molecular phylogeny of birdwing butterflies of the tribe

Biogeography 2. 103-111. Aug. 28, 2000

Molecular Phylogeny of Birdwing Butterflies of the Tribe Troidini (Lepidoptera: Papilionidae)

- Using All Species of the Genus Ornithoptera -

Sadaharu Morinakal , Nobuhiro Minaka2, Masayuki SekiguchP, Erniwati4, Siti Nuramaliati Prijono\ Ida Ketut GinarsaS, Tadashi Miyata6 and Toshitaka Hidaka7

I Aichi Study Center, The University of the Air, Yagotohonmachi, 10 1-2, Showa-ku, Nagoya 466-0825, Japan

2 National Institute of Agro-Environmental Sciences, Kannon-dai 3-1-1, Tsukuba, Ibaraki 305-8604, Japan

J National Institute of Neuroscience, Ogawahigasimachi 4-1-1, Kodaira-shi, Tokyo 187-8502, Japan 4 Biological Division, Research and Development for Biology, Indonesian Institute of Sciences,

Gedung Widyasatwaloka J1. Raya Cibinong, Cibinong Bogor, 16002 Indonesia 5 Pk. Jelati, Yeh Sumbul, Mendoyo Bali, 82261 Indonesia

h Department of Biological Mechanisms and Functions, Graduate School of Bioagricultural Sciences, Nagoya University, Huro-cho, Chikusa-ku, Nagoya 464-8601, Japan

7 The University of Shiga Prefecture, Hassaka 2500, Hikone, Shiga, 522-8533 Japan Corresponding address: S. Morinaka, Totsukahasami-cho 11-20, Kawaguchi-shi, Saitama-ken,

333-0805 Japan (e-mail: [email protected])

Abstract. The molecular phylogeny of birdwing butterflies based on the NOS gene of mitochondrial DNA (mtDNA) was studied by the maximum-likelihood method. maximum-parsimony method and neighbor-joining method. All species of the genus Omithoptera, some species of the genus Troides and other species representing most genera of the tribe Troidini were used. Results suggest the genus Omilhoptera forms a clade with Troides, supporting the previous results (Morin aka el al., 1999). In the case of the genus Omilhoptera, each of the subgenera Omithoptera and Schoenbergia was found to be monophyletic, however, phylogenetic relationships of O. alexandrae and O. vicloriae (the subgenus Aetheoptera) could not be clarified. In the subgenus Schoenbergia, two clades (0. paradisea + O. meridionalis, and O. goliath + O. chimaera + O. rothschildi) were found, however, the phylogenetic relationships of O. tithonus and other species remain unclarified, so as in the case of the genus Trogonoptera in the tribe Troidini.

Key words: Aetheoptera, birdwing butterflies, mitochondrial DNA, molecular phylogeny, NOS, Omithoptera, Ripponia, Schoenbergia, Trogolloptera, Troides, Troidini.

Introduction region), Central to South America and Indo-Australian regions. This tribe includes bird wing

The tribe Troidini includes about 10 genera, butterflies, which are important for mankind because which inhabit Madagascar Is. (the Afrotropical their fate, except some species adapting to the

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Molecular Phylogeny of Birdwing Butterflies of the Tribe Troidini

countryside, is linked to the existence of tropical rainforests. They are considered as a symbol exemplifying biodiversity.

Many taxonomic and/or phylogenetic studies on troidine butterflies have been published (Zeuner, 1943; Ford, 1944; Munroe & Ehrlich, 1960; Munroe, 1961; Hancock, 1983; Miller, 1987; Haugum & Low, 1978-1985; D' Abrera, 1975; Igarashi, 1979, 1984; Tsukada, 1980; Ohya, 1983; Tyler et al., 1994; Fujioka et al., 1997; Parsons, 1999: Morinaka et al ., 1999). Their classifications are partly different from each other. Morphological characters are useful for investigating phylogeny, whereas DNA sequences encode more discrete characters, determination of which would yield a high degree of accuracy (Brower, 1996; Su et al ., 1998; Caterino & Sperling, 1999; Yagi et ai., 1999, Maekawa et al., 1999). We have previously reported that the genera of Troidini excluding the genus Bartus are well united, forming one clade; Tl'Oides and Ornithoptera also form one clade (Morinaka et al., 1999). However, the phylogeny of Trogonoptera and the intrageneric one of Ornithoptera remain unclarified. In this study, phylogenetic analyses are carried out using Trogonoptera and all species of Ornithoptera.

Materials and Methods

Taxa used in the study Taxa used in this study are shown in Table I,

including their sampling localities and accession numbers in DDBJ/EMBLlGenBank. Species name of Troides, Ornithoptera and Tl'Ogonoptera are based on Aoki et al. (1998). O. aiotti and O. akakeae are

a: 20 mer ... 924 bp His UbP I

877 bp

treated as hybrids of O. victoriae X O. priamus, and O. rothschildi X O. priamus, respectively, and O. richmondia and O. euphorion as subspecies of O. priamus. Permission was obtained for species protected by the international contract, "Conservation on International Trade in Endangered Species of Wild Fauna and Flora" (C.I.T.E.S.) or other regulations when necessary.

Preparation of mtDNA, amplification and sequencing of ND5 gene

Details of DNA extraction, amplification and sequencing techniques for the ND5 gene of mtDNA, are described in Morinaka et ai. (1999). Nucleotide sequences of the primers are as follows: a, 5'-CCTGTTTCTGCTTTAGTTCA-3' (Su et al., 1996); and B3, 5'-TAACCTCTATATATYTCTCTT-3'.

Phylogenetic Analyses Two or more individuals from an intrataxon were

used for examination, except for some species which were difficult to obtain. In the analyses, 877 of the 924 nucleotide sequences were used (Fig. 1). Editing and aligning of the sequence data were completed utilizing DANASIS (Hitachi Software Engineering Co., Hitachi) and CLUSTAL W (Thompson et ai ., 1994). Phylogenetic trees were constructed by the maximum-likelihood (ML) method, maximum-parsimony (MP) method and neighbor-joining (NJ) method with the evolutionary distances by Kimura's two-parameter method using PAUP Version 4.0b4a (Swofford, 2000). The statistical confidence of each clade was examined with the bootstrap tests (Efron, 1982; Felsenstein,

83: 21 mer ....

Phe N05 Gene

Fig. I. Schematic representation of the amplified and coding regions of the NDS gene used in the study. a: 5'-CCTGTTTCTGCTTTAGTTCA-3'; B3: 5'-TAACCTCTATATATYTCTCTT-3'.

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S. Morinaka, N. Minaka, M. Sekiguchi, Erniwati, S. N. Prijono, l. K. Ginarsa, T. Miyata and T. Hidaka

Table I. Specimens used in the study (classified arbitrarily).

Genus (Subgenus) Species Locality DDBJI EMBU GenBank Accession Number

Parides hahneli Brasil AB027579 Par. elraces Upper HualJaga Y., Peru AB027580 Byasa alcinous Tokyo, Japan AB027583 B. polyeuctes Formosa AB044646 Atrophaneura luchti Jawa Is., Indonesia AB027584 A. nox Bali Is., Indonesia AB027586 Losaria coon Jawa Is., Indonesia AB027587 Pachliopta aristolochiae Bali Is., Indonesia AB027590 Troides (Ripponia) hypolitus Sulawesi Is., Indonesia AB027592 T. (Troides) amphrysus Jawa Is., Indonesia AB027593 T. (T. ) helena Bali Is., Indonesia AB027594 T. (T. ) haliphron Sulawesi Is ., Indonesia AB044649 T. (T. ) prattorum Buru Is., Indonesia AB044650 T. (T. ) staudingeri Lakor Is., Indonesia AB04465 I Ornithoptera (Ornithoptera) priamus Seram Is., Indonesia AB027596 O. (0. ) priamus Malaita Is., Solomon Isis AB027597 O. (0. ) priamus Timika, Irian Jaya AB044656 O. (0. ) priamus I Is., Solomon IsIs AB044657 O. (0. ) croesus Halmahera Is., Indonesia AB027595 O. (0. ) croesus Bacan Is., Indonesia AB044654 O. (0. ) aesacus Obi Is., Indonesia AB044655 O. ( Aetheoptera) alexandrae Papua New Guinea AB044652 O. (A. ) victoriae Malaita Is., Solomon Isis AB027598 O. (A.) victoriae Gela Is., Solomon Isis AB044658 O. ( Schoenbergia) paradisea Timika, Irian Jaya AB027603 O. (S. ) paradisea Arfak Mts, Irian Jaya AB044659 O. (S. ) meridionalis Timika, Irian Jaya AB044653 O. (S. ) goliath Seram Is., Indonesia AB027599 O. (S. ) goliath Arfak Mts, Irian Jaya AB027600 O. (S. ) rothschildi Arfak Mts, Irian Jaya AB027601 O. (S. ) chimaera Wayland Mts, Irian Jaya AB044660 O. (S. ) tithonus Arfak Mts, Irian Jaya AB027602 Trogonoptera brookiana Padang, Sumatera Is. AB044647 Trog. brookiana Cameron Highland, Malaysia AB044648 Papilio protenor Tokyo, Japan AB027604 Pieris (Pieridae, as outgroup) rapae Mie, Japan AB044594

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Ahhrcvialions: AI I : A.-fak MiS, lriun Jay" 8m.;: Bi1(.·tm Is Cam; Cameron Highland Gd : Gclu. Solol11on Isis GUll: GumJ<1lcanul. Solomon Isis Hal: Hnlmnhclu Is Mal: MaJaila, Solomon [sis SCI: S!.:ram Is Sum: SUIOi.llcra Tim : Tirnika, Ilian Juyu


P. ro"'poe r :;llIlding.:r; Iio/iphr. (I

v' T. prof/arum T f,elello r gmphl)'slIs

T hypolilus ,--------- O . o/sxol1drcre Aelileoptera

'---- 0 men 'ono/(s ,,,. 0.. golio/h i\rr Sclroe"hergia

0.. o llOSer 0. chimaera

r;;:--- 0 pad Tim J L ____ ":.-.:.._-:..--_-_-_-_-_- 0. lolhschildi Omifhopfero

O. filhonus L _"-.. pr/omu!> Tim J

' ()d. JflOmU5 Sar . POOIT/US Gu. 0 ill t o ptiomus M:t! rJI lOp era

o.. aesaCfiS IQoIJ O. croesus Bac 12 0. croe5u5 Hoi

o.. "it...! /i ,, 001 O. vic /a fiae M .1

B !X,I /,JeI 1'-4 B oHnous L _ __ .. ====- A luchli A. nox

L ____ '" Par. hahne/i 1---------4%

Poe ori5/%chioe 91 t coon

'-_______ -"-''',' Trag. bfLlOk/al1o :\"'" Trag brookiono Cam

prolenor -- 001 subslitutions/site

a r---------------------------------------------- P ropae

T, 510udinge ri f. ho/iphron T prof/arum

T he/ella '--------' T ompluysus T /lypo/iIV$

,--------- () 01 ondtne Aetheoplera

II 0 priomus Gua O. priomus Mal OrllltllOptera

O . oe50CUS O. croe5us Bac

Trogonoptero I

" O .... priamus Tim j 67 O.pnomus Ser

O. croesus Hal Omifhop/era

O . porodlr!)' T.m j '----- 0 me/idiono/is

.12 0., go/,a /lt Arl' Scl,oel/hergia 0 .. 9 Jlo Ser

I., 0. '--------- 0 /ilhonus

L-----------fiWll" 0.. IIICI(;>1 /oe Gel 0.. vlc/orloe Ml.1

[::---E====-EZ-::i. B. po/yeltc/es B. "'CIIlOU5

'" 1::. "-. ----- A. "d,n

flO Par e lr'i!.ces

r-or. hohne/i L ___ ori5l%chioe tn. L. coon

L.... _______ '""'''I T/Of) brookiono Sum Trog brookiono Cam

L.... _______ _______ Pap. pro/enar --- 10 changes

b-1

---------...I

Trogonoplera I

Fig. 2 Phylogenetic trees of birdwing butterflies based on 877 nucleotide sequences of the N05 gene (mtONA), constructed by the three methods using PAUP 4.0b4a. The bootstrap values of 50% or more besed on 1000 replicates are shown at each branching point. Abbreviations are shown in Fig. 2a. a: By ML method (Stepwise addition: as-is; Branch swapping: tree-bisection-reconnection); b(1-2): By MP method (General:

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S. Morinaka, N. Minaka, M. Sekiguchi, Erniwati, S. N. Prijono, I. K. Ginarsa, T. Miyata and T. Hidaka

r----------------------------------------------------- rJpoe T ./oudlll ali T hnl/{"Ihr q

'------- T p/o/torum T '------------- T amphrysu5

T l"!}"polfllJ5 ,---------------- U ·, o/exandtae

1IJ1J u . Gl,.la O. ptlamU5 M .lIl Or"itllOptera

D . oesocus ,-------l ..

"D._plio!'"lS j 67 a nncupvs 5tl

v 0 croesus Bac O. croesus Hal Omithoplera

r::,.-- 0 porod/seo Arf J "" D porodlseo Tim '-------- O . meridionoli5 .. O . goJiruh Arf Sc/wel/bergia

901/0 Sel' 0 , chlm era

., 0 ro/hscMdl '------------------ 0

6.' "

'------------------------l'W 0 viclorioe Gel o victoriae Mal ______ --'

B. polyeuc1es .. B. a lcrnous L ____ -{ ... A. Iltchli A. /lOX

"

L ___ elmc&1 ... Par I1nhnell L ____ orisl%chioe L coon

'-_____________ ..ll"'''''I. Trag. brookinno Sum

'--------------------------- Pap. prolenor Trog . brookiono Cam

---- 10 changes

b-2 r-------------------------------------------------------------------- P. rapae

1. staud,rgeri 1. l'lCl /iphron

F.:----- T. pralt . lum T he lena

T '----------- T hYRD"lus

,-------------------- 0 oIe)(o,.,d,oe ".::-, ---------0. poroelisea Al'f

I 0 pCllor/i .• eo Tim

'------ O . mer/clonol'5 '---------------------- O. lilllolwS

,"0 o goliolh Arf , O . go/ia Ser

O . Chlmtlyl,('Id '-'-'------- O . rothscnrl< I O. victorioe Gel

VI 0 vicloriae Mal £ O. pflO/IJu .• Tim 16 0 eriamu5 Ser

I II O . prfomvs Gua '----------1'00 0 priam Mal

0 , Oe50C(JS V'r 9\10 croesus Bac

(,) t. f' Hal .-------------------'"",'l'l II'P9 Grookiono Sum j Tr g. bro kiano Cam

POc:. orisloIor.;hfoe L. coon B. polyeIJdes OJ B. a/croous

A IlJchl/ '- A nox L ___ ., Par hahneli

'------------------------------------ Pap. prolenor --- 001 changes

c

Trogonopleral

Aetheoptera ,,_.J 'J Omithoptera

Trogonopleral

Minimum trees only; Starting trees: Obtained by stepwise addition; Stepwise addition: 200 random reps; Branch swapping: tree-bisection-reconnection). Two most parsimonious trees (tree length: 1186, CI:0.460) were obtained; c: By NJ method with the evolutionary distances by Kimura's two-parameter method.

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1985) based on 1000 replicates in the three methods using the same software above. The values of 50% or more are shown at each branching point. Phylogenetic trees constructed based on amino acid sequences encoded in the same region were supportively confirmed by MP and NJ (not shown). Pieris rapae (Lepidoptera: Pieridae) was used as an outgroup species for the analyses.

Results

Only very few differences in their pairwise nucleotide sequences were found in some individuals of the same troidine species for the same area. The number of differences in sequences among troidine species was I - 133/877 bp (0.1 - 15.2%). The G+C content of the sequenced region ranged from 16 to 20 %. Neither deletions nor insertions were found. This sequenced region was considered to be useful for this analysis.

A phylogenetic tree constructed by ML, two most parsimonious trees (tree length: 1186; CI: 0.460) by MP and a tree by NJ are shown in Fig. 2 with the bootstrap values of 50% or more. In these trees, the same phylogenetic relationships of some birdwing butterflies are found . T. staudingeri and T. haliphron, O. paradisea and O. meridionalis, and O. chimaera and O. rothschildi are shown to be sister species. O. goliath forms one clade with another clade of O. chimaera and O. rothschildi.

In Ornithoptera, each of the subgenera Schoenbergia and Ornithoptera forms one clade. T. hypolitus (the Subgenus Ripponia) forms one clade with another clade of all other species of Troides and Troides forms one group. Ornithoptera forms one clade with Troides based on their high bootstrap values in all trees. Other relationships, however, are inconsistent depending on the methods . The genus Ornithoptera forms one clade in MP and NJ, however, it was divided into two groups by ML. In particular, the relationship of O. victoriae (the subgenus Aetheoptera) is markedly inconsistent among trees, forming a clade with Troides and Ornithoptera (ML), with Ornithoptera (MP), and

with O. alexandrae and Schoenbergia (NJ) . Trogonoptera brookiana is not shown to form a clade with other birdwing butterflies in any trees.

Discussion

Previous studies suggest that birdwing butterflies underwent diversification over a long period (Zeuner, 1943; Corbet , 1944); therefore, results of phylogenetic analysis tend to be ambiguous. We attempted to analyze as many sequence data and genera of Troidini as possible. We analyzed 6 species of Troides and all species of Ornithoptera; however, Euryades, Cressida and Pharmacophagus were not included because of the lack of some nucleotide sequence data.

In Ornithoptera, relationships between species in the subgenus Ornithoptera, O. tithonus and two clades (0. paradisea + O. meridionalis, and O. goliath + O. chimaera + O. rothschildi) in Schoenbergia remain unclarified . In bird wing butterflies, the relationship of Trogonoptera with other genera was also unclear. These obscure results are considered to be caused by decreasing accuracy of nucleotide sequence information because of their rather long evolutionary period. In addition , it seemed that the lack of nucleotide sequence data for some genera rendered the results unclear.

However, some interesting results were obtained. Results suggest that each of the subgenera Ornithoptera and Schoenbergia is monophyletic. Two groups (0. paradisea + O. meridionalis, and O. goliath + O. chimaera + O. rothschildi) were found to be one group, although the confidence of the clades was not so high. Troides was found to be one group with high bootstrap values. Ornithoptera formed one group as determination by MP and NJ, however, the bootstrap value was considerably low (52% in MP). Moreover, taking into consideration the relationships of G. victoriae with other species as obtained by ML, more studies should be carried out in determining phylogenetic position of Ornithoptera.

Comparing our results with Parsons, phylogenetic trees of Ornithoptera (Parsons, 1996 [Fig. 17 A)), the

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S. Morinaka, N. Minaka, M. Sekiguchi, Erniwati, S. N. Prijono, 1. K. Ginarsa, T. Miyata and T. Hidaka

relationship between O. paradisea and O. meridionalis as well as that between O. chimaera and O. rothschildi are similarly shown to be sister species. These results are considered to be good examples of compatibility between molecular and morphological approaches. O. richmondia has been treated as another species distinct from O. priamus (Common & Waterhouse, 198). Parsons (1996) also concluded that O. richmondia is another species phylogenetically far from O. priamus as compared to O. croesus or O. aesac us . This idea is very interesting subject for our future studies of molecular phylogeny.

In conclusion, the present study confirmed the close relationship between Ornithoptera and Troides, as well as the subgenera Ornithoptera and Schoenbergia to be monophyletic, respectively, as reported by many previous investigators based on the morphology. The relationships of O. alexandrae and O. victoriae with other species, as in the case of Trogonoptera in Troidini, however, remain unclarified and therefore should be the subject of future studies.

Acknowledgments

We expres s our gratitude to Dr Sugihiko Hoshizaki, Dr Yukio Ishikawa and Dr Sadahiro Tatsuki (University of Tokyo) for their kind support and advice on molecular biology . We wish to acknowledge Dr Kenji Tanaka (Aichi Study Center, The University of the Air) for supporting our study. We express our thanks to Dr Soetikno Wirjoantmodio and Dr Mohamad Amir (Indonesian Institute of Science) for their kind support of our study since "International Butterfly Conference" in 1993, and Dr Hideo Mohri (National Institute for Basic Biology), Dr Tohru Nakazawa (The University of the Air), Dr Tomohiro Maeyama, Dr Kiyoto Maekawa, Dr Tadao Matsumoto (University of Tokyo), Mr Shigero Sugi (Tokyo), Mr Kazuhisa Otsuka (Tokyo University of Agriculture) and Dr Osamu Kitade (Ibaraki University) for support of our study. We express our thanks to Mr Kunio Matsuda (Tokyo Women's

Physical Culture Junior College), Mr Keiichi Matsumoto, Mr Jiro Arai and Mr Ichiro Kurosaki (Tokyo Metropolitan Takao Meseum of Natural History) for lending precious materials. We express our thanks to Mr Shinichi Oshima (Saitama), Mr Yasusuke Nishiyama (Tokyo), Mr Yasushi Sorimachi (Saitama), Mr Tetsuo Miyashita (Tokyo), Mr Kaoru Adachi (Tokyo), Mr Akihiko Takenaka (Hyogo) and Mr Hiromi Detani (Bali, Indonesia) for their great efforts to obtain permission and/or precious specimens for the study. We thank Dr Takashi Yagi (Osaka Prefecture University), Mr Katsuya Natsuhara (Nagoya University), Mr Noriaki Asou (Kanagawa), Mr Kazuaki Seta (Tokyo) and Mr Naokazu Nagahata (Saitama) for their kind help and also Mr Yoso Bumantoro (Irian Jaya, Indonesia) for obtaining permission from C.I.T.E.S and precious specimens. We are grateful for the grant-in-aid No. 99-B3-008 from "The Toyota Foundation".

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allies: Disdtribution and phylogeny in relation to (Accepted July 21,2000) the geological history of the Australian

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molecular phylogeny of birdwing butterflies of the tribe

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