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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Systematics of the Ogyris aenone (Waterhouse, 1902) complex (Lepidoptera: Lycaenidae): threatened Australian butterflies of national conservation significance

Ethan P. Beaver https://orcid.org/0000-0002-0613-7046 A B * , Michael F. Braby https://orcid.org/0000-0002-5438-587X A B and Alexander S. Mikheyev https://orcid.org/0000-0003-4369-1019 A
+ Author Affiliations
- Author Affiliations

A Division of Ecology and Evolution, Research School of Biology, RN Robertson Building, 46 Sullivans Creek Road, The Australian National University, Acton, ACT 2601, Australia.

B Australian National Insect Collection, GPO Box 1700, Canberra, ACT 2601, Australia.

* Correspondence to: ethan.beaver@anu.edu.au

Handling Editor: Andy Austin

Invertebrate Systematics 37(7) 457-497 https://doi.org/10.1071/IS23003
Submitted: 12 January 2023  Accepted: 26 May 2023   Published: 10 July 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

The butterfly genus Ogyris Angas, 1847 consists of several striking but poorly resolved complexes endemic to Australia and New Guinea, many of which have an obligate association with ants. Here, we revise the systematics of the Ogyris aenone (Waterhouse, 1902) complex through an integrative taxonomic approach based on molecular phylogenetic analysis, morphological examination, life histories and ecology. Mitochondrial sequence data based on concatenated cytochrome oxidase I (COI) and cytochrome b (cytb) (total of 1203 bp) for 36 ingroup samples were generated and combined with sequences available on NCBI GenBank for Ogyris. Phylogenetic analysis inferred by maximum likelihood methods resolved five taxa within this group, with one taxon, Ogyris caelestia Beaver & Braby sp. nov., described as a new species and another, O. doddi stat. rev., raised to full species. Phylogenetic relationships among the five taxa are as follows: (O. caelestia + O. aenone) + (O. ianthis + (O. iphis + O. doddi)). This revision brings the number of recognised Ogyris species to 16 and for the tribe Ogyrini to 18. This group of butterflies was found to be scarce – field samples of host trees that had the co-occurrence of both mistletoe and the appropriate attendant ant at 12 locations in eastern and northern Australia revealed low rates of occupancy (<50%, with an overall average of 17%) based on the presence of immature stages of the five butterfly species. The complete life histories, general biology and ecology of all members of this species-group are illustrated and diagnosed for the first time and confusing aspects of the literature are clarified. Several taxa are of conservation significance, including the new species, and future directions are discussed in relation to this.

ZooBank: urn:lsid:zoobank.org:pub:FC258ED6-AA1F-4E11-BFE1-D0A612E4F166

Keywords: conservation status, dolichoderine ants, Endangered, IUCN Red List Criteria, Loranthaceae, molecular phylogeny, taxonomy, threatened species, Vulnerable.


References

Angas GF (1847) ‘South Australia Illustrated’. (Thomas McLean: London, UK)

Atkins, AF (1975). Larval food plants of some Queensland butterflies. News Bulletin of the Entomological Society of Queensland 3, 117–119.

Atkins, AF (1984). Notes and records for some butterflies from eastern Australia. Victorian Entomologist 15, 9.

Atkins, AF (1993). Biological, behavioural, and distributional records of some butterflies from New South Wales. Victorian Entomologist 23, 54–56.

Avise, JC, and Wollenberg, K (1997). Phylogenetics and the origin of species. Proceedings of the National Academy of Sciences 94, 7748–7755.
Phylogenetics and the origin of species.Crossref | GoogleScholarGoogle Scholar |

Barrett C, Burns AN (1951) ‘Butterflies of Australia & New Guinea.’ (N.H. Seward: Melbourne, Vic., Australia)

Bethune-Baker, GT (1905). A monograph of the genus Ogyris. Transactions of the Entomological Society of London 1905, 269–292, pl XV.

Bowman, DMJS, Brown, GK, Braby, MF, et al. (2010). Biogeography of the Australian monsoon tropics. Journal of Biogeography 37, 201–216.
Biogeography of the Australian monsoon tropics.Crossref | GoogleScholarGoogle Scholar |

Braby, MF (1992). Conservation needs of lowland, coastal paperbark woodlands and eucalypt forests in northern Queensland – notes on some rare and threatened butterflies. News Bulletin of the Entomological Society of Queensland 20, 76–88.

Braby, MF (1997). New larval food plants for some butterflies (Lepidoptera) from northern and central Queensland, Australia. The Australian Entomologist 24, 97–108.
New larval food plants for some butterflies (Lepidoptera) from northern and central Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Braby MF (2000) ‘Butterflies of Australia. Their Identification, Biology and Distribution.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Braby, MF (2008). Biogeography of butterflies in the Australian monsoon tropics. Australian Journal of Zoology 56, 41–56.
Biogeography of butterflies in the Australian monsoon tropics.Crossref | GoogleScholarGoogle Scholar |

Braby, MF (2010). The merging of taxonomy and conservation biology: a synthesis of Australian butterfly systematics (Lepidoptera: Hesperioidea and Papilionoidea) for the 21st century. Zootaxa 2707, 1–76.
The merging of taxonomy and conservation biology: a synthesis of Australian butterfly systematics (Lepidoptera: Hesperioidea and Papilionoidea) for the 21st century.Crossref | GoogleScholarGoogle Scholar |

Braby, MF (2015). A butterfly found again. Wildlife Australia 52, 38–41.
A butterfly found again.Crossref | GoogleScholarGoogle Scholar |

Braby MF (2016 ) ‘The complete field guide to Butterflies of Australia’, 2nd edn. (CSIRO Publishing: Melbourne, Vic., Australia)

Braby, MF, and Dunn, KL (1991). Range extensions and distribution records for some butterflies from north-eastern Queensland. Victorian Entomologist 21, 62–66.

Braby, MF, and Müller, CJ (2022). Pseudogyris gen. nov. (Lepidoptera: Lycaenidae), a new genus for two rare thecline butterflies from New Guinea, including the description of a new species. Tropical Lepidoptera Research 32, 1–15.
Pseudogyris gen. nov. (Lepidoptera: Lycaenidae), a new genus for two rare thecline butterflies from New Guinea, including the description of a new species.Crossref | GoogleScholarGoogle Scholar |

Braby, MF, and Nielsen, J (2011). Review of the conservation status of the Atlas Moth, Attacus wardi Rothschild, 1910 (Lepidoptera: Saturniidae) from Australia. Journal of Insect Conservation 15, 603–608.

Braby MF, Woinarski JCZ (2007) Dodd’s Azure, Ogyris iphis doddi. In ‘Lost from our Landscape: Threatened Species of the Northern Territory’. (Eds JCZ Woinarski, C Pavey, R Kerrigan, I Cowie, S Ward) pp. 137–138. (Northern Territory Government: Darwin, NT, Australia)

Braby, MF, Atkins, AF, Dunn, KL, Woodger, TA, and Quick, WNB (1997). A provisional list of common names for Australian butterflies. Australian Journal of Entomology 36, 197–212.

Braby, MF, Eastwood, R, and Murray, N (2012). The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society 106, 699–716.
The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness?Crossref | GoogleScholarGoogle Scholar |

Braby MF, Franklin DC, Bisa DE, Williams MR, Williams AAE, Bishop CL, Coppen RAM (2018) ‘Atlas of Butterflies and Diurnal Moths in the Monsoon Tropics of Northern Australia.’ (ANU Press: Canberra, ACT, Australia)

Bryant, LM, and Krosch, MN (2016). Lines in the land: a review of evidence for eastern Australia’s major biogeographical barriers to closed forest taxa. Biological Journal of the Linnean Society 119, 238–264.
Lines in the land: a review of evidence for eastern Australia’s major biogeographical barriers to closed forest taxa.Crossref | GoogleScholarGoogle Scholar |

Common IFB (1964) ‘Australian Butterflies.’ (Jacaranda Press: Brisbane, Qld, Australia)

Common IFB, Waterhouse DF (1972) ‘Butterflies of Australia.’ (Angus & Robertson: Sydney, NSW, Australia)

Common IFB, Waterhouse DF (1981) ‘Butterflies of Australia’, revised edn. (Angus and Robertson: Sydney, NSW, Australia)

Cracraft J (1983) Species concepts and speciation analysis. In ‘Current Ornithology. Vol. 1’. (Ed. RF Johnston) pp. 159–187. (Springer: New York, NY, USA)

D’Abrera B (1971) ‘Butterflies of the Australian Region.’ (Lansdowne Press: Melbourne, Vic., Australia)

De Baar, M, and Franzen, D (2003). Additional information from the Franzen family collection. Butterfly & Other Invertebrates Club Newsletter 30, 15–16.

Dobzhansky T (1937) ‘Genetics and the Origin of Species.’ (Columbia University Press: New York, NY, USA)

Dodd WD (1935) Meanderings of a naturalist. No. 6. The North Queensland Register, 9 March 1935. Cairns, Qld, Australia.

Doubleday E, Westwood JO (1851) ‘The genera of diurnal Lepidoptera: comprising their generic characters, a notice of their habits and transformations, and a catalogue of the species of each genus’. Illustrated with eight-six plates by William C. Hewitson. (Longman, Brown, Green and Longmans: London, UK)

Dunn KL, Dunn LE (1991) Part 3. Family. In ‘Review of Australian Butterflies, distribution, life history, and taxonomy, Part 3: Family Lycaenidae’. pp. 366–431. (Power Press: Melbourne, Vic., Australia)

Eastwood, R, and Fraser, AM (1999). Associations between lycaenid butterflies and ants in Australia. Australian Journal of Ecology 24, 503–537.
Associations between lycaenid butterflies and ants in Australia.Crossref | GoogleScholarGoogle Scholar |

Edwards ED (1996) Lycaenidae. In ‘Checklist of the Lepidoptera of Australia. Monographs on Australian Lepidoptera. Vol. 4’. (Eds ES Nielsen, ED Edwards, TV Rangsi) pp. 249–254. (CSIRO Publishing: Melbourne, Vic., Australia)

Edwards ED, Newland J, Regan L (2001) ‘Zoological Catalogue of Australia. Vol. 31.6. Lepidoptera: Hesperioidea, Papilionoidea.’ (CSIRO Publishing: Melbourne, Vic., Australia)

Eldridge, MDB, Potter, S, and Cooper, SJB (2012). Biogeographic barriers in north-western Australia: an overview and standardisation of nomenclature. Australian Journal of Zoology 59, 270–272.
Biogeographic barriers in north-western Australia: an overview and standardisation of nomenclature.Crossref | GoogleScholarGoogle Scholar |

Eliot, JN (1973). The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement. Bulletin of the British Museum (Natural History) Entomology 28, 371–505.
The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement.Crossref | GoogleScholarGoogle Scholar |

Espeland, M, Breinholt, J, Willmott, KR, Warren, AD, Vila, R, Toussaint, EFA, et al. (2018). A comprehensive and dated phylogenomic analysis of butterflies. Current Biology 28, 770–778.e5.
A comprehensive and dated phylogenomic analysis of butterflies.Crossref | GoogleScholarGoogle Scholar |

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.

Geyle, HM, Braby, MF, Andren, M, Beaver, EP, Bell, P, Byrne, C, et al. (2021). Butterflies on the brink: identifying the Australian butterflies (Lepidoptera) most at risk of extinction. Austral Entomology 60, 98–110.
Butterflies on the brink: identifying the Australian butterflies (Lepidoptera) most at risk of extinction.Crossref | GoogleScholarGoogle Scholar |

Hagan, CE (1983). The occurrence of ‘Ogyris’ (Lepidoptera: Lycaenidae) in empty saturniid cocoons. Australian Entomological Magazine 9, 95–96.

Hebert, PDN, Cywinska, A, Ball, SL, and deWaard, JR (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London. Series B: Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar |

Hoang, DT, Chernomor, O, von Haeseler, A, Minh, BQ, and Vinh, LS (2018). UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518–522.
UFBoot2: improving the ultrafast bootstrap approximation.Crossref | GoogleScholarGoogle Scholar |

Hojo, MK, Pierce, NE, and Tsuji, K (2015). Lycaenid caterpillar secretions manipulate attendant ant behavior. Current Biology 25, 2260–2264.
Lycaenid caterpillar secretions manipulate attendant ant behavior.Crossref | GoogleScholarGoogle Scholar |

IUCN Standards and Petitions Subcommittee (2022) ‘Guidelines for using the IUCN Red List Categories and Criteria. Version 15.1.’ (Standards and Petitions Subcommittee of the IUCN Species Survival Commission: Gland, Switzerland)

Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, von Haeseler, A, and Jermiin, LS (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 |

Klots AB (1970) Lepidoptera. In ‘Taxonomist’s Glossary of Genitalia in Insects’, 2nd edn. (Ed. SL Tuxen) pp. 115–130. (Munksgaard: Copenhagen, Denmark)

Lane DA (1979) Life history notes and distribution records for some Queensland butterflies. Australian Entomological Magazine 5, 115-117.
| Crossref |

Lane, DA (1985). Notes on the biology and distribution of some Queensland butterflies. Australian Entomological Magazine 12, 77–80.

Le Souëf, JC (1975a). Notes on a visit to the Burra Range. News Bulletin of the Entomological Society of Queensland 3, 42–43.

Le Souëf, JC (1975b). Spring camp on Blackdown Plateau. Victorian Entomologist 5, 99–101.

Le Souëf, JC (1975c). A winter visit to inland Queensland. Victorian Entomologist 5, 145–149.

Lewis, J, and Sands, D (2021). Anonychomyrma inclinata sp. nov. (Hymenoptera: Formicidae): description, biology and interaction with the endangered bulloak jewel butterfly, Hypochrysops piceatus Kerr, Macqueen & Sands, 1969 (Lepidoptera: Lycaenidae). Austral Entomology 60, 461–472.
Anonychomyrma inclinata sp. nov. (Hymenoptera: Formicidae): description, biology and interaction with the endangered bulloak jewel butterfly, Hypochrysops piceatus Kerr, Macqueen & Sands, 1969 (Lepidoptera: Lycaenidae).Crossref | GoogleScholarGoogle Scholar |

Lundie-Jenkins G, Payne A (2000) ‘Recovery plan for the bull oak jewel butterfly (Hypochrysops piceatus) 1993–2003.’ (Queensland Parks and Wildlife Service: Brisbane, Qld, Australia)

Macqueen, J (1965). Notes on Australian Lycaenidae (Lepidoptera). Australian Journal of Entomology 4, 56–57.
Notes on Australian Lycaenidae (Lepidoptera).Crossref | GoogleScholarGoogle Scholar |

Mayo, RP, Atkins, AF, and White, B (1989). New records for butterflies (Lepidoptera) in eastern New South Wales. Australian Entomological Magazine 16, 109–110.
New records for butterflies (Lepidoptera) in eastern New South Wales.Crossref | GoogleScholarGoogle Scholar |

Mayr E (1942) ‘Systematics and the Origin of Species.’ (Columbia University Press: New York, NY, USA)

McCubbin C (1971) ‘Australian butterflies.’ (Nelson: Melbourne, Vic., Australia)

Meyer, CE, Weir, RP, and Wilson, DN (2006). Butterfly (Lepidoptera) records from the Darwin region, Northern Territory. The Australian Entomologist 33, 9–22.
Butterfly (Lepidoptera) records from the Darwin region, Northern Territory.Crossref | GoogleScholarGoogle Scholar |

Minh, BQ, Schmidt, HA, Chernomor, O, Schrempf, D, Woodhams, MD, von Haeseler, A, and Lanfear, R (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530–1534.
IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era.Crossref | GoogleScholarGoogle Scholar |

Monteith, GB, and Yeates, DK (1988). The Butterflies of Mount Moffatt and Carnarvon National Parks, Queensland. Queensland Naturalist 28, 14–22.

Moss, JT (2006). Note on Ogyris butterfly hostplants and amendments to the “hostplant book” information. Butterfly and Other Invertebrates Club Newsletter 41, 14–15.

Moss JT (2019) ‘Butterfly Host Plants of South-east Queensland and Northern New South Wales’, 4th edn. (Butterfly and Other Invertebrates Club Inc.: Runcorn, Brisbane, Qld, Australia)

Moss, JT, and Lithgow, G (1994). New butterfly records from the Chinchilla region, Queensland, with special reference to mistletoe butterflies and their larval host plants at Barakula State Forest. Queensland Naturalist 33, 10–16.

Müller, CJ (1998). New larval foodplant records for butterflies (Lepidoptera) in northern Queensland. The Australian Entomologist 25, 33–38.
New larval foodplant records for butterflies (Lepidoptera) in northern Queensland.Crossref | GoogleScholarGoogle Scholar |

Nelson GJ, Platnick N (1981) ‘Systematics and Biogeography: Cladistics and Vicariance.’ (Columbia University Press: New York, NY, USA)

Orr AG, Kitching RL (2010) ‘The Butterflies of Australia.’ (Allen and Unwin: Sydney, NSW, Autsralia)

Peters JV (1971) ‘A catalogue of the type specimens of the Hesperioidea and Papilionoidea (Lepidoptera) in the Australian Museum.’ (Australian Entomological Press: Sydney, NSW, Australia)

Pierce NE, Dankowicz E (2022) The natural history of caterpillar–ant associations. In ‘Caterpillars in the Middle. Fascinating Life Sciences’. (Eds RJ Marquis, S Koptur) pp. 319–391. (Springer: Cham, Switzerland)
| Crossref |

Pierce, NE, Kitching, RL, Buckley, RC, Taylor, MFJ, and Benbow, KF (1987). The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants. Behavioral Ecology and Sociobiology 21, 237–248.
The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants.Crossref | GoogleScholarGoogle Scholar |

Pierce, NE, Braby, MF, Heath, A, Lohman, DJ, Mathew, J, Rand, DB, and Travassos, MA (2002). The ecology and evolution of ant association in the Lycaenidae (Lepidoptera. Annual Review of Entomology 47, 733–771.
The ecology and evolution of ant association in the Lycaenidae (Lepidoptera.Crossref | GoogleScholarGoogle Scholar |

Sands DPA, New TR (2002) ‘The action plan for Australian butterflies.’ (Environment Australia: Canberra, ACT, Australia)

Sankowsky G (2020) ‘A Field Guide to Butterflies of Australia. Their Life Histories and Larval Host Plants.’ (Reed New Holland Publishers: Sydney, NSW, Australia)

Schmidt, DJ, Grund, R, Williams, MR, and Hughes, JM (2014). Australian parasitic Ogyris butterflies: east–west divergence of highly-specialized relicts. Biological Journal of the Linnaean Society 111, 473–484.
Australian parasitic Ogyris butterflies: east–west divergence of highly-specialized relicts.Crossref | GoogleScholarGoogle Scholar |

Shattuck, SO (1996). The Australian ant genus Froggattella Forel (Hymenoptera: Formicidae) revisited. Australian Journal of Entomology 35, 43–47.
The Australian ant genus Froggattella Forel (Hymenoptera: Formicidae) revisited.Crossref | GoogleScholarGoogle Scholar |

Simmons, RB, and Weller, SJ (2001). Utility and evolution of cytochrome b in insects. Molecular Phylogenetics and Evolution 20, 196–210.
Utility and evolution of cytochrome b in insects.Crossref | GoogleScholarGoogle Scholar |

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 |

Su, YN (2016). A simple and quick method of displaying liquid-preserved morphological structures for microphotography. Zootaxa 4208, 592–593.
A simple and quick method of displaying liquid-preserved morphological structures for microphotography.Crossref | GoogleScholarGoogle Scholar |

Taylor, GS, Braby, MF, Moir, ML, Harvey, MS, Sands, DPA, New, TR, Kitching, RL, McQuillan, PB, Hogendoorn, K, Glatz, RV, Andren, M, Cook, JM, Henry, SC, Valenzuela, I, and Weinstein, P (2018). Strategic national approach for improving the conservation management of insects and allied invertebrates in Australia. Austral Entomology 57, 124–149.
Strategic national approach for improving the conservation management of insects and allied invertebrates in Australia.Crossref | GoogleScholarGoogle Scholar |

Valentine, PS (1984). Sound production in lycaenid larvae and pupae. Victorian Entomologist 14, 22.

Valentine PS (1988) ‘Australian Tropical Butterflies.’ (Tropical Australilan Graphics: Townsville, Qld, Australia)

Volp, TM, and Lach, L (2019). An epiphytic ant-plant mutualism structures arboreal ant communities. Environmental Entomology 48, 1056–1062.
An epiphytic ant-plant mutualism structures arboreal ant communities.Crossref | GoogleScholarGoogle Scholar |

Ward, PS, Brady, SG, Fisher, BL, and Schultz, TR (2010). Phylogeny and biogeography of dolichoderine ants: effects of data partitioning and relict taxa on historical inference. Systematic Biology 59, 342–362.
Phylogeny and biogeography of dolichoderine ants: effects of data partitioning and relict taxa on historical inference.Crossref | GoogleScholarGoogle Scholar |

Waterhouse, GA (1902). Notes on Australian Rhopalocera: Lycaenidae. Part 1. Proceedings of the Linnean Society of New South Wales 27, 331–342.

Waterhouse, GA (1900). Descriptions of New Species of Australian Rhopalocera. Proceedings of the Linnean Society of New South Wales 25, 52–57.

Waterhouse, GA (1903). Notes on Australian Rhopalocera: Lycaenidae. Part III Revisional. Proceedings of the Linnean Society of New South Wales 28, 132–275.

Waterhouse GA (1932) ‘What Butterfly is That?’ (Angus and Robertson: Sydney, NSW, Australia)

Waterhouse, GA (1937). Presidential address: The biology and taxonomy of the Australian butterflies. Report of the Australian and New Zealand Association for the Advancement of Science, Auckland Meeting, January 1937 23, 101–133.

Waterhouse GA, Lyell G (1914) ‘The Butterflies of Australia. A Monograph of the Australian Rhopalocera.’ (Angus and Robertson: Sydney, NSW, Australia)