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Phylogeny of Ladybirds (Coleoptera: Coccinellidae): Are the Subfamilies Monophyletic?

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Phylogeny of Ladybirds (Coleoptera: Coccinellidae): Are the Subfamilies Monophyletic? Molecular Phylogenetics and Evolution 54 (2010) 833–848 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny of ladybirds (Coleoptera: Coccinellidae): Are the subfamilies monophyletic? A. Magro a,b,1, E. Lecompte b,c,*,1, F. Magné b,c, J.-L. Hemptinne a,b, B. Crouau-Roy b,c a Université de Toulouse, ENFA, EDB (Laboratoire Evolution et Diversité Biologique), 2 route de Narbonne, F-31320 Castanet Tolosan, France b CNRS, EDB (Laboratoire Evolution et Diversité Biologique), F-31062 Toulouse, France c Université de Toulouse, UPS, EDB (Laboratoire Evolution et Diversité Biologique), 118 route de Narbonne, F-31062 Toulouse, France article info abstract Article history: The Coccinellidae (ladybirds) is a highly speciose family of the Coleoptera. Ladybirds are well known Received 20 April 2009 because of their use as biocontrol agents, and are the subject of many ecological studies. However, little Revised 15 October 2009 is known about phylogenetic relationships of the Coccinellidae, and a precise evolutionary framework is Accepted 16 October 2009 needed for the family. This paper provides the first phylogenetic reconstruction of the relationships Available online 10 November 2009 within the Coccinellidae based on analysis of five genes: the 18S and 28S rRNA nuclear genes and the mitochondrial 12S, 16S rRNA and cytochrome oxidase subunit I (COI) genes. The phylogenetic relation- Keywords: ships of 67 terminal taxa, representative of all the subfamilies of the Coccinellidae (61 species, 37 genera), Phylogeny and relevant outgroups, were reconstructed using multiple approaches, including Bayesian inference Coccinellidae Partitioned analyses with partitioning strategies. The recovered phylogenies are congruent and show that the Coccinellinae Evolution is monophyletic but the Coccidulinae, Epilachninae, Scymninae and Chilocorinae are paraphyletic. The Food preference tribe Chilocorini is identified as the sister-group of the Coccinellinae for the first time. Ó 2009 Elsevier Inc. All rights reserved. 1. Introduction 2007) and two myrmecophagous (Harris, 1921; Pope and Lawrence, 1990). The Coccinellidae, commonly called Ladybirds or Ladybugs, be- Ladybirds’ predatory habits make them well-known biocontrol long to the superfamily Cucujoidea and the Coleoptera suborder agents, mainly as a result of the success of the Australian ladybird Polyphaga (Kovárˇ, 1996; Hunt et al., 2007). This family comprises Rodolia cardinalis (Mulsant) in controlling citrus infestation by the about 360 genera and nearly 6000 species (Vandenberg, 2002). It cottony-cushion scale Icerya purchasi (Maskell), at the end of the displays several characteristics which make it an interesting mod- 19th century. Although there are many cases of successful control, el, from a biological as well as economical point of view. Found mainly involving coccidophagous ladybirds (Dixon and Kindlmann, worldwide, they are present in many diverse habitats and range 1998), some of the introduced species have become invasive and widely from stenotopic to eurytopic species (Honk and Hodek, are seen as a threat to native species. For example, Coccinella sep- 1996). Food relationships are also highly diverse in the group: tempunctata L. and Harmonia axyridis (Pallas), both introduced in ladybirds are mainly predators but there is also a group of phy- North America to control aphids, became extremely abundant tophagous species, including serious pests of economically impor- and conspicuous in their new range, which has raised concern over tant crops (Shaefer, 1983) and even some mycophagous species. their potential effects on local biological diversity (Horn, 1991; The predatory species mainly eat either coccids (Coccoidea) or Howarth, 1991; Simberloff and Stiling, 1996; Koch et al., 2003, aphids (Aphidoidea), but some are predators of aleyrods (Aleyro- 2005). A growing number of studies on life history strategies, doidea), psyllids (Psylloidea), chrysomelids (Chrysomeloidea) or chemical defense, reproductive behavior, species interactions and mites (Acari). The fact they mostly prey on Hemiptera often brings other aspects of the ecology of ladybirds suffer from a lack of an them into contact with ants, which exploit the same resources: evolutionary framework (e.g. Dixon, 2000). Such a framework will some species are myrmecophilous (review in Majerus et al., facilitate a more rigorous interpretation of ecological data and testing of hypotheses about Coccinellidae biology, including bioge- ography and the evolution of their morphology and food relation- * Corresponding author. Address: Université de Toulouse, UPS, UMR 5174, ships. Therefore, a robust and comprehensive phylogeny of Evolution et Diversité Biologique, 118 route de Narbonne Bat 4R3-b2, 31062 relationships within the family is needed. Toulouse cedex 9, France. Fax: +33 05 61 55 73 27. E-mail address: [email protected] (E. Lecompte). Historically, the comparative studies of Coleoptera morphology 1 These authors have equally contributed. placed the Coccinellidae among the Polyphaga (Cucujoidea) 1055-7903/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2009.10.022 834 A. Magro et al. / Molecular Phylogenetics and Evolution 54 (2010) 833–848 (Crowson, 1981). A recent large-scale molecular phylogeny con- the subfamilies of Coccinellidae; (2) assess phylogenetic relation- firms previous morphological studies: Coccinellidae were placed ships at the inter- and intra-subfamily level; (3) test the current among the Cucujiformia in the Cerylonid series (Hunt et al., higher classification of the family and (4) analyse patterns of evo- 2007). Moreover, together with a great number of morphological lution for food preference. traits, a molecular phylogeny of the Cerylonid series (Robertson et al., 2008) confirms the monophyly of the Coccinellidae and sug- 2. Materials and methods gests that the sister-group is a member of the current Endomychi- dae or Corylophidae. Thus, at present, the uncertainty is not about 2.1. Taxon sampling and laboratory procedures the position of the family among the Coleoptera but the phyloge- netic relationships within the family, for which molecular analyses We obtained samples of species belonging to all the subfamilies are lacking and classical morphological analyses are inconclusive. of Coccinellidae: Coccinellinae, Scymninae, Coccidulinae, Chiloc- Since Latreille (1807) first coined the family name ‘‘Coccinelli- horinae, Epilachninae, Ortaliinae and Sticholotidinae (present tax- dae” (Watt, 1975), the systematics of the whole group has been onomic position from Kovárˇ, 1996). A total of 37 genera and 61 unstable: authors have suggested new classifications, created or species of Coccinellidae were analyzed (Tables 1 and 2). It should redefined the subdivisions, transferred genera or tribes from one be noted however, that not all the tribes were included in the anal- subfamily to another (review in Sasaji, 1968; Chazeau et al., ysis (Supplementary Table 1). Other taxa of the infraorder Cucuji- 1989; Kovárˇ, 1996; Fürsch, 1990, 1996; S´lipin´ ski, 2007, this later formia (Chrysomelidae, Cucujidae, Endomychidae, Cerylonidae, only for Australian species) (see Supplementary Table 1). To date, Oedemeridae and Cleroidea), to which Coccinellidae belong, were few studies have attempted to reconstruct the phylogeny of the included as outgroups (Table 2). The choice of these latter taxa as whole group rather than make intuitive reconstructions (Sasaji, valid outgroups was based on the results of a recent phylogenetic 1968; Kovárˇ, 1996: Fig. 1) or preliminary morphological cladistic study of Coleoptera (Hunt et al., 2007). analyses (Guoyue, 1994). The intuitive trees differ in the number Sequences were obtained from two specimens per species with of recognized subfamilies (six or seven) and the tribal or generic the exception of Subcoccinella, for which only one individual was component of each subfamily, but agree about the relationships available. Most taxa are represented by sequences from a mini- between the subfamilies Chilocorinae and Scymninae, and Cocci- mum of three or four genes. Chimeric data (i.e. different sequences nellinae and Epilachninae. Guoyue (1994) suggests, based on mor- derived from more than one species of a genus) were used only for phological characters, the paraphyly of the Coccidulinae and the outgroup taxa and the Coccinellidae taxa that were only repre- Scymninae. sented by sequences from Genbank (Table 2). The taxonomy of A recent molecular phylogeny of the family Coccinellidae (20 coccinellids suggested by Kovárˇ (1996) was used, with three species), based on the 18S and 28S rDNA genes, indicated that exceptions: we recognize the Noviini as belonging to the Coccidu- the Scymninae and Chilocorinae are paraphyletic, although there linae, the Diomini as one of tribes of the Scymninae, and the genus is incongruence between analyses and low statistical support (Rob- Crypolaemus in the Scymnini (as Vandenberg, 2002). For the names ertson et al., 2008). Among the subfamilies, only the phytophagous of species we use those cited by Hodek and Honk (1996). Epilachninae have been subject to a molecular phylogenetic study The specimens were field-collected mostly in the western part (e.g. Ohta et al., 2004; Kobayashi et al., 1998). However, these anal- of the Paleartic region, either by the authors or numerous collabo- yses were done on beetles from a restricted geographical area and rators
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