Phylogeny of Bembidion and Related Ground Beetles (Coleoptera: Carabidae: Trechinae: Bembidiini: Bembidiina)
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Molecular Phylogenetics and Evolution 63 (2012) 533–576 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Phylogeny of Bembidion and related ground beetles (Coleoptera: Carabidae: Trechinae: Bembidiini: Bembidiina) David R. Maddison Department of Zoology, Oregon State University, Corvallis, OR 97331, USA article info abstract Article history: The phylogeny of the large genus Bembidion and related genera is inferred from four nuclear protein-cod- Received 22 July 2011 ing genes (CAD, wingless, arginine kinase, and topoisomerase I), ribosomal DNA (28S and 18S), and the Revised 11 January 2012 mitochondrial gene cytochrome oxidase I (COI). 230 of the more than 1200 species of Bembidion are sam- Accepted 16 January 2012 pled, as well as 26 species of five related genera, and 14 outgroups. Nuclear copies (numts) of COI were Available online 13 March 2012 found sparsely scattered through sampled species. The resulting phylogeny, based upon individual gene analyses and combined analyses using maximum likelihood and parsimony, is very well supported at Keywords: most nodes. Minute ground beetles Additional analyses explored the evidence, and corroborate the phylogeny. Seven analyses, each with DNA Molecular phylogeny one of the seven genes removed from the combined matrix, were also conducted, and yielded maximum Bembidion likelihood bootstrap trees sharing over 92% of their nodes with the original, well-resolved bootstrap trees Bembidiina based on the complete set of seven genes. All key nodes were present in all seven analyses missing a sin- Evolution gle gene, indicating that support for these nodes comes from at least two genes. In addition, the inferred Systematics maximum likelihood tree based on the combined matrix is well-behaved and self-predicting, in that sim- ulated evolution of sequences on the inferred tree under the inferred model of evolution yields a matrix from which all but one of the model tree’s clades are recovered with bootstrap value >50, suggesting that internal branches in the tree may be of a length to yield sequences sufficient to allow their inference. All likelihood analyses were conducted under both a proportion-invariable plus gamma site-to-site rate var- iation model, as well as a simpler gamma model. The choice of model did not have a major effect on inferred phylogenies or their bootstrap values. The inferred phylogeny shows that Bembidarenas is not closely related to Bembidiina, and Phrypeus is likely distant as well; the remaining genera of Bembidiina form a monophyletic group. Lionepha, formerly considered a subgenus of Bembidion, is shown to be outside of the clade of Asaphidion + Bembidion, and is separated as its own genus. B. (Phyla) obtusum is quite isolated within Bembidion, and there is some evi- dence that the remaining Bembidion form a clade. Within Bembidion, there are three large clades that are well-supported, the Bembidion, Odontium, and Ocydromus Series. The Bembidion Series contains Bembidion (s. str.), Notaphus, Furcacampa, Emphanes, Trepanedoris, Diplocampa, and related Holarctic species; all species from South America, Australia, New Zealand; and most species from southern Africa and Madagascar. All species in South America, except for members of Notaphus and Nothocys, form a clade, the Antiperyphanes Complex, which has indepen- dently radiated into body forms and niches occupied by multiple, independent Northern-Hemisphere forms. All species from New Zealand, including Zecillenus, and Australian species formerly placed in Ana- notaphus together form a clade. Bembidion (s. str.) and Cyclolopha are in a clade with the Old World, South- ern Hemisphere lineages Notaphocampa, Sloanephila, and Omotaphus. The large subgenus Notaphus appears to have originated in South America, with all Northern Hemisphere Notaphus arising from within a south-temperate grade. All major variation in frontal furrows on the head is contained within the Bembidion Series. The Odontium Series contains subgenera Hirmoplataphus and Hydriomicrus, which together are the sister clade of Odontium, Bracteon, Ochthedromus, Pseudoperyphus, and Microserrullula. The very large Ocydromus Series, dominant in the Holarctic region, includes the Ocydromus Complex, with many subgenera, including Hypsipezum and Leuchydrium; the phylogeny within this group is notably at odds with the current classification. Also included in the Ocydromus Series are Nepha and Bembidioneto- litzkya, as well as the Princidium Complex, in which the intertidal B. (Cillenus) laterale falls. Outside these three series are a number of smaller groups, including the Plataphus Complex (containing Blepharoplataphus, Plataphus, the latter including Plataphodes); the Hydrium Complex (Metallina, E-mail address: [email protected] 1055-7903/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ympev.2012.01.015 534 D.R. Maddison / Molecular Phylogenetics and Evolution 63 (2012) 533–576 Chlorodium, and Hydrium, which contains Eurytrachelus), whose sister group might be subgenus Andre- wesa; Trechonepha and Liocosmius, which might be sisters; and B. (Melomalus) planatum, which is not close to Plataphus. There is some evidence that these groups plus the Ocydromus and Odontium Series form a clade. A few enigmatic groups were harder to place. The sister group of the pair Philochthus plus Philochthem- phanes might be B. wickhami; Eupetedromus is well outside the three major series and not related to Nota- phus; the high-elevation Asian group Hoquedela is a very isolated lineage. Notaphiellus is removed from synonymy with Nothocys, and placed in synonymy with Notaphus; Pla- taphodes is synonymized with Plataphus,asPlataphus is paraphyletic otherwise; Eurytrachelus is synon- ymized with Hydrium. A new subgenus, Lindrochthus, is described to house the distinctive B. wickhami. The implications of the inferred phylogeny for some morphological characters used in Bembidiina sys- tematics are explored, and some of the most widely used (e.g., location of discal seta ed3 on the elytron, and shape of the shoulder) are shown to be notably homoplastic. For example, the location of elytral seta ed3 has undergone at least nine transitions between two states. Ó 2012 Elsevier Inc. All rights reserved. 1. Introduction and suggests that many Northern Hemisphere subgenera, or per- haps the entire subtribe of Bembidiina, have a Gondwanan origin. In the early 1970s, while exploring the garden of my backyard Although the biogeographic hypotheses have been moderately in Burlington, Ontario, Canada, I found a small beetle running on explicit, the phylogenetic hypotheses have been less so. This is the soil. It was about 3 mm long, shiny black with yellowish spots; perhaps not surprising given the extreme diversity of the group, I was fascinated by its elegant form, quick movements, and intri- and the complexity of patterns of variation of morphological cacy of its structure for something so small. The beetle was a characters. Bembidion quadrimaculatum Linnaeus, type species of the world- The boundaries of Bembidion are not well defined, in part as wide genus Bembidion Latreille, although it would take a few years there are no apparent synamorphies for its members. To the fol- before I was to learn its identity. When I did I was even more intri- lowers of Netolitzky (1942, 1943) and Lindroth (1963, 1980), gued by this genus: although nearly 0.1% of all known species on Bembidion consists of all members of the supertribe Trechitae that Earth is a Bembidion, and the genus is common in habitats often have a reduced apical palpomere, a brush sclerite in the endophal- visited by people, they are unknown to most humans. Among sys- lus of the male genitalia, male foretarsomeres with adhesive setae tematic entomologists, this large branch of the tree of life is also arranged in rows, and that also do not possess the apomorphies of mysterious, as it has no explicit phylogenetic hypothesis about other taxa such as subtribe Xystosomina or the genus Asaphidion. its broad structure. The character states defining Bembidion are either plesiomorphic Bembidion is one of the commonest and most diverse groups of within Trechitae (e.g., male adhesive setal characteristics), or de- small predators on shores of bodies of water in temperate regions rived states for groups broader than just Bembidion (palpomere of the world. This genus, with over 1200 described (Lorenz, 2005) size, brush sclerite). and many undescribed species, is most diverse in the Holarctic re- In addition to a lack of knowledge about their cladistic struc- gion, but there are also centers of diversity in temperate South ture, there have been two schools of thought about the most func- America (Argentina, Chile, and northward in the Andes) and New tional classification to use. In contrast to Netolitzky’s and Zealand. Adults range in size from 2 to 9 mm in length, with the Lindroth’s broad concept of Bembidion, Jeannel (1941) split the majority between 3 and 6 mm. French fauna of this group into 15 genera. That philosophy proved Most species live along banks of running (Fig. 1A) or standing difficult to apply to other faunas. A lack of clarity as to how the rest (Fig. 1B) waters, where they feed on arthropods, including adult in- of the world’s Bembidiina related to the fauna of France left sects emerging from the water (Hering, 1998; Hering and Plachter, numerous species outside of France unplaced (including many in 1997; Paetzold et al., 2005; personal observations). Numerous spe- North America), many other species placed into French ‘‘genera’’ cies, including Bembidion quadrimaculatum, live far from water, in based upon weak evidence (Toledano, 2002), or relegated by de- open fields (Fig. 1C). A few species occur along the edge of perma- fault into many separate genera (Basilewsky, 1972; Jeannel, nent snowfields (Fig. 1D); I have watched adults walk on the snow 1962). Without a well-understood phylogeny to reign in the chaos, at night, and feed on torpid insects trapped on the cold ice. many of these groups have since been moved back into Bembidion Species of Bembidion are diverse in form (Figs.