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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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Chronogram resulting from the BEAST [38] analysis with estimated shift in the diversification rate. Background rate r = 0.02. The black stars indicate significant increase in the diversification rate to r = 0.15 (radiation Squalidae) and r = 0.05 (Etmopteridae, Oxynotidae and Somniosidae) estimated with MEDUSA [39, 40]. Scale bar in millions of years. Numbers at branches refer to node numbers given in Table 1. Pie charts indicate the probability that ancestral taxa are luminescent (blue) or not (red). Families Etmopteridae and Dalatiidae were coded as luminous as well as the genus Zameus within Somniosidae. * = Node calibrated with information from the fossil record (Table 2)
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Fig2: Chronogram resulting from the BEAST [38] analysis with estimated shift in the diversification rate. Background rate r = 0.02. The black stars indicate significant increase in the diversification rate to r = 0.15 (radiation Squalidae) and r = 0.05 (Etmopteridae, Oxynotidae and Somniosidae) estimated with MEDUSA [39, 40]. Scale bar in millions of years. Numbers at branches refer to node numbers given in Table 1. Pie charts indicate the probability that ancestral taxa are luminescent (blue) or not (red). Families Etmopteridae and Dalatiidae were coded as luminous as well as the genus Zameus within Somniosidae. * = Node calibrated with information from the fossil record (Table 2)

Mentions: Novel ecological opportunities after oceanic anoxic events have been hypothesized to trigger adaptive radiation of sharks in deep-water environments in the Lower Cretaceous [10, 24]. Results from the MEDUSA [42, 43] analysis indicate a background diversification rate r = 0.02. An elevated diversification rate was detected for families Etmopteridae, Dalatiidae, Oxynotidae and Somniosidae, (r = 0.05) and the radiation of the species-rich genus Squalus (r = 0.15, Fig. 2).Fig. 2


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)

Chronogram resulting from the BEAST [38] analysis with estimated shift in the diversification rate. Background rate r = 0.02. The black stars indicate significant increase in the diversification rate to r = 0.15 (radiation Squalidae) and r = 0.05 (Etmopteridae, Oxynotidae and Somniosidae) estimated with MEDUSA [39, 40]. Scale bar in millions of years. Numbers at branches refer to node numbers given in Table 1. Pie charts indicate the probability that ancestral taxa are luminescent (blue) or not (red). Families Etmopteridae and Dalatiidae were coded as luminous as well as the genus Zameus within Somniosidae. * = Node calibrated with information from the fossil record (Table 2)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig2: Chronogram resulting from the BEAST [38] analysis with estimated shift in the diversification rate. Background rate r = 0.02. The black stars indicate significant increase in the diversification rate to r = 0.15 (radiation Squalidae) and r = 0.05 (Etmopteridae, Oxynotidae and Somniosidae) estimated with MEDUSA [39, 40]. Scale bar in millions of years. Numbers at branches refer to node numbers given in Table 1. Pie charts indicate the probability that ancestral taxa are luminescent (blue) or not (red). Families Etmopteridae and Dalatiidae were coded as luminous as well as the genus Zameus within Somniosidae. * = Node calibrated with information from the fossil record (Table 2)
Mentions: Novel ecological opportunities after oceanic anoxic events have been hypothesized to trigger adaptive radiation of sharks in deep-water environments in the Lower Cretaceous [10, 24]. Results from the MEDUSA [42, 43] analysis indicate a background diversification rate r = 0.02. An elevated diversification rate was detected for families Etmopteridae, Dalatiidae, Oxynotidae and Somniosidae, (r = 0.05) and the radiation of the species-rich genus Squalus (r = 0.15, Fig. 2).Fig. 2

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