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Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks

BACKGROUND: Squaliform sharks represent approximately 27 % of extant shark diversity, comprising more than 130 species with a predominantly deep-dwelling lifestyle. Many Squaliform species are highly specialized, including some that are bioluminescent, a character that is reported exclusively from S...

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Autores principales: Straube, Nicolas, Li, Chenhong, Claes, Julien M., Corrigan, Shannon, Naylor, Gavin J. P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4537554/
https://www.ncbi.nlm.nih.gov/pubmed/26277575
http://dx.doi.org/10.1186/s12862-015-0446-6
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author Straube, Nicolas
Li, Chenhong
Claes, Julien M.
Corrigan, Shannon
Naylor, Gavin J. P.
author_facet Straube, Nicolas
Li, Chenhong
Claes, Julien M.
Corrigan, Shannon
Naylor, Gavin J. P.
author_sort Straube, Nicolas
collection PubMed
description BACKGROUND: Squaliform sharks represent approximately 27 % of extant shark diversity, comprising more than 130 species with a predominantly deep-dwelling lifestyle. Many Squaliform species are highly specialized, including some that are bioluminescent, a character that is reported exclusively from Squaliform sharks within Chondrichthyes. The interfamiliar relationships within the order are still not satisfactorily resolved. Herein we estimate the phylogenetic interrelationships of a generic level sampling of “squaloid” sharks and closely related taxa using aligned sequences derived from a targeted gene capture approach. The resulting phylogenetic estimate is further used to evaluate the age of first occurrence of bioluminescence in Squaliformes. RESULTS: Our dataset comprised 172 putative ortholog exon sequences. Phylogenetic estimates result in a fully resolved tree supporting a monophyletic lineage of Squaliformes excluding Echinorhinus. Non-luminous Squalidae are inferred to be the sister to a clade comprising all remaining Squaliform families. Our results suggest that the origin of photophores is coincident with an elevated diversification rate and the splitting of families Dalatiidae, Etmopteridae, Oxynotidae and Somniosidae at the transition of the Lower to the Upper Cretaceous. The presence of luminous organs was confirmed for the Sleeper shark genus Zameus. These results indicate that bioluminescence in sharks is not restricted solely to the families Etmopteridae and Dalatiidae as previously believed. CONCLUSIONS: The sister-clade to non-luminous Squalidae comprises five families. The presence of photophores is reported for extant members of three out of these five families based on results of this study, i.e. Lantern sharks (Etmopteridae), Kitefin sharks (Dalatiidae) and Sleeper sharks (Somniosidae). Our results suggest that the origin of luminous organs arose during the rapid diversification event that gave rise to the extant Squaliform families. These inferences are consistent with the idea of diversification of Squaliform sharks being associated with the emergence of new deep-sea habitats in the Lower Cretaceous, which may have been facilitated by the evolution of bioluminescence. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0446-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-45375542015-08-16 Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks Straube, Nicolas Li, Chenhong Claes, Julien M. Corrigan, Shannon Naylor, Gavin J. P. BMC Evol Biol Research Article BACKGROUND: Squaliform sharks represent approximately 27 % of extant shark diversity, comprising more than 130 species with a predominantly deep-dwelling lifestyle. Many Squaliform species are highly specialized, including some that are bioluminescent, a character that is reported exclusively from Squaliform sharks within Chondrichthyes. The interfamiliar relationships within the order are still not satisfactorily resolved. Herein we estimate the phylogenetic interrelationships of a generic level sampling of “squaloid” sharks and closely related taxa using aligned sequences derived from a targeted gene capture approach. The resulting phylogenetic estimate is further used to evaluate the age of first occurrence of bioluminescence in Squaliformes. RESULTS: Our dataset comprised 172 putative ortholog exon sequences. Phylogenetic estimates result in a fully resolved tree supporting a monophyletic lineage of Squaliformes excluding Echinorhinus. Non-luminous Squalidae are inferred to be the sister to a clade comprising all remaining Squaliform families. Our results suggest that the origin of photophores is coincident with an elevated diversification rate and the splitting of families Dalatiidae, Etmopteridae, Oxynotidae and Somniosidae at the transition of the Lower to the Upper Cretaceous. The presence of luminous organs was confirmed for the Sleeper shark genus Zameus. These results indicate that bioluminescence in sharks is not restricted solely to the families Etmopteridae and Dalatiidae as previously believed. CONCLUSIONS: The sister-clade to non-luminous Squalidae comprises five families. The presence of photophores is reported for extant members of three out of these five families based on results of this study, i.e. Lantern sharks (Etmopteridae), Kitefin sharks (Dalatiidae) and Sleeper sharks (Somniosidae). Our results suggest that the origin of luminous organs arose during the rapid diversification event that gave rise to the extant Squaliform families. These inferences are consistent with the idea of diversification of Squaliform sharks being associated with the emergence of new deep-sea habitats in the Lower Cretaceous, which may have been facilitated by the evolution of bioluminescence. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0446-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-16 /pmc/articles/PMC4537554/ /pubmed/26277575 http://dx.doi.org/10.1186/s12862-015-0446-6 Text en © Straube et al. 2015 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Straube, Nicolas
Li, Chenhong
Claes, Julien M.
Corrigan, Shannon
Naylor, Gavin J. P.
Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks
title Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks
title_full Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks
title_fullStr Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks
title_full_unstemmed Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks
title_short Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks
title_sort molecular phylogeny of squaliformes and first occurrence of bioluminescence in sharks
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4537554/
https://www.ncbi.nlm.nih.gov/pubmed/26277575
http://dx.doi.org/10.1186/s12862-015-0446-6
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