Quaternary population dynamics of an endemic conifer, Picea omorika, and their conservation implications

Serbian spruce, Picea omorika (Pan?.) Purk., is a cold-adapted conifer confined to an area of c. 10,000 km² within the Balkans. This area, which has not been exposed to severe anthropogenic disturbances in the recent past, represents a long-term cryptic refugium of this species. We studied Quaternary dynamics of fragmentary distributed Serbian spruce populations to uncover genetic and demographic processes accounting for high levels of genetic diversities in this endemic species within its long-term cryptic refugium. Based on our data set [499 trees from ten populations, five nuclear microsatellites (EST-SSRs) and a mitochondrial (mtDNA) locus], we found the following: (i) continuous increase of genetic distinctiveness of populations caused by various genetic and/or demographic processes, (ii) decreasing over generations pollen flow, and (iii) almost complete lack of seed flow, are trends applicable not only for post-glacial but also for glacial populations. As a result, populations distant few kilometers or less were poorly connected and highly differentiated (nuclear DNA: average ρ _ST , Hedrick’s G′ _ST and Jost’s D of 0.165, 0.429 and 0.385, respectively; mtDNA: G _ST  = 0.632). They were characterized as independent gene pools at the nuclear DNA level. Nonetheless, levels of genetic diversity were high at both nuclear (average allelic richness = 16.14; average H _E  = 0.776) and mtDNA (H _T  = 0.231) levels. They were maintained not by pronounced gene flow but rather by frequent admixtures of highly differentiated populations, and also by species longevity and overlapping generations in the populations. However, admixtures had been possible only if populations encountered each other over time. Particular genetic and/or demographic changes of populations, such as fragmentations, admixture, size reductions/expansions and extinctions, could not be associated exclusively neither to the post-glacial nor to the last glacial as they were detected during both periods. In accordance with expectations on range alternations in cold-adapted taxa confined to refugia during warm Quaternary periods, our study species was expanding range during the last glacial and contracting range post-glacially. Recommendations for conservation of this IUCN red-listed, endemic and relict species have been provided.