Is there a correlation between chloroplastic and nuclear divergence or what are the roles of history and selection on genetic diversity in European oaks?

Abstract

The aim of this work was to investigate whether a correlation exists between maternal lineage, assessed by variation in maternally inherited chloroplast DNA (cpDNA) and nuclear controlled variation (phenotypic traits and gene markers). Variation in cpDNA and nuclear controlled traits (62 phenotypic traits, eight isozyme and 31 RAPD loci) was studied in deciduous oak trees (mostly Q. petraea) growing in 16 provenance tests. Results from two nuclear diversity studies were also included. The test for correlation was performed using two methods by: (1) comparing provenance mean values (or allele frequencies) among different lineages using ANOVA, (2) making pairwise comparisons of chloroplastic genetic distances (CGDs) with phenotypic differentiation index (DI) (or nuclear genetic distances (GD)) among all provenances using the Mantel test. Among the 62 phenotypic traits, only seven exhibited significant associations with maternal lineages when tested using ANOVA (six using Mantel test). This number decreased to two once correction for geographic distance was introduced in the calculation for Mantel test. There were stronger correlations between maternal lineage and nuclear gene markers. The existence of cytonuclear disequilibrium was shown by the significant differences in allozyme frequencies between the four maternal lineages (at least one allele for each locus). These associations were confirmed by significant correlations between CGD and GD. Finally associations were also found between levels of diversity in nuclear markers and maternal lineages. These results are discussed in the context of the glacial and postglacial history of oak populations in Europe. The analysis suggests that the processes which led to the current structure of chloroplastic diversity and variation for phenotypic traits can be subdivided into four major phases. (1) During the last long glacial period, deciduous oaks were probably confined to three major refugia which were genetically differentiated for chloroplastic and nuclear genes. (2) At the end of the glacial period, oaks migrated northwards and established a spatial pattern of distribution for chloroplastic genes which remains largely intact to this day. (3) As oaks progressively occupied the mid and northern parts of Europe, pollen flow established communication between stands originating from eastern and western refugia. This resulted in the gradual erosion of the original nuclear differentiation while conserving the chloroplastic variation installed during colonization. (4) Local selection pressures acting on the established populations eventually caused their genetic differentiation gradually to increase with time. New patterns of differentiation now exist which are totally different from those in place immediately following colonization. During this time, chloroplastic divergence remained unchanged. These processes led to the loss of any association between chloroplastic divergence and phenotypic traits, although some association with gene markers which are less affected by selection has been retained. © 2002 Elsevier Science B.V. All rights reserved.