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Geographic patterns of genetic diversity from the native range of Cactoblastis cactorum (Berg) support the documented history of invasion and multiple introductions for invasive populations

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Abstract

Spread of the invasive cactus-feeding moth Cactoblastis cactorum has been well documented since its export from Argentina to Australia as a biocontrol agent, and records suggest that all non-native populations are derived from a single collection in the moth’s native range. The subsequent global spread of the moth has been complex, and previous research has suggested multiple introductions into North America. There exists the possibility of additional emigrations from the native range in nursery stock during the late twentieth century. Here, we present mitochondrial gene sequence data (COI) from South America (native range) and North America (invasive range) to test the hypothesis that the rapid invasive spread in North America is enhanced by unique genetic combinations from isolated portions of the native range. We found that haplotype richness in the native range of C. cactorum is high and that there was 90% lower richness in Florida than in Argentina. All Florida C. cactorum haplotypes are represented in a single, well-defined clade, which includes collections from the reported region of original export from Argentina. Thus, our data are consistent with the documented history suggesting a single exportation of C. cactorum from the eastern region of the native range. Additionally, the presence of geographic structure in three distinct haplotypes within the same clade across Florida supports the hypothesis of multiple introductions into Florida from a location outside the native range. Because the common haplotypes in Florida are also known to occur in the neighboring Caribbean Islands, the islands are a likely source for independent North American colonization events. Our data show that rapid and successful invasion within North America cannot be attributed to unique genetic combinations. This suggests that successful invasion of the southeastern US is more likely the product of a fortuitous introduction into favorable abiotic conditions and/or defense responses of specific Opuntia hosts, rapid adaptation, or a release from native enemies.

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References

  • Annecke DP, Moran VC (1978) Critical reviews of biological pest control in South Africa. 2. The prickly pear, Opuntia ficus-indica (L.) Miller. J Entomol Soc S Afr 41:161–188

    Google Scholar 

  • Baker AJ, Stiling P (2009) Comparing the effects of the exotic cactus-feeding moth, Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) and the native cactus-feeding moth, Melitara prodenialis (Walker) (Lepidoptera: Pyralidae) on two species of Florida Opuntia. Biol Invasions 11:619–624

    Article  Google Scholar 

  • Boman S, Grapputo A, Lindström L, Lyytinen A, Mappes J (2008) Quantitative genetic approach for assessing invasiveness: geographic and genetic variation in life-history traits. Biol Invasions 10:1135–1145

    Article  Google Scholar 

  • Caterino MS, Sperling FAH (1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 11:122–137

    Article  PubMed  CAS  Google Scholar 

  • Dickel TS (1991) Cactoblastis cactorum in Florida (Lepidoptera: Pyralidae: Phycitinae). Trop Lepid 2:117–118

    Google Scholar 

  • Dlugosch KM, Parker IM (2008a) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449

    Article  PubMed  CAS  Google Scholar 

  • Dlugosch KM, Parker IM (2008b) Invading populations of an ornamental shrub show rapid life history evolution despite genetic bottlenecks. Ecol Lett 11:701–709

    Article  PubMed  Google Scholar 

  • Dodd AP (1927) The biological control of prickly pear in Australia. Commonwealth Council for Scientific and Industrial Research, Bulletin no. 34, Melbourne, Australia

  • Dodd AP (1940) The biological campaign against prickly-pear. Commonwealth Prickly Pear Board, Brisbane

    Google Scholar 

  • Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  CAS  Google Scholar 

  • Foxcroft LC, Hoffmann JH, Viljoen JJ, Kotze JJ (2007) Factors influencing the distribution of Cactoblastis cactorum, a biological control agent of Opuntia stricta in Kruger National Park, South Africa. S Afr J Bot 73:113–117

    Article  Google Scholar 

  • Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94:385

    Article  PubMed  CAS  Google Scholar 

  • 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 29:113–140

    Article  Google Scholar 

  • Griffin GJ (2000) Blight control and restoration of the American chestnut. J For 98:22–27

    Google Scholar 

  • Habeck DH, Bennett FD (1990) Cactoblastis cactorum Berg (Lepidoptera: Pyralidae), a Phycitine new to Florida. Entomology Circular No. 333, Florida Department of Agriculture and Consumer Services, Division of Plant Industry

  • Hight SD, Carpenter JE, Bloem KA, Bloem S, Pemberton RW, Stiling P (2002) Expanding geographical range of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Fla Entomol 85:527–529

    Article  Google Scholar 

  • Hoffmann JH, Moran VC, Zeller DA (1998a) Evaluation of Cactoblastis cactorum (Lepidoptera: Phycitidae) as a biological control agent of Opuntia stricta (Cactaceae) in the Kruger National Park, South Africa. Biol Control 12:20–24

    Article  Google Scholar 

  • Hoffmann JH, Moran VC, Zeller DA (1998b) Long-term population studies and the development of an integrated management programme for control of Opuntia stricta in Kruger National Park, South Africa. J Appl Ecol 35:156–160

    Article  Google Scholar 

  • Holland BS (2000) Genetics of marine bioinvasions. Hydrobiologia 420:63–71

    Article  CAS  Google Scholar 

  • Holland BS (2001) Invasion without a bottleneck: microsatellite variation in natural and invasive populations of the brown mussel, Perna perna (L.). Mar Biotechnol 3:407–415

    Article  PubMed  CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Johnson DM, Stiling PD (1996) Host specificity of Cactoblastis cactorum (Lepidoptera: Pyralidae), an exotic Opuntia-feeding moth, in Florida. Environ Entomol 25:743–748

    Google Scholar 

  • Johnson DM, Stiling PD (1998) Distribution and dispersal of Cactoblastis cactorum (Lepidoptera: Pyralidae), an exotic Opuntia-feeding moth, in Florida. Fla Entomol 81:12–22

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  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  PubMed  CAS  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci USA 104:3883–3888

    Article  PubMed  CAS  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17:386–391

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Logarzo G, Varone L, Briano J (2008) Cactus moth. 2008 Annual Report. South American Biological Control Laboratory. USDA, ARS, Buenos Aires, Argentina

  • Meimberg H, Hammond JI, Jorgensen CM, Park TW, Gerlach JD, Rice KJ, McKay JK (2006) Molecular evidence for an extreme genetic bottleneck during introduction of an invading grass to California. Biol Invasions 8:1355–1366

    Article  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Novak SJ (2007) The role of evolution in the invasion process. Proc Natl Acad Sci USA 104:3671–3672

    Article  PubMed  CAS  Google Scholar 

  • Novak SJ, Mack RN (2005) Genetic bottlenecks in alien species invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, pp 201–228

    Google Scholar 

  • Pascual-Hortal L, Saura S (2006) Comparison and development of new graph-based landscape connectivity indices: towards the prioritization of habitat patches and corridors for conservation. Landsc Ecol 21:959–967

    Article  Google Scholar 

  • Payne JH (2009) US Department of Agriculture—Animal and Plant Health Inspections Services report DA-2009-25. Available via http://www.aphis.usda.gov/plant_health/plant_pest_info/cactoblastis/reports.shtml. Accessed 20 July 2009

  • Pemberton RW (1995) Cactoblastis cactorum (Lepidoptera: Pyralidae) in the United States: an immigrant biological control agent or an introduction of the nursery trade? Am Entomol 41:230–232

    Google Scholar 

  • Pemberton RW, Cordo HA (2001a) Nosema (Microsporidia: Nosematidae) species as potential biological control agents of Cactoblastis cactorum (Lepidoptera: Pyralidae): surveys for the microsporidia in Argentina and South Africa. Fla Entomol 84:527–530

    Article  Google Scholar 

  • Pemberton RW, Cordo HA (2001b) Potential and risks of biological control of Cactoblastis cactorum (Lepidoptera: Pyralidae) in North America. Fla Entomol 84:513–526

    Article  Google Scholar 

  • Pemberton RW, Liu H (2007) Control and persistence of native Opuntia on Nevis and St. Kitts 50 years after the introduction of Cactoblastis cactorum. Biol Control 41:272–282

    Article  Google Scholar 

  • Pettey FW (1947) The biological control of prickly pears in South Africa. Department of Agriculture, Science Bulletin 271. Entomology Series No. 22, Pretoria

  • Pinkava DJ (2003) Opuntia. In: Flora of North America Editorial Committee (ed) Flora of North America north of Mexico, vol 4. Oxford University Press, New York, pp 123–148

    Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–819

    Article  PubMed  CAS  Google Scholar 

  • Puillandre N, Dupas S, Dangles O, Zeddam J-L, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J-F (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333

    Article  Google Scholar 

  • Raghu S, Walton C (2007) Understanding the ghost of Cactoblastis past: historical clarifications on a poster child of classical biological control. Bioscience 57:699–705

    Article  Google Scholar 

  • Rannala B, Yang ZH (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    Article  PubMed  CAS  Google Scholar 

  • Reed DH, Frankham R (2001) How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103

    PubMed  CAS  Google Scholar 

  • Reznick DN, Shaw FH, Rodd FH, Shaw RG (1997) Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275:1934–1937

    Article  PubMed  CAS  Google Scholar 

  • Roane MK, Griffin GJ, Elkins JR (1986) Chestnut blight, other Endothia diseases and the genus Endothia. APS Press, St. Paul

    Google Scholar 

  • Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Heulsenbeck JP, van der Mark P (2005) MrBayes 3.1 Manual. Available via http://mrbayes.csit.fsu.edu/index.php. Accessed 2 October 2009

  • Rosenberg MS (2001) PASSAGE. Pattern analysis, spatial statistics, and geographic exegesis. Version 1.1. Department of Biology, Arizona State University, Tempe, AZ

  • Rubinoff D, Holland BS, Shibata A, Messing RH, Wright MG (2010) Rapid invasion despite lack of genetic variation in the erythrina gall wasp (Quadrastichus erythrinae Kim). Pac Sci 64:23–31

    Article  CAS  Google Scholar 

  • Sauby KE (2009) The ecology of Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) in Florida. Master’s thesis, Mississippi State University, Mississippi State, MS

  • Saura S, Pascual-Hortal L (2007) A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landsc Urban Plan 83:91–103

    Article  Google Scholar 

  • Simmonds FJ, Bennett FD (1966) Biological control of Opuntia spp. by Cactoblastis cactorum in the Leeward Islands (West Indies). Entomophaga 11:183–189

    Article  Google Scholar 

  • Simon C, Frati F, Breckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Simonsen TJ, Brown RL, Sperling FAH (2008) Tracing an invasion: phylogeography of Cactoblastis cactorum (Lepidoptera: Pyralidae) in the United States based on mitochondrial DNA. Ann Entomol Soc Am 101:899–905

    Article  CAS  Google Scholar 

  • Simonson SE, Stohlgren TJ, Tyler L, Gregg WP, Muir R, Garrett LJ (2005) Preliminary assessment of the potential impacts and risks of the invasive cactus moth, Cactoblastis cactorum Berg, in the U.S. and Mexico. Final Report to the International Atomic Energy Agency, IAEA

  • Suarez AV, Tsutsui ND (2008) The evolutionary consequences of biological invasions. Mol Ecol 17:351–360

    Article  PubMed  Google Scholar 

  • Torchin ME, Mitchell CE (2004) Parasites, pathogens, and invasions by plants and animals. Front Ecol Environ 2:183–190

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  PubMed  CAS  Google Scholar 

  • Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, pp 229–257

    Google Scholar 

  • Weir BS (1996) Genetic data analysis II: methods for discrete population genetic data. Sinauer, Sunderland

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whitney KD, Gabler CA (2008) Rapid evolution in introduced species, ‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Divers Distrib 14:569–580

    Article  Google Scholar 

  • Zimmerman HG, Sandi y Cuen MP, Rivera AB (2005) The status of Cactoblastis cactorum (Lepidoptera: Pyralidae) in the Caribbean and the likelihood of its spread to Mexico. Report to the IAEA—TC Project MEX/5/029

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Acknowledgments

This work was supported in part by grants from the U.S. Geological Survey Biological Resources Discipline (04HQAG0135 and 08HQAG0139) and U.S. Department of Agriculture (2007-55320-17847) to GNE. Additional funds were provided by the Mississippi State University Office of Research and Economic Development and the College of Arts and Sciences. We also thank Guillermo Logarzo and Laura Varone (USDA South American Biological Control Laboratory, Buenos Aires), James Carpenter (USDA-ARS Crop Protection and Management Research Unit, Tifton, GA), Stephen Hight (USDA-ARS Insect Behavior and Biocontrol Research Unit, Gainesville, FL), Kristen Sauby, and Anastasia Woodard for assistance with sample collection. We are grateful to Richard Brown (Mississippi Entomological Museum) who assisted in the identification of some samples. We thank three anonymous reviewers for their comments that improved the manuscript.

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  1. Jessica E. McClure

    Present address: College of Criminal Justice, Sam Houston State University, Huntsville, TX, USA

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  1. Department of Biological Sciences, Mississippi State University, Mississippi State, MS, USA

    Travis D. Marsico, Lisa E. Wallace, Gary N. Ervin, Christopher P. Brooks, Jessica E. McClure & Mark E. Welch

  2. Department of Biological Sciences, Arkansas State University, PO Box 599, State University, AR, 72467, USA

    Travis D. Marsico

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Marsico, T.D., Wallace, L.E., Ervin, G.N. et al. Geographic patterns of genetic diversity from the native range of Cactoblastis cactorum (Berg) support the documented history of invasion and multiple introductions for invasive populations. Biol Invasions 13, 857–868 (2011). https://doi.org/10.1007/s10530-010-9874-9

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