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Coleoptera: Dytiscidae) Cladistics Cladistics 24 (2008) 563–590 10.1111/j.1096-0031.2007.00192.x Phylogeny and diversification of diving beetles (Coleoptera: Dytiscidae) Ignacio Riberaa,*, Alfried P. Voglerb,c and Michael Balked aDepartamentode Biodiversidad y Biologı´a Evolutiva, Museo Nacional de Ciencias Naturales, Jose´ Gutie´rrez Abascal 2, Madrid 28006, Spain; bDepartment of Entomology, Natural History Museum, Cromwell Road, London SW7 5BD, UK; cDivision of Biology, Department of Life Sciences, Imperial College London, Silwood Park Campus, Ascot SL5 7PY, UK; dZoologische Staatssammlung, Muenchhausenstrasse 21, D-81247 Mu¨nchen, Germany Accepted 30 July 2007 Abstract Dytiscidae is the most diverse family of beetles in which both adults and larvae are aquatic, with examples of extreme morphological and ecological adaptations. Despite continuous attention from systematists and ecologists, existing phylogenetic hypotheses remain unsatisfactory because of limited taxon sampling or low node support. Here we provide a phylogenetic tree inferred from four gene fragments (cox1, rrnL, H3 and SSU, 4000 aligned base pairs), including 222 species in 116 of 174 known genera and 25 of 26 tribes. We aligned ribosomal genes prior to tree building with parsimony and Bayesian methods using three approaches: progressive pair-wise alignment with refinement, progressive alignment modeling the evolution of indels, and deletion of hypervariable sites. Results were generally congruent across alignment and tree inference methods. Basal relationships were not well defined, although we identified 28 well supported lineages corresponding to recognized tribes or groups of genera, among which the most prominent novel results were the polyphyly of Dytiscinae; the grouping of Pachydrini with Bidessini, Peschetius with Methlini and Coptotomus within Copelatinae; the monophyly of all Australian Hydroporini (Necterosoma group), and their relationship with the Graptodytes and Deronectes groups plus Hygrotini. We found support for a clade formed by Hydroporinae plus Laccophilini, and their sister relationship with Cybistrini and Copelatinae. The tree provided a framework for the analysis of species diversification in Dytiscidae. We found a positive correlation between the number of species in a lineage and the age of the crown group as estimated through a molecular clock approach, but the correlation with the stem age was non-significant. Imbalances between sister clades were significant for several nodes, but the residuals of the regression of species numbers with the crown age of the group identified only Bidessini and the Coptotomus + Agaporomorphus clade as lineages with, respectively, above and below expected levels of species diversity. Ó The Willi Hennig Society 2008. Approximately 25 families in three of four suborders They also occur in specialized habitats such as ground- of Coleoptera are typically aquatic in some of their life water aquifers, high altitude lakes and streams, or stages (Beutel and Leschen, 2005). Among these, the bromeliad water tanks in the forest canopy (Franciscolo, Dytiscidae (predaceous diving beetles), with some 4000 1979; Balke, 2005). Although most species are tightly described species (Nilsson, 2001, 2003a, 2004; Nilsson associated with their aquatic habitat throughout their and Fery, 2006) represent the perhaps most conspicuous life cycle except in the pupal stage, many species are group. Dytiscids range in size from about 1–50 mm, and strong flyers and able to disperse readily over land. are predators both as larvae and adults. They are found Diving beetles have been used as model organisms in in virtually any aquatic freshwater ecosystems, from a variety of ecological and evolutionary subjects, such as lakes, streams, springs, wet rock surfaces and puddles. coexistence and competition of closely related taxa (e.g., Juliano and Lawton, 1990a,b; Scheffer and Nes, 2006), *Corresponding author: the evolution of the stygobiontic fauna (Leys et al., E-mail address: [email protected] 2003, 2005), the role of habitat constraints in large-scale Ó The Willi Hennig Society 2008 564 I. Ribera et al./Cladistics 24 (2008) 563–590 macroecological patterns (Ribera et al., 2001, 2003b), or Hydroporinae (Wolfe, 1985, 1988). The position of the mechanics and functional morphology of swimming Laccornellus and Canthyporus within Hydroporini was behavior (Nachtigall, 1961; Ribera and Nilsson, 1995). also questioned (e.g., Roughley and Wolfe, 1987), as They are also among the best known groups of beetles, well as the composition of Bidessini and Hyphydrini being studied by an active research community, and (Bistro¨m, 1988; Bistro¨m et al., 1997). recent comprehensive revisions of many genera and an The most recent comprehensive taxonomic ordination up-to-date world catalog are available (Nilsson, 2001). of the family is that of Miller (2001a) (Table 1), based Despite this wide research interest, very few studies have on a phylogenetic analysis of morphological characters addressed phylogenetic relationships at the level of the and followed in the world catalog of Nilsson (2001). entire family using morphological (Burmeister, 1976; Main novelties were the recognition of Matinae and its Miller, 2001a) or molecular (Ribera et al., 2002b) placement as sister to the remaining Dytiscidae, the characters. These studies were limited in terms of taxon separation of Agabinae from Colymbetinae, and the sampling or the set of characters used (mostly female establishment of Hydrodytinae for some inconspicuous genitalia; small subunit rRNA, SSU), and support levels taxa previously considered within Copelatinae. The were generally low. taxon sampling and phylogenetic resolution within The most recent taxonomic revision of the whole Hydroporinae were generally limited, and no major family was that of Sharp (1882), separating two major changes were proposed. In a subsequent analysis groups according to the articulation between the meta- centered on Hydroporinae (Miller et al., 2006), and thoracic anepisternum and the mesocoxa: the ‘‘Dytisci- despite the better sampling, the phylogenetic relation- dae Fragmentati’’ (no contiguous articulation), ships were equally poorly supported. In the first family including what are now families Hygrobiidae and wide molecular phylogenetic study of Dytiscidae Noteridae plus Laccophilinae and Vatellini, and ‘‘Dyti- (Ribera et al., 2002b), based on 70 full SSU scidae Complicati’’ (contiguous articulation), including sequences, support was also generally low, although Amphizoidae and the rest of current Dytiscidae. Within some groups of genera within Hydroporinae were the latter, the major divisions separated the Hydropo- strongly supported (e.g., Hydroporus and Graptodytes rinae (excluding Vatellini) from the ‘‘Colymbetides’’ and groups, Hygrotini, Bidessini). what is the Dytiscinae in recent classifications. Here, we expand this molecular analysis of Dytiscidae In his monograph of the Palaearctic Dytiscidae, to include all major supra-generic groups and nearly Zimmermann (1930, 1933) already considered Hygro- 70% of the genera, based on four genes (4000–5000 biidae and Amphizoidae as separate families, and aligned nucleotides). Specific emphasis of taxonomic divided Dytiscidae in five subfamilies: Noterinae (now sampling was on the subfamily Hydroporinae, and in Noteridae), Laccophilinae, Hydroporinae, Colymbeti- particular Hydroporini, where the constitution and nae and Dytiscinae. The composition of these groups relationships of lineages remain particularly poorly has remained largely unchanged except for the large known. We aim to provide a phylogenetic framework Colymbetinae, which has experienced successive refine- for future evolutionary and systematic studies of Dytisc- ments by removing taxa with deviating morphologies idae, by identifying the major monophyletic lineages and no apparent close relatives. Thus, the Nearctic within the family and some of their phylogenetic Coptotomus was considered by Bo¨ving and Craighead relationships. The resulting tree was also used to study (1931) to form the subfamily Coptotominae, mostly relative diversification rates in different groups of because of the unusual larvae (with lateral gills on the Dytiscidae, as a first step of establishing the causes of abdomen). Burmeister (1976) recognized the non-mono- their high species richness relative to other aquatic phyly of the remaining ‘‘Colymbetines’’, associating lineages of beetles. Agabetes to Laccophilinae and placing the bulk of Copelatinae in an unresolved position within Dytisci- dae. Subsequent authors removed Lancetes (Ruhnau Materials and methods and Brancucci, 1984) and Hydrotrupes (Beutel, 1994) from the ‘‘Colymbetine’’ pool. Taxon sampling The phylogeny of the most diverse group of Dytisci- dae, the Hydroporinae, remains poorly understood The taxonomy here follows the most recent world (Miller et al., 2006; Michat and Alarie, in press). Several catalog of Dytiscidae (Nilsson, 2001), with the following major lineages have been recognized, with, for example, modifications: (1) Tribe Carabdytini (comprising Carab- Zimmermann (1930, 1933) considering six tribes: Vatel- dytes) was considered part of Colymbetini, as shown by lini, Methlini, Hyphydrini, Hydrovatini, Bidessini and Balke (2001), Balke et al. (2007), and confirmed here. (2) Hydroporini. The first cladistic analyses showed that Tribe Hydroporini was divided in several groups of Hydroporini as defined at the time was polyphyletic, as genera (named after the oldest valid genus name), based Laccornis
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