Larval dorsal shield morphology is highly correlated with gall type in the enigmatic gall-forming fly, Fergusonina Malloch (Diptera : Fergusoninidae)
Michaela F. Purcell A C , Thomas C. Wallenius A , David K. Yeates B and David M. Rowell A
+ Author Affiliations
- Author Affiliations
A Division of Evolution, Ecology and Genetics, Research School of Biology, Australian National University, Canberra, ACT 2601, Australia.
B Australian National Insect Collection, CSIRO National Research Collections Australia, Clunies Ross Street, Acton, ACT 2601, Australia.
C Corresponding author. Email: michaela.purcell@anu.edu.au
Australian Journal of Zoology 64(4) 233-248 https://doi.org/10.1071/ZO16037
Submitted: 24 May 2016 Accepted: 23 September 2016 Published: 27 October 2016
Abstract
The gall-forming fly family Fergusoninidae, in association with a mutualist nematode, induces galls on Myrtaceae. Traditionally, each fly species has been thought to be host-specific and targets a particular site on its host plant. One host species may be host to as many as four fly species, each with different oviposition sites, giving rise to a range of gall types. Third-instar fly larvae possess a distinctive sclerotised ‘dorsal shield’ of unknown function that varies morphologically across the genus. We use a phylogenetic approach to examine the relationship of the dorsal shield morphology to other elements of this complex system. A phylogeny of 41 species, estimated using Bayesian analysis of mtCOI sequences, indicated a strong correlation between dorsal shield morphology and the gall type associated with the larva. We discuss possible functions of the dorsal shield, and other factors that may have led to their phylogenetic distribution. In addition, we have identified cases where fly species have formed galls on more than one host species. In some instances it is possible that these associations are an opportunistic response to artificial tree plantings.
References
Brooker, I., and Kleinig, D. (2001). ‘Eucalypts: An Illustrated Guide to Identification.’ (Reed New Holland: Sydney).Brooker, M. I. H., and Nicolle, D. (2013). ‘Atlas of Leaf Venation and Oil Gland Patterns in the Eucalypts.’ (CSIRO Publishing: Melbourne.)
Chippendale, G. M., and Wolf, L. (1981). ‘The Natural Distribution of Eucalyptus in Australia.’ (Australian National Parks and Wildlife Service: Canberra.)
Currie, G. A. (1937). Galls on Eucalyptus trees. A new type of association between flies and nematodes. Proceedings of the Linnean Society of New South Wales 62, 147–174.
Davies, K. A., and Giblin-Davis, R. M. (2004). The biology and associations of Fergusobia (Nematoda) from the Melaleuca leucadendra-complex in eastern Australia. Invertebrate Systematics 18, 291–319.
| The biology and associations of Fergusobia (Nematoda) from the Melaleuca leucadendra-complex in eastern Australia.Crossref | GoogleScholarGoogle Scholar |
Davies, K. A., and Lloyd, J. (1996). Nematodes associated with Diptera in South Australia: a new species of Fergusobia Currie from a fergusoninid and a new record of Syrphonema Laumond and Lyon from a syrphid. Transactions of the Royal Society of South Australia 120, 13–20.
Davies, K. A., Makinson, J., and Purcell, M. F. (2001). Observations on the development and parasitoids of Fergusonina/Fergusobia galls on Melaleuca quinquenervia (Myrtaceae) in Australia. Transactions of the Royal Society of South Australia 125, 45–50.
Davies, K. A., Ye, W., Giblin-Davis, R. M., Taylor, G. S., Scheffer, S., and Thomas, W. K. (2010). The nematode genus Fergusobia (Nematoda: Neotylenchidae): molecular phylogeny, descriptions of clades and associated galls, host plants and Fergusonina fly larvae. Zootaxa 2633, 1–66.
Davies, K. A., Giblin-Davis, R. M., Ye, W., Taylor, G. S., and Thomas, W. K. (2012). Nematodes from galls on Myrtaceae. II. Fergusobia/Fergusonina from small axillary bud (‘stem’) and leaf (‘pea’) galls in Australia, with descriptions of two new species. Zootaxa 3415, 1–22.
| Nematodes from galls on Myrtaceae. II. Fergusobia/Fergusonina from small axillary bud (‘stem’) and leaf (‘pea’) galls in Australia, with descriptions of two new species.Crossref | GoogleScholarGoogle Scholar |
Davies, K. A., Giblin-Davis, R. M., Ye, W., Lisnawita, L, Taylor, G. S., and Thomas, W. K. (2013a). Nematodes from galls on Myrtaceae. V. Fergusobia from large multilocular shoot bud galls from Angophora and Eucalyptus in Australia, with descriptions of six new species. Zootaxa 3741, 101–140.
| Nematodes from galls on Myrtaceae. V. Fergusobia from large multilocular shoot bud galls from Angophora and Eucalyptus in Australia, with descriptions of six new species.Crossref | GoogleScholarGoogle Scholar | 25112978PubMed |
Davies, K. A., Giblin-Davis, R. M., Ye, W., Taylor, G. S., and Thomas, W. K. (2013b). Nematodes from galls on Myrtaceae. IV. Fergusobia from flat leaf galls on Eucalyptus and Corymbia, with descriptions of two new species. Zootaxa 3741, 151–171.
| Nematodes from galls on Myrtaceae. IV. Fergusobia from flat leaf galls on Eucalyptus and Corymbia, with descriptions of two new species.Crossref | GoogleScholarGoogle Scholar | 25112980PubMed |
Davies, K. A., Taylor, G. S., Nelson, L. A., Yeates, D., and Giblin-Davis, R. M. (2014a). Nematodes from galls on Myrtaceae. VI. Fergusobia from galls on Angophora in Australia, with description of F. colbrani n. sp. and key. Zootaxa 3856, 326–348.
| Nematodes from galls on Myrtaceae. VI. Fergusobia from galls on Angophora in Australia, with description of F. colbrani n. sp. and key.Crossref | GoogleScholarGoogle Scholar | 25284662PubMed |
Davies, K. A., Ye, W., Giblin-Davis, R. M., Taylor, G. S., Hodda, M., and Thomas, W. K. (2014b). Nematodes from galls on Myrtaceae. VII. Fergusobia from ‘leafy’ leaf bud galls in Australia, with re-description of Fergusobia tumifaciens (Currie 1937) Wachek 1955 and descriptions of Fergusobia planchonianae n. sp. and Fergusobia viminalisae n. sp. Zootaxa 3856, 529–554.
| Nematodes from galls on Myrtaceae. VII. Fergusobia from ‘leafy’ leaf bud galls in Australia, with re-description of Fergusobia tumifaciens (Currie 1937) Wachek 1955 and descriptions of Fergusobia planchonianae n. sp. and Fergusobia viminalisae n. sp.Crossref | GoogleScholarGoogle Scholar | 25284673PubMed |
Giblin-Davis, R. M., Makinson, J., Center, B. J., Davies, K. A., Purcell, M. F., Scheffer, S. J., Taylor, G. S., Gooslby, J, and Center, T. D. (2001). Fergusobia/Fergusonina-induced shoot bud gall development on Melaleuca quinquenervia. Journal of Nematology 33, 239–247.
| 1:STN:280:DC%2BD1M7ovFGhsw%3D%3D&md5=e6ed29d7a7fb2ba91900b96bde637909CAS | 19265887PubMed |
Giblin-Davis, R. M., Davies, K. A., Morris, K., and Thomas, W. K. (2003). Evolution of parasitism in insect-transmitted plant nematodes. Journal of Nematology 35, 133–141.
| 1:STN:280:DC%2BD1M7ovFKhsg%3D%3D&md5=c2d00e26e11045a45c72b761d21de519CAS | 19265987PubMed |
Giblin-Davis, R. M., Center, B. J., Davies, K. A., Purcell, M. F., Scheffer, S. J., Taylor, G. S., Gooslby, J, and Center, T. D. (2004). Histological comparisons of Fergusobia/Fergusonina-induced galls on different myrtaceous hosts. Journal of Nematology 36, 249–262.
| 1:STN:280:DC%2BD1M7os12mtA%3D%3D&md5=8900845a163a0605f04f6572905bfe8cCAS | 19262813PubMed |
Goolsby, J. A., Makinson, J., and Purcell, M. (2000). Seasonal phenology of the gall-making fly Fergusonina sp. (Diptera: Fergusoninidae) and its implications for biological control of Melaleuca quinquenervia. Australian Journal of Entomology 39, 336–343.
| Seasonal phenology of the gall-making fly Fergusonina sp. (Diptera: Fergusoninidae) and its implications for biological control of Melaleuca quinquenervia.Crossref | GoogleScholarGoogle Scholar |
Harris, K. M. (1982). First record of Fergusoninidae (Diptera, Schizophora) outside Australia – a new species of Fergusonina on Syzygium in India. Systematic Entomology 7, 211–216.
| First record of Fergusoninidae (Diptera, Schizophora) outside Australia – a new species of Fergusonina on Syzygium in India.Crossref | GoogleScholarGoogle Scholar |
Head, E. (2008). Ecology of the Fergusonina fly and Fergusobia nematode gall association in South Australia. M.Sc. Thesis, University of Adelaide.
Huelsenbeck, J. P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
| MRBAYES: Bayesian inference of phylogenetic trees.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvotV2isw%3D%3D&md5=573b3c35dde42776a97cee27686fecc4CAS | 11524383PubMed |
Lanfear, R., Calcott, B., Ho, S. Y. W., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1ehsbg%3D&md5=4e28f81e14ccbf37c60b04dcb713caf0CAS | 22319168PubMed |
Meier, R., Shiyang, K., Vaidya, G., and Ng, P. L. (2006). DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Systematic Biology 55, 715–728.
| DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success.Crossref | GoogleScholarGoogle Scholar | 17060194PubMed |
Milne, D. L. (1961). The function of the sternal spatula in gall midges. Proceedings of the Royal Entomological Society of London, Series A: General Entomology 36, 126–131.
National Parks Association of the ACT (2007). ‘Field Guide to the Native Trees of the ACT.’ (National Parks Association: Canberra.)
Nelson, L. A., Scheffer, S. J., and Yeates, D. K. (2011). Two new species of sympatric Fergusonina Malloch flies (Diptera: Fergusoninidae) from bud galls on high-elevation snow gums (Eucalyptus pauciflora Sieb. ex Spreng. complex) in the Australian Alps. Australian Journal of Entomology 50, 356–364.
| Two new species of sympatric Fergusonina Malloch flies (Diptera: Fergusoninidae) from bud galls on high-elevation snow gums (Eucalyptus pauciflora Sieb. ex Spreng. complex) in the Australian Alps.Crossref | GoogleScholarGoogle Scholar |
Nelson, L. A., Scheffer, S. J., and Yeates, D. K. (2012). Species diversity of Fergusonina Malloch gall flies (Diptera: Fergusoninidae) forming leaf bud galls on snow gum (Eucalyptus pauciflora Sieb. ex Spreng. complex), with a description of a new species from Tasmania. Insect Systematics & Evolution 43, 147–160.
| Species diversity of Fergusonina Malloch gall flies (Diptera: Fergusoninidae) forming leaf bud galls on snow gum (Eucalyptus pauciflora Sieb. ex Spreng. complex), with a description of a new species from Tasmania.Crossref | GoogleScholarGoogle Scholar |
Nelson, L. A., Davies, K. A., Scheffer, S. J., Taylor, G. S., Purcell, M. F., Giblin-Davis, R. M., Thornhill, A. H., and Yeates, D. K. (2014). An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on Myrtaceae host plants. Biological Journal of the Linnean Society 111, 699–718.
| An emerging example of tritrophic coevolution between flies (Diptera: Fergusoninidae) and nematodes (Nematoda: Neotylenchidae) on Myrtaceae host plants.Crossref | GoogleScholarGoogle Scholar |
Parra-O, C., Bayly, M., Udovicic, F., and Ladiges, P. (2006). ETS sequences support the monophyly of the eucalypt genus Corymbia (Myrtaceae). Taxon 55, 653–663.
| ETS sequences support the monophyly of the eucalypt genus Corymbia (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Purcell, M. F., Rowell, D. M., and Yeates, D. K. (2015). Are the shoot bud galls of Fergusonina Malloch, 1924 (Diptera: Fergusoninidae) founded by multiple mothers? Australian Entomologist 54, 286–291.
| Are the shoot bud galls of Fergusonina Malloch, 1924 (Diptera: Fergusoninidae) founded by multiple mothers?Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar | 22357727PubMed |
Scheffer, S. J., Giblin-Davis, R. M., Taylor, G. S., Davies, K. A., Purcell, M, Lewis, M. L., Goolsby, J, and Center, T. D. (2004). Phylogenetic relationships, species limits, and host specificity of gall-forming Fergusonina flies (Diptera: Fergusoninidae) feeding on Melaleuca (Myrtaceae). Annals of the Entomological Society of America 97, 1216–1221.
| Phylogenetic relationships, species limits, and host specificity of gall-forming Fergusonina flies (Diptera: Fergusoninidae) feeding on Melaleuca (Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFShsrjM&md5=67abc6dc2da391a3ac8c18483b1170d8CAS |
Scheffer, S. J., Nelson, L. A., Davies, K. A., Lewis, M. L., Giblin-Davis, R. M., Taylor, G. S., and Yeates, D. K. (2013). Sex-limited association of Fergusobia nematodes with female Fergusonina flies in a unique Australasian mutualism (Nematoda: Neotylenchidae; Diptera: Fergusoninidae). Australian Journal of Entomology 52, 125–128.
| Sex-limited association of Fergusobia nematodes with female Fergusonina flies in a unique Australasian mutualism (Nematoda: Neotylenchidae; Diptera: Fergusoninidae).Crossref | GoogleScholarGoogle Scholar |
Sen, P. (1939). On the function and development of the sternal spatula in the Cecidomyiidae or gall midges as exemplified by Rhabdophaga saliciperda Duf. Journal of Morphology 65, 1–15.
| On the function and development of the sternal spatula in the Cecidomyiidae or gall midges as exemplified by Rhabdophaga saliciperda Duf.Crossref | GoogleScholarGoogle Scholar |
Siddiqi, M. (1986). A review of the genus Fergusobia Currie (Hexatylina) with descriptions of F. jambophila n. sp. and F. magna n. sp. In ‘Plant Parasitic Nematodes of India, Problems and Progress’. (Eds E. Swarup and D. Dasgupta.) pp. 264–278. (Indian Agricultural Institute: New Delhi.)
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’. pp. 96–100. (Afro-Asian Society of Nematologists: Cairo, Egypt).
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
| Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=a3619286e790aa5d040e9047e9930facCAS |
Slee, A. V., Brooker, M. I. H., Duffy, S. M., and West, J. G. (2006). ‘EUCLID: Eucalypts of Australia.’ (CSIRO: Canberra.)
Tavaré, S. (1986). Some probabilistic and statistical problems in the analysis of DNA sequences. In ‘American Mathematical Society: Lectures on Mathematics in the Life Sciences’. (Ed. R. M. Miura.) pp. 57–86. (American Mathematical Society: Providence, RI.)
Taylor, G. S. (2004). Revision of Fergusonina Malloch gall flies (Diptera: Fergusoninidae) from Melaleuca (Myrtaceae). Invertebrate Systematics 18, 251–290.
| Revision of Fergusonina Malloch gall flies (Diptera: Fergusoninidae) from Melaleuca (Myrtaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1ahtbc%3D&md5=f7f0193b7c989dc6d40981ecb6af46e4CAS |
Taylor, G. S., and Davies, K. A. (2008). New species of gall flies (Diptera: Fergusoninidae) and an associated nematode (Tylenchida: Neotylenchidae) from flower bud galls on Corymbia (Myrtaceae). Australian Journal of Entomology 47, 336–349.
| New species of gall flies (Diptera: Fergusoninidae) and an associated nematode (Tylenchida: Neotylenchidae) from flower bud galls on Corymbia (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
Taylor, G. S., and Davies, K. A. (2010). The gall fly, Fergusonina lockharti Tonnoir (Diptera: Fergusoninidae) and description of its associated nematode, Fergusobia brittenae sp. nov. (Tylenchida: Neotylenchidae). Journal of Natural History 44, 927–957.
| The gall fly, Fergusonina lockharti Tonnoir (Diptera: Fergusoninidae) and description of its associated nematode, Fergusobia brittenae sp. nov. (Tylenchida: Neotylenchidae).Crossref | GoogleScholarGoogle Scholar |
Taylor, G. S., Austin, A. D., and Davies, K. A. (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). Transactions of the Royal Society of South Australia 120, 131–146.
Taylor, G. S., Head, E. R., and Davies, K. A. (2005). Gall flies (Diptera: Fergusoninidae) on Myrtaceae: a mutualistic association between flies and nematodes. In ‘Biology, Ecology and Evolution of Gall-Inducing Arthropods’. (Eds A. Raman, C. W. Schaefer and T. M. Withers.) pp. 634–671. (Science Publishers: New Hampshire.)
Taylor, G., Davies, K., Martin, N., and Crosby, T. (2007). First record of Fergusonina (Diptera: Fergusoninidae) and associated Fergusobia (Tylenchida: Neotylenchidae) forming galls on Metrosideros (Myrtaceae) from New Zealand. Systematic Entomology 32, 548–557.
| First record of Fergusonina (Diptera: Fergusoninidae) and associated Fergusobia (Tylenchida: Neotylenchidae) forming galls on Metrosideros (Myrtaceae) from New Zealand.Crossref | GoogleScholarGoogle Scholar |
Tonnoir, A. (1937). Revision of the genus Fergusonina Mall. (Diptera, Agromyzidae). Proceedings of the Linnean Society of New South Wales 62, 126–146.
Wiegmann, B. M., Trautwein, M. D., Winkler, I. S., Barr, N. B., Kim, J.-W., Lambkin, C, Bertone, M. A., Cassel, B. K., Bayless, K. M., Heimberg, A. M., Wheeler, B. M., Peterson, K. J., Pape, T, Sinclair, B. J., Skevington, J. H., Blagoderov, V, Caravas, J, Kutty, S. N., Schmidt-Ott, U, Kampmeier, G. E., Thompson, F. C., Grimaldi, D. A., Beckenbach, A. T., Courtney, G. W., Friedrich, M, Meier, R, and Yeates, D. K. (2011). Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences of the United States of America 108, 5690–5695.
| Episodic radiations in the fly tree of life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvVCiu7s%3D&md5=76bd7bcfd397f5541ed8e85234f7f2c2CAS | 21402926PubMed |
Ye, W., Giblin-Davis, R. M., Davies, K. A., Purcell, M. F., Scheffer, S. J., Taylor, G. S., Center, T. D., Morris, K, and Thomas, W. K. (2007). Molecular phylogenetics and the evolution of host plant associations in the nematode genus Fergusobia (Tylenchida: Fergusobiinae). Molecular Phylogenetics and Evolution 45, 123–141.
| Molecular phylogenetics and the evolution of host plant associations in the nematode genus Fergusobia (Tylenchida: Fergusobiinae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCmt7%2FO&md5=41162e18aaf135dcd09ee81bad5aa18dCAS | 17434761PubMed |
