A multisource solution for a complex problem in biodiversity research: Description of the cryptic ant species Tetramorium alpestre sp.n. (Hymenoptera: Formicidae)

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Abstract

Ants of the myrmicine Tetramorium caespitum (Linnaeus, 1758)/T. impurum (Foerster, 1850) complex have challenged taxonomy for long. Schlick-Steiner et al. (2006) made plausible that there are at least seven instead of two species to the complex in the Western Palearctic. Using an increased sample size for increased robustness of the system, we here delimit the alpine species Tetramorium sp. A sensu Schlick-Steiner et al. (2006) against the co-occurring other Western Palearctic species of the complex. The co-occurring species are T. caespitum, T. sp. B sensu Schlick-Steiner et al. (2006) – here treated together because of their extreme morphological similarity – and T. impurum. In a multi-source approach taking advantage of interdisciplinary complementarity, data from male genital morphology and worker morphometrics, thermal niche and mitochondrial DNA are integrated. The unified species concept is applied using the species-delimitation criteria of phenotypic distinctness, thermal niche divergence, reciprocal monophyly and genetic clusters. Tetramorium sp. A is confirmed to be a separate species. Possible synonyms are excluded as names for it based on biogeographic, thermal-niche and worker-morphometric arguments. Tetramorium sp. A is described as Tetramorium alpestre sp.n. It is known from alpine-mat habitats between 1300 and 2335 m above sea level in Austria, France, Italy and Switzerland. T. alpestre is the only Western Palearctic species of the species complex with functionally polygynous nests and supercolonies. Routine identification of workers can be performed using a freely accessible identification tool embedded in the internet, at http://web-resources.boku.ac.at/Discmean/. We discuss our use of species concept, species-delimitation criteria and data analyses as well as the identity of six ambiguous nests and look at some aspects of taking the multisource approach in taxonomy.

Introduction

Recently, the approach of combining data from multiple sources including molecular genetics has been shown to improve the success in disclosing cryptic biodiversity to an unparalleled degree (e.g., Bickford et al., 2007, Moreau, 2009, Seifert, 2009, Bernasconi et al., 2010, Schlick-Steiner et al., 2010). Discovery of cryptic species frequently marks the first step in resolving longstanding taxonomic disputes. However, cryptic-species identification as made plausible by modern approaches but yet to be linked to Linnean nomenclature represents special challenges to alpha taxonomy (Schlick-Steiner et al., 2007). Achieving this link is highly desirable: in taxonomy, any species delimitation and characterisation is available, and thus open to further scrutiny, only if it is associated with a formal name published in accord with nomenclature (International Commission on Zoological Nomenclature, 1999), such publications having “eternal life” (Boero, 2001). We here contribute to settling the taxonomic dispute surrounding the pavement ants, Tetramorium caespitum (Linnaeus, 1758), T. impurum (Foerster, 1850), and the cryptic species formerly attributed to these species.

Linnaeus's (1758) name caespitum was the starting point of the taxonomic dispute, followed by descriptions of numerous similar taxa, as well as constant revisions (for a summary, see Bolton et al., 2007). By the end of the millennium, taxonomists had come to believe there were just two species in the montane and subalpine altitudinal zone of Central Europe, T. caespitum and T. impurum. Disconcertingly, some samples did not fit the keys (Seifert, 1996): for example, both states of the main distinguishing character, viz. the absence and presence of rugae on the crests of petiole and postpetiole, were found within some nests (Schlick-Steiner and Steiner, 1999). In addition, Sanetra and Buschinger (2000) presented allozyme patterns for 14 Palearctic Tetramorium species and found the highest variability in T. caespitum and T. impurum (most of the species characterised by Schlick-Steiner et al. (2006) were included; for details, see Appendix A of Schlick-Steiner et al. (2006)). It was the multidisciplinary approach, starting from tentative semiochemical findings (Steiner et al., 2002), which began to shed light on the systematic enigma and revealed cryptic diversity (Schlick-Steiner et al., 2006). Sociobiology data contributed, with partial differences in the number of nest queens (Steiner et al., 2003). Findings from mitochondrial DNA (mtDNA) revealed at least seven groups, but the pattern alone was inconclusive in that divergences within groups partly exceeded those between them (Schlick-Steiner et al., 2006). Male genital morphology showed diagnostic characters for four of the groups, but could not distinguish two of them (the males of one entity remaining unknown); refined morphometrics of workers were in line with the seven-group hypothesis (Schlick-Steiner et al., 2006). But were the groupings species or did they reflect intraspecific variants? Biogeography shed some light on this question, showing sympatry for the species. In sum, these studies demonstrated that the combined evidence was required to overcome the deficits of single disciplines in this species complex. The study by Schlick-Steiner et al. (2006) resulted in neotype designations and redescriptions of T. caespitum and T. impurum. It also led to the characterisation of a further five species, under code names, A–E, because “a taxonomic decision on species A–E would require the revision of about 50 names which come into question for Palearctic Tetramorium species (Bolton, 1995).”

Here, we start to resolve the revealed cryptic diversity in nomenclatural terms by tackling the case of the alpine species Tetramorium sp. A. Applying a multisource approach that takes advantage of interdisciplinary complementarity, we first use information from morphology (male genitalia, worker morphometrics), ecology (thermal niche) and molecular genetics (mtDNA) separately and then integrate it. We focus on the species which co-occur with Tetramorium sp. A and use samples from their entire distribution ranges. In detail, there are two steps:

  • (i)

    Species delimitation: Starting from the findings of Schlick-Steiner et al. (2006) we go beyond that study by analysing a larger sample, thus increasing the system's robustness, allowing for intraspecific variation to be examined, and reducing the error rate in identifications.

  • (ii)

    Nomenclature: Building on the results from (i), we consider the relevant available names of taxa that could potentially be conspecific with Tetramorium sp. A. Following demonstration that Tetramorium sp. A represents an as yet undescribed species based on biogeographic, thermal-niche and worker-morphometric arguments, we present the taxonomic description of Tetramorium alpestre sp.n., in terms of morphology, ecology and molecular genetics.

Section snippets

The Tetramorium caespitum/impurum complex

Bolton, 1976, Bolton, 1977, Bolton, 1979, Bolton, 1980 outlined the Palearctic T. caespitum group by means of morphological characters and included 55 species (Bolton, 1995). Within this group, the species with strongest resemblance to T. caespitum and T. impurum have been termed the T. caespitum/impurum complex (Schlick-Steiner et al., 2006). Workers of the T. caespitum/impurum complex range from small to large and from light brown to black; the head is often strongly, less frequently weakly

Species concept and species delimitation criteria

We applied the unified species concept (USC; de Queiroz, 2007). The USC has been defined to accommodate the core common to all species concepts and considers a separately evolving metapopulation lineage as the only necessary conceptual property of species. The justification of a particular delimitation in practice is then based on any or several of the properties of species that other species concepts consider (Hey, 2006, de Queiroz, 2007).

As delimitation criteria we used phenotypic

Species delimitation

Type specimens of T. banyulense, T. caespitum var. fusciclavum, T. caespitum var. penninum, T. semilaeve var. kutteri and T. semilaevis subsp. italica were not included in the basic data set for species delimitation, but are checked for conspecificity with the here delimited species in Section 4.2. Four of the other nests (#260, #261, #i548, #i613) could not be tentatively identified as either Tetramorium sp. A, T. caespitum et sp. B or T. impurum (but were not identified as any of the other

Discussion

Our analyses resulted in the delimitation of Tetramorium sp. A sensu Schlick-Steiner et al. (2006) against the species of the T. caespitum/impurum complex which co-occur with it, as well as in the exclusion of all relevant available names as names for T. sp. A. Prior to the formal species description (Section 6), we give some considerations on species concepts, species-delimitation criteria and data analyses, discuss the six ambiguous nests, and highlight some aspects of the multisource

Formal description

Tetramorium alpestre sp.n. Steiner, Schlick-Steiner and Seifert (Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8, Fig. 9; Table 1, Table 2)

Type locality. Austria (Tyrol): Vent, 46.8548°N, 10.9097°E, 2000 m a.s.l.; immediately above timber line; vegetation mainly grass with interspersed dwarf shrubs (Erica sp. and others; ca. 10–20 cm high) and patches free of vegetation (small rocks, stones, bare soil); holotype nest large (ca. 3 m2); other ant species found close to holotype nest: Formica

Acknowledgements

More than 150 persons have provided material to our ongoing study on Palearctic Tetramorium which was used for establishing the phylogenetic framework published by Schlick-Steiner et al. (2006). The description of T. alpestre would not have been possible without their assistance. We are especially grateful to the following persons who contributed material for the present work: C. Bernasconi, A. Buschinger, D. Cherix, A. Freitag, R. Göls, G. Heller, H. Müller, R. Neumeyer, A. Schulz and J.

References (114)

  • B.C. Schlick-Steiner et al.

    Without morphology, cryptic species stay in taxonomic crypsis following discovery

    Trends Ecol. Evol.

    (2007)
  • B.C. Schlick-Steiner et al.

    A multidisciplinary approach reveals cryptic diversity in Western Palearctic Tetramorium ants (Hymenoptera: Formicidae)

    Mol. Phylogenet. Evol.

    (2006)
  • B.J. Adams

    The species delimitation uncertainty principle

    J. Nematol.

    (2001)
  • P.-M. Agapow et al.

    The impact of species concept on biodiversity studies

    Quart. Rev. Biol.

    (2004)
  • I. Agnarsson et al.

    Taxonomy in a changing world: seeking solutions for a science in crisis

    Syst. Biol.

    (2007)
  • E. André

    Les fourmis. [part]

  • K. Backhaus et al.

    Multivariate Analysemethoden: eine anwendungsorientierte Einführung. 8. Auflage

    (1996)
  • A.T. Beckenbach

    Numts and mitochondrial pseudogenes

    Myrmecol. News

    (2009)
  • F. Bernard

    Les fourmis et leur milieu en France méditerranéenne

    Encycl. Entomol.

    (1983)
  • C. Bernasconi et al.

    Molecular taxonomy of the Formica rufa group (red wood ants) (Hymenoptera: Formicidae): a new cryptic species in the Swiss Alps?

    Myrmecol. News

    (2010)
  • C.W. Birky

    The inheritance of genes in mitochondria and chloroplasts: laws, mechanisms, and models

    Annu. Rev. Genet.

    (2001)
  • B. Bolton

    The ant tribe Tetramoriini (Hymenoptera: Formicidae). Constituent genera, review of smaller genera and revision of Triglyphothrix Forel

    Bull. Br. Mus. (Nat. Hist.) Entomol.

    (1976)
  • B. Bolton

    The ant tribe Tetramoriini (Hymenoptera: Formicidae). The genus Tetramorium Mayr in the Oriental and Indo-Australien Regions, and in Australia

    Bull. Br. Mus. (Nat. Hist.) Entomol.

    (1977)
  • B. Bolton

    The ant tribe Tetramoriini (Hymenoptera: Formicidae). The genus Tetramorium Mayr in the Malagasy region and in the New World

    Bull. Br. Mus. (Nat. Hist.) Entomol.

    (1979)
  • B. Bolton

    The ant tribe Tetramoriini (Hymenoptera: Formicidae). The genus Tetramorium Mayr in the Ethiopian zoogeographical region

    Bull. Br. Mus. (Nat. Hist.) Entomol.

    (1980)
  • B. Bolton

    A New General Catalogue of the Ants of the World

    (1995)
  • B. Bolton et al.

    Bolton's Catalogue of Ants of the World: 1758–2005

    (2007)
  • J.E. Bond et al.

    An integrative method for delimiting cohesion species: finding the population-species interface in a group of Californian trapdoor spiders with extreme genetic divergence and geographic structuring

    Syst. Biol.

    (2008)
  • J. Bondroit

    Les fourmis de France et de Belgique

    Ann. Soc. Entomol. France

    (1918)
  • C.D. Cadena et al.

    Molecules, ecology, morphology, and songs in concert: how many species is Arremon torquatus (Aves: Emberizidae)?

    Biol. J. Linn. Soc.

    (2010)
  • M. Consani et al.

    Fauna di Romagna. Imenotteri – Formicidi

    Mem. Soc. Entomol. Ital.

    (1952)
  • K. de Queiroz

    Species concepts and species delimitation

    Syst. Biol.

    (2007)
  • M.J. Donoghue

    A critique of the biological species concept and recommendations for a phylogenetic alternative

    Bryologist

    (1985)
  • J. Duan et al.

    Population structure of the genes encoding the polymorphic Plasmodium falciparum apical membrane antigen. 1: Implications for vaccine design

    Proc. Natl. Acad. Sci. U. S. A.

    (2008)
  • S.V. Edwards

    Is a new and general theory of molecular systematics emerging?

    Evolution

    (2009)
  • C. Emery

    “1924”. Notes critiques de myrmécologie

    Ann. Soc. Entomol. Belg.

    (1925)
  • G. Evanno et al.

    Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study

    Mol. Ecol.

    (2005)
  • H. Feldhaar et al.

    Lifelong commitment to the wrong partner: hybridization in ants

    Phil. Trans. R. Soc. Lond. B: Biol. Sci.

    (2008)
  • O. Folmer et al.

    DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates

    Mol. Mar. Biol. Biotechnol.

    (1994)
  • D.J. Funk et al.

    Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA

    Annu. Rev. Ecol. Evol. Syst.

    (2003)
  • W. Godsoe

    Regional variation exaggerates ecological divergence in niche models

    Syst. Biol.

    (2010)
  • R.J. Hijmans et al.

    Very high resolution interpolated climate surfaces for global land areas

    Int. J. Climatol.

    (2005)
  • K. Hilgenboecker et al.

    How many species are infected with Wolbachia? – a statistical analysis of current data

    FEMS Microbiol. Lett.

    (2008)
  • A.A. Hoffmann et al.

    Cytoplasmatic incompatibility in insects

  • B. Hölldobler et al.

    The Ants

    (1990)
  • J.P. Huelsenbeck et al.

    Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models

    Syst. Biol.

    (2004)
  • International Commission on Zoological Nomenclature

    International Code of Zoological Nomenclature

    (1999)
  • L.S. Jermiin et al.

    The biasing effect of compositional heterogeneity on phylogenetic estimates may be underestimated

    Syst. Biol.

    (2004)
  • A. Jeyaprakash et al.

    Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species

    Insect Mol. Biol.

    (2000)
  • Klimaabteilung der Zentralanstalt für Meteorologie und Geodynamik

    Klimadaten der Welt auf CD-ROM. Version 1.0

    (1996)
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