Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-27T01:32:52.210Z Has data issue: false hasContentIssue false

Molecular markers reveal narrow genetic base and culturing-associated genetic drift in Teretrius nigrescens Lewis populations released for the biological control of the larger grain borer in Africa

Published online by Cambridge University Press:  05 December 2013

B.A. Omondi*
Affiliation:
International Centre of Insect Physiology and Ecology, P. O. Box 30772–00100, Nairobi, Kenya School of Environmental Sciences and Development, North West University, Private Bag X6001, Potchefstroom 2520, South Africa Centre for Disaster Management and Humanitarian Assistance, Masinde Muliro University, P. O. Box 190, Kakamega 50100, Kenya
J. van den Berg
Affiliation:
School of Environmental Sciences and Development, North West University, Private Bag X6001, Potchefstroom 2520, South Africa
D. Masiga
Affiliation:
International Centre of Insect Physiology and Ecology, P. O. Box 30772–00100, Nairobi, Kenya
F. Schulthess
Affiliation:
International Centre of Insect Physiology and Ecology, P. O. Box 30772–00100, Nairobi, Kenya
*
*Author for correspondence: Phone: +46-40-415384 Fax: +46-40-461991 E-mail: [email protected], [email protected]

Abstract

In biological control, successful establishment of a natural enemy species depends on its adaptability in the introduced range including its ability to re-establish desired ecological interactions with the pest. These are affected by genetic parameters hitherto largely unresolved in biological control. The larger grain borer (LGB), Prostephanus truncatus, an invasive species from meso-America, is the most important post-harvest pest of maize in Africa. We studied the genetic structure of Teretrius nigrescens, a predatory beetle previously released for the control of the pest in Africa, to test the hypothesis that establishment patterns were a result of ecotype–environment mismatch and to follow up on our earlier reports of distinct lineages of the predator. We studied 13 populations of T. nigrescens, using 16 polymorphic microsatellite markers. Five genetic populations with a hierarchical structure and significant isolation by distance were detected. The most diverse population was found in southern Mexico, consistent with earlier lineage coexistence observations. Populations introduced to Africa maintained genetic similarity to local geographic populations of their area of origin. The more successful Benin releases were also more genetically diverse. Loss of rare alleles and a higher frequency of existing private alleles in some populations indicated population expansions following bottleneck events. Sustainable biological control should accommodate pest and natural enemy species, and monitor genetic changes associated with introduction and release.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anonymous (1999) Management of Maize Pests and Diseases, Annual Report, Plant Health Management Division. Cotonou, Benin, International Institute of Tropical Agriculture.Google Scholar
Bacigalupe, D.L. (2008) Biological invasions and phenotypic evolution: a quantitative genetic perspective. Biological Invasions 11, 22432250.Google Scholar
Beaumont, M., Barratt, E.M., Gottelli, D., Kitchener, A.C., Daniels, M.J., Pritchard, J.K. & Brudford, M.W. (2001) Genetic diversity and introgression in the Scottish wildcat. Molecular Ecology 10, 319336.Google Scholar
Bekessy, S.A., Ennos, R.A., Burgman, M.A., Newton, A.C. & Ades, P.K. (2003) Neutral DNA markers fail to detect genetic divergence in an ecologically important trait. Biological Conservation 110, 267275.Google Scholar
Bigler, F. (1992) Quality Control in insect rearing systems. pp. 189210 in Ochieng-Odero, J.P.R. (ed.) Techniques of Insect Rearing for the Development of Integrated Pest and Vector Management Strategies. Proceedings of the International Group Training Course on Techniques of Insect Rearing for the Development of Integrated Pest and Vector Management. Nairobi, ICIPE.Google Scholar
Bilgin, R. (2007) Kgtests: a simple Excel Macro program to detect signatures of population expansion using microsatellites. Molecular Ecology Notes 7, 416417.Google Scholar
Böye, J. (1990) Ecological aspects of Prostephanus truncatus (Horn) (Col.: Bostrichidae) in Costa Rica. pp. 7386 in Markham, R.H. & Herren, H.R. (eds) Biological Control of the Larger Grain Borer. Proc. IITA/FAO Coordination Meeting, 2–3 June 1989. Cotonou, Republic of Benin. Ibadan, Nigeria, International Institute of Tropical Agriculture.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, 20012014.CrossRefGoogle ScholarPubMed
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology 14, 7475.CrossRefGoogle ScholarPubMed
Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of the population structure: extensions to linked loci and correlated allele frequencies. Genetics 164, 15671587.Google Scholar
Falush, D., Stephens, M. & Pritchard, J.K. (2007) Inference of the population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7, 574578.Google Scholar
Fauvergue, X., Malausa, J.–C., Giuge, L. & Courchamp, F. (2007) Invading parasitoids suffer no Alée effect: a manipulative field experiment. Ecology 88, 23922403.CrossRefGoogle Scholar
Giles, P.H., Hill, M.G., Nang'ayo, F.L.O., Farrell, G. & Kibata, G.N. (1996) Release and establishment of the predator Teretriosoma nigrescens Lewis for the biological control of Prostephanus truncatus (Horn) in Kenya. African Crop Science Journal 4, 325337.Google Scholar
Gomulkiewicz, R., Holt, R.D., Barfield, M. & Nuismer, S.L. (2010) Genetics, adaptation, and invasion in harsh environments. Evolutionary Applications 3, 97108.Google Scholar
Goudet, J. (2002) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html.Google Scholar
Grevstad, F.S. (1999) Experimental invasions using biological control introductions: the influence of release size on the chance of population establishment. Biological Invasions 1, 313323.CrossRefGoogle Scholar
Gueye, M.T., Goergen, G., Badiane, D., Hell, K. & Lamboni, L. (2008) First report on occurrence of the larger grain borer Prostephanus truncatus (Horn) (Coleoptera: Bostrychidae) in Senegal. African Entomology 16, 309311.CrossRefGoogle Scholar
Guntrip, J., Silby, R.M. & Smith, R.H. (1996) A phenotypic and genetic comparison of egg to adult life history traits between and within two strains of the Larger Grain Borer Prostephanus truncatus (Horn) (Coloeptera: Bostrichidae). Journal of Stored Products Research 32, 213223.Google Scholar
Hill, M.G., Nang'ayo, F.L.O. & Wright, D.J. (2003) Biological control of the larger grain borer Prostephanus truncatus (Coleoptera: Bostrichidae) in Kenya using a predatory beetle Teretrius nigrescens (Coleoptera: Histeridae). Bulletin of Entomological Research 93, 299306.Google Scholar
Holst, N. & Meikle, W.G. (2003) Teretrius nigrescens against larger grain borer Prostephanus truncatus in African maize stores: biological control at work? Journal of Applied Ecology 40, 307319.Google Scholar
Hopper, K.R. & Roush, R.T. (1993) Mate finding, dispersal, number released, and the success of biological control introductions. Ecological Entomology 18, 321331.Google Scholar
Hopper, K.R., Roush, R.T. & Powell, W. (1993) Management of genetics of biological-control introductions. Annual Review of Entomology 38, 2751.Google Scholar
Hufbauer, R.A. (2002) Evidence for non-adaptive evolution in parasitoid virulence following a biological control introduction. Ecological Applications 12, 6678.Google Scholar
Hufbauer, R.A., Bogdanowicz, S.M. & Harrison, R.G. (2004) The population genetics of a biological control introduction: mtDNA and microsatellite variation in native and introduced populations of Aphidius ervi, a parasitoid wasp. Molecular Ecology 13, 337348.Google Scholar
Hundertmark, K.J. & van Daele, L.J. (2010) Founder effect and bottleneck signatures in an introduced, insular population of elk. Conservation Genetics 11, 139147.Google Scholar
Jensen, J.L., Bohonak, A.J. & Kelley, S.T. (2005) Isolation by distance, web service. BMC Genetics 6, 13. v.3.16 http://ibdws.sdsu.edu/.Google Scholar
Kalinowski, S.T., Taper, M.L. & Marshall, T.C. (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16, 1099–1006.Google Scholar
Lloyd, C.J., Hufbauer, R.A., Jackson, A., Nissen, S.J. & Norton, P.N. (2005) Pre- and post-introduction patterns in neutral genetic diversity in the leafy spurge gall midge, Spurgia capitigena (Bremi) (Diptera: Cecidomyiidae). Biological Control 33, 153164.Google Scholar
Lockwood, J.L., Cassey, P. & Blackburn, T. (2005) The role of propagule pressure in explaining species invasions. Trends in Ecology and Evolution 20, 223228.Google Scholar
Luikart, G. & Cornuet, J.M. (1998) Empirical evaluation of a test identifying recently bottlenecked populations from allele frequency data. Conservation Biology 12, 228237.CrossRefGoogle Scholar
Luikart, G., Allendorf, F.W., Cornuet, J. & Sherwin, W.B. (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89, 238247.CrossRefGoogle ScholarPubMed
Mantel, N. (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209220.Google Scholar
Meikle, W.G., Rees, D. & Markham, R.H. (2002) Biological control of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). Integrated Pest Management Reviews 7, 123138.Google Scholar
Memmott, J., Craze, P.G., Harman, H.M., Syrett, P. & Fowler, S.V. (2005) The effect of propagule size on the invasion of an alien insect. Journal of Animal Ecology 74, 5062.Google Scholar
Mendiola-Olaya, E., Valencia-Jimenéz, A., Valdés-Rodríguez, S., Délano-Frier, J. & Blanco-Labra, A. (2000) Digestive amylase from the larger grain borer, Prostephanus truncatus Horn. Comparative Biochemistry and Physiology Part B 126, 425433.Google Scholar
Nei, M., Maruyama, T. & Chakraborty, R. (1975) The bottleneck effects and genetic variability in populations. Evolution 29, 110.CrossRefGoogle ScholarPubMed
Nyagwaya, L.D.M., Mvumi, B.M. & Saunyama, I.G.M. (2010) Occurrence and distribution of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) in Zimbabwe. International Journal of Tropical Insect Science 30, 221231.Google Scholar
Omondi, A.B., Orantes, L.C., van den Berg, J., Masiga, D. & Schulthess, F. (2009) Isolation and characterization of microsatellite markers from Teretrius nigrescens Lewis (Coleoptera: Histeridae), predator of the storage pest Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). Molecular Ecology Resources 9, 12361239.CrossRefGoogle ScholarPubMed
Omondi, A.B., Jiang, N., van den Berg, J. & Schulthess, F. (2011 a) Flight activity and abundance of Prostephanus truncatuss, (Horn) Coleoptera; Bostrichidae in Kenya. Journal of Stored Products Research 47, 1319.Google Scholar
Omondi, A.B., van den Berg, J., Masiga, D. & Schulthess, F. (2011 b) Phylogeographic structure of Teretrius nigrescens (Coleoptera: Histeridae) predator of the invasive post harvest pest Prostephanus truncatus (Coleoptera: Bostrichidae). Bulletin of Entomological Research 101, 521532.CrossRefGoogle ScholarPubMed
Omwega, C.O. & Overholt, W.A. (1996) Genetic changes occurring during laboratory rearing of Cotesia flavipes Cameron (Hymenoptera: Braconidae) an imported parasitoid for the control of graminaceous stem borers in Africa. African Entomology 4, 231237.Google Scholar
Peakall, R. & Smouse, P.E. (2006) GenAlex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes. 6, 288295.Google Scholar
Peakall, R. & Smouse, P.E. (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 25372539.Google Scholar
Piry, S., Luikart, G. & Cornuet, J.M. (1999) Bottleneck: a computer program for detecting recent effective population size reductions from allele frequency data. Journal of Heredity 90, 502503. available from: http://www.ensam.inra.fr/URLB.CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M. & Donnely, P. (2000) Inference of population structure from genotype data. Genetics 155, 945959.Google Scholar
Pritchard, J.K., Wen, X. & Falush, D. (2007) Documentation for structure software: version 2.2. http//pritch.bsd.uchicago.edu/software.Google Scholar
Raymond, M. & Rouset, F. (1995) Genepop (Version 3.4): population genetics software for exact tests and ecumenism. Journal of Heredity 86, 248249.Google Scholar
Reich, D.E., Feldman, M.W. & Goldstein, D.B. (1999) Statistical properties of two tests that use multilocus data sets to detect population expansions. Molecular Biology and Evolution 16, 453466.Google Scholar
Roderick, G.K. & Navajas, M. (2003) Genes in new environments: genetics and evolution in biological control. Nature Reviews – Genetics 4, 889899.Google Scholar
Roush, R.T. (1990) Genetic considerations in the propagation of entomophagous species. in Baker, R.R. & Dunn, P.E. (eds) New Directions in Biological Control. Alternatives for Suppressing Agricultural Pests and Diseases. Proceedings of a University of California Los Angeles Colloquium, 20th–27th January, 1989. Frisco, Colorado, USA.Google Scholar
Sakai, A.K., Allendorf, F.W., Holt, J.S.M., Lodge, D.M., Molofsky, J., Kimberly, W.A., Baughman, S., Cabin, R.J., Cohen, J.E., Ellstrand, N.E., McCauley, D.E., O'Neil, P., Parker, I.M., Thompson, J.N. & Weller, S.G. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics 32, 305332.Google Scholar
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning, a Laboratory Manual. 2nd edn. New York, Cold Spring Harbour Laboratory Press.Google Scholar
Schneider, H., Borgemeister, C., Setamou, M., Affognon, H., Bell, A., Zweigert, M.E., Poehling, H. & Schulthess, F. (2004) Biological control of the larger grain borer Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) by its predator Teretrius nigrescens (Lewis) (Coleoptera: Histeridae) in Togo and Benin. Biological Control 30, 241255.Google Scholar
Szpiech, Z.A. & Rosenberg, N.A. (2011) On the size distribution of private microsatellite alleles. Theoretical Population Biology 80, 100113.Google Scholar
Tigar, B.J., Osborne, P.E., Key, G.E., Flores, S.M.E. & Vazquez-Arista, M. (1994) Distribution and abundance of Prostephanus truncatus (Coleoptera: Bostrichidae) by its predator Teretriosoma nigrescens (Coleoptera: Histeridae) in Mexico. Bulletin of Entomological Research 84, 555565.Google Scholar
van Oosterhout, C., Hutchinson, W.F., Willis, D.P.M. & Shipley, P. (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535538.CrossRefGoogle Scholar
van Tienderen, P.H., de Haan, A.A., van der Linden, C.G. & Vosman, B. (2002) Biodiversity assessment using markers for ecologically important traits. Trends in Ecology and Evolution 17, 577582.Google Scholar
Vasquez-Arista, M., Smith, R.H., Martinez-Gallardo, N.A. & Blanco-Labra, A. (1999) Enzymatic differences in the digestive system of the adult and larva of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). Journal of Stored Products Research 35, 167174.CrossRefGoogle Scholar
Zayed, A., Constantin, S.A. & Packer, L. (2007) Successful biological invasion despite a severe genetic load. PLoS ONE 2, e868. doi: 10.1371/ journal.pone.0000868.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Omondi et al. Supplementary Material

Figure 1

Download Omondi et al. Supplementary Material(PDF)
PDF 749.5 KB
Supplementary material: PDF

Omondi et al. Supplementary Material

Figure 2

Download Omondi et al. Supplementary Material(PDF)
PDF 211.2 KB
Supplementary material: PDF

Omondi et al. Supplementary Material

Table 1

Download Omondi et al. Supplementary Material(PDF)
PDF 147.6 KB
Supplementary material: PDF

Omondi et al. Supplementary Material

Table 2

Download Omondi et al. Supplementary Material(PDF)
PDF 66 KB