Where are you from, stranger? The enigmatic biogeography of North African pond turtles (Emys orbicularis)

Abstract

The European pond turtle (Emys orbicularis) is a Nearctic element in the African fauna and thought to have invaded North Africa from the Iberian Peninsula. All North African populations are currently identified with the subspecies E. o. occidentalis. However, a nearly range-wide sampling in North Africa used for analyses of mitochondrial and microsatellite DNA provides evidence that only Moroccan populations belong to this taxon, while eastern Algerian and Tunisian pond turtles represent an undescribed distinct subspecies. These two taxa are most closely related to E. o. galloitalica with a native distribution along the Mediterranean coast of northern Spain through southern France to western and southern Italy. This group is sister to a clade comprising several mitochondrial lineages and subspecies of E. orbicularis from Central and Eastern Europe plus Asia, and the successive sisters are E. o. hellenica and E. trinacris. Our results suggest that E. orbicularis has been present in North Africa longer than on the Iberian Peninsula and that after an initial invasion of North Africa by pond turtles from an unknown European source region, there was a phase of diversification in North Africa, followed by a later re-invasion of Europe by one of the African lineages. The differentiation of pond turtles in North Africa parallels a general phylogeographic paradigm in amphibians and reptiles, with deeply divergent lineages in the western and eastern Maghreb. Acknowledging their genetic similarity, we propose to synonymize the previously recognized Iberian subspecies E. o. fritzjuergenobsti with E. o. occidentalis sensu stricto. The seriously imperiled Moroccan populations of E. o. occidentalis represent two Management Units different in mitochondrial haplotypes and microsatellite markers. The conservation status of eastern Algerian pond turtles is unclear, while Tunisian populations are endangered. Considering that Algerian and Tunisian pond turtles represent an endemic taxon, their situation throughout the historical range should be surveyed to establish a basis for conservation measures.

Out of Africa: did Emys orbicularis occidentalis cross the Strait of Gibraltar twice?

“…In the present study we significantly expand the previous geographical sampling ( VeloAntón et al, 2008;Stuckas et al, 2014) of E. o. occidentalis throughout the Iberian Peninsula and Morocco to achieve a better understanding of the complex biogeography and evolutionary history of European pond turtles in this region. We study the genetic diversity and structure of Iberian and Moroccan populations using 82 newly collected samples from previously unknown localities and the mitochondrial cytochrome b gene as a phylogeographic marker.…”

“…Kaliontzopoulou et al, 2011;Miraldo et al, 2011;Santos et al, 2012;Velo-Antón et al, 2012) and Morocco (Beukema et al, 2010), unveiling cryptic lineages and suggestive of complex biogeographic processes since the Pliocene. Despite the comprehensive sampling accumulated for E. o. occidentalis over the last decade (Fritz et al, 2007;Velo-Antón et al, 2008, 2011aPedall et al, 2011;Stuckas et al, 2014), isolated populations in both the Iberian Peninsula and mainly Morocco remained undetected and unstudied for a long time. In particular, recent studies discovered highly fragmented populations in the southern Iberian Peninsula (Jiménez-Cazalla and Castro-Rodríguez, 2014;Romero et al, 2014) and Morocco (Velo-Antón et al, 2015), which are imperilled by massive habitat loss.…”

Sexual dimorphism of the European Pond Turtle,Emys orbicularis(Linnaeus, 1758), in Anzali Lagoon, Iran (Reptilia: Emydidae)

“…The European Pond Turtle is a morphologically and genetically diversified species, subdivided into six named and two unnamed subspecies (Fritz et al, 2009;Pedall et al, 2011;Stuckas et al, 2014;Vamberger et al, 2015). The Iranian populations belong to the subspecies E. o. persica Eichwald, 1831 (Fritz et al, 2009).…”

“…The European Pond Turtle, Emys orbicularis (Linnaeus, 1758), has a Palaearctic distribution and is distributed over a vast range embracing northwestern Africa and much of Europe and western Asia, Turkey over to the Caspian and Aral Seas (Fritz et al, 2009;Stuckas et al, 2014). Morphological and genetic variation as well as several aspects of the natural history of this species have been studied in different parts of its range (Fritz, Guicking, Lenk, Joger, & Wink, 2004;Fritz et al, 2005Fritz et al, , 2007Fritz et al, , 2009Fritz, Schmidt, & Ernst, 2011;Kotenko, 2000;Mitrus & Zemanek, 2004;Pedall, Fritz, Stuckas, Valdeón, & Wink, 2011;Stuckas et al, 2014;Vamberger et al, 2015;Zuffi & Gariboldi, 1995a, b;Zuffi et al, 1999Zuffi et al, , 2006, but little research has been done in Iran (see Fritz et al, 2007Fritz et al, , 2009Hezaveh, Arakelyan, Danielyan, & Ghassemzadeh, 2012).…”

“…Morphological and genetic variation as well as several aspects of the natural history of this species have been studied in different parts of its range (Fritz, Guicking, Lenk, Joger, & Wink, 2004;Fritz et al, 2005Fritz et al, , 2007Fritz et al, , 2009Fritz, Schmidt, & Ernst, 2011;Kotenko, 2000;Mitrus & Zemanek, 2004;Pedall, Fritz, Stuckas, Valdeón, & Wink, 2011;Stuckas et al, 2014;Vamberger et al, 2015;Zuffi & Gariboldi, 1995a, b;Zuffi et al, 1999Zuffi et al, , 2006, but little research has been done in Iran (see Fritz et al, 2007Fritz et al, , 2009Hezaveh, Arakelyan, Danielyan, & Ghassemzadeh, 2012). The purpose of this study was to determine the morphometric characteristics of European Pond Turtles (Emys orbicularis) living in Anzali Lagoon in Iran.…”