Some like it cold: the glossiphoniid parasites of the Sicilian endemic pond turtleEmys trinacris(Testudines, Emydidae), an example of ‘parasite inertia’?

Abstract

The freshwater turtles of the genus Emys and some leech species of the family Glossiphoniidae are the only Palaearctic representatives of primarily Nearctic taxa, which jointly colonized Eurasia and the Maghreb during the Miocene. The strict trophic relationships occurring between the glossiphoniid parasite leech Placobdella costata and its host, the emydid Emys orbicularis, make them a prime example of host–parasite cophylogenetic evolution. In the light of the discovery of the Sicilian cryptic endemic species Emys trinacris, which is the sister species to the widespread Palaearctic E. orbicularis, the possible cophylogenetic divergence of the turtle hosts and their leech parasites was investigated. In spite of the deep divergence scored between the two pond turtle species and of their allopatric distribution, their leech parasites proved to be conspecific and indistinguishable based on the implemented molecular marker. This unexpected decoupling might likely be ascribed to the different dispersal abilities of the two taxa and/or to the recent, human‐mediated introduction of the leech parasites in Sicily. If this last scenario is confirmed, the long‐term effects of the introduced leech parasite on the endemic Sicilian pond turtle Emys trinacris should be carefully monitored. In the frame of this study, representatives of the widely spread predatory leech Helobdella stagnalis were observed on E. trinacris. Molecular analyses of their stomach content allowed to rule out the possibility of the existence of a trophic relationships between these two taxa, in contrast to what was previously suspected, and suggest that H. stagnalis specimens were rather attached to the turtles for non‐nutritional reasons.

Molecular Cytogenetic Characterization of the Sicilian Endemic Pond Turtle Emys trinacris and the Yellow-Bellied Slider Trachemys scripta scripta (Testudines, Emydidae)

“…In addition, identical patterns between the two species were also found for the distribution of the telomeric repeats, which are localized only at the terminal ends of chromosomes, and the distribution of the rDNA loci, which are localized in the first microchromosome pair of the complement ( [21], this study). The comparison between the two species of the genus Emys shows that they have similar karyotypes, in agreement with previous features studied [11][12][13]16]. T. s. scripta showed a similar pattern with E. trinacris (this study) and E. orbicularis for all cytogenetic markers, suggesting once more the extreme karyotypic conservation of turtle families [22,54]; these data are in agreement with previous ones on repetitive sequence conservation, which are evidence of no occurrence of genome reorganization [39,46,47].…”

“…Total DNA was isolated using the Real Genomics "Genomic DNA Extraction Kit" (RBC BioScience, New Taipei City 23145, Taiwan) following the manufacturer's protocol. A fragment of the mitochondrial gene cytochrome b was amplified and sequenced following the protocol described by Marrone et al [16].…”

“…However, recent phylogenetic reconstructions based on genomic data revealed that these two emydid species are closely related, with E. trinacris being the sister to all the known mitochondrial lineages of E. orbicularis s.l. [ 11 , 13 , 14 , 15 , 16 ].…”

The good, the bad and the ugly: Emys trinacris, Placobdella costata and Haemogregarina stepanowi in Sicily (Testudines, Annelida and Apicomplexa)

“…(see Marrone et al 2016a). Such an unexpected decoupling might be due to a recent, human-mediated introduction of the leech to Sicily, which would be also supported by the evidence of the presence of introduced specimens of E. orbicularis from Italy in Lago Urio Quattrocchi (Vamberger et al 2015), or to a natural long-range passive dispersal event of the species, which is reported to be able to be dispersed by non-chelonian vertebrates with aquatic afinity (Vamberger and Trontelj 2007, Bielecki et al 2012, Marrone et al 2016a.…”

“…In consideration of the recent finding of glossiphoniid leeches parasitising the Sicilian pond turtle (Marrone et al 2016a), the possible occurrence of apicomplexan haemoparasites in the blood cells of wild populations of E. trinacris was investigated.…”