Origin, evolution and systematics of the genus Poecilimon (Orthoptera: Tettigoniidae)—An outburst of diversification in the Aegean area

Abstract

Our study focuses on the origin, dispersal patterns, evolutionary strategies and systematics of Poecilimon, the largest bush‐cricket genus in the Palaearctic with over 150 taxa described. We employ phylogenetic and divergence time estimation analyses based on multilocus sequence data (ND2 + COI + 12 S + 16 S + ITS+28 S), perform ancestral area reconstruction, and track the evolution of behavioural (evolution of sound communication) and morpho‐physiological traits (body size and shape, and spermatophore size) in this genus. Based on our results, we propose a revised systematics of Poecilimon, including description of a new species, P. nivalis sp. n., and hypothesize three stages in the evolution of Poecilimon. (1) In the early evolution of the genus in Tortonian, when open dry habitats appeared in the Eastern Mediterranean, diversification rates were low and speciation was possibly induced by vicariance and habitat fragmentation; physiology and morphology during this period retained their ancestral states but the evolution of main lineages may have been accompanied by behavioural specializations. (2) Climate cooling and aridification during the Messinian induced dispersals and adaptation to new habitats, followed by physiological and behavioural adaptations; major clades formed or started diversifying. (3) Starting at the end of Messinian and continuing through the Plio‐ and Pleistocene, a few dispersal events from Anatolia to the Balkans took place and climatic oscillations were followed by allo‐ and parapatric divergence of habitat specialists, while ecological adaptations enhanced song diversity and led to morpho‐physiological changes.

Understudied regions and messy taxonomy: Geography, not taxonomy, is the best predictor for genetic divergence of the Poecilimon bosphoricus species group

“…Individuals from almost all of the currently recognized species of the PB species group (Orthoptera, Tettigonidae; Phaneropterinae) (Borissov et al, 2023; Chobanov et al, 2015; Kaya et al, 2012) were collected across the total geographic ranges of the species group (Figure 1) during 2015–2019 (see Table S1 for sample site details). The only exception is for P. athos that is isolated to the Athos Peninsula, Greece.…”

“…However, uncertainty about the identification of some collected individuals from portions of their purported range reduced the taxonomic representation in our study. Specifically, individuals of P. similis , P. geoktschajkus , P. djakonovi and P. oligacanthus (see Borissov et al, 2023; Kaya et al, 2012) from the northern and southern Caucasus collected from east of the Çoruh River were all identified as P. similis . In addition, P. similis ‐like individuals collected from the Black Sea Basin of Anatolia west of the Çoruh River show affinities with P. similis but also exhibit morphological differences.…”

“…Likewise, with a genetic window into the history of diversification, tests of the hypothesis that species within the Marmara Sea region are each-others closest relatives would provide support for a model of in situ diversification, whereas a model of diversity accumulation via dispersal would be supported if geographically circumscribed species are related to more geographically distant taxa. However, currently genetic studies on the genus are either limited to small species groups (e.g., Borissov et al, 2020Borissov et al, , 2021Boztepe et al, 2013;Kaya et al, 2015;Kociñski, 2020) or are constrained by limited number of sequenced individuals per species (e.g., Borissov et al, 2023;Ullrich et al, 2010) that constrains tests about putative species boundaries and tests about the geography of divergence.…”

“…Here, we use a genetic framework to investigate the geography of divergence in a species‐rich group of bush crickets ( Poecilimon bosphoricus [PB] species group) from Anatolia and adjoining Caucasian and Balkans regions, a relatively understudied region with a complex geologic history (Bozkurt, 2001; Popov et al, 2004). The PB species group is the most species‐rich (with 27 recognized species; Borissov et al, 2023; Chobanov et al, 2015; Kaya et al, 2012; Ünal, 2012) of the diverse genus Poecilimon , which contains more than 170 species arranged into 24 species groups (up from estimates of 68 species in eight groups; Ramme, 1933), with two species not assigned to any species group (Borissov et al, 2023). The genus is primarily distributed throughout the Anatolio‐Balkan region of the Western Palearctic, with a few species also occurring in Italy, the Levant, the Southern Caucasus and other parts of the Black Sea Basin (Çıplak, 2004a).…”

“…Such character‐based species definitions imply a direct link to a mechanism of reproductive isolation, and such characters are, therefore, a prime candidate for understanding the bush cricket's diversification (Heller et al, 2015; Heller & Hemp, 2020). However, sometimes there are individuals of intermediate morphologies between species, which has fuelled taxonomic discrepancies (Borissov et al, 2023; Chobanov et al, 2015; Kaya et al, 2012; Ramme, 1933; Tarbinsky, 1932; Ünal, 2012; Zhantiev & Korsunovskaya, 2015). Moreover, variation in the cerci (namely, in length, curvature, thickness, apical structure and the number/orientation of distal teeth) and variation in temporal parameters of the three types of male calling song (see Chobanov et al, 2015; Kaya et al, 2012) may represent a breakdown of reproductive barriers, or the ephemerality of incipient species divergences (Rosenblum et al, 2012).…”