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Plant host relationships of three lineages of the gall-inducing fly Fergusonina Malloch (Diptera: Fergusoninidae) on Eucalyptus L’Hérit.

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Abstract

The gall-inducing fly family Fergusoninidae, in association with a mutualist nematode, induces galls on Myrtaceae. Each fly species typically targets a particular site on its host plant, giving rise to a range of gall types, and one plant species may host at least four fly species. While incongruent fly–host evolutionary time scales preclude early cospeciation, it is possible that Fergusoninidae have been diverging with their host plants more recently at correspondingly finer taxonomic levels, such as within host subgenera. To test this possibility, we reduced the scale of our analysis and focussed on a clade of ten Eucalyptus species, sampling intensively and using a phylogenetic approach to compare the relationships between these plant hosts and their associated flies. We also took advantage of the fact that three different gall types, each with its own clade of Fergusonina flies, could be sampled on this focal host clade, in effect giving us three different host/fly association tests on the one set of hosts. The phylogenies of flies from the three different gall types were estimated using Bayesian analysis of mtCOI sequences and compared with an existing phylogeny of the eucalypt host clade. While each gall type showed a different pattern of host relationships, heuristic and quantitative analyses showed that there was little correspondence between plant and fly phylogenies and we conclude that host switching is prevalent in this system. There was more host fidelity in the flower bud gallers on this group of eucalypts, and there was least in the leaf blade gallers, with the shoot bud gallers demonstrating an intermediate level of host fidelity. We discuss the possible factors which may have led to their patterns of host association. This is the first study of Fergusonina to focus on one clade of Eucalyptus L’Hérit. (Myrtaceae) with intensive sampling and shows that each host plant species is commonly used by multiple fergusoninid species. This has provided us with the opportunity to study in detail the host relationships of three separate clades of Fergusonina from different plant tissue types, and has revealed many previously unrecorded host plant/gall site associations.

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References

  • Abrahamson WG, Weis AE (1987) Nutritional ecology of arthropod gall-makers. In: Slansky F, Rodriguez JG (eds) The nutritional ecology of insects, mites and spiders. Wiley, New York, pp 235–238

    Google Scholar 

  • Anotaux M, Toscani C, Leborgne R, Chaline N, Pasquet A (2016) Time till death affects spider mobility and web-building behavior during web construction in an orb-web spider. Curr Zool 62:123–130. doi:10.1093/cz/zow001

    Article  Google Scholar 

  • Boland D et al (2006) Forest trees of Australia. CSIRO Publishing, Melbourne

    Google Scholar 

  • Brooker I, Kleinig D (2001) Eucalypts: an illustrated guide to identification. Reed New Holland, Chatswood

    Google Scholar 

  • Brooker MIH, Nicolle D (2013) Atlas of leaf venation and oil gland patterns in the eucalypts. CSIRO Publishing, Collingwood

    Google Scholar 

  • Carey JR, Papadopoulos N, Kouloussis N, Katsoyannos B, Müller H-G, Wang J-L, Tseng Y-K (2006) Age-specific and lifetime behavior patterns in Drosophila melanogaster and the Mediterranean fruit fly, Ceratitis capitata. Exp Gerontol 41:93–97

    Article  PubMed  Google Scholar 

  • Charleston MA (1998) Jungles: a new solution to the host/parasite phylogeny reconciliation problem. Math Biosci 149:191–223

    Article  CAS  PubMed  Google Scholar 

  • Chippendale GM, Wolf L (1981) The natural distribution of Eucalyptus in Australia. Australian National Parks and Wildlife Service, Canberra

    Google Scholar 

  • Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R (2010) Jane: a new tool for the cophylogeny reconstruction problem. Algorithm Mol Biol AMB 5:16. doi:10.1186/1748-7188-5-16

    Article  PubMed  Google Scholar 

  • Craig TP, Itami JK, Horner J, Abrahamson WG (1994) Host shifts and speciation in gall-forming insects. In: Price PW, Mattson WJ, Baranchikov WJ (eds) The ecology and evolution of gall-forming insects. US Department of Agriculture, St. Paul, pp 194–207

    Google Scholar 

  • Currie GA (1937) Galls on Eucalyptus trees. A new type of association between flies and nematodes. Proc Linn Soc N S W 62:147–174

    Google Scholar 

  • Davies KA, Giblin-Davis RM (2004) The biology and associations of Fergusobia (Nematoda) from the Melaleuca leucadendra-complex in eastern Australia. Invertebr Syst 18:291–319

    Article  Google Scholar 

  • Davies KA, Makinson J, Purcell MF (2001) Observations on the development and parasitoids of Fergusonina/Fergusobia galls on Melaleuca quinquenervia (Myrtaceae) in Australia. Trans R Soc S Aust 125:45–50

    Google Scholar 

  • Davies KA, Giblin-Davis RM, Ye W, Taylor GS, Thomas WK (2010a) Nematodes from galls on Myrtaceae. I. Fergusobia/Fergusonina galls on Corymbia spp., with re-description of F. magna and notes on its phylogenetic relationships. Zootaxa 2634:25–40

    Google Scholar 

  • Davies KA, Ye W, Giblin-Davis RM, Taylor GS, Scheffer S, Thomas WK (2010b) The nematode genus Fergusobia (Nematoda: Neotylenchidae): molecular phylogeny, descriptions of clades and associated galls, host plants and Fergusonina fly larvae. Zootaxa 2633:1–66

    Google Scholar 

  • Davies KA, Ye W, Taylor GS, Scheffer S, Giblin-Davis RM (2016) Galling problems—the Fergusobia nematode/Fergusonina fly mutualism on myrtaceous hosts. Nematology 18:629–649

    Google Scholar 

  • de Vienne DM, Refregier G, Lopez-Villavicencio M, Tellier A, Hood ME, Giraud T (2013) Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytol 198:347–385. doi:10.1111/nph.12150

    Article  PubMed  Google Scholar 

  • Fisher JM, Nickle WR (1968) On the classification and life history of Fergusobia curriei (Sphaerulariidae: Nematoda). Proc Helminthol Soc Wash 35:40–46

    Google Scholar 

  • Giblin-Davis RM et al (2001) Fergusobia/Fergusonina-induced shoot bud gall development on Melaleuca quinquenervia. J Nematol 33:239–247

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giblin-Davis RM et al (2003) Coevolution between Fergusobia and Fergusonina mutualists. In: Proceeding of the fourth international congress of nematology. Nematology Monographs and Perspectives, vol 2, pp 407–417

  • Giblin-Davis RM et al (2004a) Histological comparisons of Fergusobia/Fergusonina-induced galls on different Myrtaceous hosts. J Nematol 36:249–262

    CAS  PubMed  PubMed Central  Google Scholar 

  • Giblin-Davis RM, Thomas K, Davies K, Taylor G (2004b) Entomophilic nematode models for studying biodiversity and cospeciation. In: Chen Z, Chen S, Dickson D (eds) Nematology advances and perspectives. Nematode Morphology, Physiology and Ecology, vol 1. Tsinghua University Press, Beijing, pp 493–540

    Chapter  Google Scholar 

  • Gonzalez-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr NJ, Laffan SW, Gruber B (2016) Phylogenetic approaches reveal biodiversity threats under climate change. Nat Clim Change 6:1110–1114

    Article  Google Scholar 

  • Harris KM (1982) First record of Fergusoninidae (Diptera, Schizophora) outside Australia—a new species of Fergusonina on Syzygium in India. Syst Entomol 7:211–216

    Article  Google Scholar 

  • Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501

    Article  CAS  PubMed  Google Scholar 

  • Hartley SE, Lawton JH (1992) Host-plant manipulation by gall-insects: a test of the nutrition hypothesis. J Anim Ecol 61:113–119

    Article  Google Scholar 

  • Head E (2008) Ecology of the Fergusonina fly and Fergusobia nematode gall association in South Australia. MSc thesis, University of Adelaide

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Inbar M, Wink M, Wool D (2004) The evolution of host plant manipulation by insects: molecular and ecological evidence from gall-forming aphids on Pistacia. Mol Phylogenet Evol 32:504–511. doi:10.1016/j.ympev.2004.01.006

    Article  CAS  PubMed  Google Scholar 

  • Johnson LAS, Hill KD (1990) New taxa and combinations in Eucalyptus and Angophora (Myrtaceae). Telopea 4:37–108

    Article  Google Scholar 

  • Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701. doi:10.1093/molbev/mss020

    Article  CAS  PubMed  Google Scholar 

  • Larsson S, Ekbom B (1995) Oviposition mistakes in herbivorous insects: confusion or a step towards a new host plant? Oikos 72:155–160

    Article  Google Scholar 

  • Meyer J (1987) Plant galls and gall inducers. Gebrüder Borntraeger Verlagsbuchhandlung, Berlin

    Google Scholar 

  • Morrow PA, Whitham TG, Potts BM, Ladiges P, Ashton DH, Williams JB (1994) Gall-forming insects concentrate on hybrid phenotypes of Eucalyptus hosts. The ecology and evolution of gall-forming insects. USDA Forestry Services, Asheville, pp 121–134

    Google Scholar 

  • National Parks Association of the ACT (2007) Field guide to the native trees of the ACT. National Parks Association, Canberra

    Google Scholar 

  • Nelson LA, Scheffer SJ, Yeates DK (2011) Three new species of Fergusonina Malloch gall-flies (Diptera: Fergusoninidae) from terminal leaf bud galls on Eucalyptus (Myrtaceae) in south-eastern Australia. Zootaxa 3112:36–48

    Google Scholar 

  • Nelson LA et al (2014) An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on Myrtaceae host plants. Biol J Lin Soc 111:699–718. doi:10.1111/bij.12237

    Article  Google Scholar 

  • Padovan A, Keszei A, Kollner TG, Degenhardt J, Foley WJ (2010) The molecular basis of host plant selection in Melaleuca quinquenervia by a successful biological control agent. Phytochemistry 71:1237–1244. doi:10.1016/j.phytochem.2010.05.013

    Article  CAS  PubMed  Google Scholar 

  • Pryor LD (1959) Species Distribution and Association in Eucalyptus. In: Keast A, Crocker RL, Christian CS (eds) Biogeography and ecology in Australia. Dr W. Junk Publishers, The Hague, pp 461–471

    Chapter  Google Scholar 

  • Purcell MF, Rowell DM, Yeates DK (2015) Are the shoot bud galls of Fergusonina Malloch, 1924 (Diptera: Fergusoninidae) founded by multiple mothers? Austral Entomol 54:286–291. doi:10.1111/aen.12126

    Article  Google Scholar 

  • Purcell MF, Wallenius TC, Yeates DK, Rowell DM (2016) Larval dorsal shield morphology is highly correlated with gall type in the enigmatic gall-forming fly, Fergusonina Malloch (Diptera: Fergusoninidae). Aust J Zool 64:233–248. doi:10.1071/ZO16037

    Article  Google Scholar 

  • Regier JC (2007) Protocols, concepts, and reagents for preparing DNA sequencing templates. Version 9/19/07. www.umbi.umd.edu/users/jcrlab/PCR_primers.pdf. Centre for Biosystems Research, University of Maryland Biotechnology Institute www.umbi.umd.edu/users/jcrlab/PCR_primers.pdf. Accessed 23 September 2015

  • Ronquist F, Liljeblad J (2001) Evolution of the gall wasp-host plant association. Evolution 55:2503–2522

    CAS  PubMed  Google Scholar 

  • Ronquist F et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheffer SJ, Giblin-Davis RM, Taylor GS et al (2000) Molecular systematics of Fergusonina spp (Diptera: Fergusoninidae): host-specificity, host use evolution, and implications for biocontrol of Melaleuca quinquenervia in the Florida Everglades. International Congress of Entomology, Iguassu Falls

    Google Scholar 

  • Scheffer SJ et al (2004) Phylogenetic relationships, species limits, and host specificity of gall-forming Fergusonina flies (Diptera: Fergusoninidae) feeding on Melaleuca (Myrtaceae). Ann Entomol Soc Am 97:1216–1221

    Article  CAS  Google Scholar 

  • Scheffer SJ, Nelson LA, Davies KA, Lewis ML, Giblin-Davis RM, Taylor GS, Yeates DK (2013) Sex-limited association of Fergusobia nematodes with female Fergusonina flies in a unique Australasian mutualism (Nematoda: Neotylenchidae; Diptera: Fergusoninidae). Aust J Entomol 52:125–128

    Article  Google Scholar 

  • Shorthouse JD, Rohfritsch O (1992) Biology of insect-induced galls. Oxford University Press, New York

    Google Scholar 

  • Siddiqi M (1986) A review of the genus Ferbusobia Currie (Hexatylina) with descriptions of F. jambophila n. sp. and F. magna n. sp. In: Swarup E, Dasgupta D (eds) Plant parasitic nematodes of India, problems and progress. Indian Agricultural Institute, New Delhi, pp 264–278

    Google Scholar 

  • Siddiqi M (1994) Fergusobia brevicauda, sp.n. and F. philippinensis, sp.n. (Nematoda: Hexatylina) from Eucalyptus deglupta. In: Proceedings of the second Afro-Asian nematology symposium, Cairo, Egypt, 1994. Afro-Asian Society of Nematologists, Luton, pp 96–100

  • 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 

  • Slee AV, Brooker MIH, Duffy SM, West JG (2006) EUCLID: eucalypts of Australia, 3rd edn. CSIRO, Canberra

    Google Scholar 

  • Strong DR, Lawton JH, Southwood R (1984) Insects on plants: community patterns and mechanisms. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. Amer Math Soc: Lectures Math Life Sci 17:57-86

    Google Scholar 

  • Taylor GS (2004) Revision of Fergusonina Malloch gall flies (Diptera: Fergusoninidae) from Melaleuca (Myrtaceae). Invertebr Syst 18:251–290

    Article  CAS  Google Scholar 

  • Taylor GS, Davies KA (2008) New species of gall flies (Diptera: Fergusoninidae) and an associated nematode (Tylenchida: Neotylenchidae) from flower bud galls on Corymbia (Myrtaceae). Aust J Entomol 47:336–349

    Article  Google Scholar 

  • Taylor GS, Austin AD, Davies KA (1996) Biology of the Eucalypt gall-forming fly, Fergusonina flavicornis Malloch (Diptera: Fergusoninidae) and its associated hymenopterans in South Australia, with a description of a new species of Bracon (Hymenoptera: Braconidae). Trans Royal Soc South Aust 120:131–146

    Google Scholar 

  • Taylor GS, Head ER, Davies KA (2005) Gall flies (Diptera: Fergusoninidae) on Myrtaceae: a mutualistic association between flies and nematodes. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology and evolution of gall-inducing arthropods, vol 2. Science Publishers, New Hampshire, pp 634–671

    Google Scholar 

  • Taylor G, Davies K, Martin N, Crosby T (2007) First record of Fergusonina (Diptera: Fergusoninidae) and associated Fergusobia (Tylenchida: Neotylenchidae) forming galls on Metrosideros (Myrtaceae) from New Zealand. Syst Entomol 32:548–557

    Article  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Thornhill AH, Popple LW, Carter RJ, Ho SY, Crisp MD (2012) Are pollen fossils useful for calibrating relaxed molecular clock dating of phylogenies? A comparative study using Myrtaceae. Mol Phylogenet Evol 63:15–27. doi:10.1016/j.ympev.2011.12.003

    Article  PubMed  Google Scholar 

  • Thornhill AH, Ho SY, Kulheim C, Crisp MD (2015) Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny. Mol Phylogenet Evol 93:29–43. doi:10.1016/j.ympev.2015.07.007

    Article  PubMed  Google Scholar 

  • Tonnoir A (1937) Revision of the genus Fergusonina Mall. (Diptera, Agromyzidae). Proc Linn Soc N S W 62:126–146

    Google Scholar 

  • Wheeler GS (2005) Chemotype variation of the weed Melaleuca quinquenervia influences the biomass and fecundity of the biological control agent Oxyops vitiosa. Biol Control 36:121–128

    Article  Google Scholar 

  • Wheeler GS, Ordung KM (2005) Secondary metabolite variation affects the oviposition preference but has little effect on the performance of Boreioglycaspis melaleucae: a biological control agent of Melaleuca quinquenervia. Biol Control 35:115–123

    Article  CAS  Google Scholar 

  • Whiffin T (1981) Analysis of hybridization between Eucalyptus pauciflora Sieber ex Spreng. and E. radiata Sieber ex DC. (Myrtaceae). Bot J Linn Soc 83:237–250

    Article  Google Scholar 

  • Whiffin T, Bouchier A (1992) Chemical and morphological variation within a population of Eucalyptus radiata (Myrtaceae) exhibiting leaf volatile oil chemical forms. Aust Syst Bot 5:95–107. doi:10.1071/SB9920095

    Article  Google Scholar 

  • Wiegmann BM, Trautwein MD, Winkler IS et al (2011) Episodic radiations in the fly tree of life. Proc Natl Acad Sci USA 108:5690–5695. doi:10.1073/pnas.1012675108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams MAJ (1994) Plant galls: organisms, interactions, populations. Clarendon Press, Oxford

    Google Scholar 

  • Wright SA, Pratt PD, Center TD, Buckingham GR (2013) Physiological host range of two highly specialised mutualistic symbiotes: the fly Fergusonina turneri and its obligate nematode Fergusobia quinquenerviae, potential biocontrol agents of Melaleuca quinquenervia. Biocontrol Sci Technol 23:409–422

    Article  Google Scholar 

  • Ye W, Giblin-Davis RM, Davies KA et al (2007) Molecular phylogenetics and the evolution of host plant associations in the nematode genus Fergusobia (Tylenchida: Fergusobiinae). Mol Phylogenet Evol 45:123–141

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Max Beukers, Colin Handley, Sandra Schachat, Marco Wallenius and Mark Wong for their kind assistance with collecting galls. This research was facilitated by funding from the Schlinger Foundation endowment to the Australian National Insect Collection.

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Correspondence to Michaela F. Purcell.

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Purcell, M.F., Thornhill, A.H., Wallenius, T.C. et al. Plant host relationships of three lineages of the gall-inducing fly Fergusonina Malloch (Diptera: Fergusoninidae) on Eucalyptus L’Hérit.. Arthropod-Plant Interactions 12, 133–145 (2018). https://doi.org/10.1007/s11829-017-9561-1

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