Abstract
Sharks of the genus Squalus have slow reproductive rates coupled with low genetic diversity, as is typical of deep-water sharks, making this group slow to rebound from depletion due to overfishing. The number of species within Squalus has been expanding recently due to increased attention on taxonomic revision, and a growing research focus on little-known deep-water sharks in general. Here we use genetics and morphology to describe a new species of dogfish shark, Squalus clarkae sp. nov. from the Gulf of Mexico (GoM) which replaces Squalus mitsukurii in this region, and place it in the context of congeners from the Atlantic and elsewhere. Previously, S. clarkae sp. nov. was considered a part of the Squalus mitsukurii species complex, a group of closely related but distinct species. We sequenced the mitochondrial cytochrome oxidase I and the NADH Dehydrogenase II gene of S. mitsukurii from the type location in Japan, S. clarkae sp. nov. from the GoM, as well as three closely related species (S. cubensis, S. blainville, and S. megalops) and S. cf. mitsukurii from Brazil. Squalus clarkae sp. nov. is genetically distinct from other species with significant statistical support (>98.6% bootstrap support/posterior probability), and 2.8% divergent from S. mitsukurii in the type location of Japan. Morphological estimates also revealed differences between S. clarkae sp. nov., S. mitsukurii, and other Atlantic Squalus species, with S. clarkae sp. nov. exhibiting a longer body, smaller interorbital space, shorter caudal fin, and a differently-proportioned first dorsal fin. In general, dogfish sharks in the Atlantic and GoM are characterized by similar but distinct morphology, significant genetic variation, and small species ranges.
References
Castro, A.L.F., Stewart, B.S., Wilson, S.G., Hueter, R.E., Meekan, M.G., Motta, P.J., Bowen, B.W. & Karl, S.A. (2007) Population genetic structure of Earth's largest fish, the whale shark (Rhincodon typus). Molecular Ecology, 16 (24), 5183–5192.
https://doi.org/10.1111/j.1365-294X.2007.03597.xCastro, J.I. (2010) The sharks of North America. Oxford University Press, New York, 613 pp.
https://doi.org/10.2307/41827098Chen, C., Taniuchi, T. & Nose, Y. (1979) Blainville's dogfish, Squalus blainville, from Japan, with notes on S. mitsukurii and S. japonicus. Japanese Journal of Ichthyology, 26 (1), 26–42.
https://doi.org/10.11369/jji1950.26.26Churchill, D.A., Heithaus, M.R., Vaudo, J.J., Grubbs, R.D., Gastrich, K. & Castro, J.I. (2015) Trophic interactions of common elasmobranchs in deep-sea communities of the Gulf of Mexico revealed through stable isotope and stomach content analysis. Deep Sea Research Part II: Topical Studies in Oceanography, 115, 92–102.
https://doi.org/10.1016/j.dsr2.2014.10.011Compagno, L.J.V., Dando, M. & Fowler, S.L. (2005) Sharks of the World. Princeton University Press, Princeton, NJ, 496 pp.
Cotton, C.F. & Grubbs, R.D. (2015) Biology of deep-water chondrichthyans: Introduction. Deep Sea Research Part II: Topical Studies in Oceanography, 115, 1–10.
https://doi.org/10.1016/j.dsr2.2015.02.030Cotton, C.F., Grubbs, R.D., Daly-Engel, T.S., Lynch, P.D. & Musick, J.A. (2011) Age, growth and reproduction of Squalus cf. mitsukurii from Hawaiian waters. Marine and Freshwater research, 62 (7), 811–822.
https://doi.org/10.1071/MF10307Daly-Engel, T.S., Grubbs, R.D., Feldheim, K.A., Bowen, B.W. & Toonen, R.J. (2010) Is multiple mating beneficial or unavoidable? Low multiple paternity and genetic diversity in the shortspine spurdog (Squalus mitsukurii). Marine Ecology Progress Series, 403, 255–267.
https://doi.org/10.3354/meps08417Dulvy, N.K., Sadovy, Y. & Reynolds, J.D. (2003) Extinction vulnerability in marine populations. Fish and Fisheries, 4, 25–64.
https://doi.org/10.1046/j.1467-2979.2003.00105.xEbert, D.A., White, W.T., Goldman, K.J., Compagno, L.J.V., Daly-Engel, T.S. & Ward, R.D. (2010) Resurrection and redescription of Squalus suckleyi (Girard, 1854) from the North Pacific, with comments on the Squalus acanthias subgroup (Squaliformes: Squalidae). Zootaxa, 2612, 22–40.
Fischer, A.F., Veras, D.P., Hazin, F.H.V., Broadhurst, M.K., Burgess, G.H. & Oliviera, P.G.V. (2006) Maturation of Squalus mitsukurii and Cirrhigaleus asper (Squalidae, Squaliformes) in the southwestern equatorial Atlantic Ocean. Journal of Applied Ichthyology, 22 (6), 495–501.
https://doi.org/10.1111/j.1439-0426.2006.00749.xFolmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (1), 294–299.
Graham, K.J. (2005) Distribution, population structure and biological aspects of Squalus spp. (Chondrichthyes: Squaliformes) from New South Wales and adjacent Australian waters. Marine and Freshwater research, 56 (4), 405–416. H
ttps://doi.org/10.1071/MF04275Graham, K.J., Andrew, N.L. & Hodgson, K.E. (2001) Changes in relative abundance of sharks and rays on Australian South East Fishery trawl grounds after twenty years of fishing. Marine and Freshwater research, 52, 549–561.
https://doi.org/10.1071/MF99174Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59 (3), 307–321.
https://doi.org/10.1093/sysbio/syq010Gulak, S.J.B. & Carlson, J.K. (2013) Catch and bycatch of greater amberjack in the Gulf of Mexico shark and reeffish bottom longline fishery based on observer data. SEDAR33-DW24. SEDAR, North Charleston, SC, 27 pp.
Hebert, P.D.N., Cywinska, A. & Ball, S.L. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences, 270 (1512), 313–321.
https://doi.org/10.1098/rspb.2002.2218Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17 (8), 754–755.
Jordan, D.S. & Fowler, H.W. (1903) A Review of the Elasmobranchiate Fishes of Japan. In: Proceedings of the United States National Museum. The Smithsonian Institution, Washington, pp. 629–630.
Jordan, D.S. & Snyder, J.O. (1901) A preliminary check list of the fishes of Japan. Annotationes zoologicae Japonenses, 3 (Parts 2–3), 1–159.
Katoh, K., Misawa, K., Kuma, K.i. & Miyata, T. (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30 (14), 3059–3066.
https://doi.org/10.1093/nar/gkf436Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649.
https://doi.org/10.1093/bioinformatics/bts199Kyne, P.M. & Simpfendorfer, C.A. (2007) A collation and summarization of available data on deepwater chondrichthyans: biodiversity, life history and fisheries. In: A report prepared by the IUCN SSC Shark Specialist Group for the Marine Conservation Biology Institute
Last, P. & Stevens, J.D. (1994) Sharks and Rays of Australia. CSIRO Publishing, Collingwood, Victoria, 513 pp.
Last, P.R., White, W.T. & Motomura, H. (2007a) Part 6—A description of Squalus chloroculus sp. nov., a new spurdog from southern Australia, and the resurrection of S. montalbani Whitley. In: Last, P.R., White, W.T. & Pogonoski, J.J. (Eds.), Descriptions of New Dogfishes of the Genus Squalus (Squaloidea: Squalidae). CSIRO Marine and Atmospheric Research, Hobart, Tasmania, pp. 55–69.
https://doi.org/10.4225/08/58615c42b11ceLast, P.R., White, W.T. & Pogonoski, J.J. (2007b) Descriptions of new dogfishes of the genus 'Squalus' (Squaloidea: Squalidae). CSIRO Marine and Atmospheric Research, Hobart, Tasmania, 130 pp.
https://doi.org/10.4225/08/58615c42b11ceLast, P.R., White, W.T., Pogonoski, J.J., Gledhill, D.C., Yearsley, G.K. & Ward, D.C. (2007c) Part 1—Application of a rapid taxonomic approach to the genus Squalus. In: Last, P.R., White, W.T. & Pogonoski, J.J. (Eds.), Descriptions of new dogfishes of the genus Squalus (Squaloidea: Squalidae). CSIRO Marine and Atmospheric Research, Hobart, Tasmania pp. 1–10. https://doi.org/10.4225/08/58615c42b11ce
Litvinov, F.F. (1990) Ecological characteristics of the dogfish, Squalus mitsukurii from the Sala-y-Gomez Seamounts. J. Ichth, 30, 104–115.
Lucifora, L.O., Valero, J.L. & García, V.B. (1999) Length at maturity of the greeneye spurdog shark, Squalus mitsukurii (Elasmobranchii: Squalidae), from the SW Atlantic, with comparisons with other regions. Marine and Freshwater research, 50 (7), 629–632.
https://doi.org/10.1071/MF98167Morato, T., Watson, R., Pitcher, T.J. & Pauly, D. (2006) Fishing down the deep. Fish and Fisheries, 7 (1), 24–34.
https://doi.org/10.1111/j.1467-2979.2006.00205.xMusick, J.A. (1999) Ecology and conservation of long-lived marine animals. In: Musick, J.A. (Ed.), Life in the Slow Lane: Ecology and Conservation of Long-Lived Marine Animals. American Fisheries Society Symposium, 23, pp. 1–10.
Nammack, M.F., Musick, J.A. & Colvocoresses, J.A. (1985) Life history of spiny dogfish off the northeastern United States. Transactions of the American Fisheries Society, 114 (3), 367–376.
https://doi.org/10.1577/1548-8659(1985)114Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., White, W.T. & Last, P.R. (2012) A DNA Sequence–Based Approach To the Identification of Shark and Ray Species and Its Implications for Global Elasmobranch Diversity and Parasitology. Bulletin of the American Museum of Natural History, 1–262.
https://doi.org/10.1206/754.1Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25 (7), 1253–1256.
https://doi.org/10.1093/molbev/msn083Rigby, C. & Simpfendorfer, C.A. (2015) Patterns in life history traits of deep-water chondrichthyans. Deep Sea Research Part II: Topical Studies in Oceanography, 115, 30–40.
https://doi.org/10.1016/j.dsr2.2013.09.004Simpfendorfer, C.A. & Kyne, P.M. (2009) Limited potential to recover from overfishing raises concerns for deep-sea sharks, rays and chimaeras. Environmental Conservation, 36 (02), 97–103.
https://doi.org/10.1017/S0376892909990191Sunnucks, P. & Hales, D.F. (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution, 13 (3), 510–524.
https://doi.org/10.1093/oxfordjournals.molbev.a025612Tanaka, K., Shiina, T., Tomita, T., Suzuki, S., Hosomichi, K., Sano, K., Doi, H., Kono, A., Komiyama, T. & Inoko, H. (2013) Evolutionary relations of Hexanchiformes deep-sea sharks elucidated by whole mitochondrial genome sequences. BioMed research international, 2013, 147064.
https://doi.org/10.1155/2013/147064Tanaka, S., Shiobara, Y., Hioki, S., Abe, H., Nishi, G., Yano, K. & Suzuki, K. (1990) The reproductive biology of the frilled shark, Chlamydoselachus anguineus, from Suruga Bay, Japan. Japanese Journal of Ichthyology, 37 (3), 273–291.
https://doi.org/10.11369/jji1950.37.273Tanaka, S., Teshima, K. & Mizue, K. (1975) Studies on Sharks―X Morphological and Ecological Study on the Reproductive Organs in Male Heptranchias perlo. Bulletin of the Faculty of Fisheries, Nagasaki University, 40, 15–22.
Tomita, T., Cotton, C.F. & Toda, M. (2016) Ultrasound and physical models shed light on the respiratory system of embryonic dogfishes. Zoology, 119 (1), 36–41.
https://doi.org/10.1016/j.zool.2015.09.002Veríssimo, A., McDowell, J.R. & Graves, J.E. (2010) Global population structure of the spiny dogfish Squalus acanthias, a temperate shark with an antitropical distribution. Molecular Ecology, 19 (8), 1651–1662.
https://doi.org/10.1111/j.1365-294X.2010.04598.xVeríssimo, A., Zaera‐Perez, D., Leslie, R., Iglésias, S.P., Séret, B., Grigoriou, P., Sterioti, A., Gubili, C., Barría, C. & Duffy, C. (2017) Molecular diversity and distribution of eastern Atlantic and Mediterranean dogfishes Squalus highlight taxonomic issues in the genus. Zoologica Scripta, 46 (4), 414–428.
https://doi.org/10.1111/zsc.12224Viana, S.T., Carvalho, M.R. & Gomes, U.L. (2016) Taxonomy and morphology of species of the genus Squalus Linnaeus, 1758 from the Southwestern Atlantic Ocean (Chondrichthyes: Squaliformes: Squalidae). Zootaxa, 4133 (1), 1–89.
https://doi.org/10.11646/zootaxa.4133.1.1Ward, R.D., Holmes, B.H., Zemlak, T.S. & Smith, P.J. (2007) Part 12—DNA barcoding discriminates spurdogs of the genus Squalus. In: Last, P.R., White, W.T. & Pogonoski, J.J. (Eds.), Descriptions of New Dogfishes of the Genus Squalus (Squaloidea: Squalidae). CSIRO Marine and Atmospheric Research, Tasmania, Australia pp. 117–130.
https://doi.org/10.4225/08/58615c42b11ceWatson, R.A. & Morato, T. (2013) Fishing down the deep: Accounting for within-species changes in depth of fishing. Fisheries Research, 140, 63–65.
https://doi.org/10.1016/j.fishres.2012.12.004White, W.T. & Iglésias, S.P. (2011) Squalus formosus, a new species of spurdog shark (Squaliformes: Squalidae), from the western North Pacific Ocean. Journal of Fish Biology, 79 (4), 954–968.
https://doi.org/10.1111/j.1095-8649.2011.03068.xWilson, C.D. & Seki, M.P. (1994) Biology and population characteristics of Squalus mitsukurii from a seamount in the central North Pacific Ocean. Fisheries Bulletin, 92, 851–864.
Yano, K. & Tanaka, S. (1984) Review of the deep sea squaloid shark genus Scymnodon of Japan, with a description of a new species. Japanese Journal of Ichthyology, 30 (4), 341–360.
https://doi.org/10.11369/jji1950.30.341Yano, T., Ohshimo, S., Kanaiwa, M., Hattori, T., Fukuwaka, M.A., Nagasawa, T. & Tanaka, S. (2017) Spatial distribution analysis of the North Pacific spiny dogfish, Squalus suckleyi, in the North Pacific using generalized additive models. Fisheries Oceanography, 26 (6), 668–679.
https://doi.org/10.1111/fog.12225