Register      Login
Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Two recently discovered species of Apiomorpha (Hemiptera: Eriococcidae) feeding on eudesmid eucalypts in Western Australia reaffirm host conservatism in this gall-inducing scale insect genus

Penelope J. Mills A B , Thomas L. Semple A , Kathleen L. S. Garland A and Lyn G. Cook A
+ Author Affiliations
- Author Affiliations

A The University of Queensland, School of Biological Sciences, Brisbane, Qld 4072, Australia.

B Corresponding author. Email: penelope.mills@uqconnect.edu.au

Invertebrate Systematics 30(3) 255-273 https://doi.org/10.1071/IS15039
Submitted: 25 August 2015  Accepted: 4 February 2016   Published: 29 June 2016

Abstract

Gall-inducing insects are relatively host-specific compared with their non-galling relatives. In Australia, there have been at least four origins of gall induction among eriococcid scale insects, with the most species-rich genus, Apiomorpha, inducing galls only on species of Eucalyptus. Here we describe two recently discovered species of Apiomorpha that induce galls on eudesmid eucalypts in Western Australia: Apiomorpha gongylocarpae, sp. nov., which is very similar morphologically to A. pomaphora, and A. jucundacrispi, sp. nov., the adult females of which induce an unusual gall covered in woody protrusions that, when older, have a knobbly appearance. Using molecular, morphological and host-association data, we show that these two species form a monophyletic group with the only other species of Apiomorpha that feed on eudesmid eucalypts (A. hilli and A. pomaphora). We place all four species of eudesmid-feeding Apiomorpha in the A. hilli species group, thus revising the current placement of A. pomaphora by removing it from the A. malleeacola species group. This study highlights additional faunal diversity endemic to Western Australia, with two of the four species being restricted to the globally recognised biodiversity hotspot of the South West Australia Floristic Region.

http://zoobank.org/urn:lsid:zoobank.org:pub:D6245EB6-903E-483C-B69B-3ED7EA35AD04.

Additional keywords: Eucalyptus, Eudesmia, plant galls, South West Australia Floristic Region.


References

Brooker, M. I. H. (2000). A new classification of the genus Eucalyptus L’Her. (Myrtaceae). Australian Journal of Botany 13, 79–148.

Cook, L. G. (2001). Extensive chromosomal variation associated with taxon divergence and host-specificity in the gall-inducing scale insect Apiomorpha munita (Schrader) (Hemiptera: Sternorrhyncha: Coccoidea: Eriococcidae). Biological Journal of the Linnean Society. Linnean Society of London 72, 265–278.

Cook, L. G. (2003). Apiomorpha gullanae sp. n., an unusual new species of gall-inducing scale insect (Hemiptera: Eriococcidae). Australian Journal of Entomology 42, 327–333.
Apiomorpha gullanae sp. n., an unusual new species of gall-inducing scale insect (Hemiptera: Eriococcidae).Crossref | GoogleScholarGoogle Scholar |

Cook, L. G., and Gullan, P. J. (2004). The gall-inducing habit has evolved multiple times among the eriococcid scale insects (Sternorrhyncha: Coccoidea: Eriococcidae). Biological Journal of the Linnean Society. Linnean Society of London 83, 441–452.
The gall-inducing habit has evolved multiple times among the eriococcid scale insects (Sternorrhyncha: Coccoidea: Eriococcidae).Crossref | GoogleScholarGoogle Scholar |

Cook, L. G., and Gullan, P. J. (2008). Insect, not plant, determines gall morphology in the Apiomorpha pharetrata species-group (Hemiptera: Coccoidea). Australian Journal of Entomology 47, 51–57.
Insect, not plant, determines gall morphology in the Apiomorpha pharetrata species-group (Hemiptera: Coccoidea).Crossref | GoogleScholarGoogle Scholar |

Cook, L. G., and Rowell, D. M. (2007). Genetic diversity, host-specificity and unusual phylogeography of a cryptic, host-associated species complex of gall-inducing scale insects. Ecological Entomology 32, 506–515.
Genetic diversity, host-specificity and unusual phylogeography of a cryptic, host-associated species complex of gall-inducing scale insects.Crossref | GoogleScholarGoogle Scholar |

Cook, L. G., Gullan, P. J., and Stewart, A. C. (2000). First-instar morphology and sexual dimorphism in the gall-inducing scale insect Apiomorpha Rübsaamen (Hemiptera: Coccoidae: Eriococcidae). Journal of Natural History 34, 879–894.
First-instar morphology and sexual dimorphism in the gall-inducing scale insect Apiomorpha Rübsaamen (Hemiptera: Coccoidae: Eriococcidae).Crossref | GoogleScholarGoogle Scholar |

Cook, L. G., Gullan, P. J., and Trueman, H. E. (2002). A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-subunit ribosomal DNA. Molecular Phylogenetics and Evolution 25, 43–52.
A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-subunit ribosomal DNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVeqsrY%3D&md5=3c965e04288c89aef2f4c4a8e5b40d65CAS | 12383749PubMed |

Doyle, J. J., and Doyle, J. L. (1990). Isolation of plant DNA from fresh tissue. Focus (San Francisco, Calif.) 12, 13–15.

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=3ed3b40952948838a8ebb6c4cd36ee0cCAS | 7881515PubMed |

Froggatt, W. W. (1921). A descriptive catalogue of the scale insects (‘Coccidae’) of Australia. Part II. Science Bulletin of the Department of Agriculture NSW 18, 1–159.

Gibbs, A. K., Udovicic, F., Drinnan, A., and Ladiges, P. Y. (2009). Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology. Australian Systematic Botany 22, 158–179.
Phylogeny and classification of Eucalyptus subgenus Eudesmia (Myrtaceae) based on nuclear ribosomal DNA, chloroplast DNA and morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvFygtrs%3D&md5=1c2e0076c938dae4009483e9c9decd52CAS |

Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.
A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 14530136PubMed |

Gullan, P. J. (1983). Spiracular structure of adult females of Apiomorpha Rübsaamen (Hemiptera: Coccoidea: Eriococcidae). Journal of the Australian Entomological Society 22, 25–29.
Spiracular structure of adult females of Apiomorpha Rübsaamen (Hemiptera: Coccoidea: Eriococcidae).Crossref | GoogleScholarGoogle Scholar |

Gullan, P. J. (1984). A revision of the gall-forming coccoid genus Apiomorpha Rübsaamen (Homoptera: Eriococcidae: Apiomorphinae). Australian Journal of Zoology Supplementary Series 97, 1–203.
A revision of the gall-forming coccoid genus Apiomorpha Rübsaamen (Homoptera: Eriococcidae: Apiomorphinae).Crossref | GoogleScholarGoogle Scholar |

Gullan, P. J., and Jones, M. G. (1989). A new species of gall-forming coccoid (Insecta: Homoptera: Eriococcidae) from Western Australia. Records of the Western Australian Museum 14, 321–329.

Gullan, P. J., Miller, D. R., and Cook, L. G. (2005). Gall-inducing scale insects (Hemiptera: Sternorrhyncha: Coccoidea). In ‘Biology, Ecology, and Evolution of Gall-Inducing Arthropods’. (Eds A. Raman, C. W. Schaefer, and T. M. Withers.) pp. 159–229. (Science Publishers: New Hampshire, UK.).

Hardy, N. B. (2007). Phylogenetic utility of dynamin and triose phosphate isomerase. Systematic Entomology 32, 396–403.
Phylogenetic utility of dynamin and triose phosphate isomerase.Crossref | GoogleScholarGoogle Scholar |

Hardy, N. B., and Cook, L. G. (2010). Gall-induction in insects: evolutionary dead-end or speciation driver? BMC Evolutionary Biology 10, 257.
Gall-induction in insects: evolutionary dead-end or speciation driver?Crossref | GoogleScholarGoogle Scholar | 20735853PubMed |

Hardy, N. B., Gullan, P. J., Henderson, R. C., and Cook, L. G. (2008). Relationships among felt scale insects (Hemiptera: Coccoidea: Eriococcidae) of southern beech, Nothofagus (Nothofagaceae), with the first descriptions of Australian species of the Nothofagus-feeding genus Madarococcus Hoy. Invertebrate Systematics 22, 365–405.
Relationships among felt scale insects (Hemiptera: Coccoidea: Eriococcidae) of southern beech, Nothofagus (Nothofagaceae), with the first descriptions of Australian species of the Nothofagus-feeding genus Madarococcus Hoy.Crossref | GoogleScholarGoogle Scholar |

Jermiin, L. S., Ho, S. Y. W., Ababneh, F., and Larkum, A. W. D. (2004). The biasing effect of compositional heterogeneity on phylogenetic estimates may be underestimated. Systematic Biology 53, 638–643.
The biasing effect of compositional heterogeneity on phylogenetic estimates may be underestimated.Crossref | GoogleScholarGoogle Scholar |

Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=367c17fe8bfe9a8b8cd9ac1c424a7903CAS | 23329690PubMed |

Lin, Y.-P., Gullan, P. J., and Cook, L. G. (2010). Species richness and host-plant diversity are positively correlated in Coccidae. Entomologia Hellenica 19, 90–98.

Lin, Y.-P., Kondo, T., Gullan, P. J., and Cook, L. G. (2013). Delimiting genera of scale insects: molecular and morphological evidence for synonymising Taiwansaissetia Tao, Wong and Chang with Coccus Linnaeus (Hemiptera: Coccoidea: Coccidae). Systematic Entomology 38, 249–264.
Delimiting genera of scale insects: molecular and morphological evidence for synonymising Taiwansaissetia Tao, Wong and Chang with Coccus Linnaeus (Hemiptera: Coccoidea: Coccidae).Crossref | GoogleScholarGoogle Scholar |

Lin, Y.-P., Cook, D. H., Gullan, P. J., and Cook, L. G. (2015). Does host-plant diversity explain species richness in insects? A test using Coccidae (Hemiptera). Ecological Entomology 40, 299–306.
Does host-plant diversity explain species richness in insects? A test using Coccidae (Hemiptera).Crossref | GoogleScholarGoogle Scholar |

Lockhart, P. J., Steel, M. A., Hendy, M. D., and Penny, D. (1994). Recovering evolutionary trees under a more realistic model of sequence evolution. Molecular Biology and Evolution 11, 605–612.
| 1:CAS:528:DyaK2cXlsFaks7c%3D&md5=ad6639624e1a1e0324cc7ed65038fb8cCAS | 19391266PubMed |

Mallet, J. (1995). A species definition for the modern synthesis. Trends in Ecology & Evolution 10, 294–299.
A species definition for the modern synthesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFaksA%3D%3D&md5=ba08566cfe410d486d37d857a31312b1CAS |

Mills, P. J., and Cook, L. G. (2014). Rapid chromosomal evolution in a morphologically cryptic radiation. Molecular Phylogenetics and Evolution 77, 126–135.
Rapid chromosomal evolution in a morphologically cryptic radiation.Crossref | GoogleScholarGoogle Scholar | 24680740PubMed |

Mills, P. J., Macdonald, M. L., Rigby, L. M., and Cook, L. G. (2011). A recently discovered species of Apiomorpha Rübsaamen (Hemiptera: Coccoidea: Eriococcidae) with unusual gall morphology. Zootaxa 3093, 55–63.

Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Biodiversity hotspots for conservation priorities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=2412a6d347cbab6820669438e95111a8CAS | 10706275PubMed |

Park, D.-S., Suh, S.-J., Oh, H.-W., and Hebert, P. D. (2010). Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers. BMC Genomics 11, 423.
Recovery of the mitochondrial COI barcode region in diverse Hexapoda through tRNA-based primers.Crossref | GoogleScholarGoogle Scholar | 20615258PubMed |

Penn, O., Privman, E., Ashkenazy, H., Landan, G., Graur, D., and Pupko, T. (2010). GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Research 38, W23–W28.
GUIDANCE: a web server for assessing alignment confidence scores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVSqtbs%3D&md5=74e276e2807915e393a28986935218a6CAS | 20497997PubMed |

Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.
jModelTest: Phylogenetic model averaging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXotlKgsb4%3D&md5=53928922981f8b5b3119f47393588dfaCAS | 18397919PubMed |

Rambaut, A. (2002). Se-Al Sequence Alignment Editor, v2.0a11. Supported by The Royal Society and Wellcome Trust (grant 50275). University of Oxford, Oxford.

Rogers, J., and Wall, R. (1980). A mechanism for RNA splicing. Proceedings of the National Academy of Sciences of the United States of America 77, 1877–1879.
A mechanism for RNA splicing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXktVagu7w%3D&md5=6b29b7f2596e5d2bc76a15be060dcb94CAS | 6246511PubMed |

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 |

Rübsaamen, E. H. (1894). Ueber australische Zoocecidien und deren Erzeuger. Berliner Entomologische Zeitschrift 39, 199–234.
Ueber australische Zoocecidien und deren Erzeuger.Crossref | GoogleScholarGoogle Scholar |

Song, H., Sheffield, N. C., Cameron, S. L., Miller, K. B., and Whiting, M. F. (2010). When phylogenetic assumptions are violated: base compositional heterogeneity and among-site rate variation in beetle mitochondrial phylogenomics. Systematic Entomology 35, 429–448.
When phylogenetic assumptions are violated: base compositional heterogeneity and among-site rate variation in beetle mitochondrial phylogenomics.Crossref | GoogleScholarGoogle Scholar |

Steane, D. A., Nicolle, D., McKinnon, G. E., Vaillancourt, R. E., and Potts, B. M. (2002). Higher-level relationships among the eucalypts are resolved by ITS-sequence data. Australian Systematic Botany 15, 49–62.
Higher-level relationships among the eucalypts are resolved by ITS-sequence data.Crossref | GoogleScholarGoogle Scholar |

Swofford, D. L. (2002). ‘PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10’. (Sinauer Associates: Sunderland, MA.)

Upton, M. S. (1993). Aqueous gum-chloral slide mounting media – an historical review. Bulletin of Entomological Research 83, 267–274.
Aqueous gum-chloral slide mounting media – an historical review.Crossref | GoogleScholarGoogle Scholar |

von Dohlen, C. D., and Moran, N. A. (1995). Molecular phylogeny of the Homoptera: a paraphyletic taxon. Journal of Molecular Evolution 41, 211–223.
Molecular phylogeny of the Homoptera: a paraphyletic taxon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntVSlt7g%3D&md5=b89d552ac351485756740ec2b7621c05CAS | 7666451PubMed |

Williams, D. J. (1985a). ‘Australian Mealybugs.’ (British Museum (Natural History): London.)

Williams, D. J. (1985b). The British and some other European Eriococcidae (Homoptera: Coccoidea). Bulletin of the British Museum (Natural History). Historical Series 51, 347–393.