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Phylogenetic relationships and chemical evolution of the genera Stenus and Dianous (Coleoptera: Staphylinidae)

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Abstract

The subfamily Steninae, composed of the genera Dianous Leach 1819 and Stenus Latreille 1797, belongs to the family of staphylinid beetles (Staphylinidae). Some unique features characterize Stenus beetles, e.g., a distinct prey-capture apparatus (not found in the genus Dianous) and special pygidial gland secretion constituents such as the alkaloids stenusine (1), norstenusine (2), 3-(2-methyl-1-butenyl)pyridine (3), cicindeloine (4) as well as several terpenes like α-pinene (5), 1,8-cineole (6) and 6-methyl-5-heptene-2-one (7); (only 1, 2 and terpenes found in Dianous). As the secretion composition of Stenus beetles is species specific, it can be used for a chemotaxonomic approach to investigate relationships within the Steninae. Based on the alkaloid gland content, Steninae can be grouped into three clusters: the piperidine-, the pyridine- and the epoxypiperideine group. To clarify the phylogenetic relationships within Stenus and between Stenus and Dianous, and to evaluate our chemotaxonomic approach, we analyzed a combined dataset of three gene sequences aligned of mitochondrial cytochrome c oxidase I (COI), 16S rRNA and Histone H3 of 17 Stenus and 4 Dianous species. Our investigations based on two algorithms such as Maximum Likelihood and Bayesian analyses support the chemotaxonomic approach. Furthermore, our results clearly support former analyses concerning the evolutionary origin of Dianous within Stenus, which suggests a secondary loss of the specialized prey-capture apparatus. Finally, phylogenetic aspects based on the morphology of Steninae are discussed.

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References

  • Baldo AM, Donald HL, Strausbaugh LD (1999) Potentials and limitations of histone repeat sequences for phylogenetic reconstruction of Sophophora. Mol Biol Evol 16:1511–1520

    Article  CAS  PubMed  Google Scholar 

  • Betz O (1996) Function and evolution of the adhesion-capture apparatus of Stenus species (Coleoptera: Staphylinidae). Zoomorphology 116:15–34

    Article  Google Scholar 

  • Betz O (1999) A behavioral inventory of adult Stenus species (Coleoptera: Staphylinidae). J Nat Hist 33:1691–1712

    Article  Google Scholar 

  • Betz O (2006) Der Anpassungswert morphologischer Strukturen: Integration von Form, Funktion und Ökologie am Beispiel der Kurzflügelkäfergattung Stenus (Coleoptera: Staphylinidae). Entomologie heute 18:3–26

    Google Scholar 

  • Billard G, Bruyant C (1905) Sur une mode particulier de locomotion de certains Stenus. C R Soc Biol 59:102–103

    Google Scholar 

  • Cameron M (1930) The Fauna of British India including Ceylon and Burma. Coleoptera: Staphylinidae, Vol. 1 (Micropeplinae, Oxytelinae, Oxyporinae, Steninae and Euaesthetinae), Taylor & Francis, London

  • Cilia V, Lafay B, Christen R (1996) Sequence heterogeneities among 16S ribosomal RNA sequences and their effect on phylogenetic analyses at the species level. Mol Biol Evol 13:451–461

    Article  CAS  PubMed  Google Scholar 

  • Clarke DJ, Grebennikov VV (2009) Monophyly of Euaesthetinae (Coleoptera: Staphylinidae): phylogenetic evidence from adults and larvae, review of austral genera, and new larval descriptions. Syst Entomol 34:346–397

    Article  Google Scholar 

  • Colgan DJ, McLauchlan A, Wilson GDF, Livingston SP, Edgecombe GD, Macaranas J, Cassis G, Gray MR (1998) Histone H3 and U2 snRNA DNA sequences and arthropod molecular evolution. Aust J Zool 46:419–437

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  Google Scholar 

  • Dettner K (1987) Chemosystematics and evolution of beetle chemical defense. Annu Rev Entomol 32:17–48

    Article  CAS  Google Scholar 

  • Dettner K (1991) Chemische Abwehrmechanismen bei Kurzflüglern (Coleoptera: Staphylinidae). Jahresber Naturwiss Ver Wuppertal 44:50–58

    Google Scholar 

  • Dettner K (1993) Defensive secretions and exocrine glands in free-living staphylinid beetles—their bearing on phylogeny (Coleoptera: Staphylinidae). Biochem Syst Ecol 21:143–162

    Article  CAS  Google Scholar 

  • Dinapoli A, Tamer C, Franssen S, Naduvilezhath L, Klussmann-Kolb A (2007) Utility of H3-gene sequences for phylogenetic reconstruction—a case study of heterobranch Gastropoda. Bonn Zool Beitr 55:191–202

    Google Scholar 

  • Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–297

    CAS  Google Scholar 

  • Grebennikov VV, Newton AF (2009) Good-bye Scymaenidae, or why the ant-like stone beetles should become megadiverse Staphylinidae sensu latissimo (Coleoptera). Eur J Entomol 106:275–301

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hansen M (1997) Phylogeny and classification of the staphyliniform beetle families (Coleoptera). Biol Skr Dan Vid Sel 48:1–339

    Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B 270:313–321

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heethoff M, Laumann M, Weigmann G, Raspotnig G (2011) Integrative taxonomy: combining morphological, molecular and chemical data for species delineation in the parthenogenetic Trhypochthonius tectorum complex (Acari Oribatida, Trhypochthoniidae). Front Zool 8:2

    Article  PubMed Central  PubMed  Google Scholar 

  • Hemp C, Heller KG, Kehl S, Warchalowska-Silwa E, Wägele JW, Hemp A (2010) The Phlesirtes complex (Orthoptera, Tettigoniidae, Conocephalinae, Conocephalini) reviewed: integrating morphological, molecular, chromosomal and bioacoustic data. Syst Entomol 35:554–580

    Article  Google Scholar 

  • Hermann LH (2001) Catalogue of the Staphylinidae (Insecta: Coleoptera). 1758 to the end of the second millennium. I. Introduction, history, biographical sketches and omaliine group and IV. Staphylinidae group (Part 1). Bull Amer Mus Nat Hist 265:1–650 and 1807:2440

  • Horion A (1963) Faunistik der mitteleuropäischen Käfer vol 9 Staphylinidae 1. Teil Micropeplinae bis Euaesthetinae. Kommissionsverlag Buchdruckerei August Feyel, Überlingen

  • Hunt T, Bergsten J, Levkanicova Z, Papadopoulou A, John OS, Wild R, Hammond PM, Ahrens D, Balke M, Caterino MS, Gómez-Zurita J, Ribera I, Barraclough TG, Bocakova M, Bocak L, Vogler AP (2007) A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation. Science 318:1913–1916

    Article  CAS  PubMed  Google Scholar 

  • Janda JM, Abbott SL (2007) 16S rRNA gene sequencing for bacterial identification in the diagnostic laboratory: pluses, perils, and pitfalls. J Clin Microbiol 9:2761–2764

    Article  Google Scholar 

  • Jenkins MF (1960) On the method by which Stenus and Dianous (Coleoptera: Staphylinidae) return to the bank of a pool. Trans R Ent Soc Lond 112:1–14

    Article  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A, Edwards SV, Pabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial evolution in animals: amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Koerner L, Laumann M, Betz O, Heethoff M (2013) Loss of the sticky harpoon—COI sequences indicate paraphyly of Stenus with respect to Dianous (Staphylinidae, Steninae). Zool Anz 252:337–347

    Article  Google Scholar 

  • Kohler P (1979) Die absolute Konfiguration des Stenusins und die Aufklärung weiterer Inhaltsstoffe des Spreitungsschwimmers Stenus comma. Dissertation, University of Heidelberg

  • Kovaç D, Maschwitz U (1990) Secretion-grooming in aquatic beetles (Hydradephaga): a chemical protection against contamination of the hydrofuge respiratory region. Chemoecology 1:131–138

    Article  Google Scholar 

  • Lang C, Seifert K, Dettner K (2012) Skimming behaviour and spreading potential of Stenus species and Dianous coerulescens (Coleoptera: Staphylinidae). Naturwissenschaften 99:937–947

    Article  CAS  PubMed  Google Scholar 

  • Leschen RAB, Newton AF (2003) Larval description, adult feeding behaviour, and phylogenetic placement of Megalopinus (Coleoptera: Staphylinidae). Coleopt Bull 57:469–493

    Article  Google Scholar 

  • Linsenmair KE (1963) Eine bislang unbekannte Fortbewegungsart bei Insekten: das Entspannungsschwimmen. Kosmos 59:331–334

    Google Scholar 

  • Lohse GA (1964) Staphylinidae I (Micropeplinae bis Tachyporinae). In: Freude H, Harde KW, Lohse GA (eds) Die Käfer Mitteleuropas, vol 4. Goecke & Evers, Krefeld

  • Lohse GA (1989) Ergänzungen und Berichtigungen zu Freude Harde Lohse “Die Käfer Mitteleuropas”. In: Lohse GA, Lucht W (eds) Die Käfer Mitteleuropas, vol 12. Goecke & Evers, Krefeld, pp 121–184

    Google Scholar 

  • Lusebrink I (2007) Stereoisomerie, Biosynthese und biologische Wirkung des Stenusin sowie weitere Inhaltsstoffe der Pygidialdrüsen der Kurzflüglergattung Stenus (Staphylinidae, Coleoptera). Dissertation, University of Bayreuth

  • Lusebrink I, Dettner K, Seifert K (2008a) Biosynthesis of stenusine. J Nat Prod 71:743–745

    Article  CAS  PubMed  Google Scholar 

  • Lusebrink I, Dettner K, Seifert K (2008b) Stenusine, an antimicrobial agent in the rove beetle genus Stenus (Coleoptera, Staphylinidae). Naturwissenschaften 95:751–755

    Article  CAS  PubMed  Google Scholar 

  • Lusebrink I, Dettner K, Schierling A, Müller T, Daolio C, Schneider B, Schmidt J, Seifert K (2009) New pyridine alkaloids from rove beetles of the genus Stenus (Coleoptera: Staphylinidae). Z Naturforsch 64:271–278

    CAS  Google Scholar 

  • Maddison WP (1989) Reconstructing character evolution on polytomous cladograms. Cladistics 5:365–377

    Article  Google Scholar 

  • Maus C, Peschke K, Dobler S (2001) Phylogeny of the genus Aleochara inferred from mitochondrial cytochrome oxidase sequence (Coleoptera: Staphylinidae). Mol Phylogenet Evol 18:202–216

    Article  CAS  PubMed  Google Scholar 

  • Müller T, Göhl M, Lusebrink I, Dettner K, Seifert K (2012) Cicindeloine from Stenus—isolation, structure elucidation and total synthesis. Eur J Org Chem 2012:2323–2330

    Article  Google Scholar 

  • Naomi S-I (1985) The phylogeny and higher classification of the Staphylinidae and their allied groups (Coeloptera, Staphylinoidae). Esakia 23:1–27

    Google Scholar 

  • Neumann S (1993) Die Analdrüsen der Spreitungsschwimmer (Coleoptera: Staphylinidae). Diploma thesis, University of Bayreuth

  • Piffard A (1901) Steni gliding on the surface of water. Entomol Mon Mag 12:99

    Google Scholar 

  • Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609

    Article  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Puthz V (1981) Was ist Dianous Leach, 1819, was ist Stenus Latreille, 1796? Oder: Die Aporie des Stenologen und ihre taxonomischen Konsequenzen (Coleoptera, Staphylinidae). Entomologische Abhandlungen, Staatliches Museum für Tierkunde, Dresden 44:87–132

    Google Scholar 

  • Puthz V (2000) The genus Dianous Leach in China (Coleoptera: Staphylinidae) 261. Contribution to the knowledge of Steninae. Rev Suisse Zool 107:419–559

    Google Scholar 

  • Puthz V (2001) Beiträge zur Kenntnis der Steninen CCLXIX Zur Ordnung in der Gattung Stenus Latreille, 1796 (Staphylinidae, Coleoptera). Philippia 10:31–41

  • Puthz V (2005) Notes on Chinese Dianous Leach (Coleoptera: Staphylinidae). Entomol Rev Japan 60:137–152

    Google Scholar 

  • Puthz V (2006) Revision der neotropischen Stenus (Tesnus) Arten (Coleoptera: Staphylinidae) 288. Beitrag zur Kenntnis der Steninen Rev Suisse Zool 113:617–674

    Google Scholar 

  • Puthz V (2008) Stenus LATREILLE und die segensreiche Himmelstochter (Coleoptera Staphylinidae). Linz biol Beitr 40:137–230

    Google Scholar 

  • Ribera I, Bilton DT, Vogler AP (2003) Mitochondrial DNA phylogeography and population history of Meladema diving beetles on the Atlantic Islands and in the Mediterranean basin (Coleoptera, Dytiscidae). Mol Ecol 12:153–167

    Article  CAS  PubMed  Google Scholar 

  • Ribera I, Nilsson AN, Vogler AP (2004) Phylogeny and historical biogeography of Agabinae diving beetles (Coleoptera) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 30:545–562

    Article  CAS  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Schierling A, Dettner K (2013) The pygidial defense gland system of the Steninae (Coleoptera, Staphylinidae): morphology, ultrastructure and evolution. Arthropod Struct Dev 42:197–208

    Article  PubMed  Google Scholar 

  • Schierling A, Schott M, Dettner K, Seifert K (2011) Biosynthesis of the defensive alkaloid (Z)-3-(2-methyl-1-butenyl)pyridine in Stenus similis beetles. J Nat Prod 74:2231–2234

    Article  CAS  PubMed  Google Scholar 

  • Schierling A, Dettner K, Schmidt J, Seifert K (2012) Biosynthesis of the defensive alkaloid cicindeloine in Stenus solutus beetles. Naturwissenschaften 99:665–669

    Article  CAS  PubMed  Google Scholar 

  • Schierling A, Seifert K, Sinterhauf SR, Rieß JB, Rupprecht JC, Dettner K (2013) The multifunctional pygidial gland secretion of the steninae (Coleoptera: Staphylinidae): ecological significance and evolution. Chemoecology 23:45–57

    Article  CAS  Google Scholar 

  • Schildknecht H (1970) The defensive chemistry of land and water beetles. Angew Chem Int Ed Engl 9:1–9

    Article  CAS  Google Scholar 

  • Schildknecht H, Krauss D, Connert J, Essenbreis H, Orfanides N (1975) The spreading alkaloid stenusine from the staphylinid Stenus comma (Coleoptera: Staphylinidae). Angew Chem Int Ed Engl 14:421–422

    Article  Google Scholar 

  • Shi K, Zhou HZ (2011) Taxonomy of the genus Dianous (Coleoptera: Staphylinidae: Steninae) in China and zoogeographic patterns of its distribution. Insect Sci 18:363–378

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Sperling FAH, Hickey DA (1994) Mitochondrial DNA sequence variation in the spruce budworm species complex (Lepidoptera: Choristoneura). Mol Biol Evol 11:656–665

    CAS  PubMed  Google Scholar 

  • Swofford DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang L, Li LZ, Cao GH (2011) On Chinese species of Dianous group I (Coleoptera, Staphylinidae Steninae). ZooKeys 111:67–85

    Article  PubMed  Google Scholar 

  • Thatcher TH, Gorovsky MA (1994) Phylogenetic analysis of the core histones H2A, H2B, H3 and H4. Nucleic Acids Res 22:174–179

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thayer MK (2005) Staphylinidae. In: Beutel RG, Leschen RAB (eds) Handbook of zoology, Coleoptera, vol 1. De Gruyter, Berlin, pp 296–344

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequences alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Weinreich E (1968) Über den Klebfangapparat der Imagines von Stenus Latr. (Coleopt., Staphylinidae) mit einem Beitrag zur Kenntnis der Jugendstadien dieser Gattung. Z. Morph Ökol Tiere 62:162–210

    Article  Google Scholar 

  • Zhao CY, Zhou HZ (2004) Five new species of the subgenus Hemistenus (Coleoptera: Staphylinidae, Steninae) from China. Pan Pac Entomol 80:93–108

    Google Scholar 

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Acknowledgments

We gratefully acknowledge the Deutsche Forschungsgemeinschaft for funding this project (DE 258/12-1 and SE 595/14-1). Special thanks go to Dr. A. Kleeberg, Berlin for providing rare Stenus species for molecular analyses. Furthermore we would like to thank Dr. S. Kehl, Department of Animal Ecology II, University of Bayreuth and S. Werner, Department of Mycology, University of Bayreuth for their precious help with software and tree construction, respectively. Finally, thanks go to PD Dr. Joseph Woodring for language correction.

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  1. Department of Animal Ecology II, University of Bayreuth, Universitätsstr. 30, 95440, Bayreuth, Germany

    Carolin Lang & Konrad Dettner

  2. Department of Evolutionary Biology of Invertebrates, Institute for Evolution and Ecology, University of Tübingen, Auf der Morgenstelle 28E, 72076, Tübingen, Germany

    Lars Koerner & Oliver Betz

  3. Burgmuseum Schlitz, Naturwissenschaftliche Abteilung, Vorderburg 1, 36110, Schlitz, Germany

    Volker Puthz

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  1. Carolin Lang
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  2. Lars Koerner
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  3. Oliver Betz
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  4. Volker Puthz
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  5. Konrad Dettner
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Correspondence to Carolin Lang.

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Lang, C., Koerner, L., Betz, O. et al. Phylogenetic relationships and chemical evolution of the genera Stenus and Dianous (Coleoptera: Staphylinidae). Chemoecology 25, 11–24 (2015). https://doi.org/10.1007/s00049-014-0171-4

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