Abstract
Garra is the most species-rich genus of freshwater fishes in the Arabian Peninsula, including Oman, which has eight recognized, species restricted mainly to the Hajar and Dhofar mountains. Garra species from the Dhofar region in Oman are reviewed based on integrated morphological and molecular (COI) data of newly collected fishes from the type localities of G. sindhae and G. smartae, and a new population from Wadi Laggashalyon. No diagnostic character was found to distinguish the two species and the Laggashalyon population as distinct taxa. Garra dunsirei, another species endemic to a sinkhole at Tawi Attair, a very difficult area to access at a depth of about 211 m, was examined here based on the GenBank data and the diagnostic characters given in the original descriptions of the studied Garra species. In addition, the phylogenetic tree placed the sequenced Omani Garra fishes into nine groups with K2P sequence divergence of 0.8% (G. smartae and G. smartae_Laggasaylon); 1.2% (G. smartae and G. sindhae), and 14.5% (G. Shamal and G. dunsirei) in their COI barcode region. A molecular species delimitation approach using PTP, also detected one entity for Garra species from the Dhofar region (G. dunsirei, G. sindhae and the both populations of G. smartae), which is consistent with our morphological data. Therefore, based on absence of diagnostic characters, low genetic distance, and molecular species delimitation approach, we treat G. sindhae and G. smartae as junior synonyms of G. dunsirei.
References
Banister, K.E. (1984) A subterranean population of Garra barreimiae (Teleostei: Cyprinidae) from Oman, with comments on the concept of regressive evolution. Journal of Natural History, 18, 927–938. https://doi.org/10.1080/00222938400770811
Bayçelebi, E., Kaya, C., Turan, D., Ergüden, S.A. & Freyhof, J. (2018) Redescription of Garra turcica from southern Anatolia (Teleostei: Cyprinidae). Zootaxa, 4524 (2), 227–236. https://doi.org/10.11646/zootaxa.4524.2.6
Behrens-Chapuis, S., Herder, F., Esmaeili, H.R., Freyhof, J., Hamidan, N.A., Özuluǧ, M., Šanda, R. & Geiger, M.F. (2015) Adding nuclear rhodopsin data where mitochondrial COI indicates discrepancies-can this marker help to explain conflicts in cyprinids? DNA Barcodes, 3, 187–99. https://doi.org/10.1515/dna-2015-0020
Bruford, M.W., Hanotte, O., Brokfield, J.F.Y. & Burke, T. (1992) Single-locus and multilocus DNA fingerprinting. In: Hoelzel, A.R. (Ed.), Molecular genetic analysis of populations: a practical approach. Oxford University Press, New York, New York, pp. 225–269.
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: More models, new heuristics and parallel computing. Nature Methods, 9, 772. https://doi.org/10.1038/nmeth.2109
Englmaier, G.K., Rodriguez, N.V., Waidbacher, H., Palandacic, A., Tesfaye, G., Gessl, W. & Meulenbroek, P. (2020) New data on Garra makiensis (Cyprinidae, Labeoinae) from the Awash River (Ethiopia) with remarks on its relationships to congeners on the Arabian Peninsula. ZooKeys, 984, 133–163. https://doi.org/10.3897/zookeys.984.55982
Esmaeili, H.R., Al Jufaili, S.A.U.D., Masoumi, A.H. & Zarei, F. (2022) Ichthyodiversity in southeastern Arabian Peninsula: Annotated checklist, taxonomy, short description and distribution of Inland fishes of Oman. Zootaxa, 5134 (4), 451–503. https://doi.org/10.11646/zootaxa.5134.4.1
Esmaeili, H.R., Sayyadzadeh, G., Coad, B.W. & Eagderi, S. (2016) Review of the genus Garra Hamilton, 1822 in Iran with description of a new species: a morpho-molecular approach (Teleostei:Cyprinidae). Iranian Journal of Ichthyology, 3, 82–121.
Freyhof, J., Feulner, G.R., Hamidan, N.A. & Krupp, F. (2020) Freshwater Fishes of the Arabian Peninsula. Motivate Media Group, Dubia, 272 pp.
Geiger, M.F., Herder, F., Monaghan, M.T., Almada, V., Barbieri, R., Bariche, M., Berrebi, P., Bohlen, J., Casal-Lopez, M., Delmastro, G.B., Denys, G.P.J., Dettai, A., Doadrio, I., Kalogianni, E., Kärst, H., Kottelat, M., Kovačić, M., Laporte, M., Lorenzoni, M., Marčić, Z., Özuluǧ, M., Perdices, A., Perea, S., Persat, H., Porcelotti, S., Puzzi, C., Robalo, J., Sanda, R., Schneider, M., Slechtová, V., Stoumboudi, M., Walter, S. & Freyhof, J. (2014) Spatial Heterogeneity in the Mediter- ranean Biodiversity Hotspot Affects Barcoding Accuracy of its Freshwater Fishes. Molecular Ecology Resources, 14 (6), 1210–1221. https://doi.org/10.1111/1755-0998.12257
Hall, T.A. (1999) BioEdit: a user–friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98. https://doi.org/10.14601/Phytopathol_Mediterr-14998u1.29
Hamidan, N.A., Geiger, M. & Freyhof, J. (2014) Garra jordanica, a new species from the Dead Sea basin with remarks on the relationship of G. ghorensis, G. tibanica and G. rufa (Teleostei: Cyprinidae). Ichthyological Exploration of Freshwaters, 25, 223–236.
Hashemzadeh Segherloo, I., Abdoli, A., Eagderi, S., Esmaeili, H.R., Sayyadzadeh, G., Bernatchez, L., Hallerman, E., Geiger, M.F., Özulug, M., Laroche, J. & Freyhof, J. (2017) Dressing down: convergent reduction of the mental disc in Garra (Te- leostei: Cyprinidae) in the Middle East. Hydrobiologia, 785, 47–59. https://doi.org/10.1007/s10750-016-2902-8
Hashemzadeh Segherloo, I., Normandeau, E., Benestan, L., Rougeux, C., Coté, G., Moore, J.S., Ghaedrahmati, N., Abdoli, A. & Bernatchez, L. (2018) Genetic and morphological support for possible sympatric origin of fish from subterranean habitats. Scientific Reports, 8, 2909. https://doi.org/10.1038/s41598-018-20666-w
Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A. & Flouri, T. (2017) Multi-rate Poisson Tree Processes for single-locus species delimitation under Maximum Likelihood and Markov Chain Monte Carlo. Bioinformatics, 33 (11), 1630–1638. https://doi.org/10.1093/bioinformatics/btx025
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. https://doi.org/10.1007/BF017 31581
Kirchner, S., Kruckenhauser, L., Pichler, A., Borkenhagen, K. & Freyhof, J. (2020) Revision of the Garra species of the Hajar Mountains in Oman and the United Arab Emirates with the description of two new species (Teleostei: Cyprinidae). Zootaxa, 4751 (3), 521–5456. https://doi.org/10.11646/Zootaxa.4751.3.6
Komarova, A.S., Golubtsov, A.S. & Levin, B.A. (2022) Trophic Diversification Out of Ancestral Specialization: An example from a radiating African cyprinid fish (Genus Garra). Diversity, 14, 629. https://doi.org/10.3390/d14080629
Kottelat, M. & Freyhof, J. (2007) Handbook of European freshwater fishes. Kottelat, Cornol and Freyhof, Berlin, xiv + 646 pp.
Kruckenhauser, L., Haring, E., Seemann, R. & Sattmann, H. (2011) Genetic differentiation between cave and surfacedwelling populations of Garra barreimiae (Cyprinidae) in Oman. BMC Evolutionary Biology, 11, 172. https://doi.org/10.1186/1471-2148-11-172
Krupp, F. & Budd, K. (2009) A new species of the genus Garra (Teleostei: Cyprinidae) from Oman. Aqua, International Journal of Ichthyology, 15, 117–120.
Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets.bMolecular Biology and Evolution, 33, 1870–1874. https://doi.org/10.1093/molbe v/msw054
Langecker, T.G. & Longley, G. (1993) Morphological adaptations of the Texas blind catfishes Trogloglanis pattersoni and Satan eurystomus (Siluriformes: Ictaluridae) to their underground environment. Copeia, 1993, 976–986. https://doi.org/10.2307/1447075
Lyon, R.G., Geiger, M.F. & Freyhof, J. (2016) Garra sindhi, a new species from the Jebel Samhan nature Reserve in Oman (Teleostei: Cyprinidae). Zootaxa, 4154 (1), 79–88. https://doi.org/10.11646/zootaxa.4154.1.5
Mendes, I.S., Prosdocimi, F., Schomaker-Bastos, A., Furtado, C., Ferreira, R.L., Santos Pompeu, P. & Carvalho, D.C. (2019) On the evolutionary origin of Neotropical cavefish Ancistrus cryptophthalmus (Siluriformes, Loricariidae) based on the mitogenome and genetic structure of cave and surface populations. Hydrobiologia, 842 (1), 157–171. https://doi.org/10.1007/s10750-019-04033-y
Mousavi-Sabet, H., Vatandoust, S., Fatemi, Y. & Eagderi, S. (2016) Tashan Cave a new cave fish locality for Iran; and Garra tashanensis, a new blind species from the Tigris River drainage (Teleostei: Cyprinidae). FishTaxa, 1 (3), 133–148.
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbi o/sys029
Sayyadzadeh, G., Esmaeili, H.R. & Freyhof, J. (2015) Garra mondica, a new species from the Mond River drainage with re- marks on the genus Garra from the Persian Gulf basin in Iran (Teleostei: Cyprinidae). Zootaxa, 4048 (1), 75–89. https://doi.org/10.11646/zootaxa.4048.1.4
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Ward, R.D., Zemlak, T.S., Innes, H.B., Last, R.P. & Hebert, P.D.N. (2005) DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 360 (1462), 1847–1857. https://doi.org/10.1098/rstb.2005.1716
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29 (22), 2869–2876. https://doi.org/10.1093/bioinformatics/btt499