Skip to main content

Advertisement

Log in

Strong genetic structure among populations of the invasive avocado pest Pseudacysta perseae (Heidemann) (Hemiptera: Tingidae) reveals the source of introduced populations

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

Abstract

In 2004, the avocado lace bug (ALB) Pseudacysta perseae, was discovered in San Diego County, CA, USA. Historically, California avocado producers have relied on biological control for suppression of injurious pests. A fundamental step in identifying biological control agents is determining the source of the invasive population, thus allowing a focused search of that area for natural enemies most closely adapted to the invasive pest genotype. In an attempt to determine the geographic area of origin for ALB to assist incipient biological control efforts, mitochondrial and microsatellite markers were used to compare the genetic profile of the California population of ALB with that of populations from the pest’s known range in the US, Guatemala, Mexico and the Caribbean. Both types of marker revealed evidence for strong genetic structure among the sampled populations. Mitochondrial sequences narrowed the geographic origin of the California population, to populations in Texas and several Mexican states. This geographic range was refined further with the analysis of allele frequencies at eight microsatellite loci which identified ALB populations in the state of Nayarit, Mexico, as the most probable origin of the California population. Any effort to identify natural enemies of ALB for use in biological control in California should therefore focus on Nayarit. The strong genetic structure present among the ALB populations studied is discussed with regards to the potential influence of cytoplasmic incompatibility-inducing endosymbionts, host plant variation, and the putative native range of this pest.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Almaguel L, Blanco E, Suárez P, de la Torre P, Cáceres I, Nieves C, Márquez ME, Blanco L (1999) Control de la chinche del aguacate (Pseudacysta perseae (Heidemann)) en Ciudad de La Habana. Fitosanidad 3:69–74

    Google Scholar 

  • Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MCJ, Tettelin H, Werren JH (2006) Multiolocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72:7098–7110

    Article  PubMed  CAS  Google Scholar 

  • Ballard JWO, Melvin RG (2010) Linking the mitochondrial genotype to the organismal phenotype. Mol Ecol 19:1523–1539

    Article  PubMed  CAS  Google Scholar 

  • Bender G (1993) A new mite problem on avocados. Calif Avocado Soc Yearb 77:73–77

    Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2008) GenBank. Nucleic Acids Res 36:D25–D30

    Article  PubMed  CAS  Google Scholar 

  • Braig HR, Zhou W, Dobson S, O’Neill SL (1998) Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia. J Bacteriol 180:2373–2378

    PubMed  CAS  Google Scholar 

  • Byrne FJ, Humeres EC, Urena AA, Hoddle MS, Morse JG (2010) Field evaluation of systemic imidacloprid for the management of avocado thrips and avocado lace bug in California avocado groves. Pest Manag Sci 66:1129–1136

    Article  PubMed  CAS  Google Scholar 

  • Campbell BC, Steffen-Campbell JD, Werren JH (1993) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an rDNA internal transcribed spacer (ITS2) and 28 s rDNA sequences. Insect Mol Biol 2:225–237

    Article  PubMed  CAS  Google Scholar 

  • Campbell B, Heraty JM, Rasplus J-Y, Chan K, Steffen-Campbell J, Babcock C (2000) Molecular systematics of the Chalcidoidea using 28 s-D2 rDNA. In: Austin A, Dowton M (eds) The Hymenoptera: evolution, biodiversity and biological control. CSIRO Publishing, Victoria, pp 57–71

    Google Scholar 

  • Chen H, Morrell PL, Ashworth VETM, de la Cruz M, Clegg MT (2009) Tracing the geographic origin of major avocado cultivars. J Hered 100:56–65

    Article  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Cornuet J-M, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Crane JH, Balerdi CF, Maguire I (2007) Avocado growing in the Florida home landscape. Circular 1034, Horticultural Sciences Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida

  • de la Torre P, Almaguel L, Blanco E (1999) Daños, distribución y enemigos naturales de la chinche de encaje del aguacate Pseudacysta perseae (Heidemann) (Hemiptera: Tingidae). Fitosanidad 3:69–74

    Google Scholar 

  • Dlugosch KM, Parker M (2008) 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 

  • Earl DA (2010) Structure Harvester v0.56.4. http://taylor0.biology.ucla.edu/struct_harvest/. Accessed 28 Feb 2011

  • 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

    Article  PubMed  CAS  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 Bioinforma Online 1:47–50

    CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, 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

    PubMed  CAS  Google Scholar 

  • Gagné R, Peña JE, Acevedo FE (2008) A new Lestodiplosine (Diptera: Cecidomyiidae) preying on the avocado lace bug, Pesudacysta perseae (Hemiptera: Tingidae) in southern Florida. Fla Entomol 91:43–48

    Article  Google Scholar 

  • Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-Fein E (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol 72:3646–3652

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J (2001) FSTAT, version 2.9.3: a program to estimate and test gene diversities and fixation indices. Institute of Ecology, University of Lausanne, Switzerland. http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 28 Feb 2011

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user friendly biological sequence alignment and analysis program from Windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    Article  CAS  Google Scholar 

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101:14812–14817

    Article  PubMed  CAS  Google Scholar 

  • Heidemann O (1908) Two species of North American Tingitidae (Hemiptera: Heteroptera). Proc Entomol Soc Wash 10:103–108

    Google Scholar 

  • Henry TJ, Peña JE, Long D, Acevedo F (2009) Stethoconus praefectus (Hemiptera: Miridae): first North American records of an old world plant bug predacious on avocado lace bug, Pseudacysta perseae (Hemiptera: Tingidae), in Florida. Proc Entomol Soc Wash 111:98–105

    Article  Google Scholar 

  • Hoddle MS (2004) Invasions of leaf feeding arthropods: why are so many new pests attacking California grown avocados? Calif Avocado Soc Yearb 87:65–81

    Google Scholar 

  • Hoddle MS, Morse JG (2003) Avocado thrips biology and control. AvoResearch, California Avocado Commission, Irvine

    Google Scholar 

  • Hoddle MS, Jetter KM, Morse JG (2003) The economic impact of Scirtothrips perseae Nakahara (Thysanoptera: Thripidae) on California avocado production. Crop Prot 22:485–493

    Article  Google Scholar 

  • Hoddle MS, Morse J, Stouthamer R, Humeres E, Jeong G, Roltsch W, Bender GS, Phillips P, Kellum D, Dowell R, Witney GW (2005) Avocado lace bug in California. Calif Avocado Soc Yearb 88:67–79

    Google Scholar 

  • Humeres EC, Morse JG (2006) Resistance of avocado thrips (Thysanoptera: Thripidae) to sabadilla, a botanically derived bait. Pest Manag Sci 62:886–889

    Article  CAS  Google Scholar 

  • Humeres EC, Morse JG, Roltsch W, Hoddle MS (2009a) Detection surveys and population monitoring for Pseudacysta perseae on avocados in Southern California. Fla Entomol 92:382–385

    Article  Google Scholar 

  • Humeres EC, Morse JG, Stouthamer R, Roltsch W, Hoddle MS (2009b) Evaluation of natural enemies and insecticides for control of Pseudacysta perseae (Hemiptera: Tingidae) on avocados in Southern California. Fla Entomol 92:35–42

    Article  CAS  Google Scholar 

  • Hunter MS, Perlman SJ, Kelly SE (2003) A bacterial symbiont in the Bacterioidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proc R Soc Lond B 270:2185–2190

    Article  Google Scholar 

  • Hurst GDD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond B 272:1525–1534

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v.5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet J-M, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  PubMed  CAS  Google Scholar 

  • McMurtry JA (1992) The role of exotic natural enemies in the biological control of insect and mite pests of avocado in California. In: Proceedings of II world avocado congress, pp 247–252

  • Mead F, Peña JE (1991) Avocado lace bug, Pesudacysta perseae (Hemiptera: Tingidae). Entomology Circular No. 346, Florida Department of Agriculture & Consumer Services, Division of Plant Industry

  • Mills NJ, Daane KM (2005) Biological and cultural controls … Nonpesticide alternatives can suppress crop pests. Cal Ag 59:23–28

    Article  Google Scholar 

  • Mitsuhashi W, Saiki T, Wei W, Kawakita H, Sato M (2002) Two novel strains of Wolbachia coexisting in both species of mulberry leafhoppers. Insect Mol Biol 11:577–584

    Article  PubMed  CAS  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:582–590

    Google Scholar 

  • Noda H, Koizumi Y, Zang Q, Deng K (2001) Infection density of Wolbachia and incompatibility lecel in two planthopper species, Laodelphax striatellus and Sagatella furcifera. Insect Biochem Mol Biol 31:727–737

    Article  PubMed  CAS  Google Scholar 

  • Peña JE (2003) Pests of avocado in Florida. In: Proceedings of V world avocado congress, pp 487–494

  • Peña JE, Sundhari S, Hunsberger A, Duncan R, Schaffer B (1998) Monitoring, damage, natural enemies and control of avocado lace bug, Pseudacysta perseae (Hemiptera: Tingidae). Proc Fla State Hortic Soc 111:330–334

    Google Scholar 

  • Peña JE, Triapitsyn SV, Long D, Evans GA, Roltsch W (2009) First record of Erythmelus klopomor (Hymenoptera: Mymaridae) as a parasitoid of the avocado lace bug, Pseudacysta perseae (Heteroptera: Tingidae). Fla Entomol 92:394–395

    Article  Google Scholar 

  • Perlman SJ, Hunter MS, Zchori-Fein E (2006) The emerging diversity of Rickettsia. Proc R Soc Lond B 273:2097–2106

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Pruett CL, Winker K (2008) The effects of sample size on population genetic diversity estimates in song sparrows Melospiza melodia. J Avian Biol 39:252–256

    Article  Google Scholar 

  • Rambaut A (2009) FigTree, ver. 1.3.1 [online]. http://tree.bio.ed.ac.uk/software/figtree/. Accessed 21 Dec 2010

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

    Google Scholar 

  • Rose M, Wooley JB (1984) Previously imported parasite may control invading whitefly. Calif Avocado Soc Yearb 68:127–131

    Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: methods in molecular biology. Humana Press, Totowa, pp 365–386

    Google Scholar 

  • Rugman-Jones PF, Hoddle MS, Stouthamer R (2007) Population genetics of Scirtothrips perseae: tracing the origin of a recently introduced exotic pest of Californian avocado orchards, using mitochondrial and microsatellite DNA markers. Entomol Exp Appl 124:101–115

    Article  CAS  Google Scholar 

  • Sandoval Cabrera MF, Cermeli M (2005) Presencia de Pseudacysta perseae (Heidemann, 1908) (Insecta: Hemiptera: Tingidae) en Venezuela. Entomotropica 20:271–273

    Google Scholar 

  • Sintupachee S, Milne JR, Poonchaisri S, Baimai V, Kittaypong P (2006) Closely related Wolbachia strains within the pumpkin arthropod community and the potential for horizontal transmission via the plant. Microb Ecol 51:294–301

    Article  PubMed  CAS  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci USA 105:13486–13491

    Article  PubMed  CAS  Google Scholar 

  • Stouthamer R, Breeuwer JAJ, Hurst GDD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102

    Article  PubMed  CAS  Google Scholar 

  • Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data III. Cladogram estimation. Genetics 132:619–633

    PubMed  CAS  Google Scholar 

  • van Meer MMM, Witteveldt J, Stouthamer R (1999) Phylogeny of the arthropod endosymbiont Wolbachia based on the wsp gene. Insect Mol Biol 8:399–408

    Article  PubMed  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Willls DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 270:1857–1865

    Google Scholar 

  • Werren JH, O’Neill SL (1997) The evolution of heritable symbionts. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers. Oxford University Press, New York, pp 1–41

    Google Scholar 

  • Yeh FC, Boyle TJB (1997) Population genetic analysis of codominant and dominant markers and quantitative traits. Belgian J Bot 129:157

    Google Scholar 

Download references

Acknowledgments

The authors thank collaborators listed in Table 1 for providing ALB samples, and Preston Galusky for initial assistance with DNA sequencing. This study was supported, in part, by the California Avocado Commission and the University of California Hansen Trust.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul F. Rugman-Jones.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rugman-Jones, P.F., Hoddle, M.S., Phillips, P.A. et al. Strong genetic structure among populations of the invasive avocado pest Pseudacysta perseae (Heidemann) (Hemiptera: Tingidae) reveals the source of introduced populations. Biol Invasions 14, 1079–1100 (2012). https://doi.org/10.1007/s10530-011-0140-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-011-0140-6

Keywords

Navigation