Limits...
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.

Show MeSH
Microscopic photograph of an excised ventral skin patch of Zameus squamulosus (ZSM30966). Arrows indicate photophores in open state. Scale bar indicates 200 μm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig3: Microscopic photograph of an excised ventral skin patch of Zameus squamulosus (ZSM30966). Arrows indicate photophores in open state. Scale bar indicates 200 μm

Mentions: We reviewed the presence of photophores in Somniosidae and Oxynotidae, by inspecting the ventral surface area of several specimens housed in zoological collections. The inspection of skin samples from Zameus squamulosus revealed clear presence of epidermal photophores (mean diameter = 41.75 ± 1.95 μm, density = 26 units mm−2, PAP = 3.74 %) in this taxon (Fig. 3). The majority of these organs appeared to be ring-shaped and covered with translucent dermal denticles. Zameus photophores are visible as open dark circular plaques, typical of functional photophores that are capable of producing light. Indeed, this morphology is typically adopted by dalatiid and etmopterid photophores while glowing [44–48]; the translucent nature of Z. squamulosus scales would allow efficient transmission of underlying photophore light, similar to the observation of light transmission through the ventral scales of opisthoproctid fishes [49] or through the dorsal finspines of the velvet belly lanternshark, Etmopterus spinax [50].Fig. 3


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)

Microscopic photograph of an excised ventral skin patch of Zameus squamulosus (ZSM30966). Arrows indicate photophores in open state. Scale bar indicates 200 μm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig3: Microscopic photograph of an excised ventral skin patch of Zameus squamulosus (ZSM30966). Arrows indicate photophores in open state. Scale bar indicates 200 μm
Mentions: We reviewed the presence of photophores in Somniosidae and Oxynotidae, by inspecting the ventral surface area of several specimens housed in zoological collections. The inspection of skin samples from Zameus squamulosus revealed clear presence of epidermal photophores (mean diameter = 41.75 ± 1.95 μm, density = 26 units mm−2, PAP = 3.74 %) in this taxon (Fig. 3). The majority of these organs appeared to be ring-shaped and covered with translucent dermal denticles. Zameus photophores are visible as open dark circular plaques, typical of functional photophores that are capable of producing light. Indeed, this morphology is typically adopted by dalatiid and etmopterid photophores while glowing [44–48]; the translucent nature of Z. squamulosus scales would allow efficient transmission of underlying photophore light, similar to the observation of light transmission through the ventral scales of opisthoproctid fishes [49] or through the dorsal finspines of the velvet belly lanternshark, Etmopterus spinax [50].Fig. 3

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