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Lights out: the evolution of bacterial bioluminescence in Loliginidae

  • CEPHALOPOD BIOLOGY AND EVOLUTION
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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.

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Acknowledgments

We would like to thank G.N. Mahardika (Universitas Udayana), Z. A. Muchlisin (Universitas Syiah Kuala), D.B. Thuy (Nha Trang University) and H.P. Calumpong (Silliman University) for their assistance in sample collection, P.H. Barber and K. Carpenter (UCLA) for funding and facilitation of sample collection, D. Willette, M. Weber and R. Rachmawati for field assistance, and Kevin Horn (SIUC) for assistance with DNA sequencing. We also thank U.S. National Science Foundation grants 1036516 (to P. H. Barber) and 0235794 (to FEA), the SIUC REACH program, the American Malacological Society, Conchologists of America, Explorer’s Club and the American Museum of Natural History Lerner-Grey Fund for Marine Research for funding and support.

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Authors and Affiliations

  1. Department of Zoology, Southern Illinois University, Carbondale, IL, 62901, USA

    Frank E. Anderson & Alexis Bergman

  2. Department of Ecology and Evolutionary Biology, The University of California, Los Angeles, CA, 90095, USA

    Samantha H. Cheng

  3. Department of Ecology, Evolution and Marine Biology, The University of California, Santa Barbara, CA, 93106, USA

    M. Sabrina Pankey

  4. Department of Marine Resource Management, Iranian Fisheries Research Organization, Tehran, Iran

    Tooraj Valinassab

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  1. Frank E. Anderson
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Correspondence to Frank E. Anderson.

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Guest editors: Erica A. G. Vidal, Mike Vecchione & Sigurd von Boletzky / Cephalopod Life History, Ecology and Evolution

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Anderson, F.E., Bergman, A., Cheng, S.H. et al. Lights out: the evolution of bacterial bioluminescence in Loliginidae. Hydrobiologia 725, 189–203 (2014). https://doi.org/10.1007/s10750-013-1599-1

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