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Based Phylogenetic Reconstruction of Cholevinae (Coleoptera: Leiodidae): a New View on Higher-Level Relationships

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Based Phylogenetic Reconstruction of Cholevinae (Coleoptera: Leiodidae): a New View on Higher-Level Relationships Cladistics Cladistics 35 (2019) 1–41 10.1111/cla.12230 Morphology-based phylogenetic reconstruction of Cholevinae (Coleoptera: Leiodidae): a new view on higher-level relationships Caio Antunes-Carvalhoa,*, Ignacio Riberab, Rolf G. Beutelc and Pedro Gnaspinia aDepartamento de Zoologia, Instituto de Biociencias,^ Universidade de Sao~ Paulo, Rua do Matao,~ Travessa 14, 101, Sao~ Paulo, SP 05508-090, Brazil; bInstituto de Biologıa Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Maritim de la Barceloneta 37-49, Barcelona 08003, Spain; cEntomology Group, Institut fur€ Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, FSU Jena, Erbertstrasse 1, Jena 07743, Germany Accepted 10 October 2017 Abstract The current state of knowledge of the suprageneric relationships in Cholevinae is either derived from informal evaluations of putative synapomorphies or based on molecular studies with limited taxonomic sampling. Here we assessed the higher-level rela- tionships in this subfamily based on a phylogenetic analysis of 97 morphological characters scored for 93 terminals, representing all tribes. Both parsimony and Bayesian analyses were used. The monophyletic origin of Cholevinae was corroborated, except for the unexpected inclusion of Leptinus in the implied weighting analysis. Eucatopini + Oritocatopini were retrieved as basal branches in the evolution of Cholevinae. The monophyletic origin of all remaining Cholevinae was confirmed, which is consistent with molecu- lar evidence. Anemadini was non-monophyletic, in accordance with earlier hypotheses. Cholevini was rendered non-monophyletic by the uncertain inclusion of Prionochaeta and the consistent exclusion of Cholevinus. A close affinity of Ptomaphagini to Sciaphyini and Leptodirini was suggested, although the position of Sciaphyes remains uncertain. The phylogenetic hypothesis of Cholevinae provided here is the most comprehensive presently available. The list of characters shows that a substantial part of the data was obtained from the ventral side. This is a strong argument for a detailed pictorial documentation of the ventral body parts in taxo- nomic descriptions, in contrast to the common practice of only illustrating the dorsal habitus of the beetles. © The Willi Hennig Society 2017. With more than 4100 described species (Newton, termites and stingless bees (Jeannel, 1936; Peck and 2016) and a worldwide distribution, the staphyliniform Cook, 2002, 2007; Peck, 2003), while others may be family Leiodidae has the second highest species diver- found in nests or burrows of reptiles (e.g., tortoises; sity within the megadiverse Staphylinoidea. The eclec- Peck and Skelley, 2001), birds (e.g., owls, sparrows, tic repertoire of habitats and food sources potentially starlings, buzzards; Jeannel, 1936) and mammals (e.g., utilized by these beetles is impressive, and difficult to foxes, moles, shrews and various rodents; Jeannel, synthesize concisely. According to Newton (2016), 1936; Newton, 1998; Peck and Skelley, 2001). Addi- however, most leiodids might fit into one of three tionally, there are a few highly modified ectoparasitic broad categories: (i) ground-dwelling saprophages or species of aquatic or semi-aquatic mammals (Peck, general scavengers of forest leaf litter, deep soil or 1982). cave environments; (ii) saprophagous inhabitants of Leiodidae are presently subdivided into six subfami- carrion, dung and equivalent concentrated decaying lies. Cholevinae and Leiodinae—informally called organic matter; or (iii) obligate mycophages relying on small carrion beetles and round fungus beetles, respec- various groups of fungi. Some specialized species inha- tively—are by far the most species-rich, with represen- bit nests of social insects including ants, wasps, tatives in both tropical and temperate regions. Cholevinae, the most diverse, comprises ca. 2050 spe- *Corresponding author. cies arranged in seven tribes and 17 subtribes (Perreau, E-mail address: [email protected] 2000; Bouchard et al., 2011). The geographical limits © The Willi Hennig Society 2017 2 Caio Antunes-Carvalho et al. / Cladistics 35 (2019) 1–41 of these subgroups vary substantially: while the mono- scanning electron microscopy (SEM). Studied charac- generic Sciaphyini is only known from a few localities ter systems were the head, prosternum, meso- and in the East Palearctic region, Anemadini may be found metaventrite, elytra, legs including the pretarsus and in the Holarctic, Neotropical, Oriental, Australotropi- distal margin of the terminal tarsomere, and the abdo- cal, Australotemperate, Neoguinean, Neozelandic and men including the aedeagus (the last based mainly on Andean regions (Newton, 2016). The highly species- data obtained from published descriptions). Other rich Leptodirini is mainly restricted to the western internal characters were not assessed in this study, and Palaearctic, with its greatest diversity found in the data from the literature were not considered suffi- north Mediterranean basin (Perreau, 2004; Fresneda ciently well documented for a proper interpretation of et al., 2011). Although not very appealing from an aes- structures through all the studied taxa. The ingroup thetic perspective (except for the strongly modified included representatives of all currently recognized cave-adapted leptodirines), cholevine beetles arguably cholevine tribes and subtribes, with the exception of offer a broad array of attractive topics in evolutionary Baryodirina, a monotypic subtribe proposed on the biology, ecology and biogeography. basis of a single female of Baryodirus (Perreau, 2000). Intensive investigations have been devoted to the This genus, however, was included in the matrix and taxonomy of both Leiodidae and Cholevinae in the its characters were coded based on the SEM images of last decade. Among 674 leiodid species described since Baryodirus provided in the original description of the 2005, 255 were cholevines (see Newton, 2005, 2016). taxon (Perreau, 2000: figs 1–10). The limited informa- However, these taxonomic achievements were not par- tion content of the SEM micrographs concerning the alleled by phylogenetic studies. A robust cladistic characters utilized here, in addition to the lack of data investigation explicitly focused on Leiodidae or on males, resulted in a large number of missing entries Cholevinae has not been performed. Within this sce- (~ 46%). We therefore assessed the position of Baryo- nario of limited phylogenetic insights, the molecular dirus employing an additional, separate analysis. analyses of Fresneda et al. (2011) and McKenna et al. Twelve outgroup taxa were selected from four of the (2015) are of great importance, even though these five non-cholevine subfamilies of Leiodidae (represent- studies were not explicitly designed to investigate the ing ten out of 11 non-cholevinae tribes)—Camiarinae: internal relationships throughout Cholevinae or Leio- Agyrtodes labralis and Eupelates transversestrigosus didae. The study of McKenna et al. (2015) constitutes (Agyrtodini), Camiarus thoracicus (Camiarini) and a large-scale analysis aiming at the phylogeny of Sta- Neopelatops edwardsi (Neopelatopini); Catopocerinae: phyliniformia, and included only about a dozen of Catopocerus politus (Catopocerini); Leiodinae: Coleni- selected cholevine representatives. The molecular phy- sia zelandica (Pseudoliodini), Decuria sp. (Agathidiini), logeny of Fresneda et al. (2011) is the largest for Dietta huanuco (Estadiini), Hydnodiaetus sp. (Sogdini), Cholevinae and tentatively sheds some light on its Scotocryptus sp. (Scotocryptini) and Zeadolopus vali- internal relationships. However, as it was targeted at dipes (Leiodini); and Platypsyllinae: Leptinus testaceus. Leptodirini, some cholevine subgroups were not sam- Only Coloninae (with two genera) and the monotypic pled, especially from south temperate faunas. Glacicavicolini (Catopocerinae) are not represented. Whereas the monophyly of Cholevinae was not Several cladistic studies based both on molecular data recovered by Fresneda et al. (2011) and McKenna and on morphology have consistently placed Agyrtidae et al. (2015), this subfamily has been considered as a as the sister-taxon of Leiodidae (e.g., Beutel and natural unit by Newton (1998, 2016) based on an Molenda, 1997; Beutel and Leschen, 2005; Caterino informal evaluation of putative synapomorphies. et al., 2005; McKenna et al., 2015), corroborating the Therefore, the higher level classification of Cholevinae hypothesis of previous taxonomic studies (e.g., New- remains an important area of investigation. The aim ton, 1997, 1998). The agyrtid Zeanecrophilus prolonga- of the present study was to test the monophyly of tus was then used to root the tree. Most species used Cholevinae on the basis of phylogenetic analyses, and in the present study were obtained from museums or to propose a hypothesis for the higher-level relation- from private collections. The list of species we exam- ships in the subfamily, based on the broadest taxo- ined with their systematic assignment and authorities nomic sampling ever conducted. are provided in Table 1. Most terminal taxa represent single species. Only in three cases was the terminal taxon scored based on two different congeneric spe- Material and methods cies: Anthroherpon hoermanni + A. primitivum; Pri- onochaeta harmandi + P. opaca; and Platycholeus Morphological study and taxonomic sampling leptinoides + P. opacellus. It is assumed that these spe- cies are more closely related to one another than to Ninety-seven characters were
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