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Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks.

Straube N, Li C, Claes JM, Corrigan S, Naylor GJ - BMC Evol. Biol. (2015)

Bottom Line: Phylogenetic estimates result in a fully resolved tree supporting a monophyletic lineage of Squaliformes excluding Echinorhinus.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.

View Article: PubMed Central - PubMed

Affiliation: Friedrich Schiller Universität Jena, Leutragraben 1, 07743, Jena, Germany. nicolas.straube@uni-jena.de.

ABSTRACT

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.

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Maximum likelihood phylogenetic estimate of squalomorph sharks based on gene capture data of 172 nucleotide loci under a GTR + Gamma model using RAxML [35] partitioned into two sets, 1st and 2nd codon position as well as 3rd codon only. Analyzed specimens are listed in Additional file 1: Table S1. Nodes marked with black dots indicate 100 % bootstrap support and a posterior probability of 1 assessed in the Bayesian inference from the Phylobayes 3 analysis applying the CAT model [36, 37, 64]. Tree rooted midpoint, no outgroup defined.
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Fig1: Maximum likelihood phylogenetic estimate of squalomorph sharks based on gene capture data of 172 nucleotide loci under a GTR + Gamma model using RAxML [35] partitioned into two sets, 1st and 2nd codon position as well as 3rd codon only. Analyzed specimens are listed in Additional file 1: Table S1. Nodes marked with black dots indicate 100 % bootstrap support and a posterior probability of 1 assessed in the Bayesian inference from the Phylobayes 3 analysis applying the CAT model [36, 37, 64]. Tree rooted midpoint, no outgroup defined.

Mentions: Phylogenetic estimates presented herein provide a fully resolved and well-supported molecular hypothesis for the phylogeny of Squaliform sharks. The Maximum Likelihood trees as well as the Bayesian inferences resulting from different types of analyses carried out using RaxML [35] and PhyloBayes 3.3f [36, 37] were broadly congruent in topology except for the phylogenetic placement of Oxynotus. This taxon appears as sister taxon to all somniosid genera except for Somniosus in an analysis of all 1265 loci, but is nested among somniosid genera except for Somniosus in the analyses of the reduced dataset comprising 174 and 172 loci, respectively. The topology used for further analysis is summarized in Fig. 1, and is based on the 172 concatenated nucleotide loci that were selected through the MARE matrix reduction process and re-blasting analysis. The concatenated and aligned 172 nucleotide loci are deposited in the Dryad data repository [38] (Additional file 1: Tables S3 and S4, Figures S3 to S6).Fig. 1


Molecular phylogeny of Squaliformes and first occurrence of bioluminescence in sharks.

Straube N, Li C, Claes JM, Corrigan S, Naylor GJ - BMC Evol. Biol. (2015)

Maximum likelihood phylogenetic estimate of squalomorph sharks based on gene capture data of 172 nucleotide loci under a GTR + Gamma model using RAxML [35] partitioned into two sets, 1st and 2nd codon position as well as 3rd codon only. Analyzed specimens are listed in Additional file 1: Table S1. Nodes marked with black dots indicate 100 % bootstrap support and a posterior probability of 1 assessed in the Bayesian inference from the Phylobayes 3 analysis applying the CAT model [36, 37, 64]. Tree rooted midpoint, no outgroup defined.
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4537554&req=5

Fig1: Maximum likelihood phylogenetic estimate of squalomorph sharks based on gene capture data of 172 nucleotide loci under a GTR + Gamma model using RAxML [35] partitioned into two sets, 1st and 2nd codon position as well as 3rd codon only. Analyzed specimens are listed in Additional file 1: Table S1. Nodes marked with black dots indicate 100 % bootstrap support and a posterior probability of 1 assessed in the Bayesian inference from the Phylobayes 3 analysis applying the CAT model [36, 37, 64]. Tree rooted midpoint, no outgroup defined.
Mentions: Phylogenetic estimates presented herein provide a fully resolved and well-supported molecular hypothesis for the phylogeny of Squaliform sharks. The Maximum Likelihood trees as well as the Bayesian inferences resulting from different types of analyses carried out using RaxML [35] and PhyloBayes 3.3f [36, 37] were broadly congruent in topology except for the phylogenetic placement of Oxynotus. This taxon appears as sister taxon to all somniosid genera except for Somniosus in an analysis of all 1265 loci, but is nested among somniosid genera except for Somniosus in the analyses of the reduced dataset comprising 174 and 172 loci, respectively. The topology used for further analysis is summarized in Fig. 1, and is based on the 172 concatenated nucleotide loci that were selected through the MARE matrix reduction process and re-blasting analysis. The concatenated and aligned 172 nucleotide loci are deposited in the Dryad data repository [38] (Additional file 1: Tables S3 and S4, Figures S3 to S6).Fig. 1

Bottom Line: Phylogenetic estimates result in a fully resolved tree supporting a monophyletic lineage of Squaliformes excluding Echinorhinus.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.

View Article: PubMed Central - PubMed

Affiliation: Friedrich Schiller Universität Jena, Leutragraben 1, 07743, Jena, Germany. nicolas.straube@uni-jena.de.

ABSTRACT

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.

Show MeSH