High pollen immigration but no gene flow via-seed into a Genetic Conservation Unit of the endangered Picea omorika after disturbance

• Disturbance promotes natural regeneration and pollen, but not seed, immigration. • Post-disturbance pollen immigration helps maintaining neutral genetic diversity. • Contrasting spatial genetic patterns are present in cohorts of adults and juveniles. • Gene flow monitoring is crucial to develop conservation plans, in particular in GCUs. • Skewed reproductive success might impact the adaptive potential of forest remnants. Studying how genetic diversity is transmitted between generations is critical for assessing the survival prospects of fragmented forest tree populations. This is especially urgent in the case of rare, endangered species that are at high risk of extinction and/or exceptionally susceptible to climate change, and are thus to be prioritised for conservation initiatives. We performed the first assessment of gene flow patterns by parentage analysis in the IUCN red-listed Serbian spruce [ Picea omorika (Panč.) Purk.], within a Genetic Conservation Unit (GCU) which was exposed to fire disturbance 30 years ago. Parentage analysis was based on assigning the parentage of 104 juveniles to all the adult trees (48) present in the 2.8 ha population. All individuals were genotyped at 11 highly informative nuclear microsatellite markers. We found that fire disturbance triggered natural regeneration, usually poor to absent in Serbian spruce, and boosted pollen immigration (66%), which is reported as rather modest among undisturbed populations of this species. Seed immigration was absent, coherently with what was previously hypothesised for natural, undisturbed populations. Thus, the immigration of new gametes into the studied Serbian spruce population was accomplished exclusively through pollen gene flow, at a rate sufficient to counteract, at least in the short term, genetic drift. Furthermore, the abundant post-disturbance pollen immigration most likely accounts for the lack of fine-scale spatial genetic structure (SGS) in the juvenile cohort, contrary to the SGS observed in the adult cohort which is amongst the strongest ever recorded in anemophilous forest tree species. Finally, as generally found in forest trees, individual reproductive success was uneven among individuals, with 25% of local adults siring 70% of the sampled juveniles. Our results on post-disturbance gene flow patterns in the only Serbian spruce population with reportedly abundant regeneration complement the outcomes of previous genetic studies while providing essential information for the dynamic management and conservation of this rare and endangered species severely threatened by climate warming. Tracking the temporal development of gene flow parameters and the consequences of gene flow on genetic diversity are two cornerstones of future forest genetic monitoring programs, which are particularly important for GCUs. In particular, monitoring the genetic diversity of forest regeneration is deemed as the key for understanding changes that otherwise would remain mostly untraceable in long-lived organisms such as forest trees.