Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-25T18:44:12.356Z Has data issue: false hasContentIssue false
  • English
  • Français

Inconsistent genetic structure among members of a multitrophic system: did bruchid parasitoids (Horismenus spp.) escape the effects of bean domestication?

Published online by Cambridge University Press:  04 October 2012

S. Laurin-Lemay ,
B. Angers ,
B. Benrey  and
J. Brodeur
S. Laurin-Lemay
Affiliation:
Department of Biological Sciences, Université de Montréal, CP 6128, Succursale Centre-Ville, Montréal, Québec, CanadaH3C 3J7
B. Angers
Affiliation:
Department of Biological Sciences, Université de Montréal, CP 6128, Succursale Centre-Ville, Montréal, Québec, CanadaH3C 3J7
B. Benrey*
Affiliation:
Laboratoire d'Entomologie Évolutive, Université de Neuchâtel, 11 rue Emile-Argand, CP 158, CH-2009, Neuchâtel, Switzerland
J. Brodeur
Affiliation:
Department of Biological Sciences, Université de Montréal, CP 6128, Succursale Centre-Ville, Montréal, Québec, CanadaH3C 3J7
*
*Author for correspondence Fax: +41 327183001 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Anthropogenic range expansion and cultural practices have modified the distribution, abundance and genetic diversity of domesticated organisms, thereby altering multitrophic assemblages through space and time. The putative Mesoamerican domestication centre of the common bean, Phaseolus vulgaris L., in Mexico allows investigating the effects of plant domestication on the genetic structure of members of a multitrophic system. The aim of this study was to compare the evolutionary history of Horismenus parasitoids (Hymenoptera: Eulophidae) to those of their bruchid beetle hosts (Coleoptera: Bruchidae) and their domesticated host plant (P. vulgaris), in the context of traditional agriculture in Mexico. We analyzed the population genetic structure of four Horismenus species in Mexico using mitochondrial COI haplotype data. The two most abundant parasitoid species were Horismenus depressus and Horismenus missouriensis. Horismenus missouriensis were infected by Wolbachia endosymbionts and had little to no population differentiation (FST = 0.06). We suspect the mitochondrial history of H. missouriensis to be blurred by Wolbachia, because differentiation among infected vs. non-infected individuals exists (FST = 0.11). Populations of H. depressus were found to be highly differentiated (FST = 0.34), but the genetic structuring could not be explained by tested spatial components. We then compared the genetic structure observed in this parasitoid species to previously published studies on bruchid beetles and their host plants. Despite extensive human-mediated migration and likely population homogenization of its two Acanthoscelides bruchid beetle hosts, H. depressus populations are structured like its host plant, by a recent dispersal from a diverse ancestral gene pool. Distinct evolutionary dynamics may explain inconsistent patterns among trophic levels. Parasitoids likely migrate from wild bean populations and are poorly adapted to bean storage conditions similar to their bruchid beetle hosts. Integrating several trophic levels to the study of evolutionary history has proven to be fruitful in detecting different ecological responses to human-mediated disturbances and host parasite interactions.

Keywords

Wolbachiacomparative phylogeographyhuman-mediated migrationplant domesticationmultitrophic systemparasitoids
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 2 , April 2013 , pp. 182 - 192
Copyright
Copyright © Cambridge University Press 2012

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

Aebi, A., Shani, T., Hansson, C., Contreras-Garduno, J., Mansion, G. & Benrey, B. (2008) The potential of native parasitoids for the control of Mexican bean beetles: A genetic and ecological approach. Biological Control 47, 289–297.Google Scholar
Alvarez, N., Hossaert-Mckey, M., Rasplus, J.Y., Mckey, D., Mercier, L., Soldati, L., Aebi, A., Shani, T. & Benrey, B. (2005a) Sibling species of bean bruchids: a morphological and phylogenetic study of Acanthoscelides obtectus Say and Acanthoscelides obvelatus Bridwell. Journal of Zoological Systematics and Evolutionary Research 43, 29–37.Google Scholar
Alvarez, N., Mckey, D., Hossaert-Mckey, M., Born, C., Mercier, L. & Benrey, B. (2005b) Ancient and recent evolutionary history of the bruchid beetle, Acanthoscelides obtectus Say, a cosmopolitan pest of beans. Molecular Ecology 14, 1015–1024.Google Scholar
Alvarez, N., Hossaert-Mckey, M., Restoux, G., Delgado-Salinas, A. & Benrey, B. (2007) Anthropogenic effects on population genetics of phytophagous insects associated with domesticated plants. Evolution 61, 2986–2996.Google Scholar
Angers, B. & Bernatchez, L. (1998) Combined use of SMM and non-SMM methods to infer fine structure and evolutionary history of closely related brook charr (Salvelinus fontinalis, Salmonidea) populations from microsatellites. Molecular Biology and Evolution 15, 143–159.Google Scholar
Bassam, B.J., Caetano-Anollés, G. & Gresshoff, P.M. (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Analytical Biochemistry 196, 80–83.Google Scholar
Bertorelle, G. & Barbujani, G. (1995) Analysis of DNA diversity by spatial autocorrelation. Genetics 140, 811–819.Google Scholar
Blair, M., Díaz, L., Buendía, H. & Duque, M. (2009) Genetic diversity, seed size associations and population structure of a core collection of common beans (Phaseolus vulgaris L.). Theoretical and Applied Genetics 119, 955–972.Google Scholar
Bonet, A. (2009) New hosts, host plants, and distribution records for horismenus (Hymenoptera: Eulophidae) species in a bruchid beetle parasitoid guild attacking wild type Phaseolus coccineus and P. Vulgaris in Central Mexico. Florida Entomologist 91, 698–701.Google Scholar
Broughton, W.J., Hernández, G., Blair, M., Beebe, S., Gepts, P. & Vanderleyden, J. (2003) Beans (Phaseolus spp.) – model food legumes. Plant and Soil 252, 55–128.Google Scholar
Bryant, V.M. & Holloway, R.G. (1985) Pollen Records of Late-Quaternary North American Sediments. Dallas, TX, USA, American Association of Stratigraphic Palynologists Foundation.Google Scholar
Campan, E.D.M., Callejas, A., Rahier, M. & Benrey, B. (2005) Interpopulation variation in a larval parasitoid of bruchids, Stenocorse bruchivora (Hymenoptera: Braconidae): Host plant effects. Environmental Entomology 34, 457–465.Google Scholar
Charlat, S., Duplouy, A., Hornett, E.A., Dyson, E.A., Davies, N., Roderick, G.K., Wedell, N. & Hurst, G.D.D. (2009) The joint evolutionary histories of Wolbachia and mitochondria in Hypolimnas bolina. Bmc Evolutionary Biology 9, 64.Google Scholar
Colwell, R.R., Simidu, U. & Ohwada, K. (1996) Microbial Diversity in Time and Space. New York, USA, Plenum Press.Google Scholar
Doebley, J.F., Gaut, B.S. & Smith, B.D. (2006) The molecular genetics of crop domestication. Cell 127, 1309–1321.Google Scholar
Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1, 47–50.Google Scholar
Gonzalez-Rodriguez, A., Benrey, B., Callejas, A. & Oyama, K. (2002) Inter- and intraspecific genetic variation and differentiation in the sibling bean weevils Zabrotes subfasciatus and Z-sylvestris (Coleoptera: Bruchidae) from Mexico. Bulletin of Entomological Research 92, 185–189.Google Scholar
Grant, W.S. & Bowen, B.W. (1998) Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation. Journal of Heredity 89, 415–426.Google Scholar
Guindon, S. & Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.Google Scholar
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hansson, C., Aebi, A. & Benrey, B. (2004) Horismenus species (Hymenoptera: Eulophidae) in a bruchid beetle parasitoid guild, including the description of a new species. Zootaxa 548, 1–16.Google Scholar
Hardy, O.J. & Vekemans, X. (2002) SPAGEDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2, 618–620.Google Scholar
Hilgenboecker, K., Hammerstein, P., Schlattmann, P., Telschow, A. & Werren, J.H. (2008) How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiology Letters 281, 215–220.Google Scholar
Hurst, G.D.D., Jiggins, F.M., Von Der Schulenburg, J.H.G., Bertrand, D., West, S.A., Goriacheva, I.I., Zakharov, I.A., Werren, J.H., Stouthamer, R. & Majerus, M.E.N. (1999) Male-killing Wolbachia in two species of insect. Proceedings of the Royal Society of London, Series B: Biological Sciences 266, 735–740.Google Scholar
Karlin, S. & Nevo, E. (1986) Evolutionary Processes and Theory. Orlando, FL, USA, Academic Press.Google Scholar
Kwak, M. & Gepts, P. (2009) Structure of genetic diversity in the two major gene pools of common bean (Phaseolus vulgaris L., Fabaceae). Theoretical and Applied Genetics 118, 979–992.Google Scholar
Kwak, M., Kami, J.A. & Gepts, P. (2009) The putative Mesoamerican domestication center of Phaseolus vulgaris is located in the Lerma-Santiago Basin of Mexico. Crop Science 49, 554–563.Google Scholar
Lartillot, N., Lepage, T. & Blanquart, S. (2009) PhyloBayes 3: a Bayesian software package for phylogenetic reconstruction and molecular dating. Bioinformatics 25, 2286–2288.Google Scholar
Legendre, P. & Gallagher, E.D. (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129, 271–280.Google Scholar
Lozier, J.D., Roderick, G.K. & Mills, N.J. (2007) Genetic evidence from mitochondrial, nuclear, and endosymbiont markers for the evolution of host plant associated species in the aphid genus hyalopterus (hemiptera: Aphididae). Evolution 61, 1353–1367.Google Scholar
Macfadyen, S. & Bohan, D.A. (2010) Crop domestication and the disruption of species interactions. Basic and Applied Ecology 11, 116–125.Google Scholar
Nei, M. (1987) Molecular Evolutionary Genetics. New York, USA, Columbia University Press.CrossRefGoogle Scholar
Nei, M. & Tajima, F. (1981) DNA polymorphism detectable by restriction endonucleases. Genetics 97, 145–163.Google Scholar
Oksanen, J., Kindt, R., Legendre, P., O'hara, B., Simpson, G.L., Henry, M., Stevens, H.H. & Wagner, H. (2008) Vegan: Community Ecology Package. R package version 1.13–1.Google Scholar
Orita, M., Iwahana, H., Kanazawa, H., Hayashi, K. & Sekiya, T. (1989) Detection of polymorphisms of human DNA by gel electrophoresis as single-strand conformation polymorphisms. Proceedings of the National Academy of Sciences of the United States of America 86, 2766–2770.Google Scholar
Papa, R. & Gepts, P. (2003) Asymmetry of gene flow and differential geographical structure of molecular diversity in wild and domesticated common bean (Phaseolus vulgaris L.) from Mesoamerica. Theoretical and Applied Genetics 106, 239–250.Google Scholar
Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
Ramamoorthy, T.P. (1998) Diversidad Biológica de México: Orígenes y Distribución. México, UNAM.Google Scholar
Restoux, G., Hossaert-Mckey, M., Benrey, B. & Alvarez, N. (2010) The effect of host plant and isolation on the genetic structure of phytophagous insects: A preliminary study on a bruchid beetle. European Journal of Entomology 107, 299–304.Google Scholar
Rigaud, T., Soutygrosset, C., Raimond, R., Mocquard, J.P. & Juchault, P. (1991) Feminizing endocytobiosis in the terrestrial crustacean Armadillidium-Vulgare Latr (Isopoda) – recent acquisitions. Endocytobiosis and Cell Research 7, 259–273.Google Scholar
Romero, J. & Johnson, C.D. (1999) Zabrotes sylvestris, a new species from the United States and Mexico related to Z-subfasciatus (Boheman) (Coleoptera: Bruchidae: Amblycerinae). Coleopterists Bulletin 53, 87–98.Google Scholar
Rossi, M., Bitocchi, E., Bellucci, E., Nanni, L., Rau, D., Attene, G. & Papa, R. (2009) Linkage disequilibrium and population structure in wild and domesticated populations of Phaseolus vulgaris L. Evolutionary Applications 2, 504–522.Google Scholar
Sambrook, J. & Russell, D.W. (2001) Appendix 8: commonly used techniques in molecular cloning. pp. AB.9–AB.10in Sambrook, J. & Russell, D.W. (Eds) Molecular Cloning: A Laboratory Manual. 3rd edn, Cold Spring Harbor, NY, USA, Cold Spring Harbor Laboratory Press.Google Scholar
Sheffield, V.C., Beck, J.S., Kwitek, A.E., Sandstrom, D.W. & Stone, E.M. (1993) The sensitivity of single-strand conformation polymorphism analysis for the detection of single base substitutions. Genomics 16, 325–332.Google Scholar
Simon, C., Frati, F., Beckenbach, 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. Annals of the Entomological Society of America 87, 651–701.Google Scholar
Smith, T.B. & Wayne, R.K. (1996) Molecular Genetic Approaches in Conservation. New York, USA, Oxford University Press.Google Scholar
Stouthamer, R.& Luck, R. (1993) Influence of microbe-associated parthenogenesis on the fecundity of Trichogramma deion and T. pretiosum. Entomologia Experimentalis et Applicata 67, 183–192.Google Scholar
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.Google Scholar
Tscharntke, T. & Hawkins, B.A. (2002) Multitrophic Level Interactions. Cambridge, UK, Cambridge University Press.Google Scholar
Tuda, M., Ronn, J., Buranapanichpan, S., Wasano, N. & Arnqvist, G. (2006) Evolutionary diversification of the bean beetle genus Callosobruchus (Coleoptera: Bruchidae): traits associated with stored-product pest status. Molecular Ecology 15, 3541–3551.Google Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1371–1383.Google Scholar
Werren, J.H., Baldo, L. & Clark, M.E. (2008) Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology 6, 741–751.Google Scholar
Yen, J.H. & Barr, A.R. (1973) The etiological agent of cytoplasmic incompatibility in Culex pipiens. Journal of Invertebrate Pathology 22, 242–250.Google Scholar
Yu, M.Z., Zhang, K.J., Xue, X.F. & Hong, X.Y. (2011) Effects of Wolbachia on mtDNA variation and evolution in natural populations of Tetranychus urticae Koch. Insect Molecular Biology 20, 311–321.Google Scholar
Zizumbo-Villarreal, D., Colunga-Garciamarin, P., Payro De La Cruz, E., Delgado-Valerio, P. & Gepts, P. (2005) Population structure and evolutionary dynamics of wild-weedy-domesticated complexes of common bean in a Mesoamerican region. Crop Science 45, 1073–1083.Google Scholar