Genetic divergence and evolution of reproductive isolation in Eastern Mediterranean water frogs

Contents

Abstract

Water frogs [genus Pelophylax (Rana)] that occur around the eastern
Mediterranean Sea provide an opportunity to study early stages of speciation. The
geography of the eastern Mediterranean region has changed dramatically since the
Middle Miocene as a result of motions of adjoining lithospheric plates and regionalscale
vertical crustal motions (uplift and subsidence). For several hundred thousand
years between 6 and 5 million years ago (Mya), the Mediterranean basin was
isolated from the Atlantic Ocean, and became desiccated (the Messinian Salinity
Crisis; MSC). Geological data suggest that the endemic water frog lineage on
Cyprus was isolated by the flooding of the Mediterranean basin by salt water at
the end of the MSC, circa 5.5–5.3 Mya. This suggests a rate of uncorrected genetic divergence of approximately 1.1% per million years (My). Divergence time estimates
based on this rate are in good agreement with the chronology of events in the
history of crustal deformation and landscape development in the eastern Mediterranean
region.
Despite a high similarity in morphology, eastern Mediterranean water frogs
show considerable genetic divergence, indicating the existence of several evolutionary
species at varied levels of differentiation. Based on two mitochondrial (mt)
genes (ND2 and ND3), several lineages have been identified: Pelophylax bedriagae,
P. cretensis, P. epeiroticus, P. ridibundus (Europe), six Anatolian lineages,
all provisionally subsumed under the name P. cf. bedriagae, and a distinct lineage
restricted to Cyprus. Genetic data from transition zones in eastern Greece/western
Anatolia, south-western Anatolia, and south-eastern Anatolia, in concert with the
results of female choice experiments, indicate that antihybridization mechanisms
are only weakly developed in eastern Mediterranean water frogs. Genetic incompatibility,
as expressed by average hatching rate of heterospecific crosses, increases
with genetic divergence measured by uncorrected distance estimated from mtDNA
sequences. Hatching rates of heterospecific crosses show an extremely high variability,
however, and viable F1 hybrids originated from almost all crosses. We
conclude that speciation in eastern Mediterranean water frogs follows the allopatric
model and has been closely associated with the geodynamic evolution of the
Mediterranean since the Middle Miocene (i.e., since ~11 Mya).