, Biomarkers, Cell Survival genetics, Fluorescent Antibody Technique, Gene Expression Regulation, Signal Transduction, Stem Cells cytology, Stem Cells metabolism, Wnt Proteins genetics, Wnt Signaling Pathway, Apoptosis, Cell Self Renewal genetics, Ciona physiology, Homeostasis genetics, Regeneration genetics, Wnt Proteins metabolism
- Abstract
In the ascidian Ciona intestinalis, basal body parts regenerate distal structures but distal body parts do not replace basal structures. Regeneration involves the activity of adult stem cells in the branchial sac, which proliferate and produce migratory progenitor cells for tissue and organ replacement. Branchial sac-derived stem cells also replenish recycling cells lining the pharyngeal fissures during homeostatic growth. Apoptosis at injury sites occurs early during regeneration and continuously in the pharyngeal fissures during homeostatic growth. Caspase 1 inhibitor, caspase 3 inhibitor, or pan-caspase inhibitor Z-VAD-FMK treatment blocked apoptosis, prevented regeneration, and suppressed branchial sac growth and function. A pharmacological screen and siRNA-mediated gene knockdown indicated that regeneration requires canonical Wnt signaling. Wnt3a protein rescued both caspase-blocked regeneration and branchial sac growth. Inhibition of apoptosis did not affect branchial sac stem cell proliferation but prevented the survival of progenitor cells. After bisection across the mid-body, apoptosis occurred only in the regenerating basal fragments, although both fragments contained a part of the branchial sac, suggesting that apoptosis is unilateral at the wound site and the presence of branchial sac stem cells is insufficient for regeneration. The results suggest that apoptosis-dependent Wnt signaling mediates regeneration and homeostatic growth in Ciona., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2021. Published by The Company of Biologists Ltd.)
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- 2021
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13. Incremental Temperature Changes for Maximal Breeding and Spawning in Astyanax mexicanus.
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Ma L, Dessiatoun R, Shi J, and Jeffery WR
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- Animals, Caves, Pigmentation physiology, Breeding, Characidae physiology, Temperature
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The Mexican tetra, Astyanax mexicanus, is an emerging model system for studies in development and evolution. The existence of eyed surface (surface fish) and blind cave (cave fish) morphs in this species presents an opportunity to interrogate the mechanisms underlying morphological and behavioral evolution. Cave fish have evolved novel constructive and regressive traits. The constructive changes include increases in taste buds and jaws, lateral line sensory organs, and body fat. The regressive changes include loss or reduction of eyes. melanin pigmentation, schooling behavior, aggression, and sleep. To experimentally interrogate these changes, it is crucial to obtain large numbers of spawned embryos. Since the original A. mexicanus surface fish and cave fish were collected in Texas and Mexico in the 1990s, their descendants have been routinely stimulated to breed and spawn large numbers of embryos bimonthly in the Jeffery laboratory. Although breeding is controlled by food abundance and quality, light-dark cycles, and temperature, we have found that incremental temperature changes play a key role in stimulating maximal spawning. The gradual increase of temperature from 72 °F to 78 °F in the first three days of a breeding week provides two-three consecutive spawning days with maximal numbers of high-quality embryos, which is then followed by a gradual decrease of temperature from 78 °F to 72 °F during the last three days of the spawning week. The procedures shown in this video outline the workflow before and during a laboratory breeding week for incremental temperature stimulated spawning.
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- 2021
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14. Fundamental research questions in subterranean biology.
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Mammola S, Amorim IR, Bichuette ME, Borges PAV, Cheeptham N, Cooper SJB, Culver DC, Deharveng L, Eme D, Ferreira RL, Fišer C, Fišer Ž, Fong DW, Griebler C, Jeffery WR, Jugovic J, Kowalko JE, Lilley TM, Malard F, Manenti R, Martínez A, Meierhofer MB, Niemiller ML, Northup DE, Pellegrini TG, Pipan T, Protas M, Reboleira ASPS, Venarsky MP, Wynne JJ, Zagmajster M, and Cardoso P
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- Adaptation, Physiological, Genomics, Caves, Ecology
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Five decades ago, a landmark paper in Science titled The Cave Environment heralded caves as ideal natural experimental laboratories in which to develop and address general questions in geology, ecology, biogeography, and evolutionary biology. Although the 'caves as laboratory' paradigm has since been advocated by subterranean biologists, there are few examples of studies that successfully translated their results into general principles. The contemporary era of big data, modelling tools, and revolutionary advances in genetics and (meta)genomics provides an opportunity to revisit unresolved questions and challenges, as well as examine promising new avenues of research in subterranean biology. Accordingly, we have developed a roadmap to guide future research endeavours in subterranean biology by adapting a well-established methodology of 'horizon scanning' to identify the highest priority research questions across six subject areas. Based on the expert opinion of 30 scientists from around the globe with complementary expertise and of different academic ages, we assembled an initial list of 258 fundamental questions concentrating on macroecology and microbial ecology, adaptation, evolution, and conservation. Subsequently, through online surveys, 130 subterranean biologists with various backgrounds assisted us in reducing our list to 50 top-priority questions. These research questions are broad in scope and ready to be addressed in the next decade. We believe this exercise will stimulate research towards a deeper understanding of subterranean biology and foster hypothesis-driven studies likely to resonate broadly from the traditional boundaries of this field., (© 2020 Cambridge Philosophical Society.)
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- 2020
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15. Dual roles of the retinal pigment epithelium and lens in cavefish eye degeneration.
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Ma L, Ng M, van der Weele CM, Yoshizawa M, and Jeffery WR
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- Animals, Caves, Characidae anatomy & histology, Characidae growth & development, Eye growth & development, Eye Abnormalities embryology, Female, Lens, Crystalline growth & development, Male, Retinal Pigment Epithelium anatomy & histology, Retinal Pigment Epithelium growth & development, Characidae embryology, Eye embryology, Lens, Crystalline embryology, Retinal Pigment Epithelium embryology
- Abstract
Astyanax mexicanus consists of two forms, a sighted surface dwelling form (surface fish) and a blind cave-dwelling form (cavefish). Embryonic eyes are initially formed in cavefish but they are subsequently arrested in growth and degenerate during larval development. Previous lens transplantation studies have shown that the lens plays a central role in cavefish eye loss. However, several lines of evidence suggest that additional factors, such as the retinal pigment epithelium (RPE), which is morphologically altered in cavefish, could also be involved in the eye regression process. To explore the role of the RPE in cavefish eye degeneration, we generated an albino eyed (AE) strain by artificial selection for hybrid individuals with large eyes and a depigmented RPE. The AE strain exhibited an RPE lacking pigment granules and showed reduced expression of the RPE specific enzyme retinol isomerase, allowing eye development to be studied by lens ablation in an RPE background resembling cavefish. We found that lens ablation in the AE strain had stronger negative effects on eye growth than in surface fish, suggesting that an intact RPE is required for normal eye development. We also found that the AE strain develops a cartilaginous sclera lacking boney ossicles, a trait similar to cavefish. Extrapolation of the results to cavefish suggests that the RPE and lens have dual roles in eye degeneration, and that deficiencies in the RPE may be associated with evolutionary changes in scleral ossification., (© 2020 Wiley Periodicals, Inc.)
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- 2020
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16. Author Correction: A hypomorphic cystathionine ß-synthase gene contributes to cavefish eye loss by disrupting optic vasculature.
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Ma L, Gore AV, Castranova D, Shi J, Ng M, Tomins KA, van der Weele CM, Weinstein BM, and Jeffery WR
- Abstract
An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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- 2020
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17. Astyanax surface and cave fish morphs.
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Jeffery WR
- Abstract
The small teleost fish Astyanax mexicanus has emerged as an outstanding model for studying many biological topics in the context of evolution. A major attribute is conspecific surface dwelling (surface fish) and blind cave dwelling (cavefish) morphs that can be raised in the laboratory and spawn large numbers of transparent and synchronously developing embryos. More than 30 cavefish populations have been discovered, mostly in northeastern Mexico, and some are thought to have evolved independently from surface fish ancestors, providing excellent models of parallel and convergent evolution. Cavefish have evolved eye and pigmentation regression, as well as modifications in brain morphology, behaviors, heart regenerative capacity, metabolic processes, and craniofacial organization. Thus, the Astyanax model provides researchers with natural "mutants" to study life in the challenging cave environment. The application of powerful genetic approaches based on hybridization between the two morphs and between the different cavefish populations are key advantages for deciphering the developmental and genetic mechanisms regulating trait evolution. QTL analysis has revealed the genetic architectures of gained and lost traits. In addition, some cavefish traits resemble human diseases, offering novel models for biomedical research. Astyanax research is supported by genome assemblies, transcriptomes, tissue and organ transplantation, gene manipulation and editing, and stable transgenesis, and benefits from a welcoming and interactive research community that conducts integrated community projects and sponsors the International Astyanax Meeting (AIM)., Competing Interests: Competing interestsThe author declares no competing interests., (© The Author(s) 2020.)
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- 2020
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18. A hypomorphic cystathionine ß-synthase gene contributes to cavefish eye loss by disrupting optic vasculature.
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Ma L, Gore AV, Castranova D, Shi J, Ng M, Tomins KA, van der Weele CM, Weinstein BM, and Jeffery WR
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- Animals, Apoptosis, Biological Evolution, Brain embryology, Cardiovascular System, Cystathionine beta-Synthase metabolism, Developmental Biology, Eye cytology, Eye growth & development, Female, Fishes embryology, Fishes genetics, Gene Expression Regulation, Developmental genetics, Gene Knockdown Techniques, Head, Lens, Crystalline cytology, Lens, Crystalline metabolism, Male, Models, Animal, Cystathionine metabolism, Cystathionine beta-Synthase genetics, Eye embryology, Eye metabolism, Fishes physiology
- Abstract
Vestigial structures are key indicators of evolutionary descent, but the mechanisms underlying their development are poorly understood. This study examines vestigial eye formation in the teleost Astyanax mexicanus, which consists of a sighted surface-dwelling morph and multiple populations of blind cave morphs. Cavefish embryos initially develop eyes, but they subsequently degenerate and become vestigial structures embedded in the head. The mutated genes involved in cavefish vestigial eye formation have not been characterized. Here we identify cystathionine ß-synthase a (cbsa), which encodes the key enzyme of the transsulfuration pathway, as one of the mutated genes responsible for eye degeneration in multiple cavefish populations. The inactivation of cbsa affects eye development by increasing the transsulfuration intermediate homocysteine and inducing defects in optic vasculature, which result in aneurysms and eye hemorrhages. Our findings suggest that localized modifications in the circulatory system may have contributed to the evolution of vestigial eyes in cavefish.
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- 2020
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19. Progenitor targeting by adult stem cells in Ciona homeostasis, injury, and regeneration.
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Jeffery WR
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- Animals, Apoptosis, Branchial Region physiology, Ciona intestinalis anatomy & histology, Models, Biological, Neurons physiology, Wound Healing, Adult Stem Cells cytology, Ciona intestinalis physiology, Homeostasis, Regeneration
- Abstract
In the ascidian Ciona intestinalis, oral siphon amputation activates adult stem cell niches in the branchial sac to divide and dispatch migratory progenitor cells to a regeneration blastema at the site of injury. This study shows that progenitor cells derived from branchial sac stem cell niches have roles in homeostasis, wound repair, and regeneration of the siphons and neural complex (NC). During homeostasis, progenitor cells targeted the pharyngeal stigmata to replace ciliated cells involved in filter feeding. After individual or double siphon amputations, progenitor cells specifically targeted the oral or atrial siphons or both siphons, and were involved in the replacement of siphon circular muscle fibers. After oral siphon wounding, progenitor cells targeted the wound sites, and in some cases a supernumerary siphon was formed, although progenitor cell targeting did not predict the induction of supernumerary siphons. Following NC ablation, progenitor cells specifically targeted the regenerating NC, and supplied the precursors of new brain and neural gland cells. The tissues and organs targeted by branchial sac stem cells exhibited apoptosis during homeostasis and injury. It is concluded that branchial sac progenitor cells are multipotent and show targeting specificity that is correlated with apoptosis during homeostatic growth, tissue repair, and regeneration., (Copyright © 2018 Elsevier Inc. All rights reserved.)
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- 2019
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20. The role of gene flow in rapid and repeated evolution of cave-related traits in Mexican tetra, Astyanax mexicanus.
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Herman A, Brandvain Y, Weagley J, Jeffery WR, Keene AC, Kono TJY, Bilandžija H, Borowsky R, Espinasa L, O'Quin K, Ornelas-García CP, Yoshizawa M, Carlson B, Maldonado E, Gross JB, Cartwright RA, Rohner N, Warren WC, and McGaugh SE
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- Animals, Mexico, Models, Genetic, Phenotype, Phylogeny, Quantitative Trait Loci, Biological Evolution, Caves, Characidae genetics, Gene Flow, Genetics, Population
- Abstract
Understanding the molecular basis of repeatedly evolved phenotypes can yield key insights into the evolutionary process. Quantifying gene flow between populations is especially important in interpreting mechanisms of repeated phenotypic evolution, and genomic analyses have revealed that admixture occurs more frequently between diverging lineages than previously thought. In this study, we resequenced 47 whole genomes of the Mexican tetra from three cave populations, two surface populations and outgroup samples. We confirmed that cave populations are polyphyletic and two Astyanax mexicanus lineages are present in our data set. The two lineages likely diverged much more recently than previous mitochondrial estimates of 5-7 mya. Divergence of cave populations from their phylogenetically closest surface population likely occurred between ~161 and 191 k generations ago. The favoured demographic model for most population pairs accounts for divergence with secondary contact and heterogeneous gene flow across the genome, and we rigorously identified gene flow among all lineages sampled. Therefore, the evolution of cave-related traits occurred more rapidly than previously thought, and trogolomorphic traits are maintained despite gene flow with surface populations. The recency of these estimated divergence events suggests that selection may drive the evolution of cave-derived traits, as opposed to disuse and drift. Finally, we show that a key trogolomorphic phenotype QTL is enriched for genomic regions with low divergence between caves, suggesting that regions important for cave phenotypes may be transferred between caves via gene flow. Our study shows that gene flow must be considered in studies of independent, repeated trait evolution., (© 2018 John Wiley & Sons Ltd.)
- Published
- 2018
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21. Maternal genetic effects in Astyanax cavefish development.
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Ma L, Strickler AG, Parkhurst A, Yoshizawa M, Shi J, and Jeffery WR
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- Animals, Apoptosis genetics, Female, Male, Characiformes embryology, Characiformes genetics, Crosses, Genetic, Eye embryology, Fish Proteins biosynthesis, Fish Proteins genetics, Gene Expression Regulation, Developmental physiology, Maternal Inheritance physiology
- Abstract
The role of maternal factors in the evolution of development is poorly understood. Here we describe the use of reciprocal hybridization between the surface dwelling (surface fish, SF) and cave dwelling (cavefish, CF) morphs of the teleost Astyanax mexicanus to investigate the roles of maternal genetic effects in cavefish development. Reciprocal hybridization, a procedure in which F1 hybrids are generated by fertilizing SF eggs with CF sperm (SF × CF hybrids) and CF eggs with SF sperm (CF × SF hybrids), revealed that the CF degenerative eye phenotype showed maternal genetic effects. The eyes of CF × SF hybrids resembled the degenerate eyes of CF in showing ventral reduction of the retina and corresponding displacement of the lens within the optic cup, a smaller lens and eyeball, more lens apoptosis, a smaller cartilaginous sclera, and lens-specific gene expression characteristics compared to SF × CF hybrids, which showed eye and lens gene expression phenotypes resembling SF. In contrast, reciprocal hybridization failed to support roles for maternal genetic effects in the CF regressive pigmentation phenotype or in CF constructive changes related to enhanced jaw development. Maternal transcripts encoded by the pou2f1b, runx2b, and axin1 genes, which are involved in determining ventral embryonic fates, were increased in unfertilized CF eggs. In contrast, maternal mRNAs encoded by the ß-catenin and syntabulin genes, which control dorsal embryonic fates, showed similar expression levels in unfertilized SF and CF eggs. Furthermore, maternal transcripts of a sonic hedgehog gene were detected in SF and CF eggs and early cleaving embryos. This study reveals that CF eye degeneration is controlled by changes in maternal factors produced during oogenesis and introduces A. mexicanus as a model system for studying the role of maternal changes in the evolution of development., (Copyright © 2018 Elsevier Inc. All rights reserved.)
- Published
- 2018
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22. Seeing a bright future for a blind fish.
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Gore AV, Rohner N, Rétaux S, and Jeffery WR
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- Animals, Caves, Mexico, Blindness genetics, Blindness metabolism, Blindness physiopathology, Characiformes genetics, Characiformes metabolism, Disease Models, Animal
- Published
- 2018
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23. Neural Crest Transplantation Reveals Key Roles in the Evolution of Cavefish Development.
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Yoshizawa M, Hixon E, and Jeffery WR
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- Animals, Characidae physiology, Darkness, Light, Ocular Physiological Phenomena, Biological Evolution, Characidae embryology, Eye embryology, Neural Crest transplantation
- Abstract
Evolutionary changes in Astyanax mexicanus cavefish with respect to conspecific surface fish, including the regression of eyes, loss of pigmentation, and modification of the cranial skeleton, involve derivatives of the neural crest. However, the role of neural crest cells in cavefish evolution and development is poorly understood. One of the reasons is that experimental methods for neural crest analysis are not well developed in the Astyanax system. Here we describe neural crest transplantation between Astyanax surface fish and cavefish embryos. We found differences in the migration of cranial neural crest cells transplanted from the surface fish anterior hindbrain to the same region of surface fish or cavefish hosts. Cranial neural crest cells migrated extensively throughout the head, and to a lesser extent the trunk, in surface fish hosts but their migration was mostly restricted to the anterior and dorsal head regions in cavefish hosts. Cranial neural crest cells derived from the surface fish transplants invaded the degenerating eyes of cavefish hosts, resulting in increased eye size and suggesting that cavefish neural crest cells are defective in forming optic derivatives. We found that melanophores were formed in albino cavefish from grafts of surface fish trunk neural crest cells, showing that the cavefish tissue environment is conducive for pigment cell development, and implicating intrinsic changes in cavefish neural crest cells in loss of body pigmentation. It is concluded that changes in neural crest cells play key roles in the evolution of cavefish development.
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- 2018
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24. An epigenetic mechanism for cavefish eye degeneration.
- Author
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Gore AV, Tomins KA, Iben J, Ma L, Castranova D, Davis AE, Parkhurst A, Jeffery WR, and Weinstein BM
- Subjects
- Animals, Biological Evolution, Caves, Characidae growth & development, Phenotype, Characidae genetics, DNA Methylation, Epigenesis, Genetic genetics, Eye growth & development, Gene Silencing
- Abstract
Coding and non-coding mutations in DNA contribute significantly to phenotypic variability during evolution. However, less is known about the role of epigenetics in this process. Although previous studies have identified eye development genes associated with the loss-of-eyes phenotype in the Pachón blind cave morph of the Mexican tetra Astyanax mexicanus, no inactivating mutations have been found in any of these genes. Here, we show that excess DNA methylation-based epigenetic silencing promotes eye degeneration in blind cave A. mexicanus. By performing parallel analyses in A. mexicanus cave and surface morphs, and in the zebrafish Danio rerio, we have discovered that DNA methylation mediates eye-specific gene repression and globally regulates early eye development. The most significantly hypermethylated and downregulated genes in the cave morph are also linked to human eye disorders, suggesting that the function of these genes is conserved across vertebrates. Our results show that changes in DNA methylation-based gene repression can serve as an important molecular mechanism generating phenotypic diversity during development and evolution.
- Published
- 2018
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25. Behavioural changes controlled by catecholaminergic systems explain recurrent loss of pigmentation in cavefish.
- Author
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Bilandžija H, Abraham L, Ma L, Renner KJ, and Jeffery WR
- Subjects
- Albinism, Oculocutaneous metabolism, Anesthesia, Animals, Biological Evolution, Characidae genetics, Fish Proteins metabolism, Norepinephrine metabolism, Tyrosine metabolism, Activity Cycles, Albinism, Oculocutaneous genetics, Anesthetics pharmacology, Catecholamines metabolism, Characidae physiology, Fish Proteins genetics, Pigmentation
- Abstract
Multiple cave populations of the teleost Astyanax mexicanus have repeatedly reduced or lost eye and body pigmentation during adaptation to dark caves. Albinism, the complete absence of melanin pigmentation, is controlled by loss-of-function mutations in the oca2 gene. The mutation is accompanied by an increase in the melanin synthesis precursor l-tyrosine, which is also a precursor for catecholamine synthesis. In this study, we show a relationship between pigmentation loss, enhanced catecholamine synthesis and responsiveness to anaesthesia, determined as a proxy for catecholamine-related behaviours. We demonstrate that anaesthesia resistance (AR) is enhanced in multiple depigmented and albino cavefish (CF), inversely proportional to the degree of pigmentation loss, controlled by the oca2 gene, and can be modulated by experimental manipulations of l-tyrosine or the catecholamine norepinephrine (NE). Moreover, NE is increased in the brains of multiple albino and depigmented CF relative to surface fish. The results provide new insights into the evolution of pigment modification because NE controls a suite of adaptive behaviours similar to AR that may represent a target of natural selection. Thus, understanding the relationship between loss of pigmentation and AR may provide insight into the role of natural selection in the evolution of albinism via a melanin-catecholamine trade-off., (© 2018 The Author(s).)
- Published
- 2018
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26. Environmental DNA in subterranean biology: range extension and taxonomic implications for Proteus.
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Gorički Š, Stanković D, Snoj A, Kuntner M, Jeffery WR, Trontelj P, Pavićević M, Grizelj Z, Năpăruş-Aljančič M, and Aljančič G
- Subjects
- Animals, Polymerase Chain Reaction methods, Polymerase Chain Reaction standards, Proteidae classification, Proteidae physiology, Caves, DNA Barcoding, Taxonomic methods, Phylogeny, Proteidae genetics
- Abstract
Europe's obligate cave-dwelling amphibian Proteus anguinus inhabits subterranean waters of the north-western Balkan Peninsula. Because only fragments of its habitat are accessible to humans, this endangered salamander's exact distribution has been difficult to establish. Here we introduce a quantitative real time polymerase chain reaction-based environmental DNA (eDNA) approach to detect the presence of Proteus using water samples collected from karst springs, wells or caves. In a survey conducted along the southern limit of its known range, we established a likely presence of Proteus at seven new sites, extending its range to Montenegro. Next, using specific molecular probes to discriminate the rare black morph of Proteus from the closely related white morph, we detected its eDNA at five new sites, thus more than doubling the known number of sites. In one of these we found both black and white Proteus eDNA together. This finding suggests that the two morphs may live in contact with each other in the same body of groundwater and that they may be reproductively isolated species. Our results show that the eDNA approach is suitable and efficient in addressing questions in biogeography, evolution, taxonomy and conservation of the cryptic subterranean fauna.
- Published
- 2017
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27. Genome Editing in Astyanax mexicanus Using Transcription Activator-like Effector Nucleases (TALENs).
- Author
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Kowalko JE, Ma L, and Jeffery WR
- Subjects
- Animals, Characidae, Gene Editing, Phenotype, Transcription Activator-Like Effector Nucleases, Genome
- Abstract
Identifying alleles of genes underlying evolutionary change is essential to understanding how and why evolution occurs. Towards this end, much recent work has focused on identifying candidate genes for the evolution of traits in a variety of species. However, until recently it has been challenging to functionally validate interesting candidate genes. Recently developed tools for genetic engineering make it possible to manipulate specific genes in a wide range of organisms. Application of this technology in evolutionarily relevant organisms will allow for unprecedented insight into the role of candidate genes in evolution. Astyanax mexicanus (A. mexicanus) is a species of fish with both surface-dwelling and cave-dwelling forms. Multiple independent lines of cave-dwelling forms have evolved from ancestral surface fish, which are interfertile with one another and with surface fish, allowing elucidation of the genetic basis of cave traits. A. mexicanus has been used for a number of evolutionary studies, including linkage analysis to identify candidate genes responsible for a number of traits. Thus, A. mexicanus is an ideal system for the application of genome editing to test the role of candidate genes. Here we report a method for using transcription activator-like effector nucleases (TALENs) to mutate genes in surface A. mexicanus. Genome editing using TALENs in A. mexicanus has been utilized to generate mutations in pigmentation genes. This technique can also be utilized to evaluate the role of candidate genes for a number of other traits that have evolved in cave forms of A. mexicanus.
- Published
- 2016
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28. The Comparative Organismal Approach in Evolutionary Developmental Biology: Insights from Ascidians and Cavefish.
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Jeffery WR
- Subjects
- Animals, Biological Evolution, Characidae growth & development, Developmental Biology, Urochordata growth & development
- Abstract
Important contributions to evolutionary developmental biology have been made using the comparative organismal approach. As examples, I describe insights obtained from studies of Molgula ascidians and Astyanax cavefish., (© 2016 Elsevier Inc. All rights reserved.)
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- 2016
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29. Complex Evolutionary and Genetic Patterns Characterize the Loss of Scleral Ossification in the Blind Cavefish Astyanax mexicanus.
- Author
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O'Quin KE, Doshi P, Lyon A, Hoenemeyer E, Yoshizawa M, and Jeffery WR
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- Animals, Biological Evolution, Caves, Chromosome Mapping, Genetic Linkage, Phenotype, Sclera, Characidae genetics, Osteogenesis genetics, Quantitative Trait Loci
- Abstract
The sclera is the tough outer covering of the eye that provides structural support and helps maintain intraocular pressure. In some fishes, reptiles, and birds, the sclera is reinforced with an additional ring of hyaline cartilage or bone that forms from scleral ossicles. Currently, the evolutionary and genetic basis of scleral ossification is poorly understood, especially in teleost fishes. We assessed scleral ossification among several groups of the Mexican tetra (Astyanax mexicanus), which exhibit both an eyed and eyeless morph. Although eyed Astyanax surface fish have bony sclera similar to other teleosts, the ossicles of blind Astyanax cavefish generally do not form. We first sampled cavefish from multiple independent populations and used ancestral character state reconstructions to determine how many times scleral ossification has been lost. We then confirmed these results by assessing complementation of scleral ossification among the F1 hybrid progeny of two cavefish populations. Finally, we quantified the number of scleral ossicles present among the F2 hybrid progeny of a cross between surface fish and cavefish, and used this information to identify quantitative trait loci (QTL) responsible for this trait. Our results indicate that the loss of scleral ossification is common-but not ubiquitous-among Astyanax cavefish, and that this trait has been convergently lost at least three times. The presence of wild-type, ossified sclera among the F1 hybrid progeny of a cross between different cavefish populations confirms the convergent evolution of this trait. However, a strongly skewed distribution of scleral ossicles found among surface fish x cavefish F2 hybrids suggests that scleral ossification is a threshold trait with a complex genetic basis. Quantitative genetic mapping identified a single QTL for scleral ossification on Astyanax linkage group 1. We estimate that the threshold for this trait is likely determined by at least three genetic factors which may control the severity and onset of lens degeneration in cavefishes. We conclude that complex evolutionary and genetic patterns underlie the loss of scleral ossification in Astyanax cavefish.
- Published
- 2015
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30. Evolution of the chordate regeneration blastema: Differential gene expression and conserved role of notch signaling during siphon regeneration in the ascidian Ciona.
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Hamada M, Goricki S, Byerly MS, Satoh N, and Jeffery WR
- Subjects
- Animals, Biological Evolution, Cell Proliferation, Epidermis metabolism, Gene Expression Profiling, In Situ Hybridization, Ligands, Oligonucleotide Array Sequence Analysis, Phalloidine chemistry, RNA metabolism, Regeneration, Signal Transduction, Stem Cells cytology, Ciona intestinalis embryology, Gene Expression Regulation, Developmental, Receptors, Notch metabolism
- Abstract
The regeneration of the oral siphon (OS) and other distal structures in the ascidian Ciona intestinalis occurs by epimorphosis involving the formation of a blastema of proliferating cells. Despite the longstanding use of Ciona as a model in molecular developmental biology, regeneration in this system has not been previously explored by molecular analysis. Here we have employed microarray analysis and quantitative real time RT-PCR to identify genes with differential expression profiles during OS regeneration. The majority of differentially expressed genes were downregulated during OS regeneration, suggesting roles in normal growth and homeostasis. However, a subset of differentially expressed genes was upregulated in the regenerating OS, suggesting functional roles during regeneration. Among the upregulated genes were key members of the Notch signaling pathway, including those encoding the delta and jagged ligands, two fringe modulators, and to a lesser extent the notch receptor. In situ hybridization showed a complementary pattern of delta1 and notch gene expression in the blastema of the regenerating OS. Chemical inhibition of the Notch signaling pathway reduced the levels of cell proliferation in the branchial sac, a stem cell niche that contributes progenitor cells to the regenerating OS, and in the OS regeneration blastema, where siphon muscle fibers eventually re-differentiate. Chemical inhibition also prevented the replacement of oral siphon pigment organs, sensory receptors rimming the entrance of the OS, and siphon muscle fibers, but had no effects on the formation of the wound epidermis. Since Notch signaling is involved in the maintenance of proliferative activity in both the Ciona and vertebrate regeneration blastema, the results suggest a conserved evolutionary role of this signaling pathway in chordate regeneration. The genes identified in this investigation provide the foundation for future molecular analysis of OS regeneration., (Copyright © 2015 Elsevier Inc. All rights reserved.)
- Published
- 2015
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31. Genome editing using TALENs in blind Mexican Cavefish, Astyanax mexicanus.
- Author
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Ma L, Jeffery WR, Essner JJ, and Kowalko JE
- Subjects
- Animals, Animals, Genetically Modified, Biological Evolution, Caves, Characidae classification, Characidae physiology, Genome, Mutation, Quantitative Trait Loci, Albinism, Oculocutaneous genetics, Characidae genetics, Deoxyribonucleases metabolism, Fish Proteins genetics, Genetic Engineering methods, Receptor, Melanocortin, Type 1 genetics
- Abstract
Astyanax mexicanus, a teleost fish that exists in a river-dwelling surface form and multiple cave-dwelling forms, is an excellent system for studying the genetic basis of evolution. Cavefish populations, which independently evolved from surface fish ancestors multiple times, have evolved a number of morphological and behavioral traits. Quantitative trait loci (QTL) analyses have been performed to identify the genetic basis of many of these traits. These studies, combined with recent sequencing of the genome, provide a unique opportunity to identify candidate genes for these cave-specific traits. However, tools to test the requirement of these genes must be established to evaluate the role of candidate genes in generating cave-specific traits. To address this need, we designed transcription activator-like effector nucleases (TALENs) to target two genes that contain coding changes in cavefish relative to surface fish and map to the same location as QTL for pigmentation, oculocutaneous albinism 2 (oca2) and melanocortin 1 receptor (mc1r). We found that surface fish genes can be mutated using this method. TALEN-induced mutations in oca2 result in mosaic loss of melanin pigmentation visible as albino patches in F0 founder fish, suggesting biallelic gene mutations in F0s and allowing us to evaluate the role of this gene in pigmentation. The pigment cells in the albino patches can produce melanin upon treatment with L-DOPA, behaving similarly to pigment cells in albino cavefish and providing additional evidence that oca2 is the gene within the QTL responsible for albinism in cavefish. This technology has the potential to introduce a powerful tool for studying the role of candidate genes responsible for the evolution of cavefish traits.
- Published
- 2015
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32. Distinct genetic architecture underlies the emergence of sleep loss and prey-seeking behavior in the Mexican cavefish.
- Author
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Yoshizawa M, Robinson BG, Duboué ER, Masek P, Jaggard JB, O'Quin KE, Borowsky RL, Jeffery WR, and Keene AC
- Subjects
- Animals, Biological Evolution, Crosses, Genetic, Female, Hybridization, Genetic, Locomotion, Male, Mexico, Quantitative Trait Loci genetics, Sleep, Vibration, Caves, Characidae genetics, Predatory Behavior physiology, Sleep Deprivation genetics
- Abstract
Background: Sleep is characterized by extended periods of quiescence and reduced responsiveness to sensory stimuli. Animals ranging from insects to mammals adapt to environments with limited food by suppressing sleep and enhancing their response to food cues, yet little is known about the genetic and evolutionary relationship between these processes. The blind Mexican cavefish, Astyanax mexicanus is a powerful model for elucidating the genetic mechanisms underlying behavioral evolution. A. mexicanus comprises an extant ancestral-type surface dwelling morph and at least five independently evolved cave populations. Evolutionary convergence on sleep loss and vibration attraction behavior, which is involved in prey seeking, have been documented in cavefish raising the possibility that enhanced sensory responsiveness underlies changes in sleep., Results: We established a system to study sleep and vibration attraction behavior in adult A. mexicanus and used high coverage quantitative trait loci (QTL) mapping to investigate the functional and evolutionary relationship between these traits. Analysis of surface-cave F2 hybrid fish and an outbred cave population indicates that independent genetic factors underlie changes in sleep/locomotor activity and vibration attraction behavior. High-coverage QTL mapping with genotyping-by-sequencing technology identify two novel QTL intervals that associate with locomotor activity and include the narcolepsy-associated tp53 regulating kinase. These QTLs represent the first genomic localization of locomotor activity in cavefish and are distinct from two QTLs previously identified as associating with vibration attraction behavior., Conclusions: Taken together, these results localize genomic regions underlying sleep/locomotor and sensory changes in cavefish populations and provide evidence that sleep loss evolved independently from enhanced sensory responsiveness.
- Published
- 2015
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33. Distal Regeneration Involves the Age Dependent Activity of Branchial Sac Stem Cells in the Ascidian Ciona intestinalis .
- Author
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Jeffery WR
- Abstract
Tunicates have high capacities for regeneration but the underlying mechanisms and their relationship to life cycle progression are not well understood. Here we investigate the regeneration of distal structures in the ascidian tunicate Ciona intestinalis . Analysis of regenerative potential along the proximal-distal body axis indicated that distal organs, such as the siphons, their pigmented sensory organs, and the neural complex, could only be replaced from body fragments containing the branchial sac. Distal regeneration involves the formation of a blastema composed of cells that undergo cell proliferation prior to differentiation and cells that differentiate without cell proliferation. Both cell types originate in the branchial sac and appear in the blastema at different times after distal injury. Whereas the branchial sac stem cells are present in young animals, they are depleted in old animals that have lost their regeneration capacity. Thus Ciona adults contain a population of age-related stem cells located in the branchial sac that are a source of precursors for distal body regeneration.
- Published
- 2015
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34. Closing the wounds: one hundred and twenty five years of regenerative biology in the ascidian Ciona intestinalis.
- Author
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Jeffery WR
- Subjects
- Aging physiology, Animals, Biological Evolution, Central Nervous System physiology, Ciona intestinalis physiology, Regeneration physiology
- Abstract
This year marks the 125th anniversary of the beginning of regeneration research in the ascidian Ciona intestinalis. A brief note was published in 1891, reporting the regeneration of the Ciona neural complex and siphons. This launched an active period of Ciona regeneration research culminating in the demonstration of partial body regeneration: the ability of proximal body parts to regenerate distal ones, but not vice versa. In a process resembling regeneration, wounds in the siphon tube were discovered to result in the formation of an ectopic siphon. Ciona regeneration research then lapsed into a period of relative inactivity after the purported demonstration of the inheritance of acquired characters using siphon regeneration as a model. Around the turn of the present century, Ciona regeneration research experienced a new blossoming. The current studies established the morphological and physiological integrity of the regeneration process and its resemblance to ontogeny. They also determined some of the cell types responsible for tissue and organ replacement and their sources in the body. Finally, they showed that regenerative capacity is reduced with age. Many other aspects of regeneration now can be studied at the mechanistic level because of the extensive molecular tools available in Ciona., (© 2014 Wiley Periodicals, Inc.)
- Published
- 2015
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35. Regeneration, Stem Cells, and Aging in the Tunicate Ciona: Insights from the Oral Siphon.
- Author
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Jeffery WR
- Subjects
- Animals, Ciona intestinalis growth & development, Life Cycle Stages physiology, Stem Cells cytology, Aging physiology, Ciona intestinalis cytology, Ciona intestinalis physiology, Regeneration physiology, Stem Cells physiology
- Abstract
Regeneration studies in the tunicate Ciona intestinalis have recently been focused on the potential of adult stem cells to replace injured tissues and organs during the adult life cycle using the oral siphon (OS) as a model. The OS has oral siphon pigment organs (OPOs) along its rim and an underlying network of muscle fibers in its tube. Different regeneration processes are triggered by OS amputation at the tip, along the tube, or at the base. One process involves the replacement of OPOs without new cell division by direct differentiation of locally deployed stem cells or stem cells that migrate from the branchial sac. Another process involves blastema formation by the migration of progenitor cells produced from branchial sac stem cells. The capacity for complete and accurate OS regeneration declines continuously during the adult life cycle. Finally, after an age threshold is reached, OS regeneration ceases in old animals. The loss of regeneration capacity in old animals involves the depletion of stem cells in the branchial sac, the inability of branchial sac progenitor cells to migrate to the sites of regeneration, and defective oral pigment organ replacement. The significance of the OS model for studying regeneration, stem cells, and aging will be enhanced by the application of molecular methods., (Copyright © 2015 Elsevier Inc. All rights reserved.)
- Published
- 2015
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36. The Tunicate CIONA : A Model System for Understanding the Relationship Between Regeneration and Aging.
- Author
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Jeffery WR
- Abstract
The use of the tunicate Ciona intestinalis as a model system to study the relationship between regeneration and aging is reviewed. Ciona has powerful regeneration capacities, which fade with age. Some additional benefits are-, a relatively short life span, the ability to study regeneration in vitro , the close phylogenetic relationship between tunicates and vertebrates, and the host of molecular tools already established in this system. The neural complex (NC), the oral siphon (OS), and the oral siphon pigment organs (OPO) have high capacities for regeneration. However, these organs show an inverse relationship between rate of regeneration and age. The ability to regenerate a complete OS disappears in the oldest animals of a natural population, probably due to the inability to form a blastema at the wound site. Effects on blastema formation could also be involved in the reduction of NC regeneration capacity. The fidelity of OPO restoration is also compromised by excess differentiation of precursor cells in local siphon niches in the oldest animals. The Ciona model provides a pathway to understand the molecular basis of these phenomena.
- Published
- 2015
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37. The cavefish genome reveals candidate genes for eye loss.
- Author
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McGaugh SE, Gross JB, Aken B, Blin M, Borowsky R, Chalopin D, Hinaux H, Jeffery WR, Keene A, Ma L, Minx P, Murphy D, O'Quin KE, Rétaux S, Rohner N, Searle SM, Stahl BA, Tabin C, Volff JN, Yoshizawa M, and Warren WC
- Subjects
- Animals, Apoptosis, Characidae embryology, DNA Transposable Elements, Environment, Fish Proteins genetics, Gene Expression Profiling, Genome, In Situ Hybridization, Molecular Sequence Data, Phenotype, Quantitative Trait Loci, Retina physiology, Characidae genetics, Evolution, Molecular, Eye embryology, Gene Expression Regulation, Developmental, Retina embryology
- Abstract
Natural populations subjected to strong environmental selection pressures offer a window into the genetic underpinnings of evolutionary change. Cavefish populations, Astyanax mexicanus (Teleostei: Characiphysi), exhibit repeated, independent evolution for a variety of traits including eye degeneration, pigment loss, increased size and number of taste buds and mechanosensory organs, and shifts in many behavioural traits. Surface and cave forms are interfertile making this system amenable to genetic interrogation; however, lack of a reference genome has hampered efforts to identify genes responsible for changes in cave forms of A. mexicanus. Here we present the first de novo genome assembly for Astyanax mexicanus cavefish, contrast repeat elements to other teleost genomes, identify candidate genes underlying quantitative trait loci (QTL), and assay these candidate genes for potential functional and expression differences. We expect the cavefish genome to advance understanding of the evolutionary process, as well as, analogous human disease including retinal dysfunction.
- Published
- 2014
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38. Enhanced prey capture skills in Astyanax cavefish larvae are independent from eye loss.
- Author
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Espinasa L, Bibliowicz J, Jeffery WR, and Rétaux S
- Abstract
Background: Enhanced food-finding efficiency is an obvious adaptive response to cave environments. Here, we have compared the food-finding abilities of Astyanax surface fish and blind cavefish young larvae in their first month of life, in the dark., Results: Our results show that enhanced prey capture skills of cavefish are already in effect in fry soon after the yolk is depleted and the young larvae must find food for themselves. Moreover, using prey capture competition assays on surface fish fry with lensectomies, we showed that eye-dependent developmental processes are not the main determinant for enhanced prey capture skills. Finally, using F2 hybrid larvae resulting from crosses between surface fish and cavefish, we found that reduced eyes do not confer a selective advantage for prey capture by fry in the dark., Conclusion: We discuss these data with regards to our current developmental and genetic understanding of cavefish morphological and behavioral evolution.
- Published
- 2014
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39. The role of a lens survival pathway including sox2 and αA-crystallin in the evolution of cavefish eye degeneration.
- Author
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Ma L, Parkhurst A, and Jeffery WR
- Abstract
Background: The teleost Astyanax mexicanus is a single species consisting of eyed surface-dwelling (surface fish) and blind cave-dwelling (cavefish) morphs. Cavefish eyes are lost through apoptosis of the lens, which in turn promotes the degeneration of other optic tissues. The αA-crystallin (αA-crys) gene is strongly downregulated in the cavefish lens and is located in a genomic region (QTL) responsible for eye loss. Therefore, αA-crys has been proposed as a candidate for regulating cavefish eye degeneration. The purpose of this study was to determine the mechanism of αA-crys downregulation and its role in cavefish eye degeneration., Results: The involvement of αA-crys in eye degeneration was confirmed by knocking down its expression in surface fish, which led to apoptosis of the lens. The underlying reason for αA-crys downregulation in cavefish was investigated by comparing genomic αA-crys DNA sequences in surface fish and cavefish, however, no obvious cis-regulatory factors were discovered. Furthermore, the cavefish αA-crys allele is expressed in surface fish x cavefish F1 hybrids, indicating that evolutionary changes in upstream genes are most likely responsible for αA-crys downregulation. In other species, Sox2 is one of the transcription factors that regulate lens crystallin genes during eye development. Determination of sox2 expression patterns during surface fish and cavefish development showed that sox2 is specifically downregulated in the cavefish lens. The upstream regulatory function of Sox2 was demonstrated by knockdown in surface fish, which abolished αA-crys expression and induced lens apoptosis., Conclusions: The results suggest that αA-crys is required for normal eye development in cavefish via suppression of lens apoptosis. The regulatory changes involved in αA-crys downregulation in cavefish are in trans-acting factors rather than cis-acting mutations in the αA-crys gene. Therefore, αA-crys is unlikely to be the mutated gene(s) associated with an Astyanax eye QTL. The results reveal a genetic pathway leading from sox2 to αA-crys that is required for survival of the lens in Astyanax surface fish. Defects in this pathway may be involved in lens apoptosis and thus a cause of cavefish eye degeneration.
- Published
- 2014
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40. The sensitivity of lateral line receptors and their role in the behavior of Mexican blind cavefish (Astyanax mexicanus).
- Author
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Yoshizawa M, Jeffery WR, van Netten SM, and McHenry MJ
- Subjects
- Animals, Appetitive Behavior, Biological Evolution, Caves, Characidae anatomy & histology, Characidae genetics, Lateral Line System cytology, Mechanoreceptors cytology, Mexico, Microspheres, Models, Biological, Optical Imaging, Vibration, Behavior, Animal physiology, Characidae physiology, Lateral Line System physiology, Mechanoreceptors physiology
- Abstract
The characid fish species Astyanax mexicanus offers a classic comparative model for the evolution of sensory systems. Populations of this species evolved in caves and became blind while others remained in streams (i.e. surface fish) and retained a functional visual system. The flow-sensitive lateral line receptors, called superficial neuromasts, are more numerous in cavefish than in surface fish, but it is unclear whether individual neuromasts differ in sensitivity between these populations. The aims of this study were to determine whether the neuromasts in cavefish impart enhanced sensitivity relative to surface fish and to test whether this aids their ability to sense flow in the absence of visual input. Sensitivity was assessed by modeling the mechanics and hydrodynamics of a flow stimulus. This model required that we measure the dimensions of the transparent cupula of a neuromast, which was visualized with fluorescent microspheres. We found that neuromasts within the eye orbit and in the suborbital region were larger and consequently about twice as sensitive in small adult cavefish as in surface fish. Behavioral experiments found that these cavefish, but not surface fish, were attracted to a 35 Hz flow stimulus. These results support the hypothesis that the large superficial neuromasts of small cavefish aid in flow sensing. We conclude that the morphology of the lateral line could have evolved in cavefish to permit foraging in a cave environment.
- Published
- 2014
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41. Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish.
- Author
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Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, Borowsky RL, Lindquist S, and Tabin CJ
- Subjects
- Animals, Characidae genetics, Ecosystem, Genetic Variation, HSP90 Heat-Shock Proteins antagonists & inhibitors, HSP90 Heat-Shock Proteins metabolism, Macrolides pharmacology, Organ Size, Phenotype, Characidae growth & development, Evolution, Molecular, Eye anatomy & histology, HSP90 Heat-Shock Proteins genetics
- Abstract
In the process of morphological evolution, the extent to which cryptic, preexisting variation provides a substrate for natural selection has been controversial. We provide evidence that heat shock protein 90 (HSP90) phenotypically masks standing eye-size variation in surface populations of the cavefish Astyanax mexicanus. This variation is exposed by HSP90 inhibition and can be selected for, ultimately yielding a reduced-eye phenotype even in the presence of full HSP90 activity. Raising surface fish under conditions found in caves taxes the HSP90 system, unmasking the same phenotypic variation as does direct inhibition of HSP90. These results suggest that cryptic variation played a role in the evolution of eye loss in cavefish and provide the first evidence for HSP90 as a capacitor for morphological evolution in a natural setting.
- Published
- 2013
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42. A potential benefit of albinism in Astyanax cavefish: downregulation of the oca2 gene increases tyrosine and catecholamine levels as an alternative to melanin synthesis.
- Author
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Bilandžija H, Ma L, Parkhurst A, and Jeffery WR
- Subjects
- Animals, Base Sequence, Brain metabolism, Chromatography, High Pressure Liquid, DNA Primers, Enzyme-Linked Immunosorbent Assay, In Situ Hybridization, Kidney, Polymerase Chain Reaction, Albinism genetics, Albinism, Oculocutaneous genetics, Catecholamines metabolism, Down-Regulation, Fishes genetics, Melanins biosynthesis, Tyrosine metabolism
- Abstract
Albinism, the loss of melanin pigmentation, has evolved in a diverse variety of cave animals but the responsible evolutionary mechanisms are unknown. In Astyanax mexicanus, which has a pigmented surface dwelling form (surface fish) and several albino cave-dwelling forms (cavefish), albinism is caused by loss of function mutations in the oca2 gene, which operates during the first step of the melanin synthesis pathway. In addition to albinism, cavefish have evolved differences in behavior, including feeding and sleep, which are under the control of the catecholamine system. The catecholamine and melanin synthesis pathways diverge after beginning with the same substrate, L-tyrosine. Here we describe a novel relationship between the catecholamine and melanin synthesis pathways in Astyanax. Our results show significant increases in L-tyrosine, dopamine, and norepinephrine in pre-feeding larvae and adult brains of Pachón cavefish relative to surface fish. In addition, norepinephrine is elevated in cavefish adult kidneys, which contain the teleost homologs of catecholamine synthesizing adrenal cells. We further show that the oca2 gene is expressed during surface fish development but is downregulated in cavefish embryos. A key finding is that knockdown of oca2 expression in surface fish embryos delays the development of pigmented melanophores and simultaneously increases L-tyrosine and dopamine. We conclude that a potential evolutionary benefit of albinism in Astyanax cavefish may be to provide surplus L-tyrosine as a precursor for the elevated catecholamine synthesis pathway, which could be important for adaptation to the challenging cave environment.
- Published
- 2013
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43. Convergence in feeding posture occurs through different genetic loci in independently evolved cave populations of Astyanax mexicanus.
- Author
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Kowalko JE, Rohner N, Linden TA, Rompani SB, Warren WC, Borowsky R, Tabin CJ, Jeffery WR, and Yoshizawa M
- Subjects
- Animals, Behavior, Animal physiology, Caves, Characidae physiology, Evolution, Molecular, Feeding Behavior physiology, Genetic Loci physiology
- Abstract
When an organism colonizes a new environment, it needs to adapt both morphologically and behaviorally to survive and thrive. Although recent progress has been made in understanding the genetic architecture underlying morphological evolution, behavioral evolution is poorly understood. Here, we use the Mexican cavefish, Astyanax mexicanus, to study the genetic basis for convergent evolution of feeding posture. When river-dwelling surface fish became entrapped in the caves, they were confronted with dramatic changes in the availability and type of food source and in their ability to perceive it. In this setting, multiple independent populations of cavefish exhibit an altered feeding posture compared with their ancestral surface forms. We determined that this behavioral change in feeding posture is not due to changes in cranial facial morphology, body depth, or to take advantage of the expansion in the number of taste buds. Quantitative genetic analysis demonstrates that two different cave populations have evolved similar feeding postures through a small number of genetic changes, some of which appear to be distinct. This work indicates that independently evolved populations of cavefish can evolve the same behavioral traits to adapt to similar environmental challenges by modifying different sets of genes.
- Published
- 2013
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44. Loss of schooling behavior in cavefish through sight-dependent and sight-independent mechanisms.
- Author
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Kowalko JE, Rohner N, Rompani SB, Peterson BK, Linden TA, Yoshizawa M, Kay EH, Weber J, Hoekstra HE, Jeffery WR, Borowsky R, and Tabin CJ
- Subjects
- Adaptation, Physiological genetics, Animals, Behavior, Animal drug effects, Biological Evolution, Brain metabolism, Caves, Characidae genetics, Dopamine metabolism, Fluoxetine pharmacology, Lens, Crystalline physiology, Monoamine Oxidase Inhibitors pharmacology, Neurotransmitter Agents antagonists & inhibitors, Quantitative Trait Loci genetics, Selection, Genetic, Selegiline pharmacology, Serotonin metabolism, Selective Serotonin Reuptake Inhibitors pharmacology, Adaptation, Physiological physiology, Behavior, Animal physiology, Characidae physiology, Lateral Line System physiology, Vision, Ocular physiology
- Abstract
Background: Surface populations of Astyanax mexicanus, living in rivers like their common ancestors, school, while several, independently derived cave populations of the same species have lost schooling behavior., Results: We quantify schooling behavior in individual A. mexicanus and identify quantitative trait loci (QTL) for this trait. We find that the evolutionary modulation of schooling has both vision-dependent and -independent components. We also quantify differences in the lateral line and vision between cavefish and surface fish and relate these differences to the evolutionary loss of schooling behavior. We provide evidence that a monoamine neurotransmitter may have played a role in the evolution of schooling behavior., Conclusions: We find that vision is essential for schooling tendency in A. mexicanus, while the lateral line has a small effect on this behavior. Schooling behavior in A. mexicanus has evolved both through changes in sensory systems and through changes in genetic loci that likely act downstream of sensory inputs., (Copyright © 2013 Elsevier Ltd. All rights reserved.)
- Published
- 2013
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- View/download PDF
45. Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish: response to Borowsky (2013).
- Author
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Yoshizawa M, O'Quin KE, and Jeffery WR
- Subjects
- Animals, Female, Male, Adaptation, Physiological, Behavior, Animal physiology, Biological Evolution, Blindness physiopathology, Eye physiopathology, Fishes physiology, Sensory Receptor Cells physiology
- Abstract
Vibration attraction behavior (VAB) is the swimming of fish toward an oscillating object, a behavior that is likely adaptive because it increases foraging efficiency in darkness. VAB is seen in a small proportion of Astyanax surface-dwelling populations (surface fish) but is pronounced in cave-dwelling populations (cavefish). In a recent study, we identified two quantitative trait loci for VAB on Astyanax linkage groups 2 and 17. We also demonstrated that a small population of superficial neuromast sensors located within the eye orbit (EO SN) facilitate VAB, and two quantitative trait loci (QTL) were identified for EO SN that were congruent with those for VAB. Finally, we showed that both VAB and EO SN are negatively correlated with eye size, and that two (of several) QTL for eye size overlap VAB and EO SN QTLs. From these results, we concluded that the adaptive evolution of VAB and EO SN has contributed to the indirect loss of eyes in cavefish, either as a result of pleiotropy or tight physical linkage of the mutations underlying these traits. In a subsequent commentary, Borowsky argues that there is poor experimental support for our conclusions. Specifically, Borowsky states that: (1) linkage groups (LGs) 2 and 17 harbor QTL for many traits and, therefore, no evidence exists for an exclusive interaction among the overlapping VAB, EO SN and eye size QTL; (2) some of the QTL we identified are too broad (>20 cM) to support the hypothesis of correlated evolution due to pleiotropy or hitchhiking; and (3) VAB is unnecessary to explain the indirect evolution of eye-loss since the negative polarity of numerous eye QTL is consistent with direct selection against eyes. Borowsky further argues that (4) it is difficult to envision an evolutionary scenario whereby VAB and EO SN drive eye loss, since the eyes must first be reduced in order to increase the number of EO SN and, therefore, VAB. In this response, we explain why the evidence of one trait influencing eye reduction is stronger for VAB than other traits, and provide further support for a scenario whereby elaboration of VAB in surface fish may precede complete eye-loss.
- Published
- 2013
- Full Text
- View/download PDF
46. QTL clustering as a mechanism for rapid multi-trait evolution.
- Author
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Yoshizawa M, O'Quin KE, and Jeffery WR
- Abstract
Cave-dwelling animals exhibit remarkable convergence in multiple cave-related traits, yet the genetic mechanisms responsible for the evolution and integration of many such traits remain unclear. Astyanax mexicanus is a model cave-dwelling fish with sighted surface-dwelling (surface fish) and blind cave-dwelling (cavefish) forms. Using a genetic cross between these morphs, we discovered significant correlations among several cave-related traits, including reduced eyes, increased superficial neuromast receptors located within the eye orbit (EO SN) and a vibration-attraction behavior (VAB) that facilitates foraging in darkness. Furthermore, we discovered that the quantitative trait loci (QTL) underlying these traits are clustered within the Astyanax genome. Following an ablation experiment that demonstrated that the EO SN contribute to VAB, we concluded that the adaptive evolution of VAB and EO SN has likely contributed to eye loss in cavefish. In this addendum, we further discuss the possible role of multi-trait QTL clustering in facilitating rapid adaptation.
- Published
- 2013
- Full Text
- View/download PDF
47. Quantitative genetic analysis of retinal degeneration in the blind cavefish Astyanax mexicanus.
- Author
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O'Quin KE, Yoshizawa M, Doshi P, and Jeffery WR
- Subjects
- Alleles, Animals, Biological Evolution, Caves, Chromosome Mapping, Crosses, Genetic, Darkness, Genetic Linkage, Genome, Retina pathology, Retinal Degeneration pathology, Blindness genetics, Characidae genetics, Morphogenesis genetics, Quantitative Trait Loci, Retina metabolism, Retinal Degeneration genetics
- Abstract
The retina is the light-sensitive tissue of the eye that facilitates vision. Mutations within genes affecting eye development and retinal function cause a host of degenerative visual diseases, including retinitis pigmentosa and anophthalmia/microphthalmia. The characin fish Astyanax mexicanus includes both eyed (surface fish) and eyeless (cavefish) morphs that initially develop eyes with normal retina; however, early in development, the eyes of cavefish degenerate. Since both surface and cave morphs are members of the same species, they serve as excellent evolutionary mutant models with which to identify genes causing retinal degeneration. In this study, we crossed the eyed and eyeless forms of A. mexicanus and quantified the thickness of individual retinal layers among 115 F(2) hybrid progeny. We used next generation sequencing (RAD-seq) and microsatellite mapping to construct a dense genetic map of the Astyanax genome, scan for quantitative trait loci (QTL) affecting retinal thickness, and identify candidate genes within these QTL regions. The map we constructed for Astyanax includes nearly 700 markers assembled into 25 linkage groups. Based on our scans with this map, we identified four QTL, one each associated with the thickness of the ganglion, inner nuclear, outer plexiform, and outer nuclear layers of the retina. For all but one QTL, cavefish alleles resulted in a clear reduction in the thickness of the affected layer. Comparative mapping of genetic markers within each QTL revealed that each QTL corresponds to an approximately 35 Mb region of the zebrafish genome. Within each region, we identified several candidate genes associated with the function of each affected retinal layer. Our study is the first to examine Astyanax retinal degeneration in the context of QTL mapping. The regions we identify serve as a starting point for future studies on the genetics of retinal degeneration and eye disease using the evolutionary mutant model Astyanax.
- Published
- 2013
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48. De novo sequencing of Astyanax mexicanus surface fish and Pachón cavefish transcriptomes reveals enrichment of mutations in cavefish putative eye genes.
- Author
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Hinaux H, Poulain J, Da Silva C, Noirot C, Jeffery WR, Casane D, and Rétaux S
- Subjects
- Amino Acid Sequence, Animals, Base Sequence, Codon, Terminator genetics, Fish Proteins chemistry, Fish Proteins genetics, Gene Expression Regulation, Gene Library, Molecular Sequence Annotation, Molecular Sequence Data, Polymorphism, Genetic, RNA, Messenger genetics, RNA, Messenger metabolism, Caves, Characiformes genetics, Eye metabolism, Mutation genetics, Sequence Analysis, DNA methods, Transcriptome genetics
- Abstract
Astyanax mexicanus, a teleost species with surface dwelling (surface fish) and cave adapted (cavefish) morphs, is an important model system in evolutionary developmental biology (evodevo). Astyanax cavefish differ from surface fish in numerous traits, including the enhancement of non-visual sensory systems, and the loss of eyes and pigmentation. The genetic bases for these differences are not fully understood as genomic and transcriptomic data are lacking. We here present de novo transcriptome sequencing of embryonic and larval stages of a surface fish population and a cavefish population originating from the Pachón cave using the Sanger method. This effort represents the first large scale sequence and clone resource for the Astyanax research community. The analysis of these sequences show low levels of polymorphism in cavefish compared to surface fish, confirming previous studies on a small number of genes. A high proportion of the genes mutated in cavefish are known to be expressed in the zebrafish visual system. Such a high number of mutations in cavefish putative eye genes may be explained by relaxed selection for vision during the evolution in the absence of light. Based on these sequence differences, we provide a list of 11 genes that are potential candidates for having a role in cavefish visual system degeneration.
- Published
- 2013
- Full Text
- View/download PDF
49. Evolution of an adaptive behavior and its sensory receptors promotes eye regression in blind cavefish.
- Author
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Yoshizawa M, Yamamoto Y, O'Quin KE, and Jeffery WR
- Subjects
- Animals, Cell Count, Chromosome Mapping, Crosses, Genetic, Eye pathology, Female, Hedgehog Proteins metabolism, Lod Score, Male, Models, Biological, Orbit pathology, Organ Size, Quantitative Trait Loci genetics, Quantitative Trait, Heritable, Vibration, Adaptation, Physiological, Behavior, Animal physiology, Biological Evolution, Blindness physiopathology, Eye physiopathology, Fishes physiology, Sensory Receptor Cells physiology
- Abstract
Background: How and why animals lose eyesight during adaptation to the dark and food-limited cave environment has puzzled biologists since the time of Darwin. More recently, several different adaptive hypotheses have been proposed to explain eye degeneration based on studies in the teleost Astyanax mexicanus, which consists of blind cave-dwelling (cavefish) and sighted surface-dwelling (surface fish) forms. One of these hypotheses is that eye regression is the result of indirect selection for constructive characters that are negatively linked to eye development through the pleiotropic effects of Sonic Hedgehog (SHH) signaling. However, subsequent genetic analyses suggested that other mechanisms also contribute to eye regression in Astyanax cavefish. Here, we introduce a new approach to this problem by investigating the phenotypic and genetic relationships between a suite of non-visual constructive traits and eye regression., Results: Using quantitative genetic analysis of crosses between surface fish, the Pachón cavefish population and their hybrid progeny, we show that the adaptive vibration attraction behavior (VAB) and its sensory receptors, superficial neuromasts (SN) specifically found within the cavefish eye orbit (EO), are genetically correlated with reduced eye size. The quantitative trait loci (QTL) for these three traits form two clusters of congruent or overlapping QTL on Astyanax linkage groups (LG) 2 and 17, but not at the shh locus on LG 13. Ablation of EO SN in cavefish demonstrated a major role for these sensory receptors in VAB expression. Furthermore, experimental induction of eye regression in surface fish via shh overexpression showed that the absence of eyes was insufficient to promote the appearance of VAB or EO SN., Conclusions: We conclude that natural selection for the enhancement of VAB and EO SN indirectly promotes eye regression in the Pachón cavefish population through an antagonistic relationship involving genetic linkage or pleiotropy among the genetic factors underlying these traits. This study demonstrates a trade-off between the evolution of a non-visual sensory system and eye regression during the adaptive evolution of Astyanax to the cave environment.
- Published
- 2012
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50. Evolution and development in cave animals: from fish to crustaceans.
- Author
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Protas M and Jeffery WR
- Subjects
- Animals, Crustacea genetics, Crustacea metabolism, Eye growth & development, Eye metabolism, Fishes genetics, Fishes metabolism, Genome, Hedgehog Proteins metabolism, Models, Animal, Biological Evolution, Crustacea growth & development, Fishes growth & development
- Abstract
Cave animals are excellent models to study the general principles of evolution as well as the mechanisms of adaptation to a novel environment: the perpetual darkness of caves. In this article, two of the major model systems used to study the evolution and development (evo-devo) of cave animals are described: the teleost fish Astyanax mexicanus and the isopod crustacean Asellus aquaticus. The ways in which these animals match the major attributes expected of an evo-devo cave animal model system are described. For both species, we enumerate the regressive and constructive troglomorphic traits that have evolved during their adaptation to cave life, the developmental and genetic basis of these traits, the possible evolutionary forces responsible for them, and potential new areas in which these model systems could be used for further exploration of the evolution of cave animals. Furthermore, we compare the two model cave animals to investigate the mechanisms of troglomorphic evolution. Finally, we propose a few other cave animal systems that would be suitable for development as additional models to obtain a more comprehensive understanding of the developmental and genetic mechanisms involved in troglomorphic evolution.
- Published
- 2012
- Full Text
- View/download PDF
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