Poecilimon jonicus (Fieber, 1853)

Borissov Aneliya Bobeva Battal, Simeon B. & Chobanov, Dragan, 2020, Evolution of Poecilimon jonicus group (Orthoptera: Tettigoniidae): a history linked to the Aegean Neogene paleogeography, Organisms Diversity & Evolution 20 (4), pp. 803-819 : 814

Evolution of Poecilimon jonicus group

According to mitochondrial chronograms ( Fig. 6a–c ), P. jonicus group sensu lato shares a common ancestor 8–6 Ma ago, a time well corresponding to the Messinian period of the Miocene. As the Anatolian clade ( P. antalyaensis + P. isopterus ) constitutes the basal branch and the Cretan ( P. cretensis ) the subsequent one, Anatolian mainland seems to be the place of origin of the group ancestors. Hence, it can be assumed that desiccation in the Mediterranean during the Messinian salinity crisis (MSC) (5.96–5.33 Ma), especially in the Aegean area (e.g., Steininger and Rögl 1984; Dermitzakis 1990), provided distribution corridor for dispersal of an ancestral stock over the present distribution range of the group. However, the poorly resolved relationships between the Cretan, Balkan, and P. inflatus + P. martinae lineage suggest an early radiation within Anatolia or along the Aegean landmass connecting the Balkans and Anatolia during the MSC ( Fig. 7c ). The following post-Messinian transgression of the Mediterranean and Aegean area ca. 5.3–5.2 Ma ( Jolivet et al. 2006) acted as a vicariant event resulting in four geographically isolated stocks—ancestral P. inflatus + P. martinae in Anatolia and P. cretensis in Crete, the Northern, and Southern Balkan group in the southern Balkan mainland and on the Peloponnesos, respectively ( Fig. 8a ). In that case, the expected phylogeny of the group will be [( P. antalyaensis + P. isopterus ) + ( P. cretensis + ( P. inflatus + P. martinae ) + Northern Balkan clade + Southern Balkan clade)].

During Messinian, the level of the Mediterranean dropped after its isolation from the Atlantic. As a result of the MSC, the Aegean landmass was largely united again, and terrestrial migrations between the Balkan mainland and Crete were possible and documented (e.g., Dermitzakis 1990; Lymberakis et al. 2007). With the end of the Messinian 5.33 Ma ago and the Zanclean refill of the Mediterranean basin the Balkans, Anatolia and Crete were disconnected again ca. 5.2 Ma ago ( Meulenkamp 1985; Dermitzakis 1990). We believe these two periods are of major importance for dispersal, early speciation, and subsequent vicariance leading to major lineage splits within the Poecilimon jonicus group ( Figs. 7c , 8a ). Within this time frame (5.8/5.6 to 5.2 Ma), the Cretan lineage was established and shortly after that the Balkan lineage splits into a Northern and a Southern group. Roughly at the same time, the P. inflatus branch (present P. inflatus + P. martinae ) was established.

In Pliocene, the land-sea configuration further complicated with the development of many islands and peninsulas, as well as vast inland freshwater areas (marshes and lakes) ( Popov et al. 2004) ( Fig. 8a, b ). The latter may have contributed to the basal lineage splits within the Northern Balkan group ( P. werneri , P. jonicus superbus ), Southern Balkan group ( P. erimanthos ), and in the Anatolian group ( P. antalyaensis and P. isopterus ) due to vicariant events. Specifically, the lack of P. jonicus superbus in most of Puglia (southeastern corner of Italy) ( Fig. 2 ), though this area represented an island at the time this taxon originated, may possibly be explained as a result of recent climatic factors.

Latest speciation events are dated to the Pleistocene, starting with the onset of the northern hemisphere glaciation (2.5–2.6 Ma ago), when climate cycles with alternating cooler drier and warmer more humid periods dominated the area. Those climate events have been suggested as triggers for recent lineage splits in other Barbitistini ( Kaya et al. 2015; Chobanov et al. 2017). Pleistocene climate was dominated by two major climatic switches—first ca. 1.4 Ma, when 41- Ka cold-warm cycles become constant, and second, 0.8 Ma, when 100-Ka cycles established ( Lisiecki and Raymo 2007). Those periods of cooling and warming were connected not only with climate changes but also with sea level drops (glacials) and rises (interglacials). Thus, thermophilous animals dependent on modest humidity retreated to refuges and were isolated on islands during stadials (cold dry periods) and regained territories during interstadials (warm humid periods). Interesting correlation may be observed between the intraspecific divergence of the Cretan lineage ( P. cretensis ) and the second Pleistocene climatic switch ( Fig. 6b ). Patterns of the evolutionary history of Cretan lineages based on early vicariance are documented in various groups ( Parmakelis et al. 2005, 2006; Simaiakis and Mylonas 2008). Populations on the island were completely isolated after the end of the Messinian. Yet, the current appearance of Crete as a united landmass was established only recently, while many smaller island configurations existed during the Pliocene ( Creutzburg 1963; Dermitzakis 1990; Douris et al. 1998; Welter-Schultes 2000) ( Fig. 8a, b ). Relatively high genetic distances between sampled populations of P. cretensis could be a reflection of vicariant events during the Pleistocene as a result of isolation of the easternmost Cretan territory by lakes/brackish waters around that time.

Figures

Fig. 6 Timetrees for the P. jonicus group based on different phylogenies and time calibrations with node labels referring to the time estimation in millions of years. a BEAST maximum clade credibility tree inferred from COI and ND2 partitions calibrated for the substitution rate of COI; b BEAST chronogram and RelTime timetree inferred from the COI+ND2 phylogeny calibrated for the last separation of Crete (values above nodes, BEAST chronogram estimations; values below nodes, RelTime timetree estimations); c BEAST chronogram inferred from the 16S rRNA+12S rRNA phylogeny calibrated for the TMRCA (interval) of P. jonicus group (node 12) as suggested from the COI+ND2 chronogram. Different topologies of the trees are marked with “*” for the COI partitions and “**”for the ND2 partition on (a) and different topology of the BEAST and RelTime trees on (b). Numbers in white circles corre- spond to data in Supplementary material C. Light blue vertical band marks the onset of the northern hemisphere glaciation and dark blue lines mark major climatic switches in the Pleistocene. Uniform gray areas below the trees show united Aegean landmass (left) and re- unification of large areas in Messinian (right), while striped areas show disintegrated state of the Aegean

Fig. 7 Land-sea configuration in the Aegean area in different periods of the Neogene based on reconstructions by Popov et al. (2004) (with details taken from Creutzburg 1963 and Dermitzakis 1990) with historical biogeography hypothesis for the Messinian. a Late Serravallian (12–11 Ma), a possible time for the origin and early divergence of Barbitistini; b late Tortonian (8.5–7 Ma), transgression of the Mid-Aegean area in Tortonian

Fig. 8 Land-sea configuration in the Aegean area in different periods of the Neogene based on reconstructions by Popov et al. (2004) (with details taken from Creutzburg 1963 and Dermitzakis 1990) with historical biogeography hypotheses for the evolution of the P. jonicus group. a Midlate Pliocene (ca. 3.5 Ma), transgression of the Aegean area at the end of Messinian/beginning of Pliocene led to vicariant speciations in Anatolia,

Fig. 2 Distribution of the members of the Poecilimon jonicus group sensu lato—ranges of all species currently considered within the groups P. jonicus and P. inflatus including subspecies of P. jonicus shown with different colors as marked in the plates