Skip to main content
SpringerLink
Log in

Contrasting patterns of phylogeographic structuring in two key beetle pests of stored grain in India and Australia

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Rhyzopertha dominica and Tribolium castaneum are key pests of stored grains globally. Fumigation with phosphine gas is the primary control method for these beetles, so the development of phosphine resistant populations threatens the continued use of this fumigant. Developing effective strategies to manage the spread of phosphine resistance requires an understanding of the genetic diversity and structuring in these pests. We therefore assessed the phylogeographic structuring of these beetles in Australia and India, two significant grain producing countries. Genetic diversity was high in T. castaneum, with 40 discrete haplotypes identified from the 268 specimens sequenced. Four haplotypes, including the three most common haplotypes, were found in both India and Australia. Genetic diversity was notably lower in India, potentially driven by the higher frequency of phosphine fumigations in India. No genetic structuring was identified in Australia T. castaneum, but a small amount was detected in India. Genetic diversity was much lower in R. dominica, with only three discrete COI haplotypes identified from 215 specimens. The low level of genetic diversity in R. dominica suggests selection may be occurring on the mitochondrial genome, potentially driven by an endosymbiont such as Wolbachia. The contrasting phylogeographic patterns, across species and countries, emphasise the importance of developing insecticide resistance management practices that are both species specific (even if pests share a similar environment), as well as region specific. For instance, the limited genetic structuring identified in T. castaneum suggests phosphine resistance could potentially spread rapidly across Australia, meaning broad-scale resistance management strategies are essential.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmad F, Walter GH, Raghu S (2012) Comparative performance of Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) across populations, resource types and structural forms of those resources. J Stored Prod Res 48:73–80

    Article  Google Scholar 

  • Albernaz KC, Silva-Brandao KL, Fresia P, Cônsoli FL, Omoto C (2012) Genetic variability and demographic history of Heliothis virescens (Lepidoptera: Noctuidae) populations from Brazil inferred by mtDNA sequences. Bull Entomol Res 102:333–343

    Article  CAS  PubMed  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Beeman RW, Friesen KS (1999) Properties and natural occurrence of maternal-effect selfish genes (‘Medea’ factors) in the red flour beetle, Tribolium castaneum. Heredity 82:529–534

    Article  PubMed  Google Scholar 

  • Beeman RW, Friesen KS, Denell RE (1992) Maternal-effect selfish genes in flour beetles. Science 256:89–92

    Article  CAS  PubMed  Google Scholar 

  • Behere GT, Tay WT, Russell DA, Heckel DG, Appleton BR, Kranthi KR, Batterham P (2007) Mitochondrial DNA analysis of field populations of Helicoverpa armigera (Lepidoptera: Noctuidae) and of its relationship to H. zea. BMC Evol Biol 7:117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benhalima H, Chaudhry MQ, Mills KA, Price NR (2004) Phosphine resistance in stored-product insects collected from various grain storage facilities in Morocco. J Stored Prod Res 40:241–249

    Article  CAS  Google Scholar 

  • Campbell JF, Arbogast RT (2004) Stored-product insects in a flour mill: population dynamics and response to fumigation treatments. Entomol Exp Appl 112:217–225

    Article  Google Scholar 

  • Campbell J, Toews MD, Arthur FH, Arbogast RT (2010) Long-term monitoring of Tribolium castaneum in two flour mills: seasonal patterns and impact of fumigation. J Econ Entomol 103:991–1001

    Article  PubMed  Google Scholar 

  • Cariou M, Duret L, Charlat S (2017) The global impact of Wolbachia on mitochondrial diversity and evolution. J Evol Biol 30:2204–2210

    Article  CAS  PubMed  Google Scholar 

  • Chaudhry M (1997) A review of the mechanisms involved in the action of phosphine as an insecticide and phosphine resistance in stored-product insects. Pest Manag Sci 49:213–228

    Article  CAS  Google Scholar 

  • Collins PJ, Falk MG, Nayak MK, Emery RN, Holloway JC (2017) Monitoring resistance to phosphine in the lesser grain borer, Rhyzopertha dominica, in Australia: a national analysis of trends, storage types and geography in relation to resistance detections. J Stored Prod Res 70:25–36

    Article  Google Scholar 

  • Daglish GJ, Nayak MK, Pavic H, Smith LW (2015) Prevalence and potential fitness cost of weak phosphine resistance in Tribolium castaneum (Herbst) in eastern Australia. J Stored Prod Res 61:54–58

    Article  Google Scholar 

  • Daglish GJ, Ridley AW, Reid R, Walter GH (2017) Testing the consistency of spatio-temporal patterns of flight activity in the stored grain beetles Tribolium castaneum (Herbst) and Rhyzopertha dominica (F.). J Stored Prod Res 72:68–74

    Article  Google Scholar 

  • Demuth JP, Wade MJ (2006) Population differentiation in the beetle Tribolium castaneum. I. Genetic architecture. Evolution 61:494–509

    Article  Google Scholar 

  • Demuth JP, Wade MJ (2007) Population differentiation in the beetle Tribolium castaneum. II. Haldane’s rule and incipient speciation. Evolution 61:694–699

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Drury DW, Siniard AL, Wade MJ (2009) Genetic differentiation among wild populations of Tribolium castaneum estimated using microsatellite markers. J Hered 100:732–741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Edde PA, Phillips TW, Toews MD (2005) Responses of Rhyzopertha dominica (Coleoptera : Bostrichidae) to its aggregation pheromones as influenced by trap design, trap height, and habitat. Environ Entomol 34:1549–1557

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fresia P, Azeredo-Espin AML, Lyra ML (2013) The phylogeographic history of the new world screwworm fly, inferred by approximate Bayesian computation analysis. PLoS ONE 8:e76168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Galtier N, Nabholz B, Glémin S, Hurst G (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol Ecol 18:4541–4550

    Article  CAS  PubMed  Google Scholar 

  • Graham RI, Wilson K (2012) Male-killing Wolbachia and mitochondrial selective sweep in a migratory African insect. BMC Evol Biol 12:204

    Article  PubMed  PubMed Central  Google Scholar 

  • Hagstrum D, Subramanyam BH (2009) Stored-product insect resource. AACC International Inc, St. Paul

    Google Scholar 

  • Hebert PD, 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. Glob Change Biol 101:14812–14817

    CAS  Google Scholar 

  • Hereward JP, Walter GH, DeBarro PJ, Lowe AJ, Riginos C (2013) Gene flow in the green mirid, Creontiades dilutus (Hemiptera: Miridae), across arid and agricultural environments with different host plant species. Ecol Evol 3:807–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hereward JP, Hutchinson JA, McCulloch GA, Silva R, Walter GH (2017) Divergence among generalist herbivores: the Frankliniella schultzei species complex in Australia (Thysanoptera: Thripidae). Arthropod Plant Interact 11:875–887

    Article  Google Scholar 

  • Hermisson J, Pennings PS (2017) Soft sweeps and beyond: understanding the patterns and probabilities of selection footprint under rapid adaptation. Methods Ecol Evol 8:700–716

    Article  Google Scholar 

  • Hernandez Nopsa JF et al (2015) Ecological networks in stored grain: key postharvest nodes for emerging pests, pathogens, and mycotoxins. Bioscience 65:985–1002

    Article  PubMed  PubMed Central  Google Scholar 

  • Hickerson M et al (2010) Phylogeography’s past, present, and future: 10 years after. Mol Phylogenet Evol 54:291–301

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jagadeesan R, Collins PJ, Daglish GJ, Ebert PR, Schlipalius DI (2012) Phosphine resistance in the rust red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae): inheritance, gene interactions and fitness costs. PLoS ONE 7:e31582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiggins FM (2003) Male-killing Wolbachia and mitochondrial DNA: selective sweeps, hybrid introgression and parasite population dynamics. Genetics 164:5–12

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kapantaidaki DE, Ovčarenko I, Fytrou N, Knott KE, Bourtzis K, Tsagkarakou A (2014) Low levels of mitochondrial DNA and symbiont diversity in the worldwide agricultural pest, the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). J Hered 106:80–92

    Article  CAS  PubMed  Google Scholar 

  • Kaur R et al (2015) Phosphine resistance in India is characterised by a dihydrolipoamide dehydrogenase variant that is otherwise unobserved in eukaryotes. Heredity 115:188–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kébé K, Alvarez N, Espíndola A, Justy F, Olivieri I, Sembène M (2016) Insights into the genetic structure of the cowpea pest Callosobruchus maculatus in Africa. J Pest Sci 89:449–458

    Article  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Li Y-Y, Fields P, Pang B-P, Coghlin P, Floate K (2015) Prevalence and diversity of Wolbachia bacteria infecting insect pests of stored products. J Stored Prod Res 62:93–100

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lorini I, Collins PJ, Daglish GJ, Nayak MK, Pavic H (2007) Detection and characterisation of strong resistance to phosphine in Brazilian Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae). Pest Manag Sci 63:358–364

    Article  CAS  PubMed  Google Scholar 

  • Mahroof RM, Phillips TW (2007) Stable isotopes as markers to investigate host use by Rhyzopertha dominica. Entomol Exp Appl 125:205–213

    Article  CAS  Google Scholar 

  • Malekpour R, Rafter MA, Daglish GJ, Walter GH (2016) Influence of phosphine resistance genes on flight propensity and resource location in Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae): the landscape for selection. Biol J Linn Soc 119:348–358

    Article  Google Scholar 

  • Malekpour R, Rafter MA, Daglish GJ, Walter GH (2018) The movement abilities and resource location behaviour of Tribolium castaneum: phosphine resistance and its genetic influences. J Pest Sci 91:739–749

    Article  Google Scholar 

  • Mau YS, Collins PJ, Daglish GJ, Nayak MK, Pavic H, Ebert PR (2012) The rph1 gene is a common contributor to the evolution of phosphine resistance in independent field isolates of Rhyzopertha dominica. PLoS ONE 7:e31541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mayr E (1942) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, Cambridge

    Google Scholar 

  • Nakakita H (1987) The mode of action of phosphine. J Pestic Sci 12:299–309

    Article  CAS  Google Scholar 

  • Nath NS, Bhattacharya I, Tuck AG, Schlipalius DI, Ebert PR (2011) Mechanisms of phosphine toxicity. J Toxicol 2011:494168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ochando MD, Reyes A, Segura D, Callejas C (2010) Phylogeography: its importance in insect pest control. Nova Science Publishers Inc, New York

    Google Scholar 

  • Opit GP, Phillips TW, Aikins MJ, Hasan MM (2012) Phosphine resistance in Tribolium castaneum and Rhyzopertha dominica from stored wheat in Oklahoma. J Econ Entomol 105:1107–1114

    Article  CAS  PubMed  Google Scholar 

  • Pai A, Bernasconi G (2008) Polyandry and female control: the red flour beetle Tribolium castaneum as a case study. J Exp Zool B Mol Dev Evol 310B:148–159

    Article  Google Scholar 

  • Porretta D, Canestrelli D, Bellini R, Celli G, Urbanelli S (2007) Improving insect pest management through population genetic data: a case study of the mosquito Ochlerotatus caspius (Pallas). J Appl Ecol 44:682–691

    Article  CAS  Google Scholar 

  • Potter C (1935) The biology and distribution of Rhizopertha dominica (Fab.). Trans R Entomol Soc Lond 83:449–482

    Article  Google Scholar 

  • Rafter MA, McCulloch GA, Daglish GJ, Walter GH (2017) Progression of phosphine resistance in susceptible Tribolium castaneum (Herbst) populations under different immigration regimes and selection pressures. Evol Appl 10:907–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rafter MA, McCulloch GA, Daglish GJ, Gurdasani K, Walter GH (2018) Polyandry, genetic diversity and fecundity of emigrating beetles: understanding new foci of infestation and selection. J Pest Sci 91:287–298

    Article  Google Scholar 

  • Rajan TS et al (2018) Flight of three major insect pests of stored grain in the monsoonal tropics of India, by latitude, season and habitat. J Stored Prod Res 76:43–50

    Article  Google Scholar 

  • Ridley AW, Hereward JP, Daglish GJ, Raghu S, Collins PJ, Walter GH (2011) The spatiotemporal dynamics of Tribolium castaneum (Herbst): adult flight and gene flow. Mol Ecol 20:1635–1646

    Article  CAS  PubMed  Google Scholar 

  • Ridley AW, Hereward JP, Daglish GJ, Raghu S, McCulloch GA, Walter GH (2016) Flight of Rhyzopertha dominica (Coleoptera: Bostrichidae)—a spatio-temporal analysis with pheromone trapping and population genetics. J Econ Entomol 109:2561–2571

    Article  CAS  PubMed  Google Scholar 

  • Rodgers WA, Panwar HS, Mathur VB (2000) Wildlife protected area network in India: a review: executive summary. Wildlife Institute of India, Dehradun

    Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Sakai AK et al (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schlipalius DI et al (2012) A core metabolic enzyme mediates resistance to phosphine gas. Science 338:807–810

    Article  CAS  PubMed  Google Scholar 

  • Schmidt S, Schmid-Egger C, Morinière J, Haszprunar G, Hebert PD (2015) DNA barcoding largely supports 250 years of classical taxonomy: identifications for Central European bees (Hymenoptera, Apoidea partim). Mol Ecol Resour 15:985–1000

    Article  CAS  PubMed  Google Scholar 

  • Sezonlin M et al (2006) Phylogeography and population genetics of the maize stalk borer Busseola fusca (Lepidoptera, Noctuidae) in sub-Saharan Africa. Mol Ecol 15:407–420

    Article  CAS  PubMed  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. Ann Entomol Soc Am 87:651–701

    Article  CAS  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Smith EH, Whitman RC (1992) Field guide to structural pests. National Pest Management Association, Dunn Loring

    Google Scholar 

  • Sokoloff A (1977) The biology of Tribolium with special emphasis on genetic aspects, vol 3. Clarendon Press, Oxford

    Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toews MD, Campbell JF, Arthur FH, Ramaswamy SB (2006) Outdoor flight activity and immigration of Rhyzopertha dominica into seed wheat warehouses. Entomol Exp Appl 121:73–85

    Article  Google Scholar 

  • Toon A, Daglish GJ, Ridley AW, Emery RN, Holloway JC, Walter GH (2016) Random mating between two widely divergent mitochondrial lineages of Cryptolestes ferrugineus (Coleoptera: Laemophloeidae): a test of species limits in a phosphine-resistant stored product pest. J Econ Entomol 109:2221–2228

    Article  CAS  PubMed  Google Scholar 

  • Vela-Coiffier EL, Fargo WS, Bonjour EL, Cuperus GW, Warde WD (1997) Immigration of insects into on-farm stored wheat and relationships among trapping methods. J Stored Prod Res 33:157–166

    Article  Google Scholar 

  • Zhang D-X, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol 11:247–251

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Australia–India Strategic Research Grand Challenge Funded (GCF010006) project entitled “Ensuring food security: harnessing science to protect our grain harvest from insect threats,” jointly sponsored by the Department of Science and Technology, New Delhi, India, and the Department of Innovation, Industry, Science and Research, Canberra, Australia. We thank the managers and technical staff at the Food Corporation of India, Central Warehousing Corporation, and other state warehousing corporations of India for assisting in collecting samples. We also thank GrainCorp and several farming enterprises across Australia for allowing access to their land, as well as Andrew Ridley, Jo Holloway, Rob Emery, and Philip Burrill, Muralitharan, Loganathan, Manivannan, and Vimal Diwedi for providing samples.

Author information

Authors and Affiliations

  1. School of Biological Sciences, The University of Queensland, Brisbane, QLD, 4072, Australia

    Graham A. McCulloch & Gimme H. Walter

  2. Department of Zoology, University of Otago, P.O. Box 56, Dunedin, 9054, New Zealand

    Graham A. McCulloch

  3. Department of Plant Biotechnology, Centre for Plant Molecular Biology and Biotechnology, Tamil Nadu Agricultural University, Coimbatore, 03, India

    S. Mohankumar, R. Surendran & R. Gaurav

  4. Division of Entomology, Indian Agricultural Research Institute, Pusa Campus, New Delhi, 12, India

    S. Subramanian & C. Rahul

  5. Department of Agricultural Entomology, Centre for Plant Protection Studies, Tamil Nadu Agricultural University, Coimbatore, 03, India

    T. Sonai Rajan & S. Chandrasekaran

  6. Department of Agriculture and Fisheries, EcoSciences Precinct, GPO Box 267, Brisbane, QLD, 4001, Australia

    Gregory J. Daglish

Authors
  1. Graham A. McCulloch
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Mohankumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Subramanian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. Sonai Rajan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. C. Rahul
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. R. Surendran
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R. Gaurav
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. S. Chandrasekaran
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Gregory J. Daglish
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Gimme H. Walter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Graham A. McCulloch.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Communicated by C.G. Athanassiou.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 18 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McCulloch, G.A., Mohankumar, S., Subramanian, S. et al. Contrasting patterns of phylogeographic structuring in two key beetle pests of stored grain in India and Australia. J Pest Sci 92, 1249–1259 (2019). https://doi.org/10.1007/s10340-019-01121-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-019-01121-9

Keywords

Search

Navigation