Phylogeny of Carabid Beetles As Inferred from 18S Ribosomal DNA (Coleoptera: Carabidae)

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Phylogeny of Carabid Beetles As Inferred from 18S Ribosomal DNA (Coleoptera: Carabidae) R Systematic Entomology (1999) 24, 103±138 Phylogeny of carabid beetles as inferred from 18S ribosomal DNA (Coleoptera: Carabidae) DAVID R. MADDISON, MICHAEL D. BAKER and KAREN A. OBER Department of Entomology, University of Arizona, Tucson, Arizona, U.S.A. Abstract. The phylogeny of carabid tribes is examined with sequences of 18S ribosomal DNA from eighty-four carabids representing forty-seven tribes, and ®fteen outgroup taxa. Parsimony, distance and maximum likelihood methods are used to infer the phylogeny. Although many clades established with morphological evidence are present in all analyses, many of the basal relationships in carabids vary from analysis to analysis. These deeper relationships are also sensitive to variation in the sequence alignment under different alignment conditions. There is moderate evidence against the monophyly of Migadopini + Amarotypini, Scaritini + Clivinini, Bembidiini and Brachinini. Psydrini are not monophyletic, and consist of three distinct lineages (Psydrus, Laccocenus and a group of austral psydrines, from the Southern Hemisphere consisting of all the subtribes excluding Psydrina). The austral psydrines are related to Harpalinae plus Brachinini. The placements of many lineages, including Gehringia, Apotomus, Omophron, Psydrus and Cymbionotum, are unclear from these data. One unexpected placement, suggested with moderate support, is Loricera as the sister group to Amarotypus. Trechitae plus Patrobini form a monophyletic group. Brachinini probably form the sister group to Harpalinae, with the latter containing Pseudomorpha, Morion and Cnemalobus. The most surprising, well supported result is the placement of four lineages (Cicindelinae, Rhysodinae, Paussinae and Scaritini) as near relatives of Harpalinae + Brachinini. Because these four lineages all have divergent 18S rDNA, and thus have long basal branches, parametric bootstrapping was conducted to determine if their association and placement could be the result of long branch attraction. Simulations on model trees indicate that, although their observed association might be due to long branch attraction, there was no evidence that their placement near Harpalinae could be so explained. These simulations also suggest that 18S rDNA might not be suf®cient to infer basal carabid relationships. Introduction Although most non-harpaline tribes have relatively few species (more than half of the tribes have sixty or fewer species, Carabidae, with more than 30 000 described species Kryzhanovskiy, 1976), they represent the breadth of phyloge- (Reichardt, 1977), is one of the largest families of organisms, netic diversity within the family. Many of these tribes appear and includes almost all terrestrial members of the suborder to be remnants of early radiations in the Triassic and Jurassic Adephaga. Most of these beetles belong to the subfamily (Ponomarenko, 1992). The pattern of these early radiations is Harpalinae (sensu Erwin, 1985), a relatively recent radiation the focus of this paper, which examines relationships of (Cretaceous to Recent; Ponomarenko, 1992) which contains carabid tribes outside of Harpalinae. the most speciose carabid clades, especially in tropical regions. A suite of exoskeletal characters has traditionally been used to infer phylogenetic structure within carabids (Jeannel, 1941; Correspondence: David R. Maddison, Department of Entomology, Ball, 1979; Kavanaugh & Erwin, 1991). The most recent University of Arizona, Tuscon, AZ 85721, U.S.A. Fax: +1 520 621 common ancestor of carabids is thought to have had a 1150. E-mail: [email protected] mandible with a scrobal seta, procoxa open behind (not # 1999 Blackwell Science Ltd 103 L 104 David R. Maddison et al. Fig. 1. Relationships of carabid beetles based on morphological evidence, focusing on groups examined in the current study. The taxa on the right are particularly enigmatic; various proposed placements for these are shown. encircled by prothoracic sclerites); foretibia with two apical number of striking apomorphies (including an explosive spurs, and with a simple, sulcate antenna cleaner; mesocoxal chemical defense mechanism in adults and myrmecophilous cavity wall composed, in part, of the mesepimeron; hindcoxal habits with associated modi®cations of larval structure), they cavities conjunct; male parameres setose and symmetrical also possess features considered present in the groundplan of (Jeannel, 1941; Ball, 1979). Many of these features are present Carabidae. Evidence for the monophyly of remaining carabids in what are proposed to be `basal grade' carabids, i.e. carabids (`Anisochaeta') is limited, consisting of a tendency of a branching off early along the path from the most recent proximal shift of one spur of the protibial antenna cleaner common ancestor of Carabidae to Harpalinae. In contrast, (Jeannel, 1941; Hlavac, 1971), characteristics of the preoral Harpalinae exhibit the derived states of mandibular scrobe ®lter in larvae (Beutel, 1993) and female genitalia (Liebherr & asetose; procoxal cavities closed; foretibia with one spur Will, 1999). Within Anisochaeta, a number of taxa, including displaced proximally, antenna cleaner complex; mesepimeron the supertribes Nebriitae (Nebriini, Opisthiini, Notiophilini, removed from coxal cavity; hindcoxal cavities disjunct; male Notiokasiini) and Carabitae (Carabini, Pamborini, Cychrini), parameres asetose and markedly asymmetrical. form an old radiation of basal lineages of carabids having, for Some aspects of carabid phylogeny have been considered the most part, exoskeletal characteristics considered primitive reasonably well established based on morphological data within carabids. In contrast, conjunct mesocoxae characterize a (Fig. 1). Paussinae (including Metrius) are considered by some large group of carabids sometimes referred to as Carabidae authors to be the sister group of remaining carabids (Fig. 1; Conjunctae (Fig. 1). These include both `middle-grade' Beutel, 1993; Liebherr & Will, 1999). Although they possess a carabids, Stylifera of Jeannel (1941), and `higher' carabids or # 1999 Blackwell Science Ltd, Systematic Entomology, 24, 103±138 R Phylogeny of carabid beetles 105 Harpalinae. The supertribe Trechitae is the most speciose adephagans (Regenfuss, 1975; Deuve, 1988) or as relatives styliferan group, containing most of the smaller carabids of the scaritine or clivinine carabids (Bell, 1967; Baehr, 1979; (Bembidiini, Trechini, Pogonini, Zolini). The predominately Beutel, 1990); Gehringiini as a basal lineage of carabids Gondwanan Psydrini include many forms that are very similar (Lindroth, 1969; Beutel, 1992) or as a relative of psydrine and to members of the massive radiation of Harpalinae, but that trechite carabids (Bell, 1967; Erwin, 1985). lack a few apomorphies of the latter (including form of It is likely that morphological data will prove more parameres and lack of a scrobal seta). informative, once a synthesis of available data is made, and Some taxa do not ®t easily into this view of morphological once characters are examined from all major lineages, so that a evolution of carabids, with suggested placements varying complete matrix of taxa and characters is available. Three greatly from author to author (those taxa shown on the right of recent studies have presented matrices of data, with associated Fig. 1). Extensive morphological specialization in some of numerical analyses on multiple tribes within carabids. Beutel these lineages may have obscured evidence of relationships. & Haas (1996) tabulated states in eighty morphological Wrinkled bark beetles (Rhysodinae) live in wood, feeding on characters of adults and larvae for nineteen carabid tribes slime molds; their exoskeleton has become thick and and eighteen noncarabids. Their parsimony analysis resulted in corrugated and their mandibles highly modi®ed (Bell, 1970; a tree with relatively unresolved basal relationships within Bell, 1994). Tiger beetles (Cicindelinae) are specialized carabids, but with the few evident clades matching reasonably predators, with larvae adapted for life in tubes from which well traditional hypotheses. Kavanaugh (1996) examined 244 they ambush their prey. Other taxa may have their history characters of adult structure across eight carabid tribes and two hidden because of miniaturization. Gehringia olympica, the noncarabids, in an effort to examine the relationships of basal only member of the tribe Gehringiini, is a minute carabid grade taxa centred around Nebriitae. The only numerical which lives interstitially in coarse sand of montane creeks. analysis of most carabid tribes was conducted by Liebherr & Some groups (e.g. the bombardier beetles, Brachinini; Morion; Will (1999) on one character system, female genitalia. These Cnemalobus) have characteristics of Harpalinae, but other papers should serve as models for future work examining features that suggest relationships with particular tribes outside morphological data from many character systems across the of Harpalinae. entire family. But for the moment, the extensive data have not The large body of literature on carabid phylogeny has failed been gathered into a matrix and analysed. to reach a consensus about many aspects of tribal-level Only recently has molecular sequence data been used to relationships (see Ball, 1979; Erwin, 1979; Kavanaugh & infer aspects of beetle phylogeny. These studies have either Erwin, 1991; Bousquet & Larochelle, 1993). Detailed focused on levels much broader than Carabidae (Howland & examination of the antenna cleaner
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