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Multiple introductions of Sirex noctilio (Hymenoptera: Siricidae) in northeastern North America based on microsatellite genotypes, and implications for biological control

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Abstract

The invasive woodwasp Sirex noctilio (Hymenoptera: Siricidae) has been moved from Eurasia into regions in the Southern Hemisphere, where extensive tree mortality has occurred in pines (Pinus spp.) introduced for forestry. More recently this woodwasp was found in northeastern North America, where pines are native, and it is a species of concern due to the economic importance of pines. Understanding the genetic diversity of North American S. noctilio points to new areas of inquiry, particularly regarding the ability of parasitic nematodes to sterilize woodwasps, which could provide control methods in the US and/or Canada. We investigated the genetic diversity of 924 S. noctilio from nine populations from New York and Pennsylvania (US), Ontario (CA), and Queensland (AU) using nine microsatellite loci. To avoid inflating the number of populations estimated by Bayesian inference, we measured the full-sibling relationships of woodwasps within 13 trees and removed all but one member of each full-sib family from the genetic analysis, resulting in a final sample size of 741 S. noctilio. Within a tree, on average 39% of woodwasps did not have a full sibling, and there were 5.6 families with at least two full-sibling members per tree. The mean family size across trees was 1.9 when single offspring (i.e., no full siblings) were included. Given the short time span since invasion, variation within North American S. noctilio is likely due to differences among founding genotypes. Genetic analyses support the hypothesis that at least two separate introductions occurred. Within North America, genetic distance measures were greatest between a site in southwestern Ontario and all other sites, suggesting that this population could represent a separate introduction event. Two methods of Bayesian clustering also support this idea; they detected 4 or 5 distinct genetic clusters with little admixture between the southwestern Ontario site and other North American populations. The wasps from Australia, where biological control with nematodes has been successful, showed low genetic diversity and clustered with the southwestern Ontario population in one out of two Bayesian analyses. Within the Ontario subset of samples, high woodwasp activity level (i.e., attack and mortality of trees) was associated with one genetic cluster more strongly than another. Population variation should be taken into account in studies of S. noctilio spread and management within North America.

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References

  • Akhurst RJ (1975) Cross-breeding to facilitate the identification of Deladenus spp., nematode parasites of woodwasps. Nematologica 21:267–272

    Google Scholar 

  • Anderson EC, Dunham KK (2008) The influence of family groups on inferences made with the program structure. Mol Ecol Res 8:1219–1229

    CAS  Google Scholar 

  • Ascunce MS, Yang C-C, Oakey J, Calcaterra L, Wu W-J, Shih C-J, Goudet J, Ross KG, Shoemaker D (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331:1066–1068

    CAS  PubMed  Google Scholar 

  • Bedding RA (1972) Biology of Deladenus siricidicola (Neotylenchidae) an entomophagous-mycetophagous nematode parasitic in Siricid woodwasps. Nematologica 18:482–493

    Google Scholar 

  • Bedding RA, Akhurst RJ (1978) Geographical distribution and host preferences of Deladenus species (Nematoda: Neotylenchidae) parasitic on siricid woodwasps and associated Hymenopterous parasitoids. Nematologica 24:286–294

    Google Scholar 

  • Bedding RA, Iede ET (2005) Application of Beddingia siricidicola for Sirex woodwasp control. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Pub, Cambridge, pp 385–399

    Google Scholar 

  • Bergeron M-J, Leal I, Foord B, Ross G, Davis C, Slippers B, de Groot P, Hamelin RC (2011) Putative origin of clonal lineages of Amylostereum areolatum, the fungal symbiont associated with Sirex noctilio, retrieved from Pinus sylvestris, in eastern Canada. Fungal Biol 115:750–758

    PubMed  Google Scholar 

  • Boc A, Diallo AB, Makarenkov V (2012) T-REX: a web server for inferring, validating and visualizing phylogenetic trees and networks. Nucl Acids Res 40:W573–W579

    PubMed Central  PubMed  Google Scholar 

  • Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    CAS  PubMed  Google Scholar 

  • Boissin E, Hurley B, Wingfield MJ, Vasaitis R, Stenlid J, Davis C, de Groot P, Ahumada R, Carnegie AJ, Goldarazena A, Klasmer P, Wermelinger B, Slippers B (2012) Retracing the routes of introduction of invasive species: the case of the Sirex noctilio woodwasp. Mol Ecol 21:5728–5744

    CAS  PubMed  Google Scholar 

  • Bordeaux JM, Lorenz WW, Johnson D, Badgett MJ, Glushka J, Orlando R, Dean JFD (2014) Noctilisin, a venom glycopeptide of Sirex noctilio (Hymenoptera:Siricidae), causes needle wilt and defense gene responses in pines. J Econ Entomol 107:1931–1945

    PubMed  Google Scholar 

  • Brownstein MJ, Carpten JD, Smith JR (1996) Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. Biotechniques 20:1004–1010

    CAS  PubMed  Google Scholar 

  • Caetano IAL, Morris EE, Hajek AE (2016) Growth of the Sirex-parasitic nematode Deladenus siricidicola on the white rot fungus Amylostereum. J Invertebr Pathol 134:12–14

    PubMed  Google Scholar 

  • Carnegie AJ, Bashford R (2012) Sirex woodwasp in Australia: current management strategies, research and emerging issues. In: Slippers B, de Groot P, Wingfield MJ (eds) The Sirex woodwasp and its fungal symbiont: research and management of a worldwide invasive pest. Springer, Dordrecht, pp 175–201

    Google Scholar 

  • Castrillo LA, Hajek AE, Pajares JA, Thomsen IM, Csóka G, Kenaley SC, Kepler RM, Zamora P, Angeli S (2015) Multilocus genotyping of Amylostereum spp. associated with Sirex noctilio and other woodwasps from Europe reveal clonal lineage introduced to the US. Fungal Biol 9:1–10. doi:10.1016/j.funbio.2015.03.004

    Google Scholar 

  • Center for Environmental and Research Information Systems (CERIS) (2015) Purdue University. Survey Status of Sirex woodwasp—Sirex noctilio. Published: 07/26/2016. http://pest.ceris.purdue.edu/map.php?code=ISBBADA&year=2015. Accessed: 07/28/2016

  • Ciesla WM (2003) European woodwasp: a potential threat to North America’s conifer forests. J For 101:18–23

    Google Scholar 

  • Corander J, Martinnen P (2006) Bayesian identification of admixture events using multi-locus molecular markers. Mol Ecol 15:2833–2843

    PubMed  Google Scholar 

  • Coutts MP (1969a) Mechanism of pathogenicity of Sirex noctilio on Pinus radiata. I. Effects of symbiotic fungus Amylostereum sp. (Thelophoraceae). Aust J Biol Sci 22:915–924

    Google Scholar 

  • Coutts MP (1969b) Mechanism of pathogenicity of Sirex noctilio on Pinus radiata. 2. Effects of S. noctilio mucus. Aust J Biol Sci 22:1153–1161

    Google Scholar 

  • Dieni A, Brodeur J, Turgeon J (2016) Reconstruction the invasion history of the lily leaf beetle, Lilioceris lilii, in North America. Biol Invasions 18:31–44

    Google Scholar 

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

    CAS  Google Scholar 

  • Dodds KJ, de Groot P (2012) Sirex, surveys and management: challenges of having Sirex noctilio in North America. In: Slippers B, de Groot P, Wingfield MJ (eds) The Sirex woodwasp and its fungal symbiont: research and management of a worldwide invasive pest. Springer, Dordrecht, pp 265–286

    Google Scholar 

  • Dodds KJ, de Groot P, Orwig DA (2010) The impact of Sirex noctilio in Pinus resinosa and Pinus sylvestris stands in New York and Ontario. Can J For Res 40:212–233

    Google Scholar 

  • Earl DA, von Holdt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fitzpatrick BM, Fordyce JA, Niemiller ML, Reynold RG (2012) What can DNA tell us about biological invasions? Biol Invasions 14:245–253

    Google Scholar 

  • Haavik LJ, Dodds KJ, Allison JD (2015) Do native insects and associated fungi limit non-native woodwasp, Sirex noctilio, survival in a newly invaded environment? PLoS ONE 10(10):e0138516

    PubMed Central  PubMed  Google Scholar 

  • Haavik LJ, Allison JD, MacQuarrie CJK, Nott RW, Ryan K, de Groot P, Turgeon JJ (2016a) Nonlethal effects of nematode infection on Sirex noctilio and Sirex nigricornis (Hymenoptera: Siricidae). Environ Entomol 45:320–327

    PubMed  Google Scholar 

  • Haavik LJ, Dodds KJ, Ryan K, Allison JD (2016b) Evidence that the availability of suitable pines limits non-native Sirex noctilio in Ontario. Agric For Entomol. doi:10.1111/afe.12167

    Article  Google Scholar 

  • Haavik LJ, Yu Q, Turgeon JJ, Allison JD (2016c) Horizontal transmission of a parasitic nematode from a non-native to a native woodwasp? Biol Invasions 18:355–358

    Google Scholar 

  • Hajek AE, Morris EE (2014) Sirex woodwasp (Sirex noctilio Fabricius) (Hymenoptera: Siricidae). In: Van Driesche R, Reardon R (eds) The use of classical biological control to preserve forests in North America. USDA For Serv FHET-2013-2, pp 331–346

  • Hajek AE, Nielsen C, Kepler R, Long SJ, Castrillo L (2013) Fidelity among Sirex woodwasps and their fungal symbionts. Microb Ecol 65:753–762

    PubMed Central  PubMed  Google Scholar 

  • Hoebeke ER, Haugen DA, Haack RA (2005) Sirex noctilio: discovery of a Palearctic siricid woodwasp in New York. Newsl Mich Entomol Soc 50:24–25

    Google Scholar 

  • Hurley BP, Slippers B, Wingfield MJ (2007) A comparison of control results for the alien invasive woodwasp, Sirex noctilio, in the southern hemisphere. Agric For Entomol 9:59–171

    Google Scholar 

  • Hurley BP, Garnas J, Cooperband MF (2015) Assessing trap and lure effectiveness for the monitoring of Sirex noctilio. Agric For Entomol 17:64–70

    Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    CAS  PubMed  Google Scholar 

  • Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Res 10:551–555

    Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    CAS  Google Scholar 

  • Klima K, Travis SE (2012) Genetic population structure of invasive nutria (Myocastor coypus) in Louisiana, USA: is it sufficient for the development of eradication units? Biol Invasions 14:1909–1918

    Google Scholar 

  • Kroll SA, Hajek AE, Morris EE, Long SJ (2013) Parasitism of Sirex noctilio by non-sterilizing Deladenus siricidicola in northeastern North America. Biol Control 67:203–211

    Google Scholar 

  • Lantschner MV, Villacide JM, Garnas JR, Croft P, Carnegie AJ, Liebhold AM, Corley JC (2014) Temperature explains variable spread rates of the invasive woodwasp Sirex noctilio in the southern hemisphere. Biol Invasions 16:329–339

    Google Scholar 

  • Le Roux J, Wieczorek AM (2009) Molecular systematic and population genetics of biological invasions: towards a better understanding of invasive species management. Ann Appl Biol 154:1–17

    Google Scholar 

  • Li D, Shi J, Lu M, Ren L, Zhen C, Luo Y (2015) Detection and identification of the invasive Sirex noctilio (Hymenoptera: Siricidae) fungal symbiont, Amylostereum areolatum (Russulales: Amylostereacea), in China and the stimulating effect of insect venom on Laccase production by A. areolatum YQL03. J Econ Entomol 108:1136–1147

    CAS  PubMed  Google Scholar 

  • Lombaert E, Guillemaud T, Lundgren J, Koch R, Facon B, Grez A, Loomans A, Malausa T, Nedved O, Rhule E, Staverlokk A, Steenberg T, Estoup A (2014) Complementarity of statistical treatments to reconstruct worldwide routes of invasion: the case of the Asian ladybird Harmonia axyridis. Mol Ecol 23:5979–5997

    PubMed  Google Scholar 

  • Madden JL (1974) Oviposition behavior of the woodwasp, Sirex noctilio F. Aust J Zool 22:341–351

    Google Scholar 

  • Madden JL (1981) Egg and larval development in the woodwasp, Sirex noctilio F. Aust J Zool 29:493–506

    Google Scholar 

  • Marisco TD, Wallace LE, Ervin GN, Brooks CP, McClure JE, Welch ME (2011) 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

    Google Scholar 

  • Morgan FD (1968) Bionomics of Siricidae. Ann Rev Entomol 13:239–256

    Google Scholar 

  • Morgan FD, Stewart NC (1966) The biology and behaviour of the woodwasp Sirex noctilio F. in New Zealand. Trans R Soc NZ Zool 7:195–204

    Google Scholar 

  • Morris EE, Jimenez A, Long SJ, Williams DW, Hajek AE (2012) Variability in growth of Deladenus siricidicola on strains of the white rot fungus Amylostereum areolatum. Biocontrol 57:677–686

    Google Scholar 

  • Morris EE, Hajek AE, Zieman E, Williams DW (2014) Deladenus (Tylenchida: Neotylenchidae) reproduction on species and strains of the white rot fungus Amylostereum. Biol Control 73:50–58

    Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Google Scholar 

  • Nielsen C, Williams DW, Hajek AE (2009) Putative source of the invasive Sirex noctilio fungal symbiont, Amylostereum areaolatum, in the eastern United States and its association with native siricid woodwasps. Mycol Res 113:1242–1253

    PubMed  Google Scholar 

  • Park M, Kim K-S, Lee J-H (2013) Genetic structure of Lycorma delicatula (Hemiptera: Fulgoridae) populations in Korea: implication for invasion processes in heterogeneous landscapes. Bull Entomol Res 103:414–424

    CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenA1Ex 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed Central  CAS  PubMed  Google Scholar 

  • Purcell KM, Stockwell CA (2015) An evaluation of the genetic structure and post-introduction dispersal of a non-native invasive fish to the North Island of New Zealand. Biol Invasions 17:625–636

    Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242

    PubMed  Google Scholar 

  • Rodríguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Mol Ecol Res 12:873–884

    Google Scholar 

  • Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Google Scholar 

  • Ryan K, de Groot P, Nott RW, Drabble S, Ochoa I, Smith SM, Turgeon JJ (2012) Natural enemies associated with Sirex noctilio (Hymenoptera: Siriciade) and S. nigricornis in Ontario, Canada. Environ Entomol 42:289–297

    Google Scholar 

  • Ryan K, de Groot P, Smith SM, Turgeon JJ (2013) Seasonal occurrence and spatial distribution of resinosis, a symptom of Sirex noctilio (Hymenoptera: Siriciade) injury, on boles of Pinus sylvestris (Pinaceae). Can Entomol 145:117–122

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  Google Scholar 

  • Santana QC, Coetzee MPA, Steenkamp ET, Mlonyeni OX, Hammond GNA, Wingfield MJ, Wingfield BD (2009) Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques 46:217–223

    CAS  Google Scholar 

  • Spradbery JP (1977) The oviposition biology of siricid woodwasps in Europe. Ecol Entomol 2:225–230

    Google Scholar 

  • Takezaki N, Nei M, Tamura K (2014) POPTREEW: web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Mol Biol Evol 31:1622–1624

    CAS  PubMed  Google Scholar 

  • Taylor KL (1978) Evaluation of the insect parasitoids of Sirex noctilio (Hymenoptera: Siricidae) in Tasmania. Oecologia 32:1–10

    CAS  PubMed  Google Scholar 

  • Thompson BM, Bodart J, McEwen C, Gruner DS (2014) Adaptations for symbiont-mediated external digestion in Sirex noctilio (Hymenoptera: Siricidae). Ann Entomol Soc Am 107:453–460

    Google Scholar 

  • Williams DW, Zylstra KE, Mastro VC (2012) Ecological considerations in using Deladenus (= Beddingia) siricidicola for the biological control of Sirex noctilio in North America. In: Slippers B, de Groot P, Wingfield MJ (eds) The Sirex woodwasp and its fungal symbiont: research and management of a worldwide invasive pest. Springer, Dordrecht, pp 119–134

    Google Scholar 

  • Wu Y, Molongoski JJ, Winograd DF, Bogdanowicz SM, Louyakis AS, Lance DR, Mastro VC, Harrison RG (2015) Genetic structure, admixture and invasion success in a Holarctic defoliator, the gypsy moth (Lymantria dispar, Lepidoptera: Erebidae). Mol Ecol 24:1275–1291

    CAS  PubMed  Google Scholar 

  • Yu Q, de Groot P, Leal I, Davis C, Ye W, Foord B (2009) Characterization of Deladenus siricidicola (Tylenchida: Neotylenchidae) associated with Sirex noctilio (Hymenoptera: Siricidae) in Canada. Int J Nematol 19:23–32

    Google Scholar 

  • Zondag R (1969) A nematode infection of Sirex noctilio (F.) in New Zealand. NZ J Sci 12:732–747

    Google Scholar 

  • Zondag R (1974) A non-sterilising strain of Deladenus siricidicola. For Res Inst Rep 1974, Rotorua, NZ pp 51–52

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Acknowledgements

We thank Bernard Slippers (Forestry and Agricultural Biotechnology Institute, South Africa) for providing the microsatellite primer sequences, Steve Bogdanowicz (Cornell University) for advice on molecular methods, Claire Moreland-Ochoa and Jacob Henry (Cornell University) for assistance in the lab, Christopher Foelker and Melissa Fierke (State University of New York College of Environmental Science and Forestry) for access to some New York samples, Brad Regester, Bill Laubscher, and Eric Butters (Pennsylvania Bureau of Forestry) for field assistance in Pennsylvania, and Martin Ziech (Cornell University) for creating the regional map in GIS. This project was funded by a USDA Forest Service Cooperative Agreement Grant to A.E. Hajek.

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Bittner, T.D., Hajek, A.E., Haavik, L. et al. Multiple introductions of Sirex noctilio (Hymenoptera: Siricidae) in northeastern North America based on microsatellite genotypes, and implications for biological control. Biol Invasions 19, 1431–1447 (2017). https://doi.org/10.1007/s10530-016-1365-1

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