Abstract
Understanding and interpreting the host plant interactions of “generalist” herbivorous insects requires that species limits are accurately defined, as such taxa frequently harbour cryptic species with restricted host use. We tested for the presence of cryptic species across different host plant species in Australian Frankliniella schultzei using a combination of gene sequencing and newly developed microsatellite markers. We detect deep divergence between three colour morphs (black, brown and yellow) but no discordance between mitochondrial and nuclear genes in areas of sympatry, indicating the presence of at least three species in Australia (and potentially six globally). Microsatellite markers were developed for the brown species but could not be amplified in the black or yellow species because the divergence between them is too great. When applied to six populations across Queensland and New South Wales the microsatellites showed high levels of gene flow across thrips collected from Gossypium hirsutum (cotton), Hibiscus rosa-sinensis and Malvaviscus arboreus, and over distances of at least 950 km, indicating considerable movement by these insects and no host-associated genetic differentiation in the brown species. Significantly, the divergence between the three species in Australia was not associated with any noticeable host specialisation. The substantial overlap in geographical distribution and host plant range raises questions about the process of speciation in generalist insects. Our results provide the basis from which detailed quantification of relative host use can be conducted for each species within the F. schultzei complex; this next step is crucial to fully understanding the host plant relationships of each and, thus, the basis of their speciation.
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References
Belshaw R, Quicke DL (1997) A molecular phylogeny of the Aphidiinae (Hymenoptera: Braconidae). Mol Phylogenetic Evol 7:281–293
Bernays E (1998) Evolution of feeding behavior in insect herbivores. Bioscience 48:35–44. doi:10.2307/1313226
Bhatti J, Alavi J, zur Strassen R, Telmadarraiy Z (2009) Thysanoptera in Iran 1938–2007. An overview. Part 1. Thrips 7–8:1–373
Bickford D, Lohman D, Sodhi N et al (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. doi:10.1016/j.tree.2006.11.004
Brookes DR, Hereward JP, Terry LI, Walter GH (2015) Evolutionary dynamics of a cycad obligate pollination mutualism—pattern and process in extant Macrozamia cycads and their specialist thrips pollinators. Mol Phylogenetic Evol 93:83–93. doi:10.1016/j.ympev.2015.07.003
Brunner PC, Frey JE (2010) Habitat-specific population structure in native western flower thrips Frankliniella occidentalis (Insecta, Thysanoptera). J Evol Biol 23:797–804. doi:10.1111/j.1420-9101.2010.01946.x
Campbell B, Steffen-Campbell J, Werren J (1993) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Mol Biol 2:225–237. doi:10.1111/j.1365-2583.1994.tb00142.x
Chapuis M-P, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631. doi:10.1093/molbev/msl191
Danforth B, Fang J, Sipes S (2006) Analysis of family-level relationships in bees (Hymenoptera: Apiformes) using 28S and two previously unexplored nuclear genes: CAD and RNA polymerase II. Mol Phylogenetic Evol 39:358–372
Darriba D, Taboada G, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. doi:10.1038/nmeth.2109
Desprès L, Imbert-Establet D, Monnerot M (1993) Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America. Mol Biochem Parasitol 60:221–229. doi:10.1016/0166-6851(93)90133-I
Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. doi:10.1093/nar/gkh340
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. doi:10.1111/j.1365-294X.2005.02553.x
Finlay-Doney M, Walter G (2012) The conceptual and practical implications of interpreting diet breadth mechanistically in generalist predatory insects. Biol J Linn Soc 107:737–763. doi:10.1111/j.1095-8312.2012.01991.x
Folmer O, Black M, Hoeh W et al (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299
Gikonyo M, Niassy S, Moritz G et al (2016) Resolving the taxonomic status of Frankliniella schultzei (Thysanoptera: Thripidae) colour forms in Kenya—a morphological, biological, molecular and ecological based approach. Int J Trop Insect Sci. doi:10.1017/S1742758416000126
Huelsenbeck J, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754
Jacobson A, Nault B, Vargo E, Kennedy G (2016) Restricted gene flow among lineages of Thrips tabaci supports genetic divergence among cryptic species groups. PLoS ONE 11:e0163882. doi:10.1371/journal.pone.0163882
Jakobsson M, Rosenberg N (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. doi:10.1093/bioinformatics/btm233
Kakkar G, Seal D, Stansly P et al (2012) Abundance of Frankliniella schultzei (Thysanoptera: Thripidae) in flowers on major vegetable crops of south Florida. Florida Entomol 97:468–475. doi:10.1653/024.095.0231
Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. doi:10.1093/bioinformatics/bts199
Kopelman N, Mayzel J, Jakobsson M et al (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. doi:10.1111/1755-0998.12387
Loxdale H, Lushai G, Harvey J (2011) The evolutionary improbability of “generalism” in nature, with special reference to insects. Biol J Linn Soc 103:1–18. doi:10.1111/j.1095-8312.2011.01627.x
Macharia I, Backhouse D, Skilton R et al (2015) Diversity of thrips species and vectors of tomato spotted wilt virus in tomato production systems in Kenya. J Econ Entomol 108:20–28. doi:10.1093/jee/tou010
Mayhew P (2007) Why are there so many insect species? Perspectives from fossils and phylogenies. Biol Rev 82:425–454. doi:10.1111/j.1469-185x.2007.00018.x
Meglécz E, Pech N, Gilles A et al (2014) QDD version 3.1: a user-friendly computer program for microsatellite selection and primer design revisited: experimental validation of variables determining genotyping success rate. Mol Ecol Resour 14:1302–1313. doi:10.1111/1755-0998.12271
Milne M, Walter G (2000) Feeding and breeding across host plants within a locality by the widespread thrips Frankliniella schultzei, and the invasive potential of polyphagous herbivores. Divers Distrib 6:243–257. doi:10.1046/j.1472-4642.2000.00089.x
Milne M, Walter G, Milne J (2007) Mating behavior and species status of host-associated populations of the polyphagous thrips, Frankliniella schultzei. J Insect Behav 20:331–346. doi:10.1007/s10905-007-9081-4
Mitter C, Farrell B, Wiegmann B (1988) The phylogenetic study of adaptive zones: has phytophagy promoted Insect diversification? Am Nat 132:107–128. doi:10.1086/284840
Mound LA (1968) A review of R. S. Bagnall’s Thysanoptera collections. Bullet Br Mus suppl 11:1–181 (Natural History) (Ent.)
Mound LA, Tree DJ, Paris D (2015) OzThrips—Thysanoptera in Australia. http://www.ozthrips.org/. Accessed 2015–2016
Paterson H (1991) The recognition of cryptic species among economically important insects. In: Zalucki MP (ed) Heliothis, research methods and prospects. Springer, New York, pp 1–10
Peakall R, Smouse P (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi:10.1093/bioinformatics/bts460 (Oxford, England)
Pritchard J, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rafter M, Walter G (2013) Mate recognition in the South African Citrus Thrips Scirtothrips aurantii (Faure) and cross-mating tests with populations from Australia and South Africa. J Insect Behav 26:780–795. doi:10.1007/s10905-013-9391-7
Rafter M, Hereward J, Walter G (2013) Species limits, quarantine risk and the intrigue of a polyphagous invasive pest with highly restricted host relationships in its area of invasion. Evol Appl 6:1195–1207. doi:10.1111/eva.12096
Rambaut A, Drummond AJ (2017) Tracer v1.4. http://tree.bio.ed.ac.uk/software/tracer/
Rosenberg N (2004) distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138. doi:10.1046/j.1471-8286.2003.00566.x
Rotenberg D, Jacobson A, Schneweis D, Whitfield A (2015) Thrips transmission of tospoviruses. Curr Opin Virol 15:80–89. doi:10.1016/j.coviro.2015.08.003
Rugman-Jones P, Hoddle M, Stouthamer R (2010) Nuclear-mitochondrial barcoding exposes the global pest Western Flower Thrips (Thysanoptera: Thripidae) as two sympatric cryptic species in its native California. J Econ Entomol 107:877–886. doi:10.1603/EC09300
Sakimura K (1969) A comment on the color forms of Frankliniella schultzei (Thysanoptera: Thripidae) in relation to transmission of the tomato-spotted wilt virus. Pac Insects 11:761–762
Sakurai T (2004) Transmission of tomato spotted wilt virus by the dark form of Frankliniella schultzei (Thysanoptera: Thripidae) originating in tomato fields in Paraguay. Appl Entomol Zool 39:189–194. doi:10.1303/aez.2004.189
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234. doi:10.1038/72708
Silva R (2015) Invasion ecology of thrips in relation to seedling cotton. Unpublished PhD thesis. The University of Queensland, Brisbane. doi:10.14264/uql.2015.853, pp 227
Simon C, Frati F, Beckenbach A et al (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–704. doi:10.1093/aesa/87.6.651
Smith M, Wood D, Janzen D et al (2007) DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera, Tachinidae) are not all generalists. Proc Natl Acad Sci USA 104:4967–4972. doi:10.1073/pnas.0700050104
Toon A, Daglish G, Ridley A et al (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. doi:10.1093/jee/tow178
Untergasser A, Cutcutache I, Koressaar T et al (2012) Primer3—new capabilities and interfaces. Nucleic Acids Res 40:e115. doi:10.1093/nar/gks596
Walter GH (2003) Insect pest management and ecological research. Cambridge University Press, Cambridge, p 387
Walter GH, Hengeveld R (2014) Autecology: organisms, interactions and environmental dynamics. CRC Press, Boca Raton, p 467
Wijkamp I (1995) Distinct levels of specificity in Thrips transmission of Tospoviruses. Phytopathology 85:1069. doi:10.1094/Phyto-85-1069
Wilson L, Bauer L (1993) Species composition and seasonal abundance of thrips (Thysanoptera) on cotton in the Namoi Valley. Aust J Entomol 32:187–192. doi:10.1111/j.1440-6055.1993.tb00569.x
Yaku A, Walter G, Najar-Rodriguez AJ (2007) Thrips see red—flower colour and the host relationships of a polyphagous anthophilic thrips. Ecol Entomol 32:527–535. doi:10.1111/j.1365-2311.2007.00899.x
Zhang D, Hewitt GM (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends Ecol Evol 11:247–251. doi:10.1016/0169-5347(96)10031-8
Acknowledgements
The authors acknowledge the Cruiser fund (Under the grant “Invasion ecology of thrips in relation to seedling cotton”) granted for financial support towards this project. We would like to thank Sharon Van Brunschot, Dean Brookes, Justin Cappadonna and Murray Sharman for collecting specimens. We are also very grateful to Mark Schutze for lodging the specimens in the Queensland Primary Industries Insect Collection.
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Hereward, J., Hutchinson, J.A., McCulloch, G.A. et al. Divergence among generalist herbivores: the Frankliniella schultzei species complex in Australia (Thysanoptera: Thripidae). Arthropod-Plant Interactions 11, 875–887 (2017). https://doi.org/10.1007/s11829-017-9543-3
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DOI: https://doi.org/10.1007/s11829-017-9543-3