Skip to main content
SpringerLink
Log in

Genetic exchange between two freshwater apple snails, Pomacea canaliculata and Pomacea maculata invading East and Southeast Asia

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Two species of apple snails, Pomacea canaliculata and Pomacea maculata (formerly Pomacea insularum), have invaded many countries of East and Southeast Asia from their native range in South America. This study investigated the genetic structure of the two species invading these areas. Phylogenetic analysis based on sequences of the nuclear gene elongation factor 1-alpha (EF1α) detected two well-supported clades (Clade C and Clade M). Both P. canaliculata and P. maculata were represented in each clade. Some snails had both Clade C and Clade M EF1α sequences. These results suggest genetic exchange between snails of the two clades. A mating experiment between P. canaliculata with Clade C EF1α sequences and P. maculata with Clade M EF1α sequences resulted in viable F1 progeny under laboratory conditions. The genetic exchange was also inferred in some populations collected from Argentina, suggesting an existence of hybrid in the native range. Simple identification of EF1α types using a restriction enzyme, ApaLI, detected significant geographical structure of the EF1α variants in the invaded area. The divergent geographical structure could have resulted from either the founder effect or the bridgehead effect, although further genetic analysis is needed to clarify this. Average individual egg weight, which is an indicator of egg size, was higher in P. canaliculata than P. maculata in both field and laboratory reared samples, suggesting that some (probably most) P. canaliculata and P. maculata invading East and Southeast Asia still maintain species-specific populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbott RJ, Brennan AC, James JK, Forbes DG, Hegarty MJ, Hiscock SJ (2009) Recent hybrid origin and invasion of the British Isles by a self-incompatible species, Oxford ragwort (Senecio squalidus L., Asteraceae). Biol Invasions 11:1145–1158

    Article  Google Scholar 

  • Andrews EB (1964) The functional anatomy and histology of the reproductive system of some pilid gastropod molluscs. Proc Malacol Soc 36:121–140

    Google Scholar 

  • Blair AC, Hufbauer RA (2010) Hybridization and invasion: one of North America’s most devastating invasive plants shows evidence for a history of interspecific hybridization. Evol Appl 3:40–51

    Article  Google Scholar 

  • Carlsson NOL, Brönmark C, Hansson L (2004) Invading herbivory: the golden apple snail alters ecosystem functioning in Asian wetlands. Ecology 85:1575–1580

    Article  Google Scholar 

  • Cowie RH, Hayes KA, Thiengo SC (2006) What are apple snails? Confused taxonomy and some preliminary resolution. In: Joshi RC, Sebastian LS (eds) Global advances in ecology and management of golden apple snails. Philippine Rice Research Institute, Nueva Ecija, pp 3–23

    Google Scholar 

  • Cox GW (2004) Alien species and evolution. Island Press, Washington, DC

    Google Scholar 

  • Ellstrand NC, Schierenbeck KA (2006) Hybridization as a stimulus for the evolution of invasiveness in plants? Euphytica 148:35–46

    Article  Google Scholar 

  • Ficetola GF, Bonin A, Miaud C (2008) Population genetics reveals origin and number of founders in a biological invasion. Mol Ecol 17:773–782

    Article  CAS  PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz W, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Gonthier P, Nicolotti G, Linzer R, Guglielmo F, Garbelotto M (2007) Invasion of European pine stands by a North American forest pathogen and its hybridization with a native interfertile taxon. Mol Ecol 16:1389–1400

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Halwart M (1994) The golden apple snail Pomacea canaliculata in Asian rice farming systems: present impact and future threat. Int J Pest Manag 40:199–206

    Article  Google Scholar 

  • Hayes KA, Joshi RC, Thiengo SC, Cowie RH (2008) Out of South America: multiple origins of non-native apple snails in Asia. Divers Distrib 14:701–712

    Article  Google Scholar 

  • Hayes KA, Cowie RH, Thiengo SC (2009) A global phylogeny of apple snails: Gondwanan origin, generic relationships, and the influence of outgroup choice (Caenogastropoda: Ampullariidae). Biol J Linn Soc 98:61–76

    Article  Google Scholar 

  • Hayes KA, Cowie RH, Thiengo SC, Strong EE (2012) Comparing apples with apples: clarifying the identities of two highly invasive neotropical Ampullariidae (Caenogastropoda). Zool J Linn Soc 166:723–753

    Article  Google Scholar 

  • Jaquiéry J, Vogel V, Keller L (2005) Multilevel genetic analyses of two European supercolonies of the Argentine ant, Linepithema humile. Mol Ecol 14:589–598

    Article  PubMed  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    Article  CAS  PubMed  Google Scholar 

  • Kwong KL, Robert KY, Qiu JW (2009) The potential of the invasive snail Pomacea canaliculata as a predator of various life-stages of five species of freshwater snails. Malacologia 51:343–356

    Article  Google Scholar 

  • Kwong KL, Dudgeon D, Wong PK, Qiu J-W (2010) Secondary production and diet of an invasive snail in freshwater wetlands: implications for resource utilization and competition. Biol Invasions 12:1153–1164

    Article  Google Scholar 

  • Lambrions JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics? Ecology 52:2061–2070

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet J-M, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS One 5:e9743

    Article  PubMed  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species a selection from the global invasive species database. Aliens 12, December 2000. The Invasive Species Specialist Group (ISSG)

  • Lv S, Zhang Y, Chen S-R, Wang L-B, Fang W, Chen F, Jiang J-Y, Li Y-L, Du Z-W, Zhou X-N (2009) Human angiostrongyliasis outbreak in Dali, China. PLoS Negl Trop Dis 3:e520

    Article  PubMed  Google Scholar 

  • Matsukura K, Okuda M, Kubota K, Wada T (2008) Genetic divergence of the genus Pomacea (Gastropoda: Ampullariidae) distributed in Japan, and a simple molecular method to distinguish between P. canaliculata and P. maculata. Appl Entomol Zool 43:535–540

    Article  CAS  Google Scholar 

  • Milne RI, Abbott RJ (2004) Geographic origin and taxonomic status of the invasive Privet, Ligustrum robustum (Oleaceae), in the Mascarene Islands, determined by chloroplast DNA and RAPDs. Heredity 92:78–87

    Article  CAS  PubMed  Google Scholar 

  • Navia D, de Moraes GJ, Roderick G, Navajas M (2005) The invasive coconut mite Aceria guerreronis (Acari: Eriophyidae): origin and invasion sources inferred from mitochondrial (16S) and nuclear (ITS) sequences. Bull Entomol Res 95:205–516

    Article  Google Scholar 

  • Nishimura K, Saito Y (1986) Natural infection with Angiostrongylus cantonensis in Ampullarius canaliculatus (Lamarck) in the Ryukyu Islands, Japan. Jpn J Parasitol 35:469–470

    Google Scholar 

  • Perry WL, Feder JL, Dwyer G, Lodge DM (2001) Hybrid zone dynamics and species replacement between Orconectes crayfishes in a Northern Wisconsin lake. Evolution 55:1153–1166

    CAS  PubMed  Google Scholar 

  • Petit RJ (2004) Biological invasions at the gene level. Divers Distrib 10:159–165

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rawlings TA, Hayes KA, Cowie RH, Collins TM (2007) The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evol Biol 7:97

    Article  PubMed  Google Scholar 

  • Wada T (2004) Strategies for controlling the apple snail Pomacea canaliculata (Lamarck) (Gastropoda: Ampullariidae) in Japanese direct-sown paddy fields. Jpn Agric Res Quart 38:75–80

    Google Scholar 

  • Yang X-M, Sun J-T, Xue X-F, Li J-B, Hong X-Y (2012) Invasion genetics of the western flower thrips in China: evidence for genetic bottleneck, hybridization and bridgehead effect. PLoS One 7:e34567

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank K. Ito, M. Doi, A. Ozawa, Y. Yusa, K. Yoshida, K. Hidaka, S. Hoshino, A. Murakami, C. Moromizato, M. Daiku, T. Imbe, F. Nagumo, N. Horisue, A. Hoshikawa, T. Watanabe and K. Ichinose for collecting snails. We thank K. Hayes and R. Cowie for extensive help with the manuscript. And we thank all members of the Research Team for Insect and Nematode Management and the Research Team for Vegetables and Ornamental Crops in Southern Japan for their valuable suggestions regarding our study.

Author information

Authors and Affiliations

  1. National Agricultural Research Center for Kyushu Okinawa Region, Suya 2421, Koshi, Kumamoto, 861-1192, Japan

    Keiichiro Matsukura, Mitsuru Okuda & Takashi Wada

  2. Universidad Nacional del Sur, San Juan 670, 8000, Bahia Blanca, Argentina

    Néstor Jorge Cazzaniga

Authors
  1. Keiichiro Matsukura
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mitsuru Okuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Néstor Jorge Cazzaniga
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takashi Wada
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Keiichiro Matsukura.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Matsukura, K., Okuda, M., Cazzaniga, N.J. et al. Genetic exchange between two freshwater apple snails, Pomacea canaliculata and Pomacea maculata invading East and Southeast Asia. Biol Invasions 15, 2039–2048 (2013). https://doi.org/10.1007/s10530-013-0431-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-013-0431-1

Keywords

Search

Navigation