A genome-wide approach for uncovering evolutionary relationships of Australian Bactrocera species complexes (Diptera: Tephritidae)
Renee A. Catullo
A B C D I , Heng L. Yeap B , Siu F. Lee B C , Jason G. Bragg E , Jodie Cheesman F , Stefano De Faveri F , Owain Edwards B , Alvin K. W. Hee G , Angel D. Popa B C , Michele Schiffer H and John G. Oakeshott B
+ Author Affiliations
- Author Affiliations
A School of Science and Health and Hawkesbury Institute of the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW 2751, Australia.
B Land and Water Flagship, The Commonwealth Scientific and Industrial Research Organisation, Black Mountain, ACT 2601, Australia.
C Department of Biological Sciences, Macquarie University, North Ryde, NSW 2109, Australia.
D Centre for Biodiversity Analysis, Ecology & Evolution, The Australian National University, Canberra, ACT 2601, Australia.
E Royal Botanic Gardens, Mrs Macquaries Road, Sydney, NSW 2000, Australia.
F Department of Agriculture and Fisheries, 28 Peters Street, Mareeba, QLD 4880, Australia.
G Department of Biology, Universiti Putra Malaysia, Serdang, Malaysia.
H Daintree Rainforest Observatory, James Cook University, Cape Tribulation, Qld 4873, Australia.
I Corresponding author. Email: renee.catullo@gmail.com
Invertebrate Systematics 33(4) 618-627 https://doi.org/10.1071/IS18065
Submitted: 10 August 2018 Accepted: 4 February 2019 Published: 2 August 2019
Abstract
Australia and Southeast Asia are hotspots of global diversity in the fruit-fly genus Bactrocera. Although a great diversity of species has been long recognised, evolutionary relationships are poorly understood, largely because previous sequencing techniques have provided insufficient historical signal for phylogenetic reconstruction. Poorly understood biogeographic history in Bactrocera has prevented a deeper understanding of migratory patterns in this economically important pest group. Using representatives from Australia and Malaysia, we tested the utility of a genome-reduction approach that generates thousands of single-nucleotide polymorphisms for phylogenetic reconstructions. This approach has high utility for species identification because of the ease of sample addition over time, and the species-level specificity able to be achieved with the markers. These data have provided a strongly supported phylogenetic tree congruent with topologies generated using more intensive sequencing approaches. In addition, our results do not support taxonomic assignments to species complex for a number of species, such as B. endiandrae in the dorsalis complex, yet find a close relationship between B. pallida and the dorsalis species. Our data have further validated non-monophyletic evolution of male response to primary attractants. We also showed at least two diversification events between Australia and Southeast Asia, indicating trans-regional dispersal in important pest species.
References
Abdalla, A., Millist, N., Buetre, B., and Bowen, B. (2012). Benefit–cost analysis of the National Fruit Fly Strategy Action Plan. ABARES report to client prepared for Plant Health Australia, Canberra, ACT, Australia.Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.-H., Xie, D., Suchard, M. A., Rambaut, A., and Drummond, A. J. (2014). BEAST 2: a software platform for bayesian evolutionary analysis. PLoS Computational Biology 10, e1003537.
| BEAST 2: a software platform for bayesian evolutionary analysis.Crossref | GoogleScholarGoogle Scholar | 24722319PubMed |
Bryant, D., Bouckaert, R., Felsenstein, J., Rosenberg, N.A., and Choudhury, R. A. (2012). Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis. Molecular Biology and Evolution 29, 1917–1932.
| Inferring species trees directly from biallelic genetic markers: bypassing gene trees in a full coalescent analysis.Crossref | GoogleScholarGoogle Scholar | 22422763PubMed |
Cantrell, B., Chadwick, B., and Cahill, A. (2002). ‘Fruit Fly Fighters.’ (CSIRO Publishing: Melbourne, Vic., Australia.)
Chifman, J., and Kubatko, L. (2014). Quartet inference from SNP data under the coalescent model. Bioinformatics 30, 3317–3324.
| Quartet inference from SNP data under the coalescent model.Crossref | GoogleScholarGoogle Scholar | 25104814PubMed |
Chifman, J., and Kubatko, L. (2015). Identifiability of the unrooted species tree topology under the coalescent model with time-reversible substitution processes, site-specific rate variation, and invariable sites. Journal of Theoretical Biology 374, 35–47.
| Identifiability of the unrooted species tree topology under the coalescent model with time-reversible substitution processes, site-specific rate variation, and invariable sites.Crossref | GoogleScholarGoogle Scholar | 25791286PubMed |
Clarke, A. R., Armstrong, K. F., Carmichael, A. E., Milne, J. R., Raghu, S., Roderick, G. K., and Yeates, D. K. (2005). Invasive phytophagous pest arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies. Annual Review of Entomology 50, 293–319.
| Invasive phytophagous pest arising through a recent tropical evolutionary radiation: the Bactrocera dorsalis complex of fruit flies.Crossref | GoogleScholarGoogle Scholar | 15355242PubMed |
Copeland, R. S., White, I. M., Okumu, M., Machera, P., and Wharton, R. A. (2004). Insects associated with fruits of the Oleaceae (Asteridae, Lamiales) in Kenya, with special reference to the Tephritidae (Diptera). Bishop Museum Bulletin in Entomology 12, 135–164.
Cruickshank, L., Jessup, A. J., and Cruickshank, D. J. (2001). Interspecific crosses of Bactrocera tryoni (Froggatt) and Bactrocera jarvisi (Tryon) (Diptera: Tephritidae) in the laboratory. Australian Journal of Entomology 40, 278–280.
| Interspecific crosses of Bactrocera tryoni (Froggatt) and Bactrocera jarvisi (Tryon) (Diptera: Tephritidae) in the laboratory.Crossref | GoogleScholarGoogle Scholar |
De Meyer, M., Delatte, H., Mwatawala, M., Quilici, S., Vayssières, J.-F., and Virgilio, M. (2015). A review of the current knowledge on Zeugodacus cucurbitae (Coquillett) (Diptera, Tephritidae) in Africa, with a list of species included in Zeugodacus. ZooKeys 540, 539–557.
| A review of the current knowledge on Zeugodacus cucurbitae (Coquillett) (Diptera, Tephritidae) in Africa, with a list of species included in Zeugodacus.Crossref | GoogleScholarGoogle Scholar |
Drew, R. A. I. (1989). The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Memoirs of the Queensland Museum 26, 521–525.
Drew, D., and Hancock, M. (1999). Phylogeny of the tribe Dacini (Dacinae) based on morphological, distributional, and biological data. In ‘Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior’. (Eds M. Aluja and A. L. Norrbom.) pp. 491–504. (CRC Press: Boca Raton, FL, USA.)
Drew, R. A. I., and Romig, M. C. (2013). ‘Tropical Fruit Flies of South-east Asia.’ (CABI: Wallingford, UK.)
Drew, R. A. I., and Romig. M. C. (2016) Keys to the tropical fruit flies (Tephritidae: Dacinae) of South-East Asia: Indomalaya to North-West Australasia. (CABI; Wallingford, UK.)
Dupuis, J. R., Bremer, F. T., Kauwe, A., Jose, M. S., Leblanc, L., Rubinoff, D., and Geib, S. M. (2018). HiMAP: robust phylogenomics from highly multiplexed amplicon sequencing. Molecular Ecology Resources 18, 1000–1019.
| HiMAP: robust phylogenomics from highly multiplexed amplicon sequencing.Crossref | GoogleScholarGoogle Scholar |
Hafi, A., Arthur, T., Symes, M., and Millist, N. (2013) Benefit-cost analysis of the long term containment strategy for exotic fruit flies in the Torres Strait. ABARES Report to client prepared for the National Biosecurity committee, Canberra.
Gilchrist, A. S., Shearman, D. C., Frommer, M., Raphael, K. A., Deshpande, N. P., Wilkins, M. R., Sherwin, W. B., and Sved, J. A. (2014). The draft genome of the pest tephritid fruit fly Bactrocera tryoni: resources for the genomic analysis of hybridising species. BMC Genomics 15, 1153.
| The draft genome of the pest tephritid fruit fly Bactrocera tryoni: resources for the genomic analysis of hybridising species.Crossref | GoogleScholarGoogle Scholar | 25527032PubMed |
Gruber, B., Unmack, P. J., Berry, O. F., and Georges, A. (2018). dartr: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources 18, 691–699.
| dartr: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing.Crossref | GoogleScholarGoogle Scholar | 29266847PubMed |
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
| New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 20525638PubMed |
Hammer, Ø., Harper, D. A. T., and Ryan, P. D. (2001). PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 9.
Hancock, D. L., Hamacek, E. L., Lloyd, A. C., and Elson-Harris, M. M. (2000). ‘The Distribution and Host Plants of Fruit Flies (Diptera: Tephritidae) in Australia.’ (Queensland Department of Primary Industries Publications: Brisbane, Qld, Australia.)
Hardy, D. E. (1951). The Krauss collection of Australian fruit flies (Tephritidae-Diptera). Pacific Science 5, 115–189.
Hardy, D. E. (1969). Taxonomy and distribution of the oriental fruit fly and related species (Tephritidae-Diptera). Proceedings of the Hawaiian Entomological Society 20, 395–428.
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A., and Jermiin, L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589.
| ModelFinder: fast model selection for accurate phylogenetic estimates.Crossref | GoogleScholarGoogle Scholar | 28481363PubMed |
Krosch, M. N., Schutze, M. K., Armstrong, K. F., Graham, G. C., Yeates, D. K., and Clarke, A. R. (2012). A molecular phylogeny for the tribe Dacini (Diptera: Tephritidae): systematic and biogeographic implications. Molecular Phylogenetics and Evolution 64, 513–523.
| A molecular phylogeny for the tribe Dacini (Diptera: Tephritidae): systematic and biogeographic implications.Crossref | GoogleScholarGoogle Scholar | 22609822PubMed |
Leaché, A. D., and Oaks, J. R. (2017). The utility of single nucleotide polymorphism (SNP) data in phylogenetics. Annual Review of Ecology Evolution and Systematics 48, 69–84.
| The utility of single nucleotide polymorphism (SNP) data in phylogenetics.Crossref | GoogleScholarGoogle Scholar |
Leblanc, L., Jose, M. S., Barr, N., and Rubinoff, D. (2015). A phylogenetic assessment of the polyphyletic nature and intraspecific color polymorphism in the Bactrocera dorsalis complex (Diptera, Tephritidae). ZooKeys 540, 339–367.
| A phylogenetic assessment of the polyphyletic nature and intraspecific color polymorphism in the Bactrocera dorsalis complex (Diptera, Tephritidae).Crossref | GoogleScholarGoogle Scholar |
Matzke, N. J. (2014). Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades. Systematic Biology 63, 951–970.
| Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades.Crossref | GoogleScholarGoogle Scholar | 25123369PubMed |
McVay, J. D., and Carstens, B. C. (2013). Phylogenetic model choice: justifying a species tree or concatenation analysis. Journal of Phylogenetics & Evolutionary Biology 1, 1–8.
| Phylogenetic model choice: justifying a species tree or concatenation analysis.Crossref | GoogleScholarGoogle Scholar |
Meats, A., Fay, H. A. C., and Drew, R. A. I. (2008). Distribution and eradication of an exotic tephritid fruit fly in Australia: relevance of invasion theory. Journal of Applied Entomology 132, 406–411.
| Distribution and eradication of an exotic tephritid fruit fly in Australia: relevance of invasion theory.Crossref | GoogleScholarGoogle Scholar |
Melville, J., Haines, M. L., Boysen, K., Hodkinson, L., Kilian, A., Date, K. L. S., Potvin, D. A., and Parris, K. M. (2017). Identifying hybridization and admixture using SNPs: application of the DArTseq platform in phylogeographic research on vertebrates. Royal Society Open Science 4, 161061.
| Identifying hybridization and admixture using SNPs: application of the DArTseq platform in phylogeographic research on vertebrates.Crossref | GoogleScholarGoogle Scholar | 28791133PubMed |
Minh, B. Q., Nguyen, M. A. T., and von Haeseler, A. (2013). Ultrafast approximation for phylogenetic bootstrap. Molecular Biology and Evolution 30, 1188–1195.
| Ultrafast approximation for phylogenetic bootstrap.Crossref | GoogleScholarGoogle Scholar | 23418397PubMed |
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A., and Minh, B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.
| IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies.Crossref | GoogleScholarGoogle Scholar | 25371430PubMed |
Pazmiño, D. A., Maes, G. E., Simpfendorfer, C. A., Salinas-de-León, P., and van Herwerden, L. (2017). Genome-wide SNPs reveal low effective population size within confined management units of the highly vagile Galapagos shark (Carcharhinus galapagensis). Conservation Genetics 18, 1151–1163.
| Genome-wide SNPs reveal low effective population size within confined management units of the highly vagile Galapagos shark (Carcharhinus galapagensis).Crossref | GoogleScholarGoogle Scholar |
Pembleton, L. W., Cogan, N. O. I., and Forster, J. W. (2013). StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources 13, 946–952.
| StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations.Crossref | GoogleScholarGoogle Scholar | 23738873PubMed |
Petroli, C. D., Sansaloni, C. P., Carling, J., Steane, D. A., Vaillancourt, R. E., Myburg, A. A., da Silva, O. B., Pappas, G. J., Kilian, A., and Grattapaglia, D. (2012). Genomic characterization of DArT Markers based on high-density linkage analysis and physical mapping to the eucalyptus genome. PLoS One 7, e44684.
| Genomic characterization of DArT Markers based on high-density linkage analysis and physical mapping to the eucalyptus genome.Crossref | GoogleScholarGoogle Scholar | 22984541PubMed |
R Core Team (2017). ‘R: a Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.)
Rambaut, A., Suchard, M. A., and Drummond, A. J. (2013) ‘Tracer.’ (Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, Scotland.)
Royer, J. E., and Hancock, D. L. (2012). New distribution and lure records of Dacinae (Diptera: Tephritidae) from Queensland, Australia, and description of a new species of Dacus fabricius. Australian Journal of Entomology 51, 239–247.
| New distribution and lure records of Dacinae (Diptera: Tephritidae) from Queensland, Australia, and description of a new species of Dacus fabricius.Crossref | GoogleScholarGoogle Scholar |
San Jose, M., Doorenweerd, C., Leblanc, L., Barr, N., Geib, S., and Rubinoff, D. (2018). Incongruence between molecules and morphology: a seven-gene phylogeny of Dacini fruit flies paves the way for reclassification (Diptera: Tephritidae). Molecular Phylogenetics and Evolution 121, 139–149.
| Incongruence between molecules and morphology: a seven-gene phylogeny of Dacini fruit flies paves the way for reclassification (Diptera: Tephritidae).Crossref | GoogleScholarGoogle Scholar | 29224785PubMed |
Schutze, M. K., Aketarawong, N., Amornsak, W., Armstrong, K. F., Augustinos, A. A., Barr, N., Bo, W., Bourtzis, K., Boykin, L. M., Cáceres, C., Cameron, S. L., Chapman, T. A., Chinvinijkul, S., Chomič, A., De Meyer, M., Drosopoulou, E., Englezou, A., Ekesi, S., Gariou-Papalexiou, A., Geib, S. M., Hailstones, D., Hasanuzzaman, M., Haymer, D., Hee, A. K. W., Hendrichs, J., Jessup, A., Ji, Q., Khamis, F. M., Krosch, M. N., Leblanc, L., Mahmood, K., Malacrida, A. R., Mavragani-Tsipidou, P., Mwatawala, M., Nishida, R., Ono, H., Reyes, J., Rubinoff, D., San Jose, M., Shelly, T. E., Srikachar, S., Tan, K. H., Thanaphum, S., Haq, I., Vijaysegaran, S., Wee, S. L., Yesmin, F., Zacharopoulou, A., and Clarke, A. R. (2015). Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data. Systematic Entomology 40, 456–471.
| Synonymization of key pest species within the Bactrocera dorsalis species complex (Diptera: Tephritidae): taxonomic changes based on a review of 20 years of integrative morphological, molecular, cytogenetic, behavioural and chemoecological data.Crossref | GoogleScholarGoogle Scholar |
Schutze, M. K., Bourtzis, K., Cameron, S. L., Clarke, A. R., De Meyer, M., Hee, A. K. W., Hendrichs, J., Krosch, M. N., and Mwatawala, M. (2017). Integrative taxonomy versus taxonomic authority without peer review: the case of the oriental fruit fly, Bactrocera dorsalis (Tephritidae). Systematic Entomology 42, 609–620.
| Integrative taxonomy versus taxonomic authority without peer review: the case of the oriental fruit fly, Bactrocera dorsalis (Tephritidae).Crossref | GoogleScholarGoogle Scholar |
Shearman, D. C. A., Frommer, M., Morrow, J. L., Raphael, K. A., and Gilchrist, A. S. (2010). Interspecific hybridization as a source of novel genetic markers for the sterile insect technique in Bactrocera tryoni (Diptera: Tephritidae). Journal of Economic Entomology 103, 1071–1079.
| Interspecific hybridization as a source of novel genetic markers for the sterile insect technique in Bactrocera tryoni (Diptera: Tephritidae).Crossref | GoogleScholarGoogle Scholar |
Simpson, M., and Srinivansen, V. (2014). ‘Australia’s Biosecurity Future: Preparing for Future Biological Challenges.’ (CSIRO: Canberra, ACT, Australia.)
Smith, P. T., Kambhampati, S., and Armstrong, K. A. (2003). Phylogenetic relationships among Bactrocera species (Diptera: Tephritidae) inferred from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 26, 8–17.
| Phylogenetic relationships among Bactrocera species (Diptera: Tephritidae) inferred from mitochondrial DNA sequences.Crossref | GoogleScholarGoogle Scholar | 12470933PubMed |
Stephens, A. E. A., Kriticos, D. J., and Leriche, A. (2007). The current and future potential geographical distribution of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). Bulletin of Entomological Research 97, 369–378.
| The current and future potential geographical distribution of the oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae).Crossref | GoogleScholarGoogle Scholar |
Swofford, D. L. (2002). ‘PAUP*, Phylogenetic Analysis using Parsimony (*and Other Methods).’ (Sinauer Associates: Sunderland, MA, USA.)
Vargas, R. I., Piñero, J. C., and Leblanc, L. (2015). An overview of pest species of Bactrocera fruit flies (Diptera: Tephritidae) and the integration of biopesticides with other biological approaches for their management with a focus on the Pacific region. Insects 6, 297–318.
| An overview of pest species of Bactrocera fruit flies (Diptera: Tephritidae) and the integration of biopesticides with other biological approaches for their management with a focus on the Pacific region.Crossref | GoogleScholarGoogle Scholar | 26463186PubMed |
Virgilio, M., Jordaens, K., Verwimp, C., White, I. M., and De Meyer, M. (2015). Higher phylogeny of frugivorous flies (Diptera, Tephritidae, Dacini): localised partition conflicts and a novel generic classification. Molecular Phylogenetics and Evolution 85, 171–179.
| Higher phylogeny of frugivorous flies (Diptera, Tephritidae, Dacini): localised partition conflicts and a novel generic classification.Crossref | GoogleScholarGoogle Scholar | 25681676PubMed |
Warren, D. L., Geneva, A. J., and Lanfear, R. (2017). RWTY (R We There Yet): an R package for examining convergence of Bayesian phylogenetic analyses. Molecular Biology and Evolution 34, 1016–1020.
| RWTY (R We There Yet): an R package for examining convergence of Bayesian phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 28087773PubMed |
Wenzl, P., Carling, J., Kudrna, D., Jaccoud, D., Huttner, E., Kleinhofs, A., and Kilian, A. (2004). Diversity Arrays Technology (DArT) for whole-genome profiling of barley. Proceedings of the National Academy of Sciences of the United States of America 101, 9915–9920.
| Diversity Arrays Technology (DArT) for whole-genome profiling of barley.Crossref | GoogleScholarGoogle Scholar | 15192146PubMed |
White, I. M., and Elson-Harris, M. M. (1992). ‘Fruit Flies of Economic Significance: Their Identification and Bionomics.’ (CAB International: Wallingford, UK.)
