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Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes

Seadragons are a remarkable lineage of teleost fishes in the family Syngnathidae, renowned for having evolved male pregnancy. Comprising three known species, seadragons are widely recognized and admired for their fantastical body forms and coloration, and their specific habitat requirements have mad...

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Autores principales: Small, Clayton M., Healey, Hope M., Currey, Mark C., Beck, Emily A., Catchen, Julian, Lin, Angela S. P., Cresko, William A., Bassham, Susan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9245644/
https://www.ncbi.nlm.nih.gov/pubmed/35733255
http://dx.doi.org/10.1073/pnas.2119602119
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author Small, Clayton M.
Healey, Hope M.
Currey, Mark C.
Beck, Emily A.
Catchen, Julian
Lin, Angela S. P.
Cresko, William A.
Bassham, Susan
author_facet Small, Clayton M.
Healey, Hope M.
Currey, Mark C.
Beck, Emily A.
Catchen, Julian
Lin, Angela S. P.
Cresko, William A.
Bassham, Susan
author_sort Small, Clayton M.
collection PubMed
description Seadragons are a remarkable lineage of teleost fishes in the family Syngnathidae, renowned for having evolved male pregnancy. Comprising three known species, seadragons are widely recognized and admired for their fantastical body forms and coloration, and their specific habitat requirements have made them flagship representatives for marine conservation and natural history interests. Until recently, a gap has been the lack of significant genomic resources for seadragons. We have produced gene-annotated, chromosome-scale genome models for the leafy and weedy seadragon to advance investigations of evolutionary innovation and elaboration of morphological traits in seadragons as well as their pipefish and seahorse relatives. We identified several interesting features specific to seadragon genomes, including divergent noncoding regions near a developmental gene important for integumentary outgrowth, a high genome-wide density of repetitive DNA, and recent expansions of transposable elements and a vesicular trafficking gene family. Surprisingly, comparative analyses leveraging the seadragon genomes and additional syngnathid and outgroup genomes revealed striking, syngnathid-specific losses in the family of fibroblast growth factors (FGFs), which likely involve reorganization of highly conserved gene regulatory networks in ways that have not previously been documented in natural populations. The resources presented here serve as important tools for future evolutionary studies of developmental processes in syngnathids and hold value for conservation of the extravagant seadragons and their relatives.
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spelling pubmed-92456442022-07-01 Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes Small, Clayton M. Healey, Hope M. Currey, Mark C. Beck, Emily A. Catchen, Julian Lin, Angela S. P. Cresko, William A. Bassham, Susan Proc Natl Acad Sci U S A Biological Sciences Seadragons are a remarkable lineage of teleost fishes in the family Syngnathidae, renowned for having evolved male pregnancy. Comprising three known species, seadragons are widely recognized and admired for their fantastical body forms and coloration, and their specific habitat requirements have made them flagship representatives for marine conservation and natural history interests. Until recently, a gap has been the lack of significant genomic resources for seadragons. We have produced gene-annotated, chromosome-scale genome models for the leafy and weedy seadragon to advance investigations of evolutionary innovation and elaboration of morphological traits in seadragons as well as their pipefish and seahorse relatives. We identified several interesting features specific to seadragon genomes, including divergent noncoding regions near a developmental gene important for integumentary outgrowth, a high genome-wide density of repetitive DNA, and recent expansions of transposable elements and a vesicular trafficking gene family. Surprisingly, comparative analyses leveraging the seadragon genomes and additional syngnathid and outgroup genomes revealed striking, syngnathid-specific losses in the family of fibroblast growth factors (FGFs), which likely involve reorganization of highly conserved gene regulatory networks in ways that have not previously been documented in natural populations. The resources presented here serve as important tools for future evolutionary studies of developmental processes in syngnathids and hold value for conservation of the extravagant seadragons and their relatives. National Academy of Sciences 2022-06-22 2022-06-28 /pmc/articles/PMC9245644/ /pubmed/35733255 http://dx.doi.org/10.1073/pnas.2119602119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Small, Clayton M.
Healey, Hope M.
Currey, Mark C.
Beck, Emily A.
Catchen, Julian
Lin, Angela S. P.
Cresko, William A.
Bassham, Susan
Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes
title Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes
title_full Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes
title_fullStr Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes
title_full_unstemmed Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes
title_short Leafy and weedy seadragon genomes connect genic and repetitive DNA features to the extravagant biology of syngnathid fishes
title_sort leafy and weedy seadragon genomes connect genic and repetitive dna features to the extravagant biology of syngnathid fishes
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9245644/
https://www.ncbi.nlm.nih.gov/pubmed/35733255
http://dx.doi.org/10.1073/pnas.2119602119
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