Morphological and Molecular Evidence Converge Upon a Robust Phylogeny of the Megadiverse Holometabola
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Cladistics Cladistics 27 (2011) 341–355 10.1111/j.1096-0031.2010.00338.x Morphological and molecular evidence converge upon a robust phylogeny of the megadiverse Holometabola Rolf G. Beutela,*, Frank Friedrichb, Thomas Ho¨ rnschemeyerc, Hans Pohla, Frank Hu¨ nefelda, Felix Beckmannd, Rudolf Meiere, Bernhard Misof f, Michael F. Whitingg and Lars Vilhelmsenh aEntomology Group, Institut fu¨r Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, FSU Jena, Erbertstrasse 1, 07743 Jena, Germany; bBiozentrum Grindel und Zoologisches Museum, Martin-Luther-King-Platz 3, Universita¨t Hamburg, 20146 Hamburg, Germany; cInstitut fu¨r Zoologie und Anthropologie der Universita¨t, Berlinerstr. 28, 37073 Go¨ttingen, Germany; dInstitute for Materials Research GKSS-Research Center, c ⁄ o GKSS at DESY, Notkestr. 85, 22607 Hamburg, Germany; eDepartment of Biological Sciences, National University of Singapore, 14 Science Dr 4, Block S2 #02-01, Singapore 117543; fZoologisches Forschungsmuseum Alexander Ko¨nig, Abteilung Molekulare Biodiversita¨tsforschung, Adenauerallee 160, 53113 Bonn, Germany; gDepartment of Biology, 693 Widtsoe Building, Brigham Young University, Provo, UT 84602, USA; hNatural History Museum of Denmark, University of Copenhagen, Universitetsparken 15, DK-2100, Denmark Accepted 26 June 2010 Abstract We present the largest morphological character set ever compiled for Holometabola. This was made possible through an optimized acquisition of data. Based on our analyses and recently published hypotheses based on molecular data, we discuss higher- level phylogeny and evolutionary changes. We comment on the information content of different character systems and discuss the role of morphology in the age of phylogenomics. Microcomputer tomography in combination with other techniques proved highly efficient for acquiring and documenting morphological data. Detailed anatomical information (356 characters) is now available for 30 representatives of all holometabolan orders. A combination of traditional and novel techniques complemented each other and rapidly provided reliable data. In addition, our approach facilitates documenting the anatomy of model organisms. Our results show little congruence with studies based on rRNA, but confirm most clades retrieved in a recent study based on nuclear genes: Holometabola excluding Hymenoptera, Coleopterida (= Strepsiptera + Coleoptera), Neuropterida excl. Neuroptera, and Mecoptera. Mecopterida (= Antliophora + Amphiesmenoptera) was retrieved only in Bayesian analyses. All orders except Megaloptera are monophyletic. Problems in the analyses are caused by taxa with numerous autapomorphies and ⁄or inapplicable character states due to the loss of major structures (such as wings). Different factors have contributed to the evolutionary success of various holometabolan lineages. It is likely that good flying performance, the ability to occupy different habitats as larvae and adults, parasitism, liquid feeding, and co-evolution with flowering plants have played important roles. We argue that even in the ‘‘age of phylogenomics’’, comparative morphology will still play a vital role. In addition, morphology is essential for reconstructing major evolutionary transformations at the phenotypic level, for testing evolutionary scenarios, and for placing fossil taxa. Ó The Willi Hennig Society 2010. Holometabola or Endopterygota are ‘‘the most suc- what is known today is doubtlessly only the tip of the cessful lineage of living organisms’’ according to Kris- iceberg. Erwin (1997) estimated 7.5 million extant tensen (1999a). They comprise ca. 780 000 described species for Coleoptera, based on investigations carried species (Grimaldi and Engel, 2005), which is equivalent out in the tropical forests of Central and South America, to more than 50% of the animal kingdom. Moreover, and a recent survey of dipteran diversity also provides evidence for a large number of undescribed species in most biogeographical regions (Pape et al., 2009). *Corresponding author: Holometabola also includes groups of almost unparal- E-mail address: [email protected] leled medical and economic importance (e.g. biting flies, Ó The Willi Hennig Society 2010 342 R.G. Beutel et al. / Cladistics 27 (2011) 341–355 bees, leaf beetles, weevils). The most conspicuous Giribet et al., 2005; Meier and Lim, 2009; see also characteristic of the group as a whole, and possibly Wheeler, 2008) in order to make further progress in one reason for its unrivalled evolutionary success, is the inter-ordinal-level insect phylogenetics. occurrence of complete metamorphosis, with a pupal A comprehensive morphological data matrix focused stage preceding the adult (Cameron et al., 2009). specifically on the phylogeny of Holometabola has not The monophyly of Holometabola has never been previously been compiled. Our primary aim in this study seriously questioned. However, as pointed out by is to provide an extensive and well documented mor- Kristensen (1999a,b), convincing morphological aut- phological character set for a carefully chosen sample apomorphies are scarce. The interrelationships of the across all holometabolan orders and several outgroup orders are also far from being settled. Widely accepted taxa. Further aims are to describe how the acquisition of phylogenetic hypotheses, originating with Hennig (1969) anatomical data can be optimized, to compare mor- and thoroughly re-evaluated by Kristensen (e.g. 1981, phology-based phylogenies with those based on molec- 1999a; see also Beutel and Pohl, 2006), were challenged ular data, to evaluate the phylogenetic information by the results of molecular studies using different content of different subsets of data, and to discuss analytical approaches and data sets (Wheeler et al., possible factors that may have contributed to the 2001; Whiting, 2002a,b; Kjer, 2004; Savard et al., 2006; extreme diversification in holometabolan lineages. Cameron et al., 2009; Wiegmann et al., 2009). Argu- The work was carried out in the framework of a ably, morphology-based reconstructions of holometa- project funded by the Deutsche Forschungsgemeinschaft bolan interrelationships have recently fallen behind (DFG; German Research Foundation). It was an molecular studies, especially as only limited new com- international cooperation with research groups in Ger- parative anatomical data had been acquired, and some many, Denmark and the USA. Notably, the cooperation morphological analyses were either not numerical with the Deutsches Elektronen-Synchrotron (DESY) was (Hennig, 1969; Kristensen, 1999a; Beutel and Pohl, crucial for assembling the morphological data within a 2006) or employed only moderately sized data sets time span of 30 months. The data presented here are coded across the entire Hexapoda (Beutel and Gorb, based mainly on the results of 20 original studies on 2001, 2006). In contrast, the past decade has seen a larval and adult morphology (see Appendix S3 in considerable number of studies presenting new molec- Supporting Information), two PhD theses, and a series ular data sets analysed with state-of-the-art methodol- of unpublished Diploma theses. A positive side-effect of ogy (see references above). the project was intensive training of a new generation of Beutel and Friedrich (2008b) pointed out that morphologists who employ innovative anatomical tech- detailed insect morphology flourished in the first two- niques. A combined effort and a strong synergy effect thirds of the 20th century, but has suffered a decline between the research groups finally resulted in the since then. This development was arguably linked with largest and arguably best documented morphological the rise of molecular systematics (e.g. Scotland et al., data set ever used in insect systematics. 2003). The novelty of molecular techniques, the opportunities of throwing new light on phylogenetic problems that had proved difficult to solve with Materials and methods morphological techniques (such as the ‘‘Strepsiptera problem’’; see Kristensen, 1999a), and the ability to Taxa examined generate large data sets across extensive taxon samples in a comparatively short time all contributed to the For a list of taxa examined, see Appendix S1. We appeal of molecular systematics. Some analyses yielded selected mainly so-called ‘‘basal’’ representatives of taxa peculiar results (such as non-monophyly of Coleoptera; as exemplars, that is, those that have a large number of Whiting et al., 1997), which may have contributed putative plesiomorphies splitting off close to the basal indirectly to the realization that morphological data node of each order (e.g. Nevrorthidae for Neuroptera, are still needed. However, the controversial hypotheses Xyelidae for Hymenoptera, Micropterigidae and Agathi- also provided a healthy shake-up and forced morphol- phagidae for Lepidoptera, Mengenillidae for Strepsi- ogists to re-evaluate time-honoured hypotheses and to ptera). We included the largest number of terminals for generate new morphological data. Furthermore, in Mecoptera, as the monophyly and intra-ordinal phy- recent years new technologies such as computer-based logeny of this group are controversial (see e.g. Whiting, 3D reconstruction, confocal laser scanning microscopy 2002b). The outgroup comprises representatives of (CLSM), and microcomputer tomography (l-CT) have Plecoptera (Pteronarcyidae, Pteronarcys californica become available to reinvigorate morphological sys- Newport, 1848); Orthoptera (Tettigoniidae, Tettigonia tematics. It is conceivable that this will lead to sp.);