Research Paper
Cryptic diversity of Rhinogobius rubromaculatus species complex (Gobiidae) in Taiwan: mitogenomes reveal their evolutionary history
Yu-Min Ju, Po-Hsun Kuo, Jui-Hsien Wu, Kui-Ching Hsu
Published on: 22 April 2025
Page: 343 - 352
DOI: 10.6165/tai.2025.70.343
Abstract
Rhinogobius rubromaculatus species complex is a group of freshwater gobies endemic to Taiwan. To understand the cryptic species diversity of R. rubromaculatus species complex, this study collected 501 specimens of the genus Rhinogobius from 34 rivers in Taiwan and used the sequences of mitochondrial DNA cytochrome b gene (1140 bp) as a DNA barcoding tool to identify species. In total, four allopatric lineages were found within R. rubromaculatus species complex, and large genetic divergences (p-distances > 0.043) support that they are distinct species. To better understand their evolutionary history, the complete mitochondrial genomes (mitogenomes) of these four lineages were sequenced. These results showed that (1) the mitogenomes characteristics of these four lineages were similar to those of other Rhinogobius species; (2) the mitogenome genetic distances (p-distances > 0.045) also supported that these four lineages are different species; (3) the results of the Approximate Bayesian Computation analyses support that these four species colonized Taiwan through four different colonization routes; (4) the R. rubromaculatus species complex reveal an evolutionary history similar to other Taiwanese freshwater fish such as Squalidus, Cobitis sinensis and Acrossocheilus paradoxus; and (5) the complex geological history of Taiwan has shaped the colonization history and distribution patterns of R. rubromaculatus species complex. These results have important implications for the conservation, population genetics and evolution of freshwater fishes in Taiwan.
Keyword: Approximate Bayesian Computation, cryptic species, mitogenome, Rhinogobius yangminshanensis
Literature Cited
Arrondo, N.V., Gomes-dos-Santos, A., Marcote, E.R., Perez, M., Froufe, E., Castro, L.F.C. 2020 A new gene order in the mitochondrial genome of the deep-sea diaphanous hatchet fish Sternoptyx diaphana Hermann, 1781 (Stomiiformes: Sternoptychidae). Mitochondrial DNA B 5(3): 2859–2861.
DOI: 10.1080/23802359.2020.1790325View Article
Google Scholar
Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K., Das, I. 2006 Cryptic species as window on diversity and conservation. Trends Ecol. Evol. 22(3): 148–155.
DOI: 10.1016/j.tree.2006.11.004View Article
Google Scholar
Boggs, S., Wang, W.C., Lewis, F.S., Chen, J.C. 1979 Sediment properties and water characteristics of the Taiwan shelf and slope. Acta Oceanogr. Taiwan 10: 10–49.
Chang, H.Y., Wang, W.K., Chen, K.N., Su, J.K., Hsin, C.Y., Li, J., Wang, Y.K., Lin, H.D. 2016 Phylogeography and genetic structure of the endemic cyprinid fish Microphysogobio brevirostris in northern Taiwan. Biochem. Syst. Ecol. 65: 176–184.
DOI: 10.1016/j.bse.2016.02.020View Article
Google Scholar
Chen, W.S., Erh, C.H., Chen, M.M., Yang, C.C., Chang, I.S., Liu, T.K., Horng, C.S., Shea, K.S., Yeh, M.G., Wu, J.C., Ko, C.T., Lin, C.C., Huang, N.W. 1999 The evolution of foreland basins in western Taiwan: evidence from Plio–Pleistocene sequences. Bull. Central Geol. Surv. 13: 137–156 (In Chinese).
Chen, I.S., Wu, J.H., Huang, S.P. 2009 The taxonomy and phylogeny of the cyprinid genus Opsariichthys Bleeker (Teleostei: Cyprinidae) from Taiwan, with description of a new species. Environ. Biol. Fishes 86(1): 165–183.
DOI: 10.1007/s10641-009-9499-yView Article
Google Scholar
Chen, I.S., Wang, S.C., Shao, K.T. 2022 A new freshwater gobiid species of Rhinogobius Gill, 1859 (Teleostei: Gobiidae) from northern Taiwan. Zootaxa 5189(1): 29-44.
DOI: 10.11646/zootaxa.5189.1.6View Article
Google Scholar
Cheng, H.L., Huang, S., SC, S.C. 2005 Morphological and molecular variation in Rhinogobius rubromaculatus (Pisces: Gobiidae) in Taiwan. Zool. Stud. 44(1): 119–129.
Chiang, T.Y., Lin, H.D., Shao, K.T., Hsu, K.C. 2010 Multiple factors have shaped the phylogeography of Chinese spiny loach (Cobitis sinensis) in Taiwan as inferred from mitochondrial DNA variation. J. Fish Biol. 76(5): 1173–1189.
DOI: 10.1111/j.1095-8649.2010.02589.xView Article
Google Scholar
Chiang, T.Y., Lin, H.D., Zhao, J., Kuo, P.H., Lee, T.W., Hsu, K.C. 2013 Diverse processes shape deep phylogeographical divergence in Cobitis sinensis (Teleostei: Cobitidae) in East Asia. J. Zool. Syst. Evol. Res. 51(4): 316–326.
DOI: 10.1111/jzs.12030View Article
Google Scholar
Chiang, T.Y., Chen, Y.Y., Lee, T.W., Hsu, K.C., Lin, F.J., Wang, W.K., Lin, H.D. 2017 Comparative phylogeography of two codistributed endemic cyprinids in southeastern Taiwan. Biochem. Syst. Ecol. 70: 283–290.
DOI: 10.1016/j.bse.2016.12.010View Article
Google Scholar
Chiu, Y.W., Bor, H., Kuo, P.H., Hsu, K.C., Tan, M.S., Wang, W.K., Lin, H.D. 2017 Origins of Semisulcospira libertina (Gastropoda: Semisulcospiridae) in Taiwan. Mitochondrial DNA A 28(4): 518–525.
DOI: 10.3109/24701394.2016.1149823View Article
Google Scholar
Cornuet, J.M., Pudlo, P., Veyssier, J., Dehne-Garcia, A., Gautier, M., Leblois, R., Marin, J.M., Estoup, A. 2014 DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics 30(8): 1187–1189.
DOI: 10.1093/bioinformatics/btt763View Article
Google Scholar
Darriba, D., Taboada, G.L., Doallo, R., Posada, D. 2012 jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9(8): 772–772.
DOI: 10.1038/nmeth.2109View Article
Google Scholar
Deconinck, D., Robbens, J., Volckaert, F.A.M., Derycke, S. 2023 Rapid and low-cost identification of common sole (Solea solea) in the field using a fast DNA isolation protocol and loop-mediated isothermal amplification (LAMP). J. Food Compos. Anal. 118: 105166.
DOI: 10.1016/j.jfca.2023.105166View Article
Google Scholar
Delic?, T., Trontelj, P., Rendo?, M., Fi?er, C. 2017 The importance of naming cryptic species and the conservation of endemic subterranean amphipods. Sci. Rep. 7: 3391.
DOI: 10.1038/s41598-017-02938-zView Article
Google Scholar
Fairbanks, R.G. 1989 A 17,000-year glacio-eustatic sea level record: influence of glacial melting rates on the Younger Dryas event and deep-ocean circulation. Nature 342(6250): 637– 642.
DOI: 10.1038/342637a0View Article
Google Scholar
Fricke, R., Eschmeyer, W.N., Van der Laan, R., 2024 Eschmeyer’s Catalog of Fishes: genera, species, references. Electronic version accessed mmm 2024.
Froese, R., Pauly, D. 2024 FishBase. World Wide Web Electronic Publication. http://www.fishbase.org. (Accessed June 2024).
Gascoyne, M., Benjamin, G.J., Schwarcz, H.P., Ford, D.C. 1979 Sea level lowering during the Illinoian glaciation: evidence from a Bahama ‘Blue Bole’. Science 205(4408): 806–808.
DOI: 10.1126/science.205.4408.806View Article
Google Scholar
Ghouri, M.Z., Ismail, M., Javed, M.A., Khan, S.H., Munawar, N., Umar, A.B., Nisa, M., Aftab, S.O., Amin, S., Khan, Z., Ahmad, A. 2020 Identification of edible fish species of Pakistan through DNA barcoding. Front. Mar. Sci. 7: 554183.
G?mez-L?piz, A., Sampaio, S., Hughes, J.J., Vald?s, S.M.C., Alves, P.C., Paip?rio, J., Searle, J.B. 2024 A first species-wide phylogenetic analysis of small mammals from Costa Rica using mitochondrial cytochrome b. Mamm. Res. 69(3): 365-378.
DOI: 10.1007/s13364-024-00757-yView Article
Google Scholar
Ghouri, M.Z., Ismail, M., Javed, M.A., Khan, S.H., Munawar, N., Umar, A.B., Nisa, M., Aftab, S.O., Amin, S., Khan, Z., Ahmad, A. 2020 Identification of edible fish species of Pakistan through DNA barcoding. Front. Mar. Sci. 7: 554183.
DOI: 10.3389/fmars.2020.554183View Article
Google Scholar
Gong, L., Shi, W., Si, L.Z., Wang, Z.M., Kong, X.Y. 2015 The complete mitochondrial genome of peacock sole Pardachirus pavoninus (Pleuronectiformes: Soleidae) and comparative analysis of the control region among 13 soles. Mol. Biol. 49(3): 408–417.
DOI: 10.1134/S0026893315030061View Article
Google Scholar
Hall, T.A. 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98.
DOI: 10.1093/nar/27.13.2682View Article
Google Scholar
Han, C.C., Hsu, K.C., Fang, L.S., Cheng, I.M., Lin, H.D. 2019 Geographical and temporal origins of Neocaridina species (Decapoda: Caridea: Atyidae) in Taiwan. BMC Genet. 20: 86.
DOI: 10.1186/s12863-019-0788-yView Article
Google Scholar
Hending, D. 2024 Cryptic species conservation: a review. Biol. Rev. 100(1): 258–274.
DOI: 10.1111/brv.13139View Article
Google Scholar
Hsu, V. 1990 Seismicity and tectonics of a continental-island arc collision zone at the island of Taiwan. J. Geophys. Res. 95(B4): 4725–4734.
DOI: 10.1029/JB095iB04p04725View Article
Google Scholar
Hsu, K.C., Bor, H., Lin, H.D., Kuo, P.H., Tan, M.S., Chiu, Y.W. 2014 Mitochondrial DNA phylogeography of Semisulcospira libertina (Gastropoda: Cerithioidea: Pleuroceridae): implications the history of landform changes in Taiwan. Mol. Biol. Rep. 41(6): 3733–3743.
DOI: 10.1007/s11033-014-3238-yView Article
Google Scholar
Hu, J., Li, Y.H., Liu, J., Xu, Z., Wu, H.B., Cheng, C., Chu, X.D., Wu, Z.D. 2023 The complete mitochondrial genome of Rhinogobius maculagenys (Gobiidae: Gobionellinae). Mitochondrial DNA B 8(11): 1141–1144.
DOI: 10.1080/23802359.2023.2274617View Article
Google Scholar
Ju, Y.M., Hsu, K.C., Yang, J.Q., Wu, J.H., Li, S., Wang, W.K., Ding, F., Li, J., Lin, H.D. 2018 Mitochondrial diversity and phylogeography of Acrossocheilus paradoxus (Teleostei: Cyprinidae). Mitochondrial DNA A 29(8): 1194–1202.
DOI: 10.1080/24701394.2018.1431227View Article
Google Scholar
Ju, Y.M., Wu, J.H., Hsu, K.C., Chiu, Y.W., Wang, W.K., Chen, C.W., Lin, H.D. 2021 Genetic diversity of Rhinogobius delicatus: origins of the freshwater fish in East Taiwan. Mitochondrial DNA A 32(1): 12–19.
DOI: 10.1080/24701394.2020.1844678View Article
Google Scholar
Ju, Y.M., Wu, J.H., Kuo, P.H., Hsu, K.C. 2024 Population genetic diversity and structure of the Taiwan endemic cyprinid fish Candidia barbata (Cyprinidae): human intervention. Hydrobiologia 851(6): 1435–1453.
DOI: 10.1007/s10750-023-05406-0View Article
Google Scholar
Kang, B., Hsu, K.C., Wu, J.H., Chiu, Y.W., Lin, H.D., Ju, Y.M. 2022 Population genetic diversity and structure of Rhinogobius candidianus (Gobiidae) in Taiwan: translocation and release. Ecol. Evol. 12(8): e9154.
DOI: 10.1002/ece3.9154View Article
Google Scholar
Kimura, M. 2000 Paleography of the Ryukyu Islands. Tropics 10(1): 5–24.
DOI: 10.3759/tropics.10.5View Article
Google Scholar
Kumar, S., Steecher, G., Li, M., Knyaz, C., Tamura, K. 2018 MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35(6): 1547–1549.
DOI: 10.1093/molbev/msy096View Article
Google Scholar
Lee, S.C., Chang, J.T. 1996 A new goby, Rhinogobius rubromaculatus (Teleostei: Gobiidae), from Taiwan. Zool. Stud. 35(1): 30–35.
Li, P., Ju, D.D., Peng, Z.G., Zhang, Y.G. 2012 The complete mitochondrial genome of the spotted steed, Hemibarbus maculates (Teleostei, Cypriniformes). Mitochondrial DNA 23(1): 34–36.
DOI: 10.3109/19401736.2011.643880View Article
Google Scholar
Li, F., Li, S., Chen, J.K. 2018 Rhinogobius immaculatus, a new species of freshwater goby (Teleostei: Gobiidae) from the Qiantang River, China. Zool. Res. 39(6): 396–405.
Li, Y.R., Wang, Z.W., Corlett, R.T., Yu, W.B. 2024 Comparative analyses of mitogenomes in the social bees with insights into evolution of long inverted repeats in the Meliponini. Zool. Res. 45(1): 160–175.
DOI: 10.24272/j.issn.2095-8137.2023.169View Article
Google Scholar
Liao, T.Y., Wang, T.Y., Lin, H.D., Shen, S.C., Tzeng, C.S. 2008 Phylogeography of the endangered species, Sinogastromyzon puliensis (Cypriniformes: Balitoridae), in southwestern Taiwan based on mtDNA. Zool. Stud. 47(4): 383–392.
Librado, P., Rozas, J. 2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11): 1451–1452.
DOI: 10.1093/bioinformatics/btp187View Article
Google Scholar
Lin, H.D., Hsu, K.C., Shao, K.T., Chang, Y.C., Wang, J.P., Lin, C.J., Chiang, T.Y. 2008 Population structure and phylogeography of Aphyocypris kikuchii (Oshima) based on mitochondrial DNA variation. J. Fish Biol. 72(8): 2011–2025.
DOI: 10.1111/j.1095-8649.2008.01836.xView Article
Google Scholar
Lin, H.D., Kuo, P.H., Wang, W.K., Chiu, Y.W., Ju, Y.M., Lin, F.J., Hsu, K.C. 2016 Speciation and differentiation of the genus Opsariichthys (Teleostei: Cyprinidae) in East Asia. Biochem. Syst. Ecol. 68: 92–100.
DOI: 10.1016/j.bse.2016.07.001View Article
Google Scholar
Lin, H., Dai, C., Yu, H., Tu, J., Yu, J., He, J., Jiang, H. 2023 Historical connectivity and environmental filtering jointly determine the freshwater fish assemblages on Taiwan and Hainan Islands of China. Curr. Zool. 69(1): 12–20.
DOI: 10.1093/cz/zoac015View Article
Google Scholar
Maeda, K., Shinzato, C., Koyanagi, R., Kunishima, T., Kobayashi, H., Satoh, N., Palla, H.P. 2021 Two new species of Rhinogobius (Gobiiformes: Oxudercidae) from Palawan, Philippines, with their phylogenetic placement. Zootaxa 5068(1): 81–98.
DOI: 10.11646/zootaxa.5068.1.3View Article
Google Scholar
Ota, H. 1998 Geographic patterns of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographic implications. Res. Popul. Ecol. 40(2): 189–204.
DOI: 10.1007/BF02763404View Article
Google Scholar
Papetti, C., Lio, P., R?ber, L., Patarnello, T., Zardoya, R. 2007 Antarctic fish mitochondrial genomes lack ND6 gene. J. Mol. Evol. 65(5): 519–528.
DOI: 10.1007/s00239-007-9030-zView Article
Google Scholar
Perna, N.T., Kocher, T.D. 1995 Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J. Mol. Evol. 41(3): 353–35.
DOI: 10.1007/BF01215182View Article
Google Scholar
Struck, T.H., Feder, J.L., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V.I., Kistenish, S., Larsson, L., Liow, L.H., Nowak, M.D., Stedje, B., Bachmann, L., Dimitrov, D. 2018. Finding evolutionary processes hidden in cryptic species. Trends Ecol. Evol. 33(3): 153–163.
DOI: 10.1016/j.tree.2017.11.007View Article
Google Scholar
Sun, S.E., Xiao, N. Sha, Z.L. 2022 Complete mitochondrial genomes of four deep-sea echinoids: conserved mitogenome organization and new insights into the phylogeny and evolution of Echinoidea. PeerJ 10: e13730.
DOI: 10.7717/peerj.13730View Article
Google Scholar
Tang, J.Y., Wei, R., Zhang, X.C., Jiang, Q.P. 2023 Mitogenome-based phylogenomics provides insights into the positions of the enigmatic sinensis group and the sanguinolenta group in Selaginellaceae (Lycophyte). Mol. Phylogenet. Evol. 179: 107673.
DOI: 10.1016/j.ympev.2022.107673View Article
Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.G. 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25(24): 4876–4882.
DOI: 10.1093/nar/25.24.4876View Article
Google Scholar
Wang, H.Y., Tsai, M.P., Yu, M.J., Lee, S.C. 1999 Influence of glaciation on divergence patterns of the endemic minnow, Zacco pachycephalus, in Taiwan. Mol. Ecol. 8(11): 1879–1888.
DOI: 10.1046/j.1365-294x.1999.00787.xView Article
Google Scholar
Wang, C.F., Hsieh, C.H., Lee, S.C., Wang, H.Y. 2011 Systematics and phylogeography of the Taiwanese endemic minnow Candidia barbatus (Pisces: Cyprinidae) based on DNA sequence, allozymic, and morphological analyses. Zool. J. Linn. Soc. 161(3): 613–632.
DOI: 10.1111/j.1096-3642.2010.00646.xView Article
Google Scholar
Wang, D., Dai, C., Li, Q., Li, Y., Liu, Z. 2019 Complete mitochondrial genome and phylogenic analysis of Rhinogobius cliffordpopei (Perciformes, Gobiidae). Mitochondrial DNA B 4(2): 2473–2474.
DOI: 10.1080/23802359.2019.1637287View Article
Google Scholar
Wang, S.C. 2022 The systematic and phylogenetic studies of Rhinogobius (Teleostei: Gobiidae) in Minjiang basin. Ph.D. dissertation, Institute of Marine Biology, National Taiwan Ocean University, Keelung, Taiwan. (In Chinese)
Wang, S.C., Chen, I.S. 2022 A new freshwater goby, Rhinogobius lianchengensis (Teleostei: Gobiidae) from the Minjiang river basin, Fujian Province, China. Zootaxa 5189(1): 45–56.
DOI: 10.11646/zootaxa.5189.1.7View Article
Google Scholar
Yamasaki, Y.Y., Nishida, M., Suzuki, T., Mukai, T., Watanabe, K. 2015 Phylogeny, hybridization, and life history evolution of Rhinogobius gobies in Japan, inferred from multiple nuclear gene sequences. Mol. Phylogenet. Evol. 90: 20–33.
DOI: 10.1016/j.ympev.2015.04.012View Article
Google Scholar
Yang, J.Q., Hsu, K.C., Liu, Z.Z., Su, L.W., Kuo, P.H., Tang, W.Q., Zhou, Z.C., Liu, D., Bao, B.L., Lin, H.D. 2016 The population history of Garra orientalis (Teleostei: Cyprinidae) using mitochondrial DNA and microsatellite data with approximate Bayesian computation. BMC Evol. Biol. 16: e73.
DOI: 10.1186/s12862-016-0645-9View Article
Google Scholar
Yi, M.R., Hsu, K.C., Gu, S., He, X.B., Luo, Z.S., Lin, H.D., Yan, Y.R. 2022 Complete mitogenomes of four Trichiurus species: a taxonomic review of the T. lepturus species complex. Zookeys 1084: 1–26.
DOI: 10.3897/zookeys.1084.71576View Article
Google Scholar
Zhao, J., Hsu, KC., Luo, J.Z., Wang, C.H., Chan,B.P., Li, J., Kuo, P.H., Lin, H.D. 2018 Genetic diversity and population history of Tanichthys albonubes (Teleostei: Cyprinidae): implications for conservation. Aquat. Conserve.: Mar. Freshw. Ecosyst. 28(2): 422–434.
DOI: 10.1002/aqc.2840View Article
Google Scholar