Kyonemichthys rumengani (Teleostei: Syngnathidae) is Sister Taxon to the Pipefish Genus Urocampus: Genetic and Morphological Evidence

A single female specimen (25.6 mm in standard length) of the thread-like Indo-Pacific pygmy syngnathid Kyonemichthys rumengani Gomon, 2007 was collected from fringing reef at eight meters depth from Okinawa Island in the Ryukyu Archipelago of southern Japan. It represents the first specimen of this...

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Published inSpecies Diversity Vol. 27; no. 2; pp. 293 - 299
Main Authors Tanimoto, Miyako, Hanahara, Nozomi, Shirakawa, Naoki
Format Journal Article
LanguageEnglish
Published The Japanese Society of Systematic Zoology 13.10.2022
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Abstract A single female specimen (25.6 mm in standard length) of the thread-like Indo-Pacific pygmy syngnathid Kyonemichthys rumengani Gomon, 2007 was collected from fringing reef at eight meters depth from Okinawa Island in the Ryukyu Archipelago of southern Japan. It represents the first specimen of this species to be housed in a museum fish collection in Japan, where for the first time it is available for molecular analysis. We assessed the morphological hypothesis that previously suggested Kyonemichthys Gomon, 2007 is allied with the Indo-Pacific pygmy pipehorse genera Acentronura Kaup, 1853 and Idiotropiscis Whitley, 1947 based on similar characteristics of the head angled slightly ventrally from the abdominal axis, dermal appendages, and flexible tail lacking a caudal fin. However, Kyonemichthys differs from these genera in having a dorsal-fin origin on the tail versus the trunk, a characteristic shared by two Indo-Pacific pipefish genera: the morphologically similar Urocampus Günther, 1870 and the distinct worm-like Siokunichthys Herald, 1953. We therefore investigated the evolutionary relationships of K. rumengani within Syngnathidae based on the genetic divergence of the mitochondrial CO1 gene (uncorrected p-distances) and a phylogenetic hypothesis generated from the analysis of three partial mitochondrial genes (12S, 16S, and CO1). Genetic analyses demonstrated that Kyonemichthys and Urocampus are closely related and form a strongly supported clade that excludes the phylogenetically distant Acentronura, Idiotropiscis, and Siokunichthys. Furthermore, morphological comparisons of K. rumengani with members of Urocampus revealed numerous synapomorphies distinct from the pygmy pipehorses, including meristic characters, trunk and tail ridge configurations, placement of dorsal fin on the tail, and shape of the prehensile tail. Therefore, based on the genetic and morphological characteristics, we suggest that Kyonemichthys is sister to Urocampus and is allied with pipefishes rather than with pygmy pipehorses. In addition, the Japanese standard name “Hari-youji” was proposed for K. rumengani.
AbstractList A single female specimen (25.6 mm in standard length) of the thread-like Indo-Pacific pygmy syngnathid Kyonemichthys rumengani Gomon, 2007 was collected from fringing reef at eight meters depth from Okinawa Island in the Ryukyu Archipelago of southern Japan. It represents the first specimen of this species to be housed in a museum fish collection in Japan, where for the first time it is available for molecular analysis. We assessed the morphological hypothesis that previously suggested Kyonemichthys Gomon, 2007 is allied with the Indo-Pacific pygmy pipehorse genera Acentronura Kaup, 1853 and Idiotropiscis Whitley, 1947 based on similar characteristics of the head angled slightly ventrally from the abdominal axis, dermal appendages, and flexible tail lacking a caudal fin. However, Kyonemichthys differs from these genera in having a dorsal-fin origin on the tail versus the trunk, a characteristic shared by two Indo-Pacific pipefish genera: the morphologically similar Urocampus Günther, 1870 and the distinct worm-like Siokunichthys Herald, 1953. We therefore investigated the evolutionary relationships of K. rumengani within Syngnathidae based on the genetic divergence of the mitochondrial CO1 gene (uncorrected p-distances) and a phylogenetic hypothesis generated from the analysis of three partial mitochondrial genes (12S, 16S, and CO1). Genetic analyses demonstrated that Kyonemichthys and Urocampus are closely related and form a strongly supported clade that excludes the phylogenetically distant Acentronura, Idiotropiscis, and Siokunichthys. Furthermore, morphological comparisons of K. rumengani with members of Urocampus revealed numerous synapomorphies distinct from the pygmy pipehorses, including meristic characters, trunk and tail ridge configurations, placement of dorsal fin on the tail, and shape of the prehensile tail. Therefore, based on the genetic and morphological characteristics, we suggest that Kyonemichthys is sister to Urocampus and is allied with pipefishes rather than with pygmy pipehorses. In addition, the Japanese standard name “Hari-youji” was proposed for K. rumengani.
ArticleNumber SD22-11
Author Hanahara, Nozomi
Tanimoto, Miyako
Shirakawa, Naoki
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References Araki, M. and Motomura, H. 2022. Review of the Indo-West Pacific pipefish genus Urocampus (Syngnathidae), with descriptions of two new species. Ichthyological Research doi 10.1007/s10228-022-00872-3 (24 May 2022).
Baldwin, C. C., Mounts, J. H., Smith, D. G., and Weigt, L. A. 2009. Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa 2008: 1–22.
Hanahara, N., Miyamoto, K., and Oka, S. 2021. Northernmost record of the surgeonfish Acanthurus nigros (Teleostei: Acanthuridae) from Minamidaitojima Island, southern Japan. Species Diversity 26: 43–47.
Wibowo, K. and Motomura, H. 2017. First confirmed record of the samoan pipefish Halicampus mataafae (Perciformes: Syngnathidae) from Japan. Species Diversity 22: 219–223.
Palumbi, S. R., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. 1991. The Simple Fool’s Guide to PCR. University of Hawaii, Honolulu, 46 pp.
Allen, G. R. and Erdmann, M. V. 2012. Reef Fishes of the East Indies. Volumes I−III. Tropical Reef Research, Perth, 1292 pp.
FishPix. 2022. Kyonemichthys rumengani. Available at https://fishpix.kahaku.go.jp/fishimage-e/search.html (23 March 2022).
Kuiter, R. H. 2009. Seahorses and Their Relatives. Aquatic Photographics, Seaford, 334 pp.
Truett, G. E., Heeger, P., Mynatt, R. L., Truett, A. A., Walker, J. A., and Warman, M. L. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29: 52–54.
Araki, M., Uehara, K., Senou, H., and Motomura, H. 2020. First records of the pughead-pipefish Bulbonaricus davaoensis (Teleostei: Syngnathidae) from Japan. Species Diversity 25: 163–169.
Bogorodsky, S. V., Randall, J. E., and Golani, D. 2011. Four new records of shore fishes for the Red Sea, with notes on Parupeneus heptacanthus and Diodon liturosus. Zootaxa 3057: 49–60.
Dawson, C. E. 1985. Indo-Pacific Pipefishes (Red Sea to the Americas). Gulf Coast Research Laboratory, Ocean Springs, vi+230 pp.
Lourie, S. A. and Randall, J. E. 2003. A new pygmy seahorse, Hippocampus denise (Teleostei: Syngnathidae), from the Indo-Pacific. Zoological Studies 42: 284–291.
Matsunuma, M., Senou, H., and Motomura, H. 2013. First Japanese records of Halicampus spinirostris (Syngnathidae) from the Ryukyu Islands, Japan. Japanese Journal of Ichthyology 66: 157–161. [In Japanese with English abstract]
Motomura, H and Uehara, K. 2020. An annotated checklist of marine and freshwater fishes of Okinoerabu Island in the Amami Islands, Kagoshima, southern Japan, with 361 new records. Bulletin of the Kagoshima University Museum 12: 1–125.
Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
Yoshigou, H. 2014. First Japanese record of Corythoichthys polynotatus Dawson, 1977 (Gasterosteiformes, Syngnathidae) from Iriomote Island, Ryukyu Archipelago, Japan. Fauna Ryukyuana 11: 9–14. [In Japanese with English abstract]
Gomon, M. F. 2007. A new genus and miniature species of pipehorse (Syngnathidae) from Indonesia. Aqua 13: 25–30.
Tamura, K., Stecher, G., and Kumar, S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38: 3022–3027.
Stiller, J., Short, G., Hamilton, H., Saarman, N., Longo, S., Wainwright, P., Rouse, G. W., and Simison, W. B. 2022. Phylogenomic analysis of Syngnathidae reveals novel relationships, origins of endemic diversity and variable diversification rates. BMC Biology 20: 75.
iNaturalist. 2022. Kyonemichthys rumengani. Available at https://www.inaturalist.org/observations (16 August 2022).
Katoh, K. and Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.
Senou, H. 2013. Syngnathidae. Pp. 615–635, 1909–1913. In: Nakabo, T. (Ed.) Fishes of Japan with Pictorial Keys to the Species. Third Edition. Tokai University Press, Hadano. [In Japanese]
Dawson, C. E. 1977. Synopsis of syngnathine pipefishes usually referred to the genus Ichthyocampus Kaup, with description of new genera and species. Bulletin of Marine Science 27: 595–650.
Hamilton, H., Saarman, N., Short, G., Sellas, A. B., Moore, B., Hoang, T., Grace, C. L., Gomon, M., Crow, K., and Simison, W. B. 2017. Molecular phylogeny and patterns of diversification in syngnathid fishes. Molecular Phylogenetics and Evolution 107: 388–403.
Short, G. A. and Trnski, T. 2021. A new genus and species of pygmy pipehorse from Taitokerau Northland, Aotearoa New Zealand, with a redescription of Acentronura Kaup, 1853 and Idiotropiscis Whitley, 1947 (Teleostei, Syngnathidae). Ichthyology & Herpetology 109: 806–835.
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References_xml – reference: Palumbi, S. R., Martin, A., Romano, S., McMillan, W. O., Stice, L., and Grabowski, G. 1991. The Simple Fool’s Guide to PCR. University of Hawaii, Honolulu, 46 pp.
– reference: Matsunuma, M., Senou, H., and Motomura, H. 2013. First Japanese records of Halicampus spinirostris (Syngnathidae) from the Ryukyu Islands, Japan. Japanese Journal of Ichthyology 66: 157–161. [In Japanese with English abstract]
– reference: Dawson, C. E. 1985. Indo-Pacific Pipefishes (Red Sea to the Americas). Gulf Coast Research Laboratory, Ocean Springs, vi+230 pp.
– reference: FishPix. 2022. Kyonemichthys rumengani. Available at https://fishpix.kahaku.go.jp/fishimage-e/search.html (23 March 2022).
– reference: Gomon, M. F. 2007. A new genus and miniature species of pipehorse (Syngnathidae) from Indonesia. Aqua 13: 25–30.
– reference: iNaturalist. 2022. Kyonemichthys rumengani. Available at https://www.inaturalist.org/observations (16 August 2022).
– reference: Yoshigou, H. 2014. First Japanese record of Corythoichthys polynotatus Dawson, 1977 (Gasterosteiformes, Syngnathidae) from Iriomote Island, Ryukyu Archipelago, Japan. Fauna Ryukyuana 11: 9–14. [In Japanese with English abstract]
– reference: Lourie, S. A. and Randall, J. E. 2003. A new pygmy seahorse, Hippocampus denise (Teleostei: Syngnathidae), from the Indo-Pacific. Zoological Studies 42: 284–291.
– reference: Kuiter, R. H. 2009. Seahorses and Their Relatives. Aquatic Photographics, Seaford, 334 pp.
– reference: Baldwin, C. C., Mounts, J. H., Smith, D. G., and Weigt, L. A. 2009. Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa 2008: 1–22.
– reference: Bogorodsky, S. V., Randall, J. E., and Golani, D. 2011. Four new records of shore fishes for the Red Sea, with notes on Parupeneus heptacanthus and Diodon liturosus. Zootaxa 3057: 49–60.
– reference: Stiller, J., Short, G., Hamilton, H., Saarman, N., Longo, S., Wainwright, P., Rouse, G. W., and Simison, W. B. 2022. Phylogenomic analysis of Syngnathidae reveals novel relationships, origins of endemic diversity and variable diversification rates. BMC Biology 20: 75.
– reference: Wibowo, K. and Motomura, H. 2017. First confirmed record of the samoan pipefish Halicampus mataafae (Perciformes: Syngnathidae) from Japan. Species Diversity 22: 219–223.
– reference: Dawson, C. E. 1977. Synopsis of syngnathine pipefishes usually referred to the genus Ichthyocampus Kaup, with description of new genera and species. Bulletin of Marine Science 27: 595–650.
– reference: Hanahara, N., Miyamoto, K., and Oka, S. 2021. Northernmost record of the surgeonfish Acanthurus nigros (Teleostei: Acanthuridae) from Minamidaitojima Island, southern Japan. Species Diversity 26: 43–47.
– reference: Araki, M., Uehara, K., Senou, H., and Motomura, H. 2020. First records of the pughead-pipefish Bulbonaricus davaoensis (Teleostei: Syngnathidae) from Japan. Species Diversity 25: 163–169.
– reference: Senou, H. 2013. Syngnathidae. Pp. 615–635, 1909–1913. In: Nakabo, T. (Ed.) Fishes of Japan with Pictorial Keys to the Species. Third Edition. Tokai University Press, Hadano. [In Japanese]
– reference: Short, G. A. and Trnski, T. 2021. A new genus and species of pygmy pipehorse from Taitokerau Northland, Aotearoa New Zealand, with a redescription of Acentronura Kaup, 1853 and Idiotropiscis Whitley, 1947 (Teleostei, Syngnathidae). Ichthyology & Herpetology 109: 806–835.
– reference: Allen, G. R. and Erdmann, M. V. 2012. Reef Fishes of the East Indies. Volumes I−III. Tropical Reef Research, Perth, 1292 pp.
– reference: Hamilton, H., Saarman, N., Short, G., Sellas, A. B., Moore, B., Hoang, T., Grace, C. L., Gomon, M., Crow, K., and Simison, W. B. 2017. Molecular phylogeny and patterns of diversification in syngnathid fishes. Molecular Phylogenetics and Evolution 107: 388–403.
– reference: Katoh, K. and Standley, D. M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780.
– reference: Truett, G. E., Heeger, P., Mynatt, R. L., Truett, A. A., Walker, J. A., and Warman, M. L. 2000. Preparation of PCR-quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29: 52–54.
– reference: Tamura, K., Stecher, G., and Kumar, S. 2021. MEGA11: Molecular Evolutionary Genetics Analysis version 11. Molecular Biology and Evolution 38: 3022–3027.
– reference: Araki, M. and Motomura, H. 2022. Review of the Indo-West Pacific pipefish genus Urocampus (Syngnathidae), with descriptions of two new species. Ichthyological Research doi 10.1007/s10228-022-00872-3 (24 May 2022).
– reference: Motomura, H and Uehara, K. 2020. An annotated checklist of marine and freshwater fishes of Okinoerabu Island in the Amami Islands, Kagoshima, southern Japan, with 361 new records. Bulletin of the Kagoshima University Museum 12: 1–125.
– reference: Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312–1313.
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marine fish
phylogeny
pygmy pipehorse
taxonomy
Title Kyonemichthys rumengani (Teleostei: Syngnathidae) is Sister Taxon to the Pipefish Genus Urocampus: Genetic and Morphological Evidence
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