Abstract
Correct identification of elasmobranch species is crucial for taxonomic and parasitological research. Although molecular barcoding may be the fastest choice to determine the identity of a given species, robust and fast species level identification in the field using morphological characters is essential. During this study, 389 specimens representing seven stingray species (Brevitrygon walga, Himantura leoparda, H. uarnak, Maculabatis randalli, M. arabica, M. gerrardi and Pateobatis fai) were examined from the Persian Gulf and the Gulf of Oman. A 1044 bp fragment of the NADH2 gene was generated for 50 specimens with representatives of all species. To verify the initial morphological identification and to compare intra- and interspecific differences a Neighbor-Joining analysis was conducted using uncorrected p-distances, whereas the Bayesian Inference was used to examine the relationships among taxa. Two species (M. arabica and M. gerrardi) are documented from the Persian Gulf for the first time. The molecular results provide the first known evidence of the sympatric distribution of M. randalli and M. arabica in the north and northwestern Indian Ocean. The results of the Bayesian Inference support the recent divergence of both species. Based on morphological comparisons and molecular support we suggest that the descriptions of M. randalli and M. arabica have been carried out on heterogeneous type series which has led to inconsistency between molecular identification and diagnostic morphological characteristics. Detailed morphological examination revealed that there is a relation between the type and number of denticles on the mid-dorsal surface of the disc and the color pattern of the tail. To address this taxonomic conflict all type materials should be re-examined. The Bayesian Inference tree showed that all specimens from the Persian Gulf and the Gulf of Oman morphologically resembling B. walga were found to group well outside those of the Indian species (B. imbricata) with an average p-distance of 0.097. The low nucleotide differences among the urogymnid taxa (P. fai and H. leoparda) from the Persian Gulf and the Gulf of Oman and their conspecific specimens in the Indo-West Pacific region revealed that philopatric behaviors may cause considerable gene flow among populations.
References
Agapow, P.M., Bininda-Emonds, O.R.P., Crandall, K.A., Gittleman, J.L., Mace, G.M., Marshall, J.C. & Purvis, A. (2004) The impact of species concept on biodiversity studies. The Quarterly Review of Biology, 79, 161–179.
Almoji, D.K., Moore, A.B.M. & White, W.T. (2015) Sharks & rays of the Arabian/Persian Gulf. MBG (INT) Ltd., London, 178 pp.
Aschliman, N.C. (2011) The Batoid Tree Of Life: Recovering The Patterns And Timing Of The Evolution Of Skates, Rays And Allies (Chondrichthyes: Batoidea). phD Dissertation, The Florida State University, Tallahassee, Florida, 198 pp.
Bazsalovicsová, E., Kralová-Hromadová, I., Brabec, J., Hanzelová, V., Oros, M. & Scholz, T. (2014) Conflict between morphology and molecular data. A case of the genus Caryophyllaeus (Cestoda: Caryophyllidea), monozoic tapeworms of cyprinid fishes. Folia parasitologica, 61, 347–354.
https://doi.org/10.14411/fp.2014.035
Caira, J.N. & Jensen, K. (2001) An investigation of the co-evolutionary relationships between onchobothriid tapeworms and their elasmobranch hosts. International Journal for Parasitology, 31, 960–975.
https://doi.org/10.1016/S0020-7519(01)00206-5
Caira, J.N. & Jensen, K. (2014) A digest of elasmobranch tapeworms. Journal of Parasitology, 100, 373–391.
https://doi.org/10.1645/14-516.1
Caira, J.N., Jensen, K., Waeschenbach, A., Olson, P.D. & Littlewood, D.T. (2014) Orders out of chaos—molecular phylogenetics reveals the complexity of shark and stingray tapeworm relationships. International Journal for Parasitology, 44, 55–73.
https://doi.org/10.1016/j.ijpara.2013.10.004
Carrier, J.C., Musick, J.A. & Heithaus, M.R. (2010) Sharks and their relatives II. Biodiversity, adaptive physiology, and conservation/edited by Jeffrey C. Carrier, John A. Musick, Michael R. Heithaus. CRC Press/Taylor & Francis, Boca Raton, Florida, 633 pp.
https://doi.org/10.1201/9781420080483
Cavalcanti, M.J. (2007) A phylogenetic supertree of the hammerhead sharks (Carcharhiniformes. Sphyrnidae). Zoological Studies, 46, 6–11.
Chapman, D.D., Simpfendorfer, C.A., Wiley, T.R., Poulakis, G.R., Curtis, C., Tringali, M., Carlson, J.K. & Feldheim, K.A. (2011) Genetic diversity despite population collapse in a critically endangered marine fish. The smalltooth sawfish (Pristis pectinata). The Journal of heredity, 102, 643–652.
https://doi.org/10.1093/jhered/esr098
Chen, X., Cai, J., Ding, W., Xiang, D. & Ai, W. (2014) Complete mitochondrial genome of the Sharpnose stingray Himantura gerrardi (Myliobatiformes: Dasyatidae). Mitochondrial DNA Part A: DNA Mapping, Sequencing, and Analysis, 27, 3989–3990.
https://doi.org/10.3109/19401736.2014.989518
Connallon, T. & Sgrò, C.M. (2018) In search of a general theory of species’ range evolution. PLoS biology, 16, e2006735.
https://doi.org/10.1371/journal.pbio.2006735
Edgar, R.C. (2004) MUSCLE. Multiple sequence alignment with high accuracy and high throughput. Nucleic acids research, 32, 1792–1797.
https://doi.org/10.1093/nar/gkh340
Fernando, D., Bown, R.M.K., Tanna, A., Gobiraj, R., Ralicki, H., Jockusch, E.L., Ebert, D.A., Jensen, K. & Caira, J.N. (2019) New insights into the identities of the elasmobranch fauna of Sri Lanka. Zootaxa, 4585 (2), 201.
https://doi.org/10.11646/zootaxa.4585.2.1
Filipiak, A., Zając, K., Kübler, D. & Kramarz, P. (2016) Coevolution of host-parasite associations and methods for studying their cophylogeny. Invertebrate Survival Journal, 13, 56–65.
Flowers, K.I., Ajemian, M.J., Bassos-Hull, K., Feldheim, K.A., Hueter, R.E., Papastamatiou, Y.P. & Chapman, D.D. (2016) A review of batoid philopatry, with implications for future research and population management. Marine Ecology Progress Series, 562, 251–261.
https://doi.org/10.3354/meps11963
Gaspar, C., Chateau, O. & Galzin, R. (2008) Feeding site frequentation by the pink whipray Himantura fai in Moorea (French Polynesia) as determined by acoustic telemetry. Cybium, 32, 153–164.
Henderson, A.C. & Reeve, A.J. (2011) Noteworthy elasmobranch records from Oman. African Journal of Marine Science, 33, 171–175.
https://doi.org/10.2989/1814232X.2011.572380
Henderson, A.C., Reeve, A.J., Jabado, R.W. & Naylor, G.J.P. (2016) Taxonomic assessment of sharks, rays and guitarfishes (Chondrichthyes. Elasmobranchii) from south-eastern Arabia, using the NADH dehydrogenase subunit 2 (NADH2) gene. Zoological Journal of the Linnean Society, 176, 399–442.
https://doi.org/10.1111/zoj.12309
Ivanova, N.V., deWaard, J.R. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Molecular Ecology Notes, 6, 998–1002.
https://doi.org/10.1111/j.1471-8286.2006.01428.x
Jabado, R., Kyne, P., Pollom, R., Ebert, D., Simpfendorfer, C., Ralph, G. & Dulvy, N. (2017) The Conservation Status of Sharks, Rays, and Chimaeras in the Arabian Sea and Adjacent Waters. Environment Agency, Abu Dhabi and IUCN Species Survival Commission Shark Specialist Group, Vancouver, 230 pp.
Jabado, R.W., Al Hameli, S.M., Grandcourt, E.M. & Al Dhaheri, S.S. (2018) Low abundance of sharks and rays in baited remote underwater video surveys in the Arabian Gulf. Scientific reports, 8, 15597.
https://doi.org/10.1038/s41598-018-33611-8
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2017) PartitionFinder 2. New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. Molecular Biology and Evolution, 34, 772–773.
https://doi.org/10.1093/molbev/msw260
Last, P.R., Manjaji-Matsumoto, B.M. & Moore, A.B. (2012) Himantura randalli sp. nov., a new whipray (Myliobatoidea: Dasyatidae) from the Persian Gulf. Zootaxa, 3327 (1), 20–32.
https://doi.org/10.11646/zootaxa.3327.1.2
Last, P.R., Naylor, G.J.P. & Manjaji-Matsumoto, B.M. (2016a) A revised classification of the family Dasyatidae (Chondrichthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa, 4139 (3), 345–368.
https://doi.org/10.11646/zootaxa.4139.3.2
Last, P.R., White, W.T., de Carvalho, M.R., Seret, B., Stehmann, M. & Naylor, G.J.P. (2016b) Rays of the World. CSIRO Publishing, Collingwood, 801 pp.
https://doi.org/10.1071/9780643109148
Lim, K.C., Lim, P.-E., Chong, V.C. & Loh, K.-H. (2015) Molecular and morphological analyses reveal phylogenetic relationships of stingrays focusing on the family Dasyatidae (Myliobatiformes). PLoS ONE, 10, e0120518.
https://doi.org/10.1371/journal.pone.0120518
Manjaji, B.M.2004 (2004) Taxonomy and phylogenetic systematics of the Indo-Pacific whip-tailed stingray genus Himantura Muller & Henle 1837 (Chondrichthyes Myliobatiformes: Dasyatidae). PhD thesis, University of Tasmania, Hobart, Launceston, 640 pp.
Manjaji-Matsumoto, B.M. & Last, P.R. (2016) Two new whiprays, Maculabatis arabica sp. nov. and M. bineeshi sp. nov. (Myliobatiformes: Dasyatidae), from the northern Indian Ocean. Zootaxa, 4144 (3), 335–353.
https://doi.org/10.11646/zootaxa.4144.3.3
Martin, A.P., Naylor, G.J. & Palumbi, S.R. (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature, 357, 153–155.
https://doi.org/10.1038/357153a0
Martin, A.P. & Palumbi, S.R. (1993) Protein evolution in different cellular environments. Cytochrome b in sharks and mammals. Molecular Biology and Evolution, 10, 873–891.
Moore, A.B., White, W.T. & Peirce, R. (2010) Additions to the shark fauna of the Persian (Arabian) Gulf. Zoology in the Middle East, 50, 83–88.
https://doi.org/10.1080/09397140.2010.10638415
Moore, A.B.M. (2012) Elasmobranchs of the Persian (Arabian) Gulf: ecology, human aspects and research priorities for their improved management. Reviews in Fish Biology and Fisheries, 22, 35–61.
https://doi.org/10.1007/s11160-011-9222-x
Naylor, 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, 367, 1–262.
https://doi.org/10.1206/754.1
Naylor, G.J.P., Ryburn, J.A., Fedrigo, O. & Lopez, J.A. (2005) Phylogenetic relationships among the major lineages of modern elasmobranchs. Reproductive Biology and Phylogeny, 3, 25.
Okonechnikov, K., Golosova, O. & Fursov, M. (2012) Unipro UGENE. A unified bioinformatics toolkit. Bioinformatics, 28, 1166–1167.
https://doi.org/10.1093/bioinformatics/bts091
Palumbi, S.R. (1994) Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology, Evolution, and Systematics, 25, 547–572.
https://doi.org/10.1146/annurev.es.25.110194.002555
Peterson, A.T. & Navarro-Sigüenza, A.G. (1999) Alternate species concepts as bases for determining priority conservation areas. Conservation Biology, 13, 427–431.
https://doi.org/10.1046/j.1523-1739.1999.013002427.x
Reyda, F.B. & Marques, F.P. (2011) Diversification and species boundaries of rhinebothrium (Cestoda; Rhinebothriidea) in South American freshwater stingrays (Batoidea; Potamotrygonidae). PLoS ONE, 6, e22604.
https://doi.org/10.1371/journal.pone.0022604
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3. Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.
https://doi.org/10.1093/bioinformatics/btg180
Sandoval-Castillo, J. & Rocha-Olivares, A. (2011) Deep mitochondrial divergence in Baja California populations of an aquilopelagic elasmobranch. The golden cownose ray. The Journal of heredity, 102, 269–274.
https://doi.org/10.1093/jhered/esr004
Straube, N., White, W.T., Ho, H.C., Rochel, E., Corriga, S., Li, C. & Naylor, G.J.P. (2013) A DNA sequence-Based identification checklist for taiwanese chondrichthyans. Zootaxa, 3752 (1), 256–278.
https://doi.org/10.11646/zootaxa.3752.1.16
Vaudo, J.J. & Heithaus, M.R. (2012) Diel and seasonal variation in the use of a nearshore sandflat by a ray community in a near pristine system. Marine and Freshwater Research, 63, 1077.
https://doi.org/10.1071/MF11226