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Pattern of Phylogenetic Relationships Among Members of the Tribe Melitaeini (Lepidoptera: Nymphalidae) Inferred from Mitochondrial DNA Sequences

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Pattern of Phylogenetic Relationships Among Members of the Tribe Melitaeini (Lepidoptera: Nymphalidae) Inferred from Mitochondrial DNA Sequences Cladistics 16, 347±363 (2000) doi:10.1006/clad.2000.0136, available online at http://www.idealibrary.com on Pattern of Phylogenetic Relationships among Members of the Tribe Melitaeini (Lepidoptera: Nymphalidae) Inferred from Mitochondrial DNA Sequences Niklas Wahlberg* and Marie Zimmermann² *Metapopulation Research Group, Department of Ecology and Systematics, Division of Population Biology, University of Helsinki, Helsinki, FIN-00014, Finland; and ²UPRES BiodiversiteÂ, Laboratoire de SysteÂmatique Evolutive, Universite de Provence, Centre Saint Charles, Marseille, France Accepted March 15, 2000; published online November 9, 2000 We report a cladistic analysis of 77 butterfly species of INTRODUCTION the tribe Melitaeini (Lepidoptera: Nymphalidae) based on mitochondrial DNA gene sequences. We sequenced ca. 536 bp from the 16S ribosomal DNA (rDNA) and a The systematics of Lepidoptera and especially but- 1422-bp sequence from the cytochrome oxidase I gene. ter¯ies has long been a controversial subject (Ehrlich, Alignments are critical to statements of homology, espe- 1958; Ehrlich and Murphy, 1981; Ackery, 1984, 1988; cially when aligning rDNA sequences. We aligned the Scoble, 1992; de Jong et al., 1996). The number of fami- 16S sequences using conventional methods and direct lies and the relationships of species groups within these optimization. We found that direct optimization of the families have continued to be a source of dispute sequences produced the best alignments and our pre- among butter¯y systematists, despite the wide interest ferred phylogenetic hypothesis. Our results suggest that in butter¯y ecology and evolution (see Vane-Wright many of the previously proposed genera are paraphyletic and Ackery, 1984; Dennis, 1992). The family Nymphali- and we conclude that there are four monophyletic groups dae has turned out to be especially dif®cult, with some of species in our cladogram: the Euphydryas group, the authors splitting it into as many as nine families. The Phyciodes group, the Chlosyne group, and the Melitaea phylogenetic structure of this speciose butter¯y family group. The following genera are found to be paraphyletic: is certainly not clear at the level of tribes and subfami- Castilia, Chlosyne, Didymaeformia, Eresia, Melitaea, and lies at the moment. Thessalia. In addition, recognition of the monophyletic DNA sequence data may clarify the phylogenetic genera Cinclidia, Mellicta, and Telenassa would render relationships of groups of species that are morphologi- other genera paraphyletic. Our phylogenetic hypothesis cally highly variable, as DNA sequences allow for re- indicates that the melitaeines originated in the Nearctic cording large numbers of characters in a relatively and have colonized the Neotropics three times and the short period of time (Caterino and Sperling, 1999). As Palaearctic twice. ᭧ 2000 The Willi Hennig Society more sequence data become available, problems associ- ated with different genes are becoming apparent (Si- mon et al., 1994). It is now appreciated that different 0748-3007/00 $35.00 347 Copyright ᭧ 2000 by The Willi Hennig Society All rights of reproduction in any form reserved 348 Wahlberg and Zimmermann genes are phylogenetically informative at different hi- The taxonomic rank of the melitaeines has changed erarchical levels. In the past few years, DNA sequence several times between tribe and subfamily (Higgins, data have been used successfully to elucidate the rela- 1941, 1981; Harvey, 1991; Karsholt and Razowski, tionships of many groups of insect species at the ge- 1996). In the most recent classi®cation of the Nymphali- neric level (Brower and Egan, 1997; Dietrich et al., 1997; dae this group represents a tribe within the subfamily Vogler and Welsh, 1997; Foley et al., 1998; Caterino and Nymphalinae, with a possible sister group relation to Sperling, 1999; Zimmermann et al., 2000). Results of the tribe Kallimini (which includes genera such as higher level phylogenies are still somewhat ambiguous Junonia and Hypolimnas) (Harvey, 1991). Here we fol- in the Lepidoptera, though the increasing number of low Harvey's (1991) classi®cation, referring to Higgins' available DNA sequences may change this in the near (1981) subfamily and tribes as tribe and subtribes, re- future. In this paper we describe a cladistic analysis of spectively (Fig. 1). the nymphalid tribe Melitaeini based on mitochondrial Higgins (1981) recognized three subtribes within the DNA (mtDNA) sequences. Melitaeini: Euphydryiti (including the Euphydryas Species belonging to the tribe Melitaeini have long group), Phycioditi (including the Phyciodes group), and been the subjects of ecological and evolutionary studies Melitaeiti (including the Chlosyne, Gnathotriche, and (Ehrlich et al., 1975; Thomas and Singer, 1998; Hanski, Melitaea groups). Higgins (1941, 1950, 1955, 1960, 1978, 1999). While the taxonomy of the group has been inten- 1981) grouped species into genera mainly on the basis sively investigated (Higgins, 1941, 1950, 1955, 1960, of characters in the male genitalia. In an investigation 1981; Scott, 1994, 1998), a cladistic analysis has not been attempted before. In part this is due to morphological characters forming continuous transformation series through many species (Higgins, 1941; Scott, 1994, 1998), making the coding of characters dif®cult. Melitaeini comprises about 250 species that have been placed into ®ve distinct generic groups, the Eu- phydryas, Phyciodes, Chlosyne, Gnathotriche, and Melitaea groups (Higgins, 1981). Melitaeines occur throughout the Palaearctic (Euphydryas and Melitaea groups), Nearctic (Euphydryas, Phyciodes and Chlosyne groups), and most of the Neotropics (Phyciodes, Chlosyne, and Gnathotriche groups). The tribe has been revised taxo- nomically by L. G. Higgins over a period of 40 years (Higgins, 1941, 1950, 1955, 1960, 1978, 1981). In his last paper on melitaeines, Higgins (1981) split the tribe (Higgins treated the group as a subfamily) into 31 gen- era. Many authors have rejected most of these genera (e.g., Scott, 1986; Karsholt and Razowski, 1996; Tolman, 1997), while others have used Higgins' taxonomy for want of a better system (e.g., DeVries, 1987). It has been shown that some genera in Higgins' classi®cation may be paraphyletic (Zimmermann et al., 2000). Also, Zimmermann et al. (1999) performed a phenetic analy- sis of allozyme and sequence data for European meli- taeines and found that species in the genus Melitaea FIG. 1. Traditional classi®cation of genera in Melitaeini after Hig- sensu stricto do not cluster together. From these studies gins (1981) drawn according to comments such as ªclosely related to,º ªdistant relationship,º ªclosely allied,º ªclose generic af®nity,º it is clear that the classi®cation of melitaeines as a in Higgins (1941, 1950, 1955, 1960, 1978, 1981). For higher taxa we whole needs to be based on more rigorous phyloge- follow Harvey (1991); i.e., subfamily ϭ tribe and tribe ϭ subtribe. netic hypotheses. Genera marked with an asterisk are included in this study. Copyright ᭧ 2000 by The Willi Hennig Society All rights of reproduction in any form reserved Phylogenetic Relationships of Melitaeini 349 on the classi®cation of the Euphydryas group Zimmer- There are ®ve additional genera that are not included mann et al. (2000) concluded that the 14 species should in the above four groups by Higgins (1981). Four gen- be placed into one genus (Euphydryas) instead of the era (with eight species) belong to the Gnathotriche four genera proposed by Higgins (1978). group, which occurs mainly in the Andes of South The Phyciodes group is the largest of the melitaeines, America. The remaining genus (Atlantea) is somewhat containing about 135 species that have been placed in of a mystery as its four species occur on the large 12 genera (Higgins, 1981). Species in Phyciodes s.s. are Caribbean islands, but the male genitalia are most simi- restricted to North America, while the species in the lar to those of Palaearctic melitaeines. Higgins (1981) remaining genera (Anthanassa, Eresia, Telenassa, Castilia, does not group this genus with any other species Tegosa, Ortilia, Dagon, Tisona, Phystis, Mazia, and Jana- groups, suggesting that perhaps it should be placed in tella) are Neotropical with a few species reaching the its own subtribe. Unfortunately we were unable to southern United States. The bulk of the species occur include these two groups in our study, due to dif®cul- in the Neotropics, primarily in northern South ties in obtaining samples. America. The North American species show a wing Here we present a cladistic analysis of the tribe Meli- pattern similar to that of other melitaeines, but this taeini (in part) based on mtDNA sequences from two pattern is lost in the Neotropical species. Several spe- genes: cytochrome oxidase subunit I (COI) and 16S cies are mimics of the Ithomiinae, Heliconiinae, and ribosomal DNA (rDNA) genes. COI sequences have Acreinae species that occur in the same area. been used successfully in previous generic level studies The Chlosyne group comprises about 30 species that (Caterino and Sperling, 1999), while the more con- have been placed into ®ve genera (Higgins, 1960, 1981). served 16S has been used mainly in higher level analy- About half of the species are distributed throughout ses (see Simon et al., 1994). We have also sequenced a North America, with the other half being mainly in portion of the ND1 gene for some species (Zimmer- Central America and a few species being found in mann et al., 2000), but this work
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