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      Cranial asymmetry arises later in the life history of the blind Mexican cavefish, Astyanax mexicanus

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          Abstract

          As a consequence of adaptation to the cave environment, the blind Mexican cavefish, Astyanax mexicanus, has evolved several cranial aberrations including changes to bone sizes, shapes and presence of numerous lateral asymmetries. Prior studies of cranial asymmetry in cavefish focused strictly on adult specimens. Thus, the extent to which these asymmetries emerge in adulthood, or earlier in the life history of cavefish, was unknown. We performed a geometric morphometric analysis of shape variation in the chondrocranium and osteocranium across life history in two distinct cavefish populations and surface-dwelling fish. The cartilaginous skull in juveniles was bilaterally symmetric and chondrocranial shape was conserved in all three populations. In contrast, bony skull shapes segregated into significantly distinct groups in adults. Cavefish demonstrated significant asymmetry for the bones surrounding the collapsed eye orbit, and the opercle bone posterior to the eye orbit. Interestingly, we discovered that cavefish also exhibit directional “bends” in skull shape, almost always biased to the left. In sum, this work reveals that asymmetric craniofacial aberrations emerge later in the cavefish life history. These abnormalities may mirror asymmetries in the lateral line sensory system, reflect a ‘handedness’ in cavefish swimming behavior, or evolve through neutral processes.

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          Most cited references63

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          Regressive evolution in Astyanax cavefish.

          A diverse group of animals, including members of most major phyla, have adapted to life in the perpetual darkness of caves. These animals are united by the convergence of two regressive phenotypes, loss of eyes and pigmentation. The mechanisms of regressive evolution are poorly understood. The teleost Astyanax mexicanus is of special significance in studies of regressive evolution in cave animals. This species includes an ancestral surface dwelling form and many con-specific cave-dwelling forms, some of which have evolved their recessive phenotypes independently. Recent advances in Astyanax development and genetics have provided new information about how eyes and pigment are lost during cavefish evolution; namely, they have revealed some of the molecular and cellular mechanisms involved in trait modification, the number and identity of the underlying genes and mutations, the molecular basis of parallel evolution, and the evolutionary forces driving adaptation to the cave environment.
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            Frequency-dependent natural selection in the handedness of scale-eating cichlid fish.

            Frequency-dependent natural selection has been cited as a mechanism for maintaining polymorphisms in biological populations, although the process has not been documented conclusively in field study. Here, it is demonstrated that the direction of mouth-opening (either left-handed or right-handed) in scale-eating cichlid fish of Lake Tanganyika is determined on the basis of simple genetics and that the abundance of individuals with left- or right-handedness depends on frequency-dependent natural selection. Attacking from behind, right-handed individuals snatched scales from the prey's left flank and left-handed ones from the right flank. Within a given population, the frequency of the two phenotypes oscillated around unity. This phenomenon was effected through frequency-dependent selection exerted by the prey's alertness. Thus, individuals of the rare phenotype had more success as predators than those of the more common phenotype.
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              Cavefish as a model system in evolutionary developmental biology.

              The Mexican tetra Astyanax mexicanus has many of the favorable attributes that have made the zebrafish a model system in developmental biology. The existence of eyed surface (surface fish) and blind cave (cavefish) dwelling forms in Astyanax also provides an attractive system for studying the evolution of developmental mechanisms. The polarity of evolutionary changes and the environmental conditions leading to the cavefish phenotype are known with certainty, and several different cavefish populations have evolved constructive and regressive changes independently. The constructive changes include enhancement of the feeding apparatus (jaws, taste buds, and teeth) and the mechanosensory system of cranial neuromasts. The homeobox gene Prox 1, which is expressed in the expanded taste buds and cranial neuromasts, is one of the genes involved in the constructive changes in sensory organ development. The regressive changes include loss of pigmentation and eye degeneration. Although adult cavefish lack functional eyes, small eye primordia are formed during embryogenesis, which later arrest in development, degenerate, and sink into the orbit. Apoptosis and lens signaling to other eye parts, such as the cornea, iris, and retina, result in the arrest of eye development and ultimate optic degeneration. Accordingly, an eye with restored cornea, iris, and retinal photoreceptor cells is formed when a surface fish lens is transplanted into a cavefish optic cup, indicating that cavefish optic tissues have conserved the ability to respond to lens signaling. Genetic analysis indicates that multiple genes regulate eye degeneration, and molecular studies suggest that Pax6 may be one of the genes controlling cavefish eye degeneration. Further studies of the Astyanax system will contribute to our understanding of the evolution of developmental mechanisms in vertebrates.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 May 2017
                2017
                : 12
                : 5
                : e0177419
                Affiliations
                [001]Department of Biological Sciences, University of Cincinnati, Cincinnati, Ohio, United States of America
                Laboratoire Arago, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: AKP JBG.

                • Data curation: AKP.

                • Formal analysis: AKP EMD SAK.

                • Funding acquisition: JBG.

                • Investigation: AKP EMD SAK.

                • Methodology: AKP JBG.

                • Project administration: AKP JBG.

                • Resources: AKP JBG.

                • Supervision: AKP JBG.

                • Validation: AKP EMD SAK.

                • Visualization: AKP EMD SAK JBG.

                • Writing – original draft: AKP.

                • Writing – review & editing: AKP EMD SAK JBG.

                Author information
                http://orcid.org/0000-0002-0032-1053
                Article
                PONE-D-17-06440
                10.1371/journal.pone.0177419
                5423691
                28486546
                c932c63f-f077-4887-863d-f3e2ad837ed7
                © 2017 Powers et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 16 February 2017
                : 26 April 2017
                Page count
                Figures: 5, Tables: 1, Pages: 17
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000072, National Institute of Dental and Craniofacial Research;
                Award ID: R01-DE025033
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB-1457630
                Award Recipient :
                This research was funded by the US National Institute of Health (NIDCR R01-DE025033) and the US National Science Foundation (DEB-1457630) awarded to JG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Cranium
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Cranium
                Biology and Life Sciences
                Anatomy
                Head
                Eyes
                Medicine and Health Sciences
                Anatomy
                Head
                Eyes
                Biology and Life Sciences
                Anatomy
                Ocular System
                Eyes
                Medicine and Health Sciences
                Anatomy
                Ocular System
                Eyes
                Physical Sciences
                Mathematics
                Geometry
                Asymmetry
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Skeleton
                Skull
                Physical Sciences
                Mathematics
                Geometry
                Symmetry
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Cartilage
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Connective Tissue
                Cartilage
                Research and Analysis Methods
                Imaging Techniques
                Morphometry
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Fishes
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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