The latitudinal trend in genetic diversity and distinctiveness ofQuercus roburrear edge forest remnants calls for new conservation priorities

Abstract

Knowledge of the spatial distribution of intraspecific genetic variation is essential for conserving biodiversity, designing rational networks of protected areas, and informing translocation strategies. Although the Italian peninsula likely harbours unique genetic variation as a legacy of Quaternary migrations towards southern Europe, few genetic data are available for many Italian forest tree species and populations.Here, we present the first, comprehensive characterisation of the nuclear genetic variation of Italian populations of pedunculate oak (Quercus roburL.), an iconic broadleaved species of lowland forests. A total of 745 individuals from 25 populations were sampled across the local range of the species and genotyped with 16 microsatellite markers. The genetic layout ofQ. roburpopulations was assessed through various metrics of diversity and distinctiveness, as well as by Bayesian clustering and multivariate methods. Based on the inferred genetic structure, the demographic history ofQ. roburgene pools was evaluated through Approximate Bayesian Computation (ABC) analysis.We found a clear spatial trend in the estimates of genetic diversity and distinctiveness of ItalianQ. roburpopulations. The genetic distinctiveness and private allelic richness values showed a linear decline with increasing latitude, while allelic richness reached its peak in central Italy. We also observed a south-to-north trend in the complexity of genetic structure, with peninsular Italy being characterised by a mosaic of gene pools, in contrast to the homogeneity exhibited by northern Italian populations. Demographic inference indicated that the southern gene pool has had separate dynamics for the last 135,000 years and, therefore, populations in central Italy did not originate from a northward migration route after the Last Glacial Maximum (LGM). Therefore, they were not only a ‘melting pot’ of multiple recolonization routes, but most likely a mosaic of small refugia where pedunculate oak persisted during the LGM.Our results shed new light on conservation priorities for highly fragmentedQ. roburpopulations, and call for consideration of whether treating the southern and central Italian populations as independent conservation units, or intervening to increase their genetic connectivity, is the best strategy for their long-term conservation.

Spatial conservation planning of forest genetic resources in a Mediterranean multi-refugial area

“…The Pan-European network of genetic conservation units (Lefèvre et al, 2013; http://portal.eufgis.org/) shows a better agreement with our SCP analyses. For instance, the southernmost Q. robur population, which represents a unique genetic lineage and nowadays consists of only 64 individuals (Avanzi et al, 2023), is recognized as a genetic conservation unit but not as a seed stand. In addition, despite the absence of seed stands, a genetic conservation unit for P. heldreichii was established in a 166-ha area of the Pollino National Park that includes five of the irreplaceable sites identified in our analysis.…”

“…The other genetic parameters tested were not related to genetic irreplaceability, except for Ne in pedunculate oak, where high GI sites display a significantly lower Ne than low GI sites. This finding may suggest the use of genetic irreplaceability in combination with Ne to simultaneously locate priority sites for IGD conservation and evaluate their genetic health status, especially when dealing with highly fragmented populations as in the case of pedunculate oak in Italy (Avanzi et al, 2023). Rapidly shrinking populations in an area characterised by a strong genetic structure may explain the occurrence of high private allelic richness in sites with low Ne (see, for example, the case of the ‘Foglino’ and ‘Bosco Pantano’ sites in central and southern Italy, where PAr is high and Ne ranges from 27 to 81; Supplementary Table 2 ).…”

“…Contrary to what is observed in other refugial areas, ‘Bosco Pantano’ is genetically depauperate, with extremely low allelic diversity and effective population size ( Ne <100) due to recent intensive human impact. The high irreplaceability of this site may rather reflect its extremely large genetic distinctiveness and the presence of private alleles (Avanzi et al, 2023). Similar to our findings, Beridze et al (2023) have also recently shown that sites within refugial areas of Castanea sativa deserve high conservation priority.…”

“…The majority of A. alba and Q. robur populations are within National and Regional Parks, or public Reserves. Nonetheless, some irreplaceable sites for Q. robur are located on private property without any protection regime (e.g., the site with the highest genetic diversity in Italy; see Avanzi et al, 2023). Our results can contribute to change the protection status of such stands or to raise awareness among private owners toward a correct management of forest genetic resources.…”

“…The correlation between D A and GI only found in A. alba may reflect the peculiar spatial genetic structure observed in this species, where highly differentiated genetic clusters were described as separated by a steep genetic barrier in central Apennines (Piotti et al, 2017). In contrast, low levels of differentiation and extensive gene flow have been described in both P. heldreichii populations (Piovesan et al, 2023) and Q. robur , particularly across the Po plain in northern Italy (Avanzi et al, 2023). This finding suggests the potential usefulness of relying on both PAr and D A in priority setting when demographic inference supports the occurrence of moderate to high genetic differentiation between sites (e.g., when F ST >0.1).…”