Molecular phylogeny and evolution of bioluminescence in Odontosyllis (Annelida, Syllidae)

Abstract

Marine worms of the genus Odontosyllis (Syllidae, Annelida) are well known for spectacular bioluminescent courtship rituals. During the reproductive period, the benthic marine worms leave the ocean floor and swim to the surface to spawn, using bioluminescent light for mate attraction. The behavioural aspects of the courtship ritual have been extensively investigated but little is known about the origin and evolution of light production in Odontosyllis that may be a key factor shaping the natural history of the group. To investigate the speciation patterns and evolutionary history of Odontosyllis, we inferred phylogenies following a gene concatenation approach using both maximum likelihood and Bayesian inference with a multilocus molecular dataset including nuclear (18S rRNA) and mitochondrial markers (16S rRNA and cytochrome c oxidase subunit I) from 51 Odontosyllis specimens. We also used the resulting phylogenetic tree to perform an ancestral state reconstruction analysis to trace the origin of bioluminescence within the group. Our results reveal that the genus Odontosyllis as currently delineated is a paraphyletic group that needs to be taxonomically revised to reflect evolutionary relationships. Nevertheless, our analyses recover two supported clades with bioluminescent species and suggest that the most recent common ancestor of luminous syllids was not bioluminescent, providing evidence that bioluminescence has evolved independently twice in the group. We discuss possible scenarios for the origin and evolution of light production and the potential role of bioluminescence courtship as a driver of speciation. Our results shed light on the evolutionary history of luminous syllids and suggest that bioluminescence might represent a key factor shaping the evolution of these organisms.