Complex within a Complex: Integrative Taxonomy Reveals Hidden Diversity in Cicadetta brevipennis (Hemiptera: Cicadidae) and Unexpected Relationships with a Song Divergent Relative

PLoS One. 2016 Nov 16;11(11):e0165562. doi: 10.1371/journal.pone.0165562. eCollection 2016.

Abstract

Multiple sources of data in combination are essential for species delimitation and classification of difficult taxonomic groups. Here we investigate a cicada taxon with unusual cryptic diversity and we attempt to resolve seemingly contradictory data sets. Cicada songs act as species-specific premating barriers and have been used extensively to reveal hidden taxonomic diversity in morphologically similar species. The Palaearctic Cicadetta montana species complex is an excellent example where distinct song patterns have disclosed multiple recently described species. Indeed, two taxa turned out to be especially diverse in that they form a "complex within the complex": the Cicadetta cerdaniensis song group (four species studied previously) and Cicadetta brevipennis (examined in details here). Based on acoustic, morphological, molecular, ecological and spatial data sampled throughout their broad European distribution, we find that Cicadetta brevipennis s. l. comprises five lineages. The most distinct lineage is identified as Cicadetta petryi Schumacher, 1924, which we re-assign to the species level. Cicadetta brevipennis litoralis Puissant & Hertach ssp. n. and Cicadetta brevipennis hippolaidica Hertach ssp. n. are new to science. The latter hybridizes with Cicadetta brevipennis brevipennis Fieber, 1876 at a zone inferred from intermediate song patterns. The fifth lineage requires additional investigation. The C. cerdaniensis and the C. brevipennis song groups exhibit characteristic, clearly distinct basic song patterns that act as reproductive barriers. However, they remain completely intermixed in the Bayesian and maximum likelihood COI and COII mitochondrial DNA phylogenies. The closest relative of each of the four cerdaniensis group species is a brevipennis group taxon. In our favoured scenario the phylogenetic pairs originated in common Pleistocene glacial refuges where the taxa speciated and experienced sporadic inter-group hybridization leading to extensive introgression and mitochondrial capture.

MeSH terms

  • Acoustics
  • Animals
  • Biodiversity*
  • DNA, Mitochondrial / genetics
  • Electron Transport Complex IV / genetics
  • Female
  • Hemiptera / anatomy & histology
  • Hemiptera / classification*
  • Linear Models
  • Male
  • Phylogeny*
  • Pigmentation
  • Principal Component Analysis
  • Quantitative Trait, Heritable
  • Temperature
  • Vocalization, Animal / physiology*
  • Wings, Animal / anatomy & histology

Substances

  • DNA, Mitochondrial
  • Electron Transport Complex IV

Grants and funding

The Swiss cicada project (TH) was financed by the following funders: Wolfermann-Nägeli Foundation; Zigerli-Hegi Foundation; Walter Haefner Foundation; Paul Schiller Foundation (http://www.paul-schiller-stiftung.ch); Biedermann-Mantel Foundation; Temperatio Foundation (http://www.temperatio.ch); Otto Gamma Foundation and Pro Natura (http://www.pronatura.ch). The travel expenses in Italy (TH) are covered by the Freiwillige Akademische Gesellschaft Basel (http://www.fag-basel.ch). The research of TT was part of the programme “Communities, relations and communications in the ecosystems” (no. P1-0255), financed by the Ministry of Higher Education, Science and Technology of the Republic of Slovenia. The work of EW and CS was supported by the US National Science Foundation (http://www.nsf.gov) under grant number DEB-0955849. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.