5S‐IGS rDNA in wind‐pollinated trees (Fagus L.) encapsulates 55 million years of reticulate evolution and hybrid origins of modern species

Abstract

SUMMARY Standard models of plant speciation assume strictly dichotomous genealogies in which a species, the ancestor, is replaced by two offspring species. The reality in wind‐pollinated trees with long evolutionary histories is more complex: species evolve from other species through isolation when genetic drift exceeds gene flow; lineage mixing can give rise to new species (hybrid taxa such as nothospecies and allopolyploids). The multi‐copy, potentially multi‐locus 5S rDNA is one of few gene regions conserving signal from dichotomous and reticulate evolutionary processes down to the level of intra‐genomic recombination. Therefore, it can provide unique insights into the dynamic speciation processes of lineages that diversified tens of millions of years ago. Here, we provide the first high‐throughput sequencing (HTS) of the 5S intergenic spacers (5S‐IGS) for a lineage of wind‐pollinated subtropical to temperate trees, the Fagus crenata – F. sylvatica s.l. lineage, and its distant relative F. japonica. The observed 4963 unique 5S‐IGS variants reflect a complex history of hybrid origins, lineage sorting, mixing via secondary gene flow, and intra‐genomic competition between two or more paralogous‐homoeologous 5S rDNA lineages. We show that modern species are genetic mosaics and represent a striking case of ongoing reticulate evolution during the past 55 million years.

Tracing the origin of Oriental beech stands across Western Europe and reporting hybridization with European beech – implications for assisted gene flow

“…No reuse allowed without permission. European and Oriental beech would hybridize because the two subspecies are known to hybridize in their natural contact zone in the Southeastern Balkans (Cardoni et al, 2021;Müller et al, 2019). Further, since European beech starts to reproduce at the age of 40-50 years (Houston Durrant et al, 2016), we expected that we would principally find F1 hybrids, but also possibly backcrosses given the age of 100 years of the studied stands.…”

Complex Scenarios of Reticulation, Polyploidization, and Species Diversity within Annual Pansies of Subsect. Bracteolatae (Viola Sect. Melanium, Violaceae) in Italy: Insights from 5S-IGS High-Throughput Sequencing and Plastid DNA Variation

“…The generated 5S-HTS sequences grouped in a variable number of high-supported (70–100% BS) major clusters in each sample. The number of the clusters identifies different intra-individual lineages and could be related with the number of 5S loci occurring in each sample [ 54 ]. In agreement, the four samples of V. tricolor displayed a variable number of major clusters (three clusters in sample T8; three clusters and a single high-diverging variant in sample T6; four clusters in samples T2 and T9), perfectly matching the ‘six to eight 5S rDNA signals on six chromosomes’ detected in different V. tricolor populations across Europe with FISH [ 55 ].…”

“…The short non-transcribed intergenic spacer of the 5S nuclear ribosomal RNA gene array is the most-divergent nuclear marker known today, e.g., [ 50 , 66 , 67 , 68 , 69 , 70 ]. More interestingly, due to its extreme inter-individual and intra-genomic variability, the multi-copy, potentially multi-locus, 5S rDNA has the potential to store signals from reticulate evolutionary processes and intra-genomic recombination, thus allowing the detection of diversity patterns and evolutionary inferences of complex species systems, e.g., [ 52 , 53 , 54 , 71 ].…”

“…In agreement with high ploidy in these taxa, the major 5S-IGS sequence clusters and the multiple sub-clusters obtained with the phylogenetic analyses ( Figure 4 and Figure 5 ) subtend the occurrence of different 5S ribosomal lineages in all investigated species. This pattern can be explained with both intra-locus and intra-genomic (multiple loci on different chromosomes) variation [ 54 ], but the number of identified sequence lineages may not directly reflect the number of 5S rDNA loci or chromosome numbers (and the ploidy level) of the investigated species owing to gene-level processes such as homogenization by concerted evolution and genome-level processes such as those following auto- or allopolyploidization, hybridization, and introgression [ 53 ]. However, the three to four 5S-IGS sequence clusters retrieved in V. tricolor ( Figure 4 and Figure 5 ) find a perfect match with the three/four 5S rDNA loci identified in different populations of this species with FISH [ 55 ].…”

“…Several studies have shown that the detected variation may result in the identification of species-specific traits and complex evolutionary signals such as hybridization, introgression, and polyploidization, e.g., [ 50 , 51 , 52 ]. A couple of recent studies have generated HTS amplicon data of the nuclear 5S spacers to improve the efficiency of signal detection and demonstrated the high potential of the technique to inspect diversity patterns and infer evolutive pathways in highly complex species systems such as Fagaceae Dumort [ 53 , 54 ].…”