Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-18T16:54:29.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Ancient origin and recent range expansion of the maize weevil Sitophilus zeamais, and its genealogical relationship to the rice weevil S. oryzae

Published online by Cambridge University Press:  03 November 2016

A.S. Corrêa ,
C.C. Vinson ,
L.S. Braga ,
R.N.C. Guedes  and
L.O. de Oliveira
A.S. Corrêa
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil Departamento de Entomologia e Acarologia, Escola Superior de Agricultura ‘Luiz de Quieroz’ – Universidade de São Paulo (ESALQ-USP), Piracicaba, SP 13418-900, Brazil
C.C. Vinson
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil
L.S. Braga
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil
R.N.C. Guedes
Affiliation:
Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil
L.O. de Oliveira*
Affiliation:
Departamento de Bioquímica e Biologia Molecular, Universidade Federal de Viçosa, Viçosa, MG 36570-900, Brazil
*
*Author for correspondence Phone: (55)(31) 3899-2964 Fax: (55)(31) 3899-2973 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Archeological records attest the early association of Sitophilus with stored cereals from the beginning of agriculture on Asia. The maize weevil (Sitophilus zeamais) became particularly damaging to maize, a cereal crop domesticated on Mesoamerica. We investigated the late evolutionary history of the maize weevil to gain insights on its origin, timing of association with maize, and genealogical relationship to the almost morphologically indistinguishable rice weevil (Sitophilus oryzae). Two mitochondrial genes (cytochrome oxidase subunit I and cytochrome oxidase subunit II) and the nuclear ribosomal gene region were partially sequenced. Analyses showed that the maize weevil shared no haplotypes with the rice weevil; instead, each species exhibited distinct mitogroups and ribogroups. The two weevil species likely split about 8.7 million years ago (95% highest posterior density: 4.0–15.0). Microsatellite data analyses sorted the 309 specimens from 15 populations of the maize weevil into three genotypic groups, which displayed low genetic differentiation and widespread occurrence worldwide. The maize weevil and the rice weevil are each a distinct species; both of which emerged prior to the onset of agriculture. The maize–maize weevil association took place after maize became widespread as a global crop. The maize weevil populations lack spatial genetic structure at the regional, continental, and intercontinental scales.

Keywords

cerealmaize weevilphylogeographypopulation geneticsSSR markersstored grain pest
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 107 , Issue 1 , February 2017 , pp. 9 - 20
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Akaike, H. (1974) A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Bandelt, H.J., Forster, P. & Rohl, A. (1999) Median–joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 37–48.CrossRefGoogle ScholarPubMed
Barat, A., Bravo, S.P., Chandra, S., Corrêa, A.S., Giombini, M.I., Guedes, R.N., Huailei, M., Lal, K.K., Liang, L., Matura, R., Mohindra, V., Oliveira, L.O., Patangia, R., Qiyong, L., Sah, R.S., Singh, A., Singh, B.K., Singh, R.K., Tosto, D.S., Tripathi, R.K. & Vinson, C.C. (2012) Permanent genetic resources added to molecular ecology resources database 1 June 2012–31 July 2012. Molecular Ecology Resources 12, 1196–1197.Google ScholarPubMed
Brown, T.A., Jones, M.K., Powell, W. & Allaby, R.G. (2009) The complex origins of domesticated crops in the Fertile Crescent. Trends in Ecology & Evolution 24, 103–109.CrossRefGoogle ScholarPubMed
Buckland, P.C. (1981) The early dispersal of insect pests of stored products as indicated by archeological records. Journal of Stored Products Research 17, 1–12.CrossRefGoogle Scholar
Carvalho, G.A., Vieira, J.L., Haro, M.M., Corrêa, A.S., Ribon, A.O.B., Oliveira, L.O. & Guedes, R.N.C. (2014) Pleiotropic impacto f endosymbiont load and co-occurrence in the maize weevil Sitophilus zeamais . PLoS ONE 9(10), e111396.CrossRefGoogle Scholar
Champ, B.R. & Dyte, C.E. (1977) FAO global survey of pesticide susceptibility of stored grain pests. FAO Plant Protection Bulletin 25, 49–67.Google Scholar
Chu, H.F. & Wang, L.Y. (1975) Insect carcasses unearthed from Chinese antique tombs. Acta Entomologica Sinica 18, 333–337.Google Scholar
Clark, T.L., Meinke, L.J. & Foster, J.E. (2001) Molecular phylogeny of Diabrotica beetles (Coleoptera: Chrysomelidae) inferred from analysis of combined mitochondrial and nuclear DNA sequences. Insect Molecular Biology 10, 303–314.CrossRefGoogle ScholarPubMed
Coelho-Bortolo, T., Mangolin, C.A. & Lapenta, A.S. (2016) Genetic Variability in the natural populations of Lasioderma serricorne (F.) (Coleoptera: Anobiidae), detected by RAPD markers and the esterase isozymes. Bulletin of Entomological Research 106, 47–53.CrossRefGoogle ScholarPubMed
Corrêa, A.S., Pereira, E.J.G., Cordeiro, E.M.G., Braga, L.S. & Guedes, R.N.C. (2011) Insecticide resistance, mixture potentiation and fitness in populations of the maize weevil (Sitophilus zeamais). Crop Protection 30, 1655–1666.CrossRefGoogle Scholar
Corrêa, A.S., Oliveira, L.O., Braga, L.S. & Guedes, R.N.C. (2013) Distribution of the related weevil species Sitophilus oryzae and S. zeamais in Brazil. Insect Science 20, 763–770.CrossRefGoogle ScholarPubMed
Corrêa, A.S., Tomé, H.V.V., Braga, L.S., Martins, G.F., Oliveira, L.O. & Guedes, R.N.C. (2014) Are mitochondrial lineages, mitochondrial lysis and respiration rate associated with phosphine susceptibility in the maize weevil Sitophilus zeamais? Annals of Applied Biology 165, 137–146.CrossRefGoogle Scholar
Cotton, R.T. (1920) Tamarind Pod Borer, Sitophilus linearis (Hbst.). Journal of Agricultural Research 20, 439–446.Google Scholar
Crandall, K.A. & Templeton, A.R. (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134, 959–969.CrossRefGoogle ScholarPubMed
Crosby, A.W. (2003) The Columbian Exchange: Biological and Cultural Consequences of 1492. Westport, USA, Praeger.Google Scholar
Daglish, G.J. (2004) Effect of exposure period on degree of dominance of phosphine resistance in adults of Rhyzopertha dominica (Coleoptera: Bostrychidae) and Sitophilus oryzae (Coleoptera: Curculionidae). Pest Management Science 60, 822–826.CrossRefGoogle ScholarPubMed
Drummond, A.J., Suchard, M.A., Xie, D., & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.CrossRefGoogle ScholarPubMed
Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4, 359–361.CrossRefGoogle Scholar
Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Excoffier, L., Laval, G. & Schneider, S. (2006) ARLEQUIN Version 3. 1: an Integrated Software Package for Populations Genetics Data Analysis. Bern, Switzerland, University of Bern. http://citeseerx.ist.psu.edu/viewdoc/summary?doi=10.1.1.132.1270.Google Scholar
Fuller, D.Q., Harvey, E. & Qin, L. (2007) Presumed domestication? Evidence for wild rice cultivation and domestication in the fifth millennium BC of the Lower Yangtze region. Antiquity 81, 316–331.CrossRefGoogle Scholar
Goudet, J. (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485–486.CrossRefGoogle Scholar
Goudet, J. (2002) FSTAT: a Computer Program to Calculate F Statistics. Version 2.9.3.2. http://www2.unil.ch/popgen/softwares/fstat.htm.Google Scholar
Grenier, A.M., Nardon, C. & Nardon, P. (1994) The role of symbiotes in flight activity of Sitophilus weevils. Entomologia Experimentalis et Applicata 70, 201–208.CrossRefGoogle Scholar
Guedes, N.M.P., Tolledo, J., Corrêa, A.S. & Guedes, R.N.C. (2010) Insecticide-induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophilus zeamais . Journal of Applied Entomology 134, 142–148.CrossRefGoogle Scholar
Guedes, R.N.C., Oliveira, E.E., Guedes, N.M.P., Ribeiro, B. & Serrão, J.E. (2006) Cost and mitigation of insecticide resistance in the maize weevil, Sitophilus zeamais . Physiological Entomology 31, 30–38.CrossRefGoogle Scholar
Haddi, K., Mendonça, L.P., Santos, M.F., Guedes, R.N.C. & Oliveira, E.E. (2015) Metabolic and behavioral mechanisms of indoxacarb resistance in Sitophilus zeamais (Coleoptera: Curculionidae). Journal of Economic Entomology 108, 362–369.CrossRefGoogle ScholarPubMed
Haines, C.P. (1981) Insects and Arachnids from Stored Products: a Report on Specimens Received by the Tropical Stored Products Center. London, TDRI, pp. 1973–1977.Google Scholar
Halstead, D.G.H. (1963) External sex differences in stored-product Coleoptera. Bulletin of Entomological Research 54, 118–134.CrossRefGoogle Scholar
Hidayat, P., Phillips, T.W., & Ffrench-Constant, R.H. (1996) Molecular and morphological characters discriminate Sitophilus oryzae and S. zeamais (Coleoptera: Curculionidae) and confirm reproductive isolation. Annals of the Entomological Society of America 89, 645–652.CrossRefGoogle Scholar
Iriarte, J., Holst, I., Marozzi, O., Listopad, C., Alonso, E., Rinderknecht, A. & Montaña, J. (2004) Evidence for cultivar adoption and emerging complexity during the mid-Holocene in the La Plata basin. Nature 432, 614–617.CrossRefGoogle ScholarPubMed
Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure, version 1.1. Bioinformatics 23, 1801–1806.CrossRefGoogle Scholar
Kealhofer, L. & Piperno, D.R. (1994) Early agriculture in southeast Asia: phytolith evidence from Bang Pakong Valley, Thailand. Antiquity 68, 564–572.CrossRefGoogle Scholar
Kiritani, K. (1956) On the local distribution of two allied species of the rice weevils Calandra oryzae and C. sasaki . Japanese Journal of Applied Zoology 21, 74–77.Google Scholar
Kuschel, G. (1961) On problems of synonymy in the Sitophilus oryzae complex (30th contribution, Col. Curculionidae). Annals and Magazine of Natural History: Ser. 13 4, 241–244.CrossRefGoogle Scholar
Levinson, H. & Levinson, A. (1994) Origin of grain storage and insect species consuming desiccated food. Anz Schädl kd Pflanzenschutz Umweltschutz 67, 47–59.CrossRefGoogle Scholar
Lev-Yadun, S., Gopher, A. & Abbo, S. (2000) The cradle of agriculture. Science 288, 1602.CrossRefGoogle ScholarPubMed
Lewis, P.O. & Zaykin, D. (2001) Genetic Data Analysis: Computer Program for the Analysis of Allelic Data. 1.0 ed. http://hydrodictyon.eeb.uconn.edu/people/plewis/software.php (accessed December 2013).Google Scholar
Librado, P.O. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Longstaff, B.C. (1981) Biology of the grain pest species of the genus Sitophilus (Coleotpera: Curculionidae): a critical review. Protection Ecology 2, 83–130.Google Scholar
Lopez, J.V., Yuhki, N., Masuda, R., Modi, W. & O'Brien, S.J. (1994) Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution 39, 174–190.CrossRefGoogle Scholar
Madeira Santos, M.E. & Ferraz Torrão, M.M. (1998) Entre lÁmérrique et l'Afrique, les îles du Cap-Vert et São Tomé: les cheminements des milhos (mil, sorgho et maïs). pp. 69–83 in Chastanet, M. (Ed.) Plantes et Paisages d'Afrique. Une Historie à Explorer. Paris, Karthala-CRA.Google Scholar
Malia, H.A.E., Rosi-Denadai, C.A., Cardoso, D.G. & Guedes, R.N.C. (2016) Dust to weevils, weevils to dust: maize weevil personality and susceptibility to diatomaceous earth. Journal of Pest Science 89, 469–478.CrossRefGoogle Scholar
Matsuoka, Y., Vigouroux, Y., Goodman, M.M., Sanchez, J., Buckler, E. & Doebley, J. (2002) A single domestication for maize shown by multilocus microsatellite genotyping. Proceedings of the National Academy of Sciences of the United States of America 99, 6080–6084.CrossRefGoogle ScholarPubMed
Mir, C., Zerjal, T., Combes, V., Dumas, F., Madur, D., Bedoya, C., Dreisigacker, S., Franco, J., Grudloyma, P., Hao, P.X., Hearne, S., Jampatong, C., Laloë, D., Muthamia, Z., Nguyen, T., Presanna, B.M., Taba, S., Xie, C.X., Yunus, M., Zhang, S., Warburton, M.L. & Hearne, S. (2013) Out of America: tracing the genetic footprints of the global diffusion of maize. Theoretical and Applied Genetics 126, 2671–2682.CrossRefGoogle ScholarPubMed
Morales, J.A., Cardoso, D.G., Della Lucia, T.M.C. & Guedes, R.N.C. (2013) Weevil x insecticide: does “personality” matter? PLoS ONE 8, e67283.CrossRefGoogle ScholarPubMed
Nei, M. (1973) Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America 70, 3321–3323.CrossRefGoogle ScholarPubMed
Nylander, J.A.A. (2004) MrModeltest v2. Program Distributed by the Author. Uppsala, Sweden, Evolutionary Biology Centre, Uppsala University.Google Scholar
Obata, H., Manabe, A., Nakamura, N., Onishi, T. & Senba, Y. (2011) A new light on the evolution and propagation of prehistoric grain pests: the world's oldest maize weevils found in Jomon Potteries, Japan. PLoS ONE 6, e14785.CrossRefGoogle ScholarPubMed
Oliveira, M.R.C., Corrêa, A.S., de Souza, G.A., Guedes, R.N.C. & de Oliveira, L.O. (2013) Mesoamerican origin and pre- and post-Columbian expansions of the ranges of Acanthoscelides obtectus Say, a cosmopolitan insect pest of the common bean. PLoS ONE 8, e70039.CrossRefGoogle Scholar
Panagiotakopulu, E. (2001) New records for ancient pests: archaeoentomology in Egypt. Journal of Archaeological Science 28, 1235–1246.CrossRefGoogle Scholar
Papadopoulou, A., Anastasiou, I. & Vogler, A.P. (2010) Revisiting the insect mitochondrial molecular clock: the mid-Aegean trench calibration. Molecular Biology and Evolution 27, 1659–1672.CrossRefGoogle ScholarPubMed
Peng, W.K., Lin, H.C., Chen, C.N. & Wang, C.H. (2003) DNA identification of two laboratory colonies of the weevils, Sitophilus oryzae (L.) and S. zeamais Motschulsky (Coleoptera: Curculionidae) in Taiwan. Journal of Stored Products Research 39, 225–235.CrossRefGoogle Scholar
Pimentel, M.A.G., Faroni, L.D.A., Guedes, R.N.C., Sousa, A.H. & Tótola, M.R. (2009) Phosphine resistance in Brazilian populations of Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae). Journal of Stored Products Research 45, 71–74.CrossRefGoogle Scholar
Piperno, D.R., Ranere, A.J., Holst, I., Iriarte, J. & Dickau, R. (2009) Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. Proceedings of the National Academy of Sciences of the United States of America 106, 5019–5024.CrossRefGoogle ScholarPubMed
Plarre, R. (2010) An attempt to reconstruct the natural and cultural history of the granary weevil, Sitophilus zeamais (Coleoptera: Curculionidae). European Journal of Entomology 107, 1–11.CrossRefGoogle Scholar
Pohl, M.E., Piperno, D.R., Pope, K.O. & Jones, J.G. (2007) Microfossil evidence for pre-Columbian maize dispersals in the neotropics from San Andres, Tabasco, Mexico. Proceedings of the National Academy of Sciences of the United States of America 104, 6870–6875.CrossRefGoogle Scholar
Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Reference of population structure using multilocus genotype data. Genetics 155, 945–959.CrossRefGoogle Scholar
Rees, D.P. (1996) Coleoptera. pp. 1–39 in Subramanyam, B. & Hagsrum, D.W. (Eds) Integrated Management of Insects in Stored Products. New York, Marcel Dekker.Google Scholar
Ribeiro, B.M., Guedes, R.N.C., Oliveira, E.E. & Santos, J.P. (2003) Insecticide resistance and synergism in Brazilian populations of Sitophilus zeamais (Coleoptera: Curculionidae). Journal of Stored Products Research 39, 21–31.CrossRefGoogle Scholar
Richards, O.W. (1944) The two strains of the rice weevil Calandra oryzae (L.) (Coleoptera Curculionidae). Transactions of the Royal Entomological Society of London 94, 187–200.CrossRefGoogle Scholar
Semeao, A.A., Campbell, J.F., Beeman, R.W., Lorenzen, M.D., Whitworth, R.J. & Sloderbeck, P.E. (2012) Genetic structure of Tribolium castaneum (Coleoptera: Tenebrionidae) populations in mills. Environmental Entomological 41, 188–199.CrossRefGoogle ScholarPubMed
Slatkin, M. (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139, 457–462.CrossRefGoogle ScholarPubMed
Solomon, M.E. (1965) Archaeological records of storage pests: Sitophilus granarius (L.) (Coleoptera, Curculionidae) from an Egyptian pyramid tomb. Journal of Stored Products Research 1, 105–107.CrossRefGoogle Scholar
Subramanyam, B.H. & Hagstrum, D.W. (1996) Integrated Management of Insects in Stored Products. Boston, MA, Marcel Dekker.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Thagaraj, S.R., McCulloch, G.A., Subbarayalu, M., Subramaniam, C. & Walter, G.H. (2016) Development of microsatellite markers and a preliminary assessment of population structuring in the rice weevil, Sitophilus oryzae (L.). Journal of Stored Products Research 66, 12–17.CrossRefGoogle Scholar
Throne, J.E. & Cline, L.D. (1989) Seasonal flight activity of the maize weevil, Sitophilus zeamais Motschulsky (Coleoptera: Curculionidae), and the rice weevil, S. oryzae (L.), in south Caroline. Journal of Agricultural Entomology 6, 183–192.Google Scholar
Throne, J.E. & Cline, L.D. (1991) Seasonal abundance of maize and rice weevils (Coleoptera: Curculionidae) in South Caroline. Journal of Agricultural Entomology 8, 93–100.Google Scholar
van Heerwaarden, J., Doebley, J., Briggs, W.H., Glaubitz, J.C., Goodman, M.M., Gonzalez, J.D.J.S. & Ross-Ibarra, J. (2011) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. Proceedings of the National Academy of Sciences of the United States of America 108, 1088–1092.CrossRefGoogle Scholar
Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.CrossRefGoogle Scholar
Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google ScholarPubMed
White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. pp. 315–322 in Innis, M.A., Gelfand, D.H., Sninsky, J.J. & White, T.J. (Eds) PCR Protocol: a Guide to Methods and Applications. New York, Academic Press.Google Scholar
Supplementary material: PDF

Corrêa supplementary material

Table S1

Download Corrêa supplementary material(PDF)
PDF 63.2 KB
Supplementary material: PDF

Corrêa supplementary material

Table S2

Download Corrêa supplementary material(PDF)
PDF 23.4 KB
Supplementary material: PDF

Corrêa supplementary material

Table S3

Download Corrêa supplementary material(PDF)
PDF 21 KB
Supplementary material: PDF

Corrêa supplementary material

Table S4

Download Corrêa supplementary material(PDF)
PDF 20.9 KB
Supplementary material: PDF

Corrêa supplementary material

Table S5

Download Corrêa supplementary material(PDF)
PDF 21 KB
Supplementary material: PDF

Corrêa supplementary material

Table S6

Download Corrêa supplementary material(PDF)
PDF 65 KB