The puzzling demographic history and genetic differentiation of the twaite shad (Alosa fallax) in the Ebro River

The Ebro, the largest Iberian river draining into the Mediterranean, historically supported one of the most important twaite shad (Alosa fallax) populations in the region. However, during the twentieth century multiple anthropogenic changes caused a severe decline and the presumed extinction of this species from the river by the 1970s. Its unexpected reappearance in 2004 thus provoked sound interest and raised important questions on the origin of those individuals and their genetic variability, which we address in this study. Adult shads captured in the Ebro from 2005 to 2008, together with samples from three other Mediterranean populations (Rhone, Corsica and Adriatic), were analyzed for two mitochondrial genes and six microsatellite loci. Results confirm the Mediterranean origin of A. fallax caught in the Ebro and reveal that it carries some genetic variation typical of Allis shad (A. alosa), suggesting historical introgression between these two closely related species. In addition, the A. fallax population from the Ebro presents a unique genetic composition and unexpectedly high levels of genetic diversity, when compared with the other Mediterranean populations analyzed. These findings raise important doubts on the demographic history of this population and underline the need for further studies to disentangle natural population dynamics from the role of anthropogenic factors on abrupt population fluctuations such as those reported here. The puzzling demographic history of A. fallax from the Ebro not only brings some hope for the recovery of similarly endangered populations but also provides a unique opportunity to study the factors underlying species’ persistence capacity when facing changing environmental conditions.