Reconsidering invasion history of common land snails in Japan through genome-wide analyses
Tóm tắt
Understanding the method and history of introduction in non-native species are essential for conservation biology, especially in regions like Japan that have a long history of human activity. Bradybaena similaris is a circumtropical land snail that is considered a non-native species from Southeast Asia or East Asia to Japan, which was believed to be introduced by human activities such as sugarcane or sweet potato establishment several hundred years ago. Bradybaena pellucida, a sister species of B. similaris, is native to western Japan, but has recently spread throughout the eastern part of the country. We investigated genetic diversification pattern of non-native organisms using the two land snail species. We clarified the phylogenetic relationships of B. similaris and B. pellucida based on genome-wide SNPs and mtDNA. We revealed the population demographic history using ABC analysis with SNP data. Bradybaena similaris of mainland Japan could be distinguished from populations on the continent. Introgressive hybridization between the species occurred approximately 29,700 years ago. The present findings provide two new hypotheses: that agriculture began in Japan about 2800 years ago, Japanese populations of B. similaris were introduced from the continent more than 29,000 years ago by human activity other than agriculture; or B. similaris is native to a part of mainland Japan. The history of a non-native species with human activity is complex, urging us to reconsider previous hypotheses.
Tài liệu tham khảo
Alexander DH, Lange K (2011) Enhancements to the ADMIXTURE algorithm for individual ancestry estimation. BMC Bioinform 12:246. https://doi.org/10.1186/1471-2105-12-246
Asami T, Yamasita H, Park J, Ishikawa H (1997) Geographical distributions of the land snail Bradybaena pellucida (Pulmonata: Bradybaenidae). Yuriyagai 5:31–42
Azuma M (1982) Colored illustrations of the land snails of Japan. Hoikusha, Osaka
Barker GM (2001) The biology of terrestrial molluscs. CABI, Wallingford
Bednaršek N, Feely RA, Reum JCP, Peterson B et al (2014) Limacina helicina shell dissolution as an indicator of declining habitat suitability owing to ocean acidification in the California Current Ecosystem. Proc R Soc B 281:20140123. https://doi.org/10.1098/rspb.2014.0123
Blackburn TM, Pyšek P, Bacher S, Carlton JT et al (2011) A proposed unified framework for biological invasions. Trends Ecol Evol 26(7):333–339. https://doi.org/10.1016/j.tree.2011.03.023
Blair C, Ané C (2020) Phylogenetic trees and networks can serve as powerful and complementary approaches for analysis of genomic data. Syst Biol 69(3):593–601. https://doi.org/10.1093/sysbio/syz056
Boivin NL, Zeder MA, Fuller DQ, Crowther A et al (2016) Ecological consequences of human niche construction: examining long term anthropogenic shaping of global species distributions. Proc Natl Acad Sci USA 113(23):6388–6396. https://doi.org/10.1073/pnas.1525200113
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinform 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Brodie GD, Barker GM (2012) Bradybaena similaris (Rang, 1831). Family Bradybaenidae. USP introduced land snails of the Fiji Islands fact sheet series 2. http://repository.usp.ac.fj/5435/1/Bradybaena_similaris-Rang-1831.pdf
Carvalho CM, Bessa EA, D’ávila S, (2008) Life history strategy of Bradybaena similaris (Férussac, 1821) (Mollusca, Pulmonata, Bradybaenidae). Molluscan Res 28(3):171–174
Chang CP (2002) Bradybaena similaris (de Férussac) (Bradybaenidae) as a pest on grapevines of Taiwan. Molluscs as Crop Pests 241
Chiba M, Hirano T, Yamazaki D, Ye B et al (2022) The mutual history of Schlegel’s Japanese gecko (Reptilia: Squamata: Gekkonidae) and humans inscribed in genes and ancient literature. PNAS Nexus 1(5):pgac245. https://doi.org/10.1093/pnasnexus/pgac245
Cowie RH, Hayes KA, Tran CT, Meyer WM (2008) The horticultural industry as a vector of alien snails and slugs: widespread invasions in Hawaii. Int J Pest Manag 54(4):267–276. https://doi.org/10.1080/09670870802403986
Crawford GW (2011) Advances in understanding early agriculture in Japan. Curr Anthropol 52(S4):S331–S345. https://doi.org/10.1086/658369
Csilléry K, François O, Blum MGB (2012) Abc: an R package for approximate Bayesian computation (ABC). Methods Ecol Evol 3(3):475–479. https://doi.org/10.1111/j.2041-210X.2011.00179.x
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797. https://doi.org/10.1093/nar/gkh340
Essl F, Moser D, Dullinger S, Mang T et al (2010) Selection for commercial forestry determines global patterns of alien conifer invasions. Divers Distrib 16(6):911–921. https://doi.org/10.1111/j.1472-4642.2010.00705.x
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC et al (2013) Robust demographic inference from genomic and SNP data. PLoS Genet 9(10):e1003905. https://doi.org/10.1371/journal.pgen.1003905
Fitch WM, Beintema JJ (1990) Correcting parsimonious trees for unseen nucleotide substitutions: the effect of dense branching as exemplified by ribonuclease. Mol Biol Evol 7(5):438–443. https://doi.org/10.1093/oxfordjournals.molbev.a040617
Fitch WM, Bruschi M (1987) The evolution of prokaryotic ferredoxins–with a general method correcting for unobserved substitutions in less branched lineages. Mol Biol Evol 4(4):381–394. https://doi.org/10.1093/oxfordjournals.molbev.a040452
Fritts TH, Rodda GH (1998) The role of introduced species in the degradation of island ecosystems: a case history of Guam. Annu Rev Ecol Syst 29(1):113–140. https://doi.org/10.1146/annurev.ecolsys.29.1.113
Gaskin JF, Kazmer DJ (2009) Introgression between invasive saltcedars (Tamarix chinensis and T. ramosissima) in the USA. Biol Invasions 11(5):1121–1130. https://doi.org/10.1007/s10530-008-9384-1
Grayson DK (2001) The archaeological record of human impacts on animal populations. J World Prehist 15:1–68. https://doi.org/10.1023/A:1011165119141
Habe T (1953) Land molluscs of Satanomisaki, the southernmost of Kyushu. Venus 17(4):202–207. https://doi.org/10.18941/venusjjmc.17.4_202
Hayase Y, Kimura S, Kawabe K, Minato H (2016) A study on the non-marine molluscan fauna of a coastal area in northern Miyagi Prefeccture, Japan after the 2011 Great East Japan Earthquake and Tsunami. Chiribotan 46(1–2):2–62
Hirano T, Kameda Y, Chiba S (2014a) Phylogeny of the land snails Bradybaena and Phaeohelix (Pulmonata: Bradybaenidae) in Japan. J Molluscan Stud 80(2):177–183. https://doi.org/10.1093/mollus/eyu004
Hirano T, Kameda Y, Kimura K, Chiba S (2014b) Substantial incongruence among the morphology, taxonomy, and molecular phylogeny of the land snails Aegista, Landouria, Trishoplita, and Pseudobuliminus (Pulmonata: Bradybaenidae) occurring in East Asia. Mol Phylogenet Evol 70:171–181. https://doi.org/10.1016/j.ympev.2013.09.020
Hirano T, Saito T, Chiba S (2015) Phylogeny of freshwater viviparid snails in Japan. J Molluscan Stud 81(4):435–441. https://doi.org/10.1093/mollus/eyv019
Hirano T, Kameda Y, Saito T, Chiba S (2019a) Divergence before and after the isolation of islands: phylogeography of the Bradybaena land snails on the Ryukyu Islands of Japan. J Biogeogr 46(6):1197–1213. https://doi.org/10.1111/jbi.13575
Hirano T, Saito T, Tsunamoto Y, Koseki J et al (2019b) Role of ancient lakes in genetic and phenotypic diversification of freshwater snails. Mol Ecol 28(23):5032–5051. https://doi.org/10.1111/mec.15272
Hirano T, Saito T, Tsunamoto Y, Koseki J et al (2019c) Enigmatic incongruence between mtDNA and nDNA revealed by multi-locus phylogenomic analyses in freshwater snails. Sci Rep 9(1):6223. https://doi.org/10.1038/s41598-019-42682-0
Hirano T, Yamazaki D, Uchida S, Saito S et al (2019d) First record of the slug species Semperula wallacei (Issel, 1874) (Gastropoda: Eupulmonata: Veronicellidae) in Japan. BioInvasions Rec 8(2):258–265. https://doi.org/10.3391/bir.2019.8.2.07
Hirano T, Saito T, Shariar SM, Tanchangya TSR et al (2020) The first record of the introduced land snail Bradybaena similaris (Férussac, 1822) (Mollusca: Heterobranchia: Camaenidae) from Bangladesh. BioInvasions Rec 9(4):730–736. https://doi.org/10.3391/bir.2020.9.4.07
Hirano T, Kagawa O, Fujimoto M, Saito T (2022) Species identification of introduced veronicellid slugs in Japan. PeerJ 10:e13197. https://doi.org/10.7717/peerj.13197
Ikezawa H (2012) Expansion of distribution of Bradybaena pellucida in Ibaraki Prefecture and damage to crops. A Museum 73:5
Japan Meteorological Agency (2020) The 2019 edition of climate change monitoring report. https://www.data.jma.go.jp/cpdinfo/monitor/index.html
Katayama K, Kobayashi A, Sakai T, Kuranouchi T et al (2017) Recent progress in sweetpotato breeding and cultivars for diverse applications in Japan. Breed Sci 67(1):3–14. https://doi.org/10.1270/jsbbs.16129
Kim JR, Hayes KA, Yeung NW, Cowie RH (2016) Identity and distribution of introduced slugs (Veronicellidae) in the Hawaiian and Samoan Islands. Pac Sci 70(4):477–493. https://doi.org/10.2984/70.4.7
Kitamura A, Kimoto K (2004) Reconstruction of the southern channel of the Japan Sea at 3.9–1.0 Ma. Quat Res 43(6):417–434. https://doi.org/10.4116/jaqua.43.417
Kitamura A, Kimoto K (2006) History of the inflow of the warm Tsushima Current into the Sea of Japan between 3.5 and 0.8 Ma. Palaeogeogr Palaeoclimatol Palaeoecol 236(3–4):355–366. https://doi.org/10.1016/j.palaeo.2005.11.015
Komai T, Emura S (1955) A study of population genetics on the polymorphic land snail Bradybaena similaris. Evolution 9(4):400–418. https://doi.org/10.2307/2405475
Kuroda T, Habe T (1949) Katatsumuri. Sanmeisya, Tokyo
Lee Y, Schmidt H, Collier TC, Conner WR et al (2019) Genome-wide divergence among invasive populations of Aedes aegypti in California. BMC Genom 20(1):204. https://doi.org/10.1186/s12864-019-5586-4
Matsuoka M (2006) Sugarcane cultivation and sugar industry in Japan. Sugar Tech 8(1):3–9. https://doi.org/10.1007/bf02943734
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE). https://doi.org/10.1109/gce.2010.5676129
Minato H (1988) A systematic and bibliographic list of the Japanese land snails. Nihon Rikusan Kairui Sou‐mokuroku Kanko‐kai, Shirahama
Morisaki K, Sano K, Izuho M (2019) Early Upper Paleolithic blade technology in the Japanese Archipelago. Archaeol Res Asia 17:79–97. https://doi.org/10.1016/j.ara.2018.03.001
Nishi H (2013) A first record of Bradybaena pellucida (Gastropoda: Bradybaenidae) from Aichi Prefecture, central Japan. Sci Rep Toyohashi Mus Nat Hist 23:23–24
Nurinsiyah AS, Hausdorf B (2019) Listing, impact assessment and prioritization of introduced land snail and slug species in Indonesia. J Molluscan Stud 85(1):92–102. https://doi.org/10.1093/mollus/eyy062
Nyumura N, Asami T (2015) Synchronous and non-synchronous semelparity in sibling species of pulmonates. Zool Sci 32(4):372–377. https://doi.org/10.2108/zs150020
Okamoto M (1992) Bradybaena pellucida from Tateyama. Chiba Prefecture Chiribotan 23(1):13–18
Pabijan M, Zieliński P, Dudek K, Stuglik M et al (2017) Isolation and gene flow in a speciation continuum in newts. Mol Phylogenet Evol 116:1–12. https://doi.org/10.1016/j.ympev.2017.08.003
Pei Y, Wu N, Li F (2004) Terrestrial mollusk evidence for the origin and sedimentary environment of the Late Tertiary Red Clay Formation in the Loess Plateau. China Chin Sci Bull 49(10):1072–1076. https://doi.org/10.1007/BF03184039
R Core Team (2020) R: a language and environment for statistical computing. R foundation for statistical computing. https://www.R-project.org/
Rochette N, Rivera-Colón A, Catchen J (2019) Stacks 2: analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28(21):4737–4754. https://doi.org/10.1111/mec.15253
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 19(12):1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Saito T, Do VT, Prozorova L, Hirano T et al (2018) Endangered freshwater limpets in Japan are actually alien invasive species. Conserv Genet 19(4):947–958. https://doi.org/10.1007/s10592-018-1068-5
Schopf JM (1975) Modes of fossil preservation. Rev Palaeobot Palynol 20(1–2):27–53. https://doi.org/10.1016/0034-6667(75)90005-6
Seki K, Inoue S, Asami T (2002) Geographical distributions of sibling species of land snails Bradybaena pellucida and B. similaris in the Boso Peninsula. Venus 61(1–2):41–48. https://doi.org/10.18941/venus.61.1-2_41
Seki K, Wiwegweaw A, Asami T (2008) Fluorescent pigment distinguishes between sibling snail species. Zool Sci 25(12):1212–1219. https://doi.org/10.2108/zsj.25.1212
Serniotti EN, Guzmán LB, Vogler RE, Rumi A et al (2020) New record and range extension of Bradybaena similaris (Férussac, 1822) (Gastropoda, Camaenidae) in Argentina. Check List 16:211. https://doi.org/10.15560/16.1.211
Shen Y, Wang L, Fu J, Xu X et al (2019) Population structure, demographic history and local adaptation of the grass carp. BMC Genom 20(1):467. https://doi.org/10.1186/s12864-019-5872-1
Stahl PW (2009) Adventive vertebrates and historical ecology in the pre-Columbian neotropics. Diversity 1:151–165. https://doi.org/10.3390/d1020151
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: Insights from Argentine ants. Proc Natl Acad Sci USA 98(3):1095–1100. https://doi.org/10.1073/pnas.98.3.1095
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. Sci Rep 5:16963. https://doi.org/10.1038/srep16963
Suyama Y, Hirota SK, Matsuo A, Tsunamoto Y et al (2022) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecol Res 37(1):171–181. https://doi.org/10.1111/1440-1703.12270
Tanabe AS (2011) Kakusan4 and Aminosan: two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Mol Ecol Res 11(5):914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x
Uchida S, Mori H, Kojima T, Hayama K et al (2016) Effects of an invasive ant on land snails in the Ogasawara Islands. Conserv Biol 30(6):1330–1337. https://doi.org/10.1111/cobi.12724
Veeramah KR, Woerner AE, Johnstone L, Gut I et al (2015) Examining phylogenetic relationships among gibbon genera using whole genome sequence data using an approximate bayesian computation approach. Genetics 200(1):295–308. https://doi.org/10.1534/genetics.115.174425
Wegmann D, Leuenberger C, Neuenschwander S, Excoffier L (2010) ABCtoolbox: a versatile toolkit for approximate Bayesian computations. BMC Bioinform 11:116. https://doi.org/10.1186/1471-2105-11-116
Wilcove DS, Rothstein D, Dubow J, Phillips A et al (1998) Quantifying threats to imperiled species in the United States. Bioscience 48(8):607–615. https://doi.org/10.2307/1313420
Wilson KA, Carwardine J, Possingham HP (2009) Setting conservation priorities. Ann N Y Acad Sci 1162(1):237–264. https://doi.org/10.1111/j.1749-6632.2009.04149.x
Wiwegweaw A, Seki K, Mori H, Asami T (2009a) Asymmetric reproductive isolation during simultaneous reciprocal mating in pulmonates. Biol Lett 5(2):240–243. https://doi.org/10.1098/rsbl.2008.0714
Wiwegweaw A, Seki K, Utsuno H, Asami T (2009b) Fitness consequences of reciprocally asymmetric hybridization between simultaneous hermaphrodites. Zool Sci 26(3):191–196. https://doi.org/10.2108/zsj.26.191
Wu M, Asami T (2018) Taxonomical notes on Chinese camaenids with description of three new species (Gastropoda: Pulmonata). Molluscan Res 38(2):137–148. https://doi.org/10.1080/13235818.2017.1380145
Wu M, Chen Z, Zhu X (2019) Two new camaenid land snails (Eupulmonata) from Central China. ZooKeys 861:129–144. https://doi.org/10.3897/zookeys.861.35430
Yan X, Zhenyu L, Gregg WP, Dianmo L (2001) Invasive species in China—an overview. Biodivers Conserv 10(8):1317–1341
Ye B, Saito T, Hirano T, Dong Z et al (2020) Human-geographic effects on variations in the population genetics of Sinotaia quadrata (Gastropoda: Viviparidae) that historically migrated from continental East Asia to Japan. Ecol Evol 10(15):8055–8072. https://doi.org/10.1002/ece3.6456
Zenni RD (2014) Analysis of introduction history of invasive plants in Brazil reveals patterns of association between biogeographical origin and reason for introduction. Austral Ecol 4:401–407. https://doi.org/10.1111/aec.12097
Zenni RD, Nuñez MA (2013) The elephant in the room: the role of failed invasions in understanding invasion biology. Oikos 122(6):801–815. https://doi.org/10.1111/j.1600-0706.2012.00254.x