Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Interspecific hybridization in seahorses: artificially produced hybrid offspring of Hippocampus kuda and Hippocampus reidi

  • Han, Sang-Yun (Department of Marine Biology, Pukyong National University) ;
  • Rho, Sum (Haechunma Co., Ltd.) ;
  • Noh, Gyeong Eon (Genetics and Breeding Research Center, National Institute of Fisheries Science) ;
  • Kim, Jin-Koo (Department of Marine Biology, Pukyong National University)
  • Received : 2017.09.12
  • Accepted : 2018.02.07
  • Published : 2018.05.31
Download PDF
⟨ Previous Next ⟩

Abstract

Interspecific hybridization experiments were conducted between the common seahorse Hippocampus kuda (male) and the slender seahorse H. reidi (female) during artificial rearing to develop a new aquarium fish with unique polyandrous mating. Molecular analysis via mitochondrial DNA (mtDNA) cytochrome b and nuclear DNA (ncDNA) ribosomal protein S7 gene supported the hybridization between the two species, and the hybrid also showed morphological characteristics of both species. Juveniles of H. kuda have dense melanophores on the whole body or only on the trunk and tail, whereas juveniles of H. reidi have thin melanophores on the whole body or present in stripes only along their prominent trunk and tail rings. However, all the hybrid juveniles had dense melanophores only on the tail, with the striped trunk rings, thus showing an intermediate pattern, and these patterns were limited to the fairly early stage of development (1-10 days old). In contrast, the two eye spines in the hybrid were apparent after 9 days old, which were not inherited from H. kuda (one eye spine), but from H. reidi (two eye spines). According to LOESS (local regression) analysis, the growth rate increased between 20 and 25 days, and the hybrids grew faster than H. kuda when they entered the explosive second phase of growth between 25 and 45 days for all the seahorses. This study highlights the hybridization between H. kuda and H. reidi may contribute to the improved taxonomic information of young seahorses.

Keywords

References

  1. Allendorf FW, Leary RF, Spruell P, Wenburg JK. The problems with hybrids: setting conservation guidelines. Trends in Ecology and Evolution. 2001;16:613-22. https://doi.org/10.1016/S0169-5347(01)02290-X
  2. Bae SE, Kim JK, Kim JH. Evidence of incomplete lineage sorting or restricted secondary contact in Lateolabrax japonicus complex (Actinopterygii: Moronidae) based on morphological and molecular traits. Biochem Syst Ecol. 2016;66:98-108. https://doi.org/10.1016/j.bse.2016.03.006
  3. Brennan AC, Woodward G, Seehausen O, Munoz-Fuentes V, Moritz C, Guelmami A, Abbott RJ, Edelaar P. Hybridization due to changing species distributions: adding problems or solutions to conservation of biodiversity during global change? Evol Ecol Res. 2015;16:475-91.
  4. Bull CD, Mitchell JS. Seahorse husbandry in public aquaria, 2002 manual. Chicago: Project Seahorse and the John G. Shedd Aquarium; 2002.
  5. Casey SP, Hall HJ, Stanley HF, Vincent ACJ. The origin and evolution of seahorses (genus Hippocampus): a phylogenetic study using the cytochrome b gene of mitochondrial DNA. Mol Phylogenet Evol. 2004;30:261-72. https://doi.org/10.1016/j.ympev.2003.08.018
  6. Caves EM, Sutton TT, Johnsen S. Visual acuity in ray-finned fishes correlates with eye size and habitat. J Exp Biol. 2017;220:1586-96. https://doi.org/10.1242/jeb.151183
  7. Chang CH, Shao KT, Lin YS, Liao YC. The complete mitochondrial genome of the three-spot seahorse, Hippocampus trimaculatus (Teleostei, Syngnathidae). Mitochondrial DNA. 2013;24:665-7. https://doi.org/10.3109/19401736.2013.773321
  8. Choi YU, Rho S, Jung MM, Lee YD, Noh GA. Parturition and early growth of crowned seahorse, Hippocampus coronatus in Korea. Korean Journal of Aquaculture. 2006;19:109-18.
  9. Choo CK, Liew HC. Morphological development and allometric growth patterns in the juvenile seahorse Hippocampus kuda Bleeker. J Fish Biol. 2006;69:426-45. https://doi.org/10.1111/j.1095-8649.2006.01105.x
  10. Chow S, Hazama K. Universal PCR primers for S7 ribosomal protein gene introns in fish. Mol Ecol. 1998;7:1255-6.
  11. CITES. Convention on international trade in endangered species of wild fauna and flora. Appendices I, II and III valid from 4 April 2017. 2017. Retrieved from https://cites.org/sites/default/files/eng/app/2017/E-Appendices-2017-04-04.pdf on June 16.
  12. do Prado FD, Hashimoto DT, Mendonca FF, Senhorini JA, Foresti F, Porto-Foresti F. Molecular identification of hybrids between Neotropical catfish species Pseudoplatystoma corruscans and Pseudoplatystoma reticulatum. Aquac Res. 2011;42:1890-4. https://doi.org/10.1111/j.1365-2109.2010.02777.x
  13. Foster SJ, Vincent ACJ. Life history and ecology of seahorses: implications for conservation and management. J Fish Biol. 2004;65:1-61.
  14. Freret-Meurer NV, Andreata JV. Field studies of a Brazilian seahorse population, Hippocampus reidi Ginsburg, 1933. Braz Arch Biol Technol. 2008;51:543-51. https://doi.org/10.1590/S1516-89132008000400012
  15. Gatz AJ. Ecological morphology of freshwater stream fishes. Tulane Studies in Zoology and Botany. 1979;21:91-124.
  16. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:95-8.
  17. Han SY, Kim JK, Kai Y, Senou H. Seahorses of the Hippocampus coronatus complex: taxonomic revision, and description of Hippocampus haema, a new species from Korea and Japan (Teleostei, Syngnathidae). ZooKeys. 2017;712:113-39. https://doi.org/10.3897/zookeys.712.14955
  18. Han SY, Kim JK, Tashiro F, Kai Y, Yoo JT. Relative importance of ocean currents and fronts in population structures of marine fish: a lesson from the cryptic lineages of the Hippocampus mohnikei complex. Mar Biodivers. 2017:1-13. https://doi.org/10.1007/s12526-017-0792-2
  19. Hercos AP, Giarrizzo T. Pisces, Syngnathidae, Hippocampus reidi: filling distribution gaps. Check List. 2007;3:287-90. https://doi.org/10.15560/3.4.287
  20. Ho NKP, Ho ALFC, Underwood GD, Underwood A, Zhang D, Lin J. A simple molecular protocol for the identification of hybrid Western Atlantic seahorses, Hippocampus erectus $\times$ H. reidi, and potential consequences of hybrids for conservation. Journal of Zoo and Aquarium Research. 2015;3:11-20.
  21. Hubbs CL. Variations in the number of vertebrae and other meristic characters of fishes correlated with the temperature of water during development. Am Nat. 1922;56:360-72. https://doi.org/10.1086/279875
  22. Indiviglio F. Seahorses: everything about history, care, nutrition, handling, and behavior. Hauppauge: Barron's Educational Series; 2002. p. 96.
  23. Ireland SC, Anders PJ, Siple JT. Conservation aquaculture: an adaptive approach to prevent extinction of an endangered white sturgeon population. Am Fish Soc Symp. 2002;28:211-22.
  24. Jacoby WG. Loess: a nonparametric, graphical tool for depicting relationships between variables. Elect Stud. 2000;19:577-613. https://doi.org/10.1016/S0261-3794(99)00028-1
  25. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111-20. https://doi.org/10.1007/BF01731581
  26. Kvarnemo C, Moore GI, Jones AG, Nelson WS, Avise JC. Monogamous pair bonds and mate switching in the Western Australian seahorse Hippocampus subelongatus. J Evol Biol. 2000;13:882-8. https://doi.org/10.1046/j.1420-9101.2000.00228.x
  27. Kwun HJ, Kim JK. Occurrence of natural hybrid between Oplegnathus fasciatus and Oplegnathus punctatus from the South Sea of Korea. Korean Journal of Ichthyology. 2010;22:201-5.
  28. Leysen H, Roos G, Adriaens D. Morphological variation in head shape of pipefishes and seahorses in relation to snout length and developmental growth. J Morphol. 2011;272:1259-70. https://doi.org/10.1002/jmor.10982
  29. Lim ASP, Myers AJ, Yu L, Buchman AS, Duffy JF, De Jager PL, Bennett DA. Sex difference in daily rhythms of clock gene expression in the aged human cerebral cortex. J Biol Rhythm. 2013;28:117-29. https://doi.org/10.1177/0748730413478552
  30. Lindberg JC, Tigan G, Ellison L, Rettinghouse T, Nagel MM, Fisch KM. Aquaculture methods for a genetically managed population of endangered Delta Smelt. N Am J Aquac. 2013;75:186-96. https://doi.org/10.1080/15222055.2012.751942
  31. Lourie SA. Measuring seahorses. Project seahorse technical report no. 4, version 1. 0. Columbia: Project Seahorse, Fisheries Centre, University of British; 2003.
  32. Lourie SA. Seahorses: a life-size guide to every species. Brighton: Ivy Press; 2016. p. 160.
  33. Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ. A guide to the identification of seahorses. Washington: Project Seahorse and TRAFFIC North America, University of British Columbia and World Wildlife Fund; 2004.
  34. Lourie SA, Green DM, Vincent ACJ. Dispersal, habitat differences, and comparative phylogeography of Southeast Asian seahorses (Syngnathidae: Hippocampus). Mol Ecol. 2005;14:1073-94. https://doi.org/10.1111/j.1365-294X.2005.02464.x
  35. Lourie SA, Pollom RA, Foster SJ. A global revision of the Seahorses Hippocampus Rafinesque 1810 (Actinopterygii: Syngnathiformes): taxonomy and biogeography with recommendations for further research. Zootaxa. 2016;4146:1-66. https://doi.org/10.11646/zootaxa.4146.1.1
  36. Lourie SA, Vincent ACJ. A marine fish follows Wallace's Line: the phylogeography of the three-spot seahorse (Hippocampus trimaculatus, Syngnathidae, Teleostei) in Southeast Asia. J Biogeogr. 2004;31:1975-85. https://doi.org/10.1111/j.1365-2699.2004.01153.x
  37. Lourie SA, Vincent ACJ, Hall HJ. Seahorses: an identification guide to the world's species and their conservation. London: Project Seahorse; 1999. p. x + 214.
  38. Mai ACG, Loebmann D. Size and number of newborn juveniles in wild Hippocampus reidi broods. Pan-American Journal of Aquatic Sciences. 2009;4:154-7.
  39. Matarese AC, Kendall AW Jr, Blood DM, Vinter BM. Laboratory guide to early life history stages of northeast Pacific fishes. Seattle: US Department of Commerce, National Oceanic and Atmospheric Administration, National Marine Fisheries Service; 1989. p. 652.
  40. Morgan JAT, Harry AV, Welch DJ, Street R, White J, Geraghty PT, Macbeth WG, Tobin A, Simpfendorfer CA, Ovenden JR. Detection of interspecies hybridisation in Chondrichthyes: hybrids and hybrid offspring between Australian (Carcharhinus tilstoni) and common (C. limbatus) blacktip shark found in an Australian fishery. Conserv Genet. 2012;13:455-63. https://doi.org/10.1007/s10592-011-0298-6
  41. Ooi BL, Juanita J, Choo CK. Genetic mating system of spotted seahorse (Hippocampus kuda, Bleeker, 1852). Terengganu: 9th UMT International Annual Symposium on Sustainability Science and Management (UMTAS) 2010; 2010. p. 6.
  42. Otero-Ferrer F, Herrera R, Lopez A, Socorro J, Molina L, Bouza C. First records of Hippocampus algiricus in the Canary Islands (north-east Atlantic Ocean) with an observation of hybridization with Hippocampus hippocampus. J Fish Biol. 2015;87:1080-9. https://doi.org/10.1111/jfb.12760
  43. Piacentino GLM. Area de distribucion para el genero Hippocampus e H. patagonicus Piacentino & Luzzatto 2004 y nueva cita para Hippocampus reidi Guinsburg 1933 (Pisces, Syngnathiformes) en el Mar Argentino. Boletim do Laboratorio de Hidrobiologia. 2008;21:107-11.
  44. R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2017. Available online at https://www.R-project.org/
  45. Rosa IL, Oliveira TPR, Castro ALC, de Souza Moraes LE, Xavier JHA, Nottingham MC, Dias TLP, Bruto-Costa LV, Araujo ME, Birolo AB, Mai ACG, Monteiro-Neto C. Population characteristics, space use and habitat associations of the seahorse Hippocampus reidi (Teleostei: Syngnathidae). Neotropical Ichthyology. 2007;5:405-14. https://doi.org/10.1590/S1679-62252007000300020
  46. Rose E, Small CM, Saucedo HA, Harper C, Jones AG. Genetic evidence for monogamy in the dwarf seahorse, Hippocampus zosterae. Journal of Heredity. 2014;105:922-7. https://doi.org/10.1093/jhered/esu050
  47. Sonnenberg R, Nolte AW, Tautz D. An evaluation of LSU rDNA D1-D2 sequences for their use in species identification. Front Zool. 2007;4:6. https://doi.org/10.1186/1742-9994-4-6
  48. Sousa-Santos C, Robalo JI, Collares-Pereira MJ, Almada VC. Heterozygous indels as useful tools in the reconstruction of DNA sequences and in the assessment of ploidy level and genomic constitution of hybrid organisms. DNA Seq. 2005;16:462-7. https://doi.org/10.1080/10425170500356065
  49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725-9. https://doi.org/10.1093/molbev/mst197
  50. Teske PR, Cherry MI, Matthee CA. The evolutionary history of seahorses (Syngnathidae: Hippocampus): molecular data suggest a West Pacific origin and two invasions of the Atlantic Ocean. Mol Phylogenet Evol. 2004;30:273-86. https://doi.org/10.1016/S1055-7903(03)00214-8
  51. Teske PR, Hamilton H, Matthee CA, Barker NP. Signatures of seaway closures and founder dispersal in the phylogeny of a circumglobally distributed seahorse lineage. BMC Evol Biol. 2007;7:138. https://doi.org/10.1186/1471-2148-7-138
  52. Teske PR, Hamilton H, Palsboll PJ, Choo CK, Gabr H, Lourie SA, Santos M, Sreepada A, Cherry MI, Matthee CA. Molecular evidence for longdistance colonization in an indo-Pacific seahorse lineage. Mar Ecol Prog Ser. 2005;286:249-60. https://doi.org/10.3354/meps286249
  53. Van Wassenbergh S, Roos G, Aerts P, Herrel A, Adriaens D. Why the long face? A comparative study of feeding kinematics of two pipefishes with different snout lengths. J Fish Biol. 2011;78:1786-98. https://doi.org/10.1111/j.1095-8649.2011.02991.x
  54. Van Wassenbergh S, Roos G, Genbrugge A, Leysen H, Aerts P, Adriaens D, Herrel A. Suction is kid's play: extremely fast suction in newborn seahorses. Biol Lett. 2009;5:200-3. https://doi.org/10.1098/rsbl.2008.0765
  55. Vincent ACJ. The international trade in seahorses. Cambridge: Traffic International; 1996.
  56. Vincent ACJ, Foster SJ, Koldewey HJ. Conservation and management of seahorses and other Syngnathidae. J Fish Biol. 2011;78:1681-724. https://doi.org/10.1111/j.1095-8649.2011.03003.x
  57. Wayne RK, Jenks SM. Mitochondrial DNA analysis implying extensive hybridization. Nature. 1991;351:565-8. https://doi.org/10.1038/351565a0
  58. Wickham H. ggplot2: elegant graphics for data analysis. New York: Springer-Verlag New York; 2009. p. viii + 213.
  59. Woodall L, Shaw P, Koldewey H. Seahorse identification: new techniques to the rescue. EAZA News. 2009;65:14-5.
  60. Woodall LC, Otero-Ferrer F, Correia M, Curtis JMR, Garrick-Maidment N, Shaw PW, Koldewey HJ. A synthesis of European seahorse taxonomy, population structure, and habitat use as a basis for assessment, monitoring and conservation. Mar Biol. 2018;165:19. https://doi.org/10.1007/s00227-017-3274-y

Cited by

  1. Significantly Accelerated Osteoblast Cell Growth on TiO2/SrHA Composite Mediated by Phenolic Compounds (BHM) from Hippocampus kuda Bleeler vol.10, pp.36, 2018, https://doi.org/10.1021/acsami.8b12411
  2. High density, early maturing, and morphometrically unique Hippocampus erectus population makes a Bahamian pond a priority site for conservation vol.39, pp.None, 2019, https://doi.org/10.3354/esr00949
  3. Diversity of Seahorse Species (Hippocampus spp.) in the International Aquarium Trade vol.13, pp.5, 2018, https://doi.org/10.3390/d13050187