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

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.

A new Neotibicen cicada subspecies (Hemiptera: Cicadidae) from the southeastern USA forms hybrid zones with a widespread relative despite a divergent male calling song

“…Use of the subspecies classification for Neotibicen similaris apalachicola is consistent with the approach applied to cicadas in the genera Pauropsalta Goding & Froggatt (Popple 2013), Cicadetta Kolenati (Hertach et al 2016) and Thopha Amyot & Audinet-Serville , although the song differences are greater in our case. In those cases, as here, the described taxa exhibit low levels of genetic and morphological divergence and have geographic relationships ranging from allopatric to parapatric with hybridization.…”

“…Recent studies have revealed additional complexes of parapatric cicada species and/or subspecies that hybridize in apparent zones of secondary contact (Hertach et al 2016;Marshall et al 2011;Popple 2013). The case presented here is remarkable in that Neotibicen similaris apalachicola is almost surrounded by populations of N. similaris similaris, so it is possible that the latter contains cryptic lineages from different climatic refugia (one on either side of N. similaris apalachicola).…”

A molecular phylogeny of the cicadas (Hemiptera: Cicadidae) with a review of tribe and subfamily classification

“…Cicadas are hemipteran insects known for their multiple-year life cycles, some of which are the longest known in non-eusocial insects, and for their loud, complex, and usually species-specific acoustic sexual signals or songs (Myers 1929;Claridge 1985;Williams & Simon 1995). Cicadas have become useful model organisms for studies of speciation and biogeography, because songs allow rapid assessment of local cicada communities and facilitate the detection of cryptic taxa at early stages of divergence (Marshall et al 2011;Hertach et al 2016). Cicadas have also become a focus of studies of endothermy (e.g., Sanborn et al 2003;, of endosymbiosis, where extraordinary examples of genome evolution have been documented (McCutcheon et al 2009;Van Leuven et al 2014;Campbell et al 2015), and in technology where the nanostructure of cicada wings has served as a template for nanolithography to create hydrophobic, antireflective and/or antibiotic surfaces (Zhang et al 2006;Xie et al 2008;Hasan et al 2013;Zada et al 2016;Lin et al 2018).…”

Checklist and provisional atlas of singing cicadas (Hemiptera: Cicadidae) of Bulgaria, based on bioacoustics

“…General distribution (only acoustically-validated data): Southern Europe : Bulgaria, Croatia, Italy, Romania, Serbia, Slovenia; Central Europe : Austria, Hungary (summarised by Hertach et al 2016 ).…”