Lights out: the evolution of bacterial bioluminescence in Loliginidae

Abstract

Representatives of several metazoan clades engage in symbiotic interactions with bioluminescent bacteria, but the evolution and maintenance of these interactions remain poorly understood. Uroteuthis is a genus of loliginid squid (Cephalopoda: Loliginidae) characterized by paired ventral photophores (light organs) housing bioluminescent bacteria. While previous phylogenetic studies have suggested that Uroteuthis is closely related to Loliolus, a genus of non-bioluminescent species, this relationship remains unresolved. To illuminate Uroteuthis and Loliolus phylogeny and its implications for the evolution of bioluminescence in Loliginidae, we generated sequences from two mitochondrial genes from Uroteuthis specimens sampled from several sites in the Indian and western Pacific Oceans. We combined these data with data from GenBank, analyzed the concatenated data set using maximum likelihood and Bayesian methods, and reconstructed the evolution of bacterial bioluminescence on the resulting phylogenies. Our analyses support the hypothesis that Uroteuthis is paraphyletic with respect to Loliolus. Furthermore, our reconstructions suggest that the symbiosis between loliginid squid and bioluminescent bacteria evolved once in the ancestor of Loliolini (the clade comprising Uroteuthis and Loliolus), but was subsequently lost in the ancestor of Loliolus. These findings could have profound implications for our understanding of the evolution of symbiotic bioluminescence in squid.