Release of marketed individuals increases the risk of genetic disturbance in the pet insect Trypoxylus dichotomus
Authors/Creators
- 1. University of Hyogo, Himeji, Japan
- 2. Tohoku University, Osaki, Japan
- 3. GENODAS Inc., Sendai, Japan
- 4. Obihiro University of Agriculture and Veterinary Medicine, Matsudo, Japan|Natural History Museum and Institute, Chiba, Japan
- 5. Ishikawa Insect Museum, Hakusan, Japan
- 6. Museum of Nature and Human Activities, Sanda, Japan|University of Hyogo, Sanda, Japan
- 7. University of Hyogo, Sanda, Japan|Museum of Nature and Human Activities, Sanda, Japan
Description
Genetic disturbance can be caused by the release or escape of individuals with different genetic characteristics into wild habitats, risking impacts on native biodiversity. The risk of genetic disturbance in pet insects due to release and escape is particularly common because a wide variety of affordable pets are available on the market. Trypoxylus dichotomus (Coleoptera, Scarabaeidae), the Japanese rhinoceros beetle, is a renowned pet insect in Japan and thus is a suitable target species for studying genetic disturbances in pet insects. However, the detailed spatial genetic structure and genetic disturbances of this species in Japan remain unclear. Here, we estimated the genetic diversity and spatial genetic structure of wild and marketed individuals using mitochondrial DNA sequences and genome-wide single-nucleotide polymorphisms (SNPs) obtained via MIG-seq. Using MIG-seq, 570 SNPs were obtained, revealing a weak yet significant spatial genetic structure in the Japanese archipelago. Although significant isolation by distance (IBD) was observed in wild individuals, no significant IBD was observed in marketed individuals. Comparisons between wild and marketed individuals revealed clear differences in spatial genetic structure. These findings highlight the risks of releasing marketed individuals into the wild owing to their artificial long-distance migration. Our results provide valuable insights into the genetic disturbance of human-mediated distribution and underscore the need for informed management practices to protect native biodiversity.
Files
NB_article_159665.pdf
System files
(123.7 kB)
| Name | Size | |
|---|---|---|
|
md5:6fab3f67d9ac76c4ada2fbd287c1ff0b
|
123.7 kB | Download |
Linked records
Additional details
References
- Adachi N (2017) A new subspecies of Trypoxylus dichotomus (Linnaeus, 1771) (Coleoptera, Scarabaeidae, Dynastinae) from Yakushima Island and Tanegashima Island, Kagoshima Prefecture, Japan. Kogane 18: 11–16.
- Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England) 30: 2114–2120. https://doi.org/10.1093/bioinformatics/btu170
- Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics (Oxford, England) 23(19): 2633–2635. https://doi.org/10.1093/bioinformatics/btm308
- Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: Building and genotyping loci de novo from short-read sequences. G3 (Bethesda, Md. ) 1: 171–182. https://doi.org/10.1534/g3.111.000240
- Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: An analysis tool set for population genomics. Molecular Ecology 22: 3124–3140. https://doi.org/10.1111/mec.12354
- Chiba M, Yamazaki D, Ito S, Kagawa O, Chiba S (2022) Secondary contact of two cryptic Hokou gecko groups in the Izu Islands, Japan. Mitochondrial DNA, Part A, DNA Mapping, Sequencing, and Analysis 33: 53–60. https://doi.org/10.1080/24701394.2024.2310278
- Dufresnes C, Litvinchuk SN, Leuenberger J, Ghali K, Zinenko O, Stöck M, Perrin N (2016) Evolutionary melting pots: A biodiversity hotspot shaped by ring diversifications around the Black Sea in the Eastern tree frog (Hyla orientalis). Molecular Ecology 25: 4285–4300. https://doi.org/10.1111/mec.13706
- Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361. https://doi.org/10.1007/s12686-011-9548-7
- Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
- Frankham R (2010) Where are we in conservation genetics and where do we need to go? Conservation Genetics 11: 661–663. https://doi.org/10.1007/s10592-009-0010-2
- Goka K, Kojima A (2004) Ecological problem caused by exotic insects: The case of imported beetles. Environmental Entomology and Zoology 15: 137–146.
- Goka K, Kojima H, Okabe K (2004) Biological invasion caused by commercialization of stag beetles in Japan. Global Environmental Research 8: 67–74.
- Goudet J (2005) hierfstat: a package for r to compute and test hierarchical F-statistics. Molecular Ecology Notes 5: 184–186. https://doi.org/10.1111/j.1471-8286.2004.00828.x
- Hamano T, Ohba S, Kojima W, Nakahama N (2024) Discovery of genetic disturbance in Japanese rhinoceros beetles (Scarabaeidae, Coleoptera) in the Goto Islands, Japan. Kandokon 35: 57–62.
- Hosaka T, Kurimoto M, Numata S (2017) Entomological culture and insect-related tourism in Japan. International Journal of Tourism Science 10: 57–64.
- Hosoya T, Araya K (2010) Invasive species problem in stag beetles and rhinoceros beetles as pet insects. Species Biology Research 33: 135–159. [in Japanese]
- Iguchi Y (2009) The ecological impact of an introduced population on a native population in the firefly Luciola cruciata (Coleoptera, Lampyridae). Biodiversity and Conservation 18: 2119–2126. https://doi.org/10.1007/s10531-009-9576-8
- Ishibashi Y (2007) Pet industry and environmental issues. Keizai-to-Keiei 38: 33–75. [in Japanese]
- Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587–589. https://doi.org/10.1038/nmeth.4285
- Kato S, Arakaki S, Nagano AJ, Kikuchi K, Hirase S (2024) Genomic landscape of introgression from the ghost lineage in a gobiid fish uncovers the generality of forces shaping hybrid genomes. Molecular Ecology 33: e17216. https://doi.org/10.1111/mec.17216
- Kawamura K (2023) Present situation of genetic introgression by domestic alien species in Japan, inferred from genetic information. Fish Genetics and Breeding Science 52(2): 51–56.
- Kida K (2003) The situation of Shiretoko's introduced species [in Japanese]. Shiretoko Insects 212–217.
- Kojima W, Nakakura T, Fukuda A, Lin C-P, Harada M, Hashimoto Y, Kawachi A, Suhama S, Yamamoto R (2020) Latitudinal cline of larval growth rate and its proximate mechanisms in a rhinoceros beetle. Functional Ecology 34: 1577–1587. https://doi.org/10.1111/1365-2435.13572
- Kono H (1931) Die Trypoxylus-Arten aus Japan und Formosa (Col. Scarabaeidae). Insecta Matsumurana 5: 159–160.
- Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. https://doi.org/10.1093/molbev/msy096
- Kusui Y (1976) Notes on Allomyrina dichotoma from the Okinawa Islands. Entomological Review of Japan 29: 51–54.
- Li Y, Liu J (2018) StructureSelector: A web-based software to select and visualize the optimal number of clusters using multiple methods. Molecular Ecology Resources 18: 176–177. https://doi.org/10.1111/1755-0998.12719
- Mantel N (1967) Ranking procedures for arbitrarily restricted observation. Biometrics 23: 65–78.
- Ministry of the Environment Japan (2020) Red List 2020. Ministry of the Environment, Tokyo, Japan. https://www.env.go.jp/press/files/jp/114457.pdf [accessed 30 January 2025]
- Muranaka T, Ishihama F (2010) Ecology of introduced organisms: adaptive evolution into new environments and possible counter measures. Bun-ichi Co., Ltd., Tokyo.
- Nagai S (2006) A new species and new subspecies of the genus Trypoxylus from Asia and a new subspecies of the genus Beckium from New Guinea (Coleoptera, Scarabaeidae, Dynastinae). Gekkan-Mushi 428: 13–17.
- Nagai S (2007) Nihon no Kabutomushi Daizukan. BE-KUWA 22: 8–29.
- Nakahama N, Isagi Y (2018) Recent transitions in genetic diversity and structure in the endangered semi-natural grassland butterfly Melitaea protomedia in Japan. Insect Conservation and Diversity 11: 330–340. https://doi.org/10.1111/icad.12280
- Nakahama N, Asai T, Matsumoto S, Suetsugu K, Kurashima O, Matsuo A, Suyama Y (2021) Detection and dispersal risk of genetically disturbed individuals in the endangered wetland plant Pecteilis radiata (Orchidaceae) in Japan. Biodiversity and Conservation 30: 1913–1927. https://doi.org/10.1007/s10531-021-02174-y
- Nakahama N, Hanaoka T, Itoh T, Kishimoto T, Ohwaki A, Matsuo A, Kitahara M, Usami S, Suyama Y, Suka T (2022) Identification of source populations for reintroduction in extinct populations based on genome-wide SNPs and mtDNA sequence: A case study of the endangered subalpine grassland butterfly Aporia hippia (Lepidoptera, Pieridae) in Japan. Journal of Insect Conservation 26: 121–130. https://doi.org/10.1007/s10841-022-00369-4
- Nakao R (2017) Current status of genetic disturbance in wild medaka (Oryzias latipes species complex) in Japan. Nippon Suisan Gakkaishi 83: 235–235. https://doi.org/10.2331/suisan.WA2353-4
- Nei M (1972) Genetic distance between populations. The American Naturalist 106: 283–292. https://doi.org/10.1086/282771
- Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590. https://doi.org/10.1093/genetics/89.3.583
- Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. https://doi.org/10.1093/molbev/msu300
- Peakall R, Smouse PE (2006) GenAlEx 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6: 288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
- Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959. https://doi.org/10.1093/genetics/155.2.945
- Rambaut A (2018) FigTree v1.4.4. https://tree.bio.ed.ac.uk/software/figtree/
- Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annual Review of Ecology and Systematics 27: 83–109. https://doi.org/10.1146/annurev.ecolsys.27.1.83
- Roweis S (1998) EM algorithms for PCA and SPCA. Advances in Neural Information Processing Systems 10: 626–632.
- Sato Y, Ishikawa R (2004) The world of plants from the Sannai-Maruyama site: a DNA archaeological perspective. SHOKABO, Tokyo. [in Japanese]
- Satoru T (2014) A new subspecies of Trypoxylus dichotomus (Coleoptera, Scarabaeidae, Dynastinae) from China.
- Smouse PE, Peakall ROD (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82: 561–573. https://doi.org/10.1038/sj.hdy.6885180
- Suetsugu K, Nozaki T, Hirota S, Funaki S, Ito K, Isagi Y, Suyama Y, Kaneko S (2023) Phylogeographical evidence for historical long-distance dispersal in the flightless stick insect Ramulus mikado. Proceedings of the Royal Society B, Biological Sciences 290: 20231708. https://doi.org/10.1098/rspb.2023.1708
- Suyama Y, Matsuki Y (2015) MIG-seq: An effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Scientific Reports 5: 16963. https://doi.org/10.1038/srep16963
- Suyama Y, Hirota S, Matsuo A, Tsunamoto Y, Mitsuyuki C, Shimura A, Okano K (2022) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecological Research 37: 171–181. https://doi.org/10.1111/1440-1703.12270
- Takeuchi K, Ichikawa K, Elmqvist T (2016) Satoyama landscape as social–ecological system: Historical changes and future perspective. Current Opinion in Environmental Sustainability 19: 30–39. https://doi.org/10.1016/j.cosust.2015.11.001
- Tanaka Y (2017) Notes on non-native stag beetle species (Coleoptera, Lucanidae) observed in Itami City, Hyogo Prefecture, Japan. Itakon 5: 31–33.
- Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680. https://doi.org/10.1093/nar/22.22.4673
- Uchifune T (2012) Subsequent report on movement of a Japanese rhinoceros beetle (Coleoptera, Scarabaeidae) in the Miura Peninsula in 2011. Scientific Reports of Yokosuka City Museum 59: 31–32.
- Waku D, Segawa T, Yonezawa T, Akiyoshi A, Ishige T, Ueda M, Ogawa H, Sasaki H, Ando M, Kohno N, Sasaki T (2016) Evaluating the phylogenetic status of the extinct Japanese otter on the basis of mitochondrial genome analysis. PLOS ONE 11: e0149341. ttps://doi.org/10.1371/journal.pone.0149341
- Weber JN, Kojima W, Boisseau RP, Niimi T, Morita S, Shigenobu S, Gotoh H, Araya K, Lin C-P, Thomas-Bulle C, Allen CE, Tong W, Lavine LC, Swanson BO, . Emlen DJ (2023) Evolution of horn length and lifting strength in the Japanese rhinoceros beetle Trypoxylus dichotomus. Current Biology 33: 4285–4297. https://doi.org/10.1016/j.cub.2023.08.066
- Yang H, You CJ, Tsui CKM, Tembrock LR, Wu ZQ, Yang DP (2021) Phylogeny and biogeography of the Japanese rhinoceros beetle, Trypoxylus dichotomus (Coleoptera: Scarabaeidae) based on SNP markers. Ecology and Evolution 11: 153–173. https://doi.org/10.1002/ece3.6982
- Yoshitake H, Hosoya T, Yamada R (2016) Rhinoceros beetles collected aboard the ferry 'Toshima'. Sayabane, new series 23: 47.