Abstract
Except for fish whose migration is barriered by weirs and dams, there have been inadequate investigation on the population genetic structure of endangered animal species depending on riverside pools connecting to river channels (called “wando” in Japanese) in floodplains. We focused on the endangered floodplain dragonfly, Sympetrum pedemontanum elatum, which is known to live in the riverside pools during its larval stage and migrate only several kilometers by flight during adulthood. The population genetic structure in and around the central region of Japan was analyzed using approximately 20,000 SNPs obtained using double-digest restriction site-associated DNA sequencing (ddRAD-seq). Our results revealed small genetic differences over a wide area (global Fst < 0.05). However, a few genetically unique populations that might be associated with paleo-basins segregated during ancient tectonic events were detected. These populations are considered to be important conservation units. We also found a very weak gene flow among the studied populations, implying that population isolation occurs widely. While recent migrations were scarce, and detected within a direct distance of approximately 5 km, there were also some cases without migration, even at shorter distances. Genetic diversity was positively correlated with the amount of grassland within a 1 km buffer, suggesting that the preservation of grasslands surrounding aquatic habitats enhances the immigration and colonization of adult dragonflies of this endangered species. Understanding the effects of historical tectonism and terrestrial environments on the genetic diversity of semi-aquatic organisms, such as insects and amphibians, is crucial for the conservation of floodplain habitat connectivity.
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Data availability
ddRADSeq data: DDBJ Sequence Read Archive (RDA), BioProject Accession no. PRJDB15752. All other datasets generated during the study are available from the corresponding author on reasonable request.
References
Adachi K, Kawata M, Tamamura K, Tamamura Y (2007) Mark-and recapture survey of Sympetrum pedemontanum elatum. Kyousei-No-Hiroba, MNHAH 2:62–66 (in Japanese)
Alexander DH, Lange K (2011) Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinf 12:246. https://doi.org/10.1186/1471-2105-12-246
Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664. https://doi.org/10.1101/gr.094052.109
Association of Wildlife Research and EnVision (2021) Search system of Japanese Red Data. http://www.jpnrdb.com/. Accessed 10 Mar 2022 (in Japanese)
Bergl RA, Vigilant L (2007) Genetic analysis reveals population structure and recent migration within the highly fragmented range of the Cross River gorilla (Gorilla gorilla diehli). Mol Ecol 16:501–516. https://doi.org/10.1111/j.1365-294X.2006.03159.x
Bijlsma R, Bundgaard J, Boerema AC (2001) Does inbreeding affect the extinction risk of small populations?: predictions from Drosophila. J Evol Biol 13:502–514. https://doi.org/10.1046/j.1420-9101.2000.00177.x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140. https://doi.org/10.1111/mec.12354
Caterino MS, Chatzimanolis S (2009) Conservation genetics of three flightless beetle species in southern California. Conserv Genet 10:203–216. https://doi.org/10.1007/s10592-008-9548-7
Chang CC, Chow CC, Tellier LC, Vattikuti S, Purcell SM, Lee JJ (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4:7. https://doi.org/10.1186/s13742-015-0047-8
Chovanec A, Waringer J (2001) Ecological integrity of river-floodplain systems-assessment by dragonfly surveys (Insecta: Odonata). Regul Rivers 17:493–507. https://doi.org/10.1002/rrr.664
Cole TL, Hammer MP, Unmack PJ, Teske PR, Brauer CJ, Adams M, Beheregaray LB (2016) Range-wide fragmentation in a threatened fish associated with post-European settlement modification in the Murray-Darling Basin, Australia. Conserv Genet 17:1377–1391. https://doi.org/10.1007/s10592-016-0868-8
Coulon A, Cosson JF, Angibault JM, Cargnelutti B, Galan M, Morellet N, Petit E, Aulagnier S, Hewison AJM (2004) Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual–based approach. Mol Ecol 13:2841–2850. https://doi.org/10.1111/j.1365-294X.2004.02253.x
Davey JW, Blaxter ML (2011) RADSeq: next-generation population genetics. Briefings Funct Genomics 9:416–423. https://doi.org/10.1093/bfgp/elq031
Davis SR, Brown AG, Dinnin H (2007) Floodplain connectivity, disturbance and change: a palaeoentomological investigation of floodplain ecology from south-west England. J Anim Ecol 76:276–288. https://doi.org/10.1111/j.1365-2656.2006.01209.x
Duranel AJ, Acreman MC, Stratford CJ, Thompson JR, Mould DJ (2007) Assessing the hydrological suitability of floodplains for species-rich meadow restoration: a case study of the Thames floodplain, UK. Hydrol Earth Syst Sci 11:170–179. https://doi.org/10.5194/hess-11-170-2007
Feindt W, Fincke O, Hadrys H (2013) Still a one species genus? Strong genetic diversification in the world’s largest living odonate, the neotropical damselfly Megaloprepus caerulatus. Conserv Genet 15:469–481. https://doi.org/10.1007/s10592-013-0554-z
Fujii M, Miyoshi Y, Adachi I, Yagi T (2008) The practice and results of environ mental education in the “Sympetrum pedemontanum” research project: a case study of the cooperation between three elementary schools in Takarazuka, Hyogo and the museum of nature and human activities, Hyogo. Hum Nat MNHAH 19:101–113 (in Japanese)
Fujioka M, Lane SJ (1997) The impact of changing irrigation practices in rice fields on frog populations of the Kanto Plain, central Japan. Ecol Res 12:101–108. https://doi.org/10.1007/BF02523615
Fumagalli M (2013) Assessing the effect of sequencing depth and sample size in population genetics inferences. PLoS ONE 8:e79667. https://doi.org/10.1371/journal.pone.0079667
Gergel SE, Dixon MD, Turner MG (2002) Consequences of human-altered floods: levees, floods, and floodplain forests along the Wisconsin River. Ecol Appl 12:1755–1770. https://doi.org/10.1890/1051-0761(2002)012[1755:COHAFL]2.0.CO;2
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19. https://doi.org/10.18637/jss.v022.i07
Grueber CE, Knafler GJ, King TM, Senior AM, Grosser S, Robertson B, Weston KA, Brekke P, Harris CLW, Jamieson IG (2015) Toll-like receptor diversity in 10 threatened bird species: relationship with microsatellite heterozygosity. Conserv Genet 16:595–611. https://doi.org/10.1007/s10592-014-0685-x
Gu N, Chen G, Yang J, Zheng C, Gao X, Yuan L, Wang S, Fan Z, Lu Y, Song G, Chen S, Liu Y (2021) Novel microsatellite markers reveal low genetic diversity and evidence of heterospecific introgression in the critically endangered Chinese crested tern (Thalasseus bernsteini). Global Ecol Conserv 28:e01629. https://doi.org/10.1016/j.gecco.2021.e01629
Gwak WS, Roy A (2021) Genetic diversity and population genetic structure of Korean black scraper Thamnaconus modestus in Korea and Japan based on the mtDNA marker. Ocean Sci J 56:266–274. https://doi.org/10.1007/s12601-021-00017-z
Higashikawa W, Yoshimura M, Yagi T, Maeto K (2016) Microhabitat use by larvae of the endangered dragonfly Sympetrum pedemontanum elatum (Selys) in Japan. J Insect Conserv 20:407–416. https://doi.org/10.1007/s10841-016-9874-x
Higashikawa W, Yoshimura M, Yagi T, Maeto K (2017) Short and flat grass preferred by adults of the endangered dragonfly Sympetrum pedemontanum elatum (Odonata: Libellulidae). Appl Entomol Zool 52:605–613. https://doi.org/10.1007/s13355-017-0514-z
Higashikawa W, Yoshimura M, Yagi T, Maeto K (2018) Grass and water preference during oviposition by Sympetrum pedemontanum elatum in Japan (Odonata: Libellulidae). Odonatologica 47:161–178. https://doi.org/10.5281/zenodo.1239959
Higashikawa W, Yoshimura M, Yagi T, Maeto K (2019) Conservation study focusing on habitat use in darter (meadowhawk) populations that used to flourish in the rice paddy fields of Japan. Jpn J Limnol 80:107–124. https://doi.org/10.3739/rikusui.80.107. (in Japanese)
Inoue K (2004) Critical species of Odonata in Japan. Int J Odonatol 7:311–324. https://doi.org/10.1080/13887890.2004.9748219
Ishida S, Ishida K, Kojima K, Sugimura M (1988) Illustrated guide for identification of the Japanese Odonata. Tokai University Press, Tokyo (in Japanese)
Ishiyama N, Akasaka T, Nakamura F (2014) Mobility-dependent response of aquatic animal species richness to a wetland network in an agricultural landscape. Aquat Sci 76:437–449. https://doi.org/10.1007/s00027-014-0345-8
Japan Meteorological Agency (2019) Tracks of Typhoon in 2019. https://www.data.jma.go.jp/fcd/yoho/typhoon/route_map/bstv2019.html. Accessed 18 Sept 2023
Kawachino Y (2015) Conservation status of 2014 of Sympetrum pedemontanum elatum (Selys). Trans Nagasaki Biol Soc 76:16–20 (in Japanese)
Kawachino Y (2020) Conservation status of Sympetrum pedemontanum elatum (Selys) in 2020. Akagashi, Furusato Shizen-No Kai 292:1–5 (in Japanese)
Kawase N, Ushijima T, Yahiro K (2018) 2010s dragonflies and damselflies (Insecta: Odonata) of Shiga Prefecture, Honshu, Japan (Research Report of the Lake Biwa Museum vol. 30). Lake Biwa Museum, Shiga (in Japanese)
Kitanishi S, Nishio M, Uehara K, Ogawa R, Yokoyama T, Edo K (2013) Patterns of genetic diversity of mitochondrial DNA within captive populations of the endangered itasenpara bitterling: implications for a reintroduction program. Environ Biol Fish 96:567–572. https://doi.org/10.1007/s10641-012-0044-z
Kraaijeveld-Smit FJL, Beebee TJC, Griffiths RA, Moore RD, Schley L (2005) Low gene flow but high genetic diversity in the threatened Mallorcan midwife toad Alytes muletensis. Mol Ecol 14:3307–3315. https://doi.org/10.1111/j.1365-294X.2005.02614.x
Meirmans PG (2014) Nonconvergence in Bayesian estimation of migration rates. Mol Ecol Resour 14:726–733. https://doi.org/10.1111/1755-0998.12216
Miura K, Higashiura Y, Maeto K (2017) Evaluation of easy, non-destructive methods of DNA extraction from minute insects. Appl Entomol Zool 52:349–352. https://doi.org/10.1007/s13355-017-0481-4
Mosner E, Liepelt S, Ziegenhagen B, Leyer I (2012) Floodplain willows in fragmented river landscapes: understanding spatio-temporal genetic patterns as a basis for restoration plantings. Biol Conserv 153:211–218. https://doi.org/10.1016/j.biocon.2012.05.005
Muggeo VMR (2008) Segmented: an R package to fit regression models with broken-line relationships. R News 8/1:20–25. https://cran.r-project.org/doc/Rnews/. Accessed 10 Mar 2022
Munshi-South J, Zolnik CP, Harris SE (2016) Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations. Evol Appl 9:546–564. https://doi.org/10.1111/eva.12357
Mussmann SM, Douglas MR, Chafin TK, Douglas ME (2019) BA3-SNPs: contemporary migration reconfigured in BayesAss for next-generation sequence data. Methods Ecol Evol 10:1808–1813. https://doi.org/10.1111/2041-210X.13252
Naiman RJ, Décamps H, Pollock M (1993) The role of riparian corridors in maintaining regional biodiversity. Ecol Appl 3:209–212. https://doi.org/10.2307/1941822
Nakajima S, Sueyoshi M, Hirota SK, Ishiyama N, Matsuo A, Suyama Y, Nakamura F (2021) A strategic sampling design revealed the local genetic structure of cold-water fluvial sculpin: a focus on groundwater-dependent water temperature heterogeneity. Heredity 127:413–422. https://doi.org/10.1038/s41437-021-00468-z
Nakamura F (2022) Riparian forests and climate change: interactive zone of green and blue infrastructure. In: Nakamura F (ed) Green infrastructure and climate change adaptation. Springer, Singapore, pp 73–91. https://doi.org/10.1007/978-981-16-6791-6_6
Nazareno AG, Bemmels JB, Dick CW, Lohmann LG (2017) Minimum sample sizes for population genomics: an empirical study from an Amazonian plant species. Mol Ecol Resour 17:1136–1147. https://doi.org/10.1111/1755-0998.12654
Nazareno AG, Dick CW, Lohmann LG (2018) Tangled banks: a landscape genomic evaluation of Wallace’s riverine barrier hypothesis for three Amazon plant species. Mol Ecol 28:980–997. https://doi.org/10.1111/mec.14948
Parvizi E, Dhami MK, Yan J, McGaughran A (2022) Population genomic insights into invasion success in a polyphagous agricultural pest, Halyomorpha halys. Mol Ecol 32:138–151. https://doi.org/10.1111/mec.16740
Popova ON (2004) Infraspecific taxonomy of Sympetrum pedemontanum (Müller, 1766) (Anisoptera: Libellulidae). Odonatologica 32:207–216
Pröhl H, Auffarth J, Bergmann T, Buschmann H, Balkenhol N (2021) Conservation genetics of the yellow-bellied toad (Bombina variegata): population structure, genetic diversity and landscape effects in an endangered amphibian. Conserv Genet 22:513–529. https://doi.org/10.1007/s10592-021-01350-5
Qasim SZ, Qayyum A (1961) Spawning frequencies and breeding seasons of some freshwater fishes with special reference to those occurring in the plains of northern India. Indian J Fish 8:24–43
QGIS Development Team (2022) QGIS Geographic Information System. Open Source Geospatial Foundation. http://qgis.org. Accessed 10 Mar 2022
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://qgis.org. Accessed 12 May 2022
Rach J, DeSalle R, Sarkar IN, Schierwater B, Hadrys H (2007) Character-based DNA barcoding allows discrimination of genera, species and populations in Odonata. Proc R Soc B 275:237–247. https://doi.org/10.1098/rspb.2007.1290
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Sakaguchi S, Sugino T, Tsumura Y, Ito M, Crisp MD, Bowman DMJS, Nagano AJ, Honjo MN, Yasugi M, Kudoh H, Matsuki Y, Suyama Y, Isagi Y (2015) High-throughput linkage mapping of Australian white cypress pine (Callitris glaucophylla) and map transferability to related species. Tree Genet Genomes 11:121. https://doi.org/10.1007/s11295-015-0944-0
Samways MJ (2008) Dragonflies as focal organisms in contemporary conservation biology. In: Córdoba-Aquilar A (ed) Dragonflies and Damselflies. Oxford University Press, Oxford, pp 97–108. https://doi.org/10.1093/acprof:oso/9780199230693.003.0008
Satoguchi Y (2017) Consideration of paleo-water system changes based on geological history around paleo-lake Biwa basin, central Japan. J Fossil Res 50:60–70 (in Japanese)
Schindler M, Jungmann L, Donath TW, Ludewig K (2020) Influence of flood duration and aeration on saplings of ten hardwood floodplain forest species. PLoS ONE 15:e0234936. https://doi.org/10.1371/journal.pone.0234936
Tabayashi A (1987) Irrigation systems in Japan. Geogr Rev Jpn 60:41–65. https://doi.org/10.4157/grj1984b.60.41
Taguchi M, Watanabe M (1985) Ecological survey of some Sympetrum species (Selys) in the Tanito paddy field (2). Rep Environ Sci Mie Univ 10:109–116 (in Japanese)
Thompson DJ, Watts PC (2006) The structure of Coenagrion mercuriale populations in the New Forest, southern England. In: Rivera AC (ed) Forests and Dragonflies. Pensoft Publishers, Moscow, pp 239–258
Tockner K, Stanford JA (2002) Riverine flood plains: present state and future trends. Environ Conserv 29:308–330. https://doi.org/10.1017/S037689290200022X
Tomita K, Suzuki T, Yano K, Tojo K (2020) Community structure of aquatic insects adapted to lentic water environments, and fine-scale analyses of local population structures and the genetic structures of an endangered giant water Bug Appasus japonicus. InSects 11:389. https://doi.org/10.3390/insects11060389
Toogood SE, Joyce CB, Waite S (2008) Response of floodplain grassland plant communities to altered water regimes. Plant Ecol 197:285–298. https://doi.org/10.1007/s11258-007-9378-6
Torres-Cambas Y, Ferreira S, Cordero-Rivera A, Lorenzo-Carballa MO (2017) Identification of evolutionarily significant units in the Cuban endemic damselfly Hypolestes trinitatis (Odonata: Hypolestidae). Conserv Genet 18:1229–1234. https://doi.org/10.1007/s10592-017-0959-1
Ubukata H (2016) Life history of Sympetrum frequens (Selys, 1883) in Hokkaido: are migration and reproductive diapause involved? TOMBO 58:126 (in Japanese)
Wachi N, Gau J, Fujie S, Fukano K, Maeto K (2021) Genomic population structure of sympatric sexual and asexual populations in a parasitic wasp, Meteorus pulchricornis (Hymenoptera: Braconidae), inferred from six hundred single-nucleotide polymorphism loci. Mol Ecol 30:1612–1623. https://doi.org/10.1111/mec.15834
Ward JV, Tockner K, Schiemer F (1999) Biodiversity of floodplain river ecosystems: ecotones and connectivity. Regul Rivers 15:125–139. https://doi.org/10.1002/(SICI)1099-1646(199901/06)15:1/3%3C125::AID-RRR523%3E3.0.CO;2-E
Watanabe M, Matsuoka H, Taguchi M (2004) Habitat selection and population parameters of Sympetrum infuscatum (Selys) during sexually mature stages in a cool temperate zone of Japan (Anisoptera: Libellulidae). Odonatologica 33:169–179
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York. https://doi.org/10.1007/978-3-319-24277-4
Willing EM, Dreyer C, Oosterhout C (2012) Estimates of genetic differentiation measured by Fst do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7:e42649. https://doi.org/10.1371/journal.pone.0042649
Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191. https://doi.org/10.1093/genetics/163.3.1177
Wright S (1943) Isolation by distance. Genetics 28:114–138. https://doi.org/10.1093/genetics/28.2.114
Wright S (1949) The genetical structure of populations. Ann Eugen 15:323–354. https://doi.org/10.1111/j.1469-1809.1949.tb02451.x
Yang FM, Cai L, Dao Z, Sun W (2022) Genomic data reveals population genetic and demographic history of Magnolia fistulosa (Magnoliaceae), a plant species with extremely small populations in Yunnan Province. China Front Plant Sci 13:811312. https://doi.org/10.3389/fpls.2022.811312
Yonekura N, Kaizuka S, Nogami M, Chinzei K (2001) Regional geomorphology of the Japanese islands vol. 1—introduction to Japanese geomorphology. University of Tokyo Press, Tokyo (in Japanese)
Acknowledgements
We thank the members of the Aqua Restoration Research Center, Public Works Research Institute, for their assistance with the sampling survey. We appreciate Ms. Fumie Kobayashi of the Faculty of Agriculture of Ryukoku University, who supported the ddRAD-seq analysis. We are also grateful to Mr. Yoshiharu Kawachino of the Civic Association for Environmental Conservation (“Furusato Shizen no Kai”), who willingly provided a male adult of S. p. elatum and pictures of the deformed individuals (Fig. S3).
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This study was supported by the River Fund of the River Foundation, Japan Grant number 2021-5211-009 and JSPS KAKENHI Grant number 17J00154 and 23K17071.
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WH conceptualized and designed the research and conducted fieldwork and laboratory work to obtain the samples. ddRADSeq was led by AJN. Data analysis and visualization of the results were conducted by WH. Original draft was written by WH and reviewed, edited, and supervised by MY and KM.
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Higashikawa, W., Yoshimura, M., Nagano, A.J. et al. Conservation genomics of an endangered floodplain dragonfly, Sympetrum pedemontanum elatum (Selys), in Japan. Conserv Genet (2023). https://doi.org/10.1007/s10592-023-01595-2
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DOI: https://doi.org/10.1007/s10592-023-01595-2