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Phylogenetic Relationships and Chemical Evolution of the Genera Stenus and Dianous (Coleoptera: Staphylinidae)

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Phylogenetic Relationships and Chemical Evolution of the Genera Stenus and Dianous (Coleoptera: Staphylinidae) Chemoecology (2015) 25:11–24 DOI 10.1007/s00049-014-0171-4 CHEMOECOLOGY RESEARCH PAPER Phylogenetic relationships and chemical evolution of the genera Stenus and Dianous (Coleoptera: Staphylinidae) Carolin Lang • Lars Koerner • Oliver Betz • Volker Puthz • Konrad Dettner Received: 17 April 2014 / Accepted: 23 September 2014 / Published online: 8 October 2014 Ó Springer Basel 2014 Abstract The subfamily Steninae, composed of the species. Our investigations based on two algorithms such genera Dianous Leach 1819 and Stenus Latreille 1797, as Maximum Likelihood and Bayesian analyses support the belongs to the family of staphylinid beetles (Staphylini- chemotaxonomic approach. Furthermore, our results dae). Some unique features characterize Stenus beetles, clearly support former analyses concerning the evolution- e.g., a distinct prey-capture apparatus (not found in the ary origin of Dianous within Stenus, which suggests a genus Dianous) and special pygidial gland secretion con- secondary loss of the specialized prey-capture apparatus. stituents such as the alkaloids stenusine (1), norstenusine Finally, phylogenetic aspects based on the morphology of (2), 3-(2-methyl-1-butenyl)pyridine (3), cicindeloine (4)as Steninae are discussed. well as several terpenes like a-pinene (5), 1,8-cineole (6) and 6-methyl-5-heptene-2-one (7); (only 1, 2 and terpenes Keywords Steninae Á Chemotaxonomy Á found in Dianous). As the secretion composition of Stenus Molecular phylogeny Á COI Á 16S rRNA Á Histone H3 beetles is species specific, it can be used for a chemotax- onomic approach to investigate relationships within the Steninae. Based on the alkaloid gland content, Steninae can Introduction be grouped into three clusters: the piperidine-, the pyridine- and the epoxypiperideine group. To clarify the phyloge- The genera Stenus Latreille 1797 and Dianous Leach 1819 netic relationships within Stenus and between Stenus and (the only members of the subfamily Steninae) belong to the Dianous, and to evaluate our chemotaxonomic approach, large beetle family of Staphylinidae (rove beetles). The we analyzed a combined dataset of three gene sequences genus Stenus is one of the most species-rich genera within aligned of mitochondrial cytochrome c oxidase I (COI), the animal kingdom. To date, 2,612 species and eight fossil 16S rRNA and Histone H3 of 17 Stenus and 4 Dianous species are known worldwide (Puthz unpubl.). The genus Dianous covers more than 223 species (Puthz unpubl.) with a main distribution range in Asia (India, China and Handling Editor: Michael Heethoff. Southeast Asia). Generally, all staphylinid beetles including Stenus and C. Lang (&) Á K. Dettner Department of Animal Ecology II, University of Bayreuth, Dianous are characterized by a slender habitus and short Universita¨tsstr. 30, 95440 Bayreuth, Germany elytra. Because of the freely movable and, therefore, more e-mail: [email protected] vulnerable abdomen, most staphylinid beetles employ a highly evolved defensive gland system (Dettner 1991, L. Koerner Á O. Betz Department of Evolutionary Biology of Invertebrates, Institute 1993). Wide ranges of chemical gland constituents are used for Evolution and Ecology, University of Tu¨bingen, Auf der for defense (Dettner 1987). The representatives of the Morgenstelle 28E, 72076 Tu¨bingen, Germany Steninae are also equipped with a multifunctional pygidial gland secretion that acts as a defense against predators V. Puthz Burgmuseum Schlitz, Naturwissenschaftliche Abteilung, (Dettner 1987). Other functions of the secretion are Vorderburg 1, 36110 Schlitz, Germany avoidance of colonization by microorganisms when 123 12 C. Lang et al. Fig. 1 Pygidial gland secretion compounds of Stenus relevant for this study (Schildknecht 1970; Schildknecht et al. 1975; Kohler 1979; Neumann 1993; Lusebrink et al. 2009;Mu¨ller et al. 2012;): stenusine (1), norstenusine (2), 3-(2-methyl-1- butenyl)pyridine (3), cicindeloine (4), a-pinene (5), 1,8-cineole (6) and 6-methyl-5- heptene-2-one (7) secretion is applied on the body surface (‘‘secretion The genus Dianous, previously regarded as a sister grooming’’, Kovac¸ and Maschwitz 1990; Betz 1999; genus to Stenus, is currently grouped into species groups I Lusebrink 2007; Lusebrink et al. 2008b) and an extraor- and II based on the morphology of the frons (Puthz 1981, dinary movement on the water surface called ‘‘skimming’’ 2000, 2005; Shi and Zhou 2011; Tang et al. 2011). Mem- (Piffard 1901; Billard and Bruyant 1905; Jenkins 1960; bers of Dianous group I are characterized by large eyes Schildknecht et al. 1975). The multifunctional pygidial similar to those of Stenus (Puthz 1981). Therefore, these gland secretion of the Steninae consists of various piperi- beetles were traditionally placed in the genus Stenus, until dine and pyridine-derived alkaloids as well as several it was recognized that they do not possess their typical terpenes (Fig. 1; Schildknecht 1970; Schildknecht et al. prey-capture apparatus (Puthz 1981). 1975; Kohler 1979; Lusebrink et al. 2009;Mu¨ller et al. However, not only morphological characters were used 2012). to clarify complicated phylogenetic relationships within In the past, the genus Stenus was grouped into subgenera this huge subfamily of the Steninae. As already mentioned, based on various morphological features by staphylinid the pygidial secretion of the Steninae is composed of specialists (Rey, Casey, Motschulsky in Hermann 2001; several constituents (Figs. 1, 2). The secretion composition Lusebrink 2007; Puthz 2008). Originally, the genus was is species specific (Lusebrink 2007; Schierling et al. 2013) grouped into six subgenera, Stenus, Nestus, Tesnus, He- and can be used for a chemotaxonomic approach based on mistenus, Hypostenus and Parastenus (see also the the distribution of gland compounds (Fig. 2; Schierling determination key of Lohse 1964, which uses a today et al. 2013). The pygidial gland system of Steninae consists outdated subgenus-concept) mainly based on morphologi- of a pair of small and large reservoirs with the corre- cal features. These characteristics, for example, are the sponding gland tissues (Lang et al. 2012; Schierling and appearance of the 4th segment of the metatarsi (simple or Dettner 2013). In the large reservoirs, the alkaloids stenu- bi-lobed), relative length of the 1st and 5th segments of the sine (1), norstenusine (2), 3-(2-methyl-1-butenyl)pyridine metatarsi, relative length of the metatarsi and metatibiae (3) and cicindeloine (4) are stored, whereas the small res- and presence or absence of abdominal paratergites (Cam- ervoirs contain the terpenes a-pinene (5), 1,8-cineole (6) eron 1930; Lohse 1964; Zhao and Zhou 2004; Koerner and 6-methyl-5-heptene-2-one (7). According to Schierling et al. 2013). Later, subgenera were taxonomically revised et al. 2013, most of the Central European Stenus species resulting in five valid subgenera: Stenus s.str., Hemistenus can be grouped into three main groups based on their Motschulsky 1860, Hypostenus Rey 1884, Metatesnus pygidial gland content, especially concerning the alkaloids Adam 1987 and Tesnus Rey 1884 (Puthz 2001, 2008). In 1, 2, 3, and 4. Most Steninae belong to the piperidine this revision, Nestus belongs to Stenus s. str., Hemistenus is group. The secretion of this group is characterized by redefined to Metatesnus and Parastenus is renamed to alkaloids 1 as main and 2 as secondary component. In Hemistenus. However, recent findings indicate that this addition, terpenes 5, 6 and 7 represent minor and trace classification seems artificial and does probably not reflect components in the secretion. The piperidine group is authentic phylogenetic relationships. Currently, the genus regarded as chemotaxonomically basal (Schierling et al. is grouped into a large number of monophyletic species 2013). Furthermore, the pygidial gland system of basal or groups based on a wide range of morphological characters primitive Steninae is characterized by the presence of well- (Table 1; Puthz 2008). distinct small reservoirs storing terpenes. This especially 123 Phylogenetic relationships and chemical evolution 13 Table 1 Stenus, Dianous and Euaesthetus species used for phylogenetic analyses Genus Subgenus Species Species Location GenBank accession no. group/species complex Gene sequences COI Histone 16SrRNA H3 Ingroup Stenus Stenus ater juno Germany, JQ085760a KJ127165 KJ144853 s.str. (Paykull,1789) Schleswig- Holstein, Kiel Canada, Alberta JQ085761a KJ127166 KJ144854 clavicornis clavicornis Germany, Baden- JQ085764a KJ127156 KJ144844 (Scopoli, Württemberg, 1763) Tübingen Germany, JQ085765a KJ127157 KJ144845 Schleswig- Holstein, Kiel comma comma Germany, Baden- JQ085769a KJ127158 KJ144846 (LeConte, Württemberg, 1863) Tübingen Canada, Alberta JQ085771a KJ127159 KJ144847 biguttatus Germany, JQ085772a KJ127146 KJ144834 (Linnaeus, Schleswig- 1758) Holstein, Strande Germany, JQ085773a KJ127147 KJ144835 Schleswig- Holstein, Strande boops boops Germany, Baden- JQ085778a KJ127150 KJ144838 (Ljungh, Württemberg, 1804) Tübingen Germany, Baden- JQ085779a KJ127151 KJ144839 Württemberg, Tübingen canaliculatus canaliculatus Germany, Baden- JQ085780a KJ127154 KJ144842 (Gyllenhal, Württemberg, 1827) Tübingen Germany, Baden- JQ085781a KJ127155 KJ144843 Württemberg, Tübingen nitens Germany, Baden- JQ085782a KJ127169 KJ144857 (Stephens, Württemberg, 1833) Tübingen humilis humilis Germany, Baden- JQ085783a KJ127160 KJ144848 (Erichson, Württemberg, 1839) Tübingen Germany, Baden- JQ085784a KJ127161 KJ144849 Württemberg, Tübingen Tesnus brunnipes
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