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 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.
Friedrich Schiller Universität Jena, Leutragraben 1, 07743, Jena, Germany. nicolas.straube@uni-jena.de.|Hollings Marine Laboratory, 331 Fort Johnson Rd, Charleston, SC, 29412, USA. nicolas.straube@uni-jena.de.|Bavarian State Collection of Zoology, Münchhausenstraße 21, 81247, Munich, Germany. nicolas.straube@uni-jena.de.
Nicolas
N
Straube
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai, 201306, China. chli@shou.edu.cn.
Chenhong
C
Li
Marine Biology Laboratory, Earth and Life Institute, Université catholique de Louvain, Kellner building, 3 Place Croix du Sud - bte L7.06.04, 1348, Louvain-la-Neuve, Belgium. julien.claes@gmail.com.
Julien M
JM
Claes
Hollings Marine Laboratory, 331 Fort Johnson Rd, Charleston, SC, 29412, USA. corrigansl@cofc.edu.
Shannon
S
Corrigan
Hollings Marine Laboratory, 331 Fort Johnson Rd, Charleston, SC, 29412, USA. gjpnaylor@gmail.com.
Gavin J P
GJ
Naylor
D000818:Animals; D005075:Biological Evolution; D002467:Cell Nucleus / Q000235:genetics; D004284:Dogfish / Q000145:classification* / Q000235:genetics / Q000502:physiology*; D005091:Exons; D005260:Female; D005580:Fossils; D010802:Phylogeny; D016415:Sequence Alignment