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ABSTRACT Although the frequency of ancient hybridization across the Tree of Life is greater than previously thought, little work has been devoted to uncovering the extent, timeline, and geographic and ecological context of ancient hybridization. Using an expansive new dataset of nuclear and chloroplast DNA sequences, we conducted a multifaceted phylogenomic investigation to identify ancient reticulation in the early evolution of oaks (Quercus). We document extensive nuclear gene tree and cytonuclear discordance among major lineages ofQuercusand relatives in Quercoideae. Our analyses recovered clear signatures of gene flow against a backdrop of rampant incomplete lineage sorting, with gene flow most prevalent among major lineages ofQuercusand relatives in Quercoideae during their initial radiation, dated to the Early‐Middle Eocene. Ancestral reconstructions including fossils suggest ancestors ofCastanea + Castanopsis,Lithocarpus, and the Old World oak clade probably co‐occurred in North America and Eurasia, while the ancestors ofChrysolepis, Notholithocarpus, and the New World oak clade co‐occurred in North America, offering ample opportunity for hybridization in each region. Our study shows that hybridization—perhaps in the form of ancient syngameons like those seen today—has been a common and important process throughout the evolutionary history of oaks and their relatives. Concomitantly, this study provides a methodological framework for detecting ancient hybridization in other groups. 

ABSTRACT While many plant lineages display remarkable diversity in morphological form, our understanding of how phenotypic diversity, or disparity, arises in relation to genomic evolution over geologic scales remains poorly understood. Here, we investigated the relationship between phenotypic and genomic evolution in the Fagales, a lineage of woody plants that has been a dominant component of temperate and subtropical forests since the Late Cretaceous. We examine newly generated transcriptomic and trait datasets representing most extant genera and a rich diversity of Cretaceous fossil representatives. Our phylogenomic analyses identify recurrent hotspots of gene duplication and genomic conflict across the order. Our phenotypic analyses showed that the morphospace occupied by Fagales was largely filled by the early Cenozoic, and rates of evolution were highest during the early radiation of the Fagales crown and its major families. These results suggest that Fagales conforms to an “early‐burst” model of disparification, with morphospace being filled early in the order's diversification history, and that elevated levels of phenotypic evolution also often correspond to hotspots of gene duplication. Species diversification appears decoupled from patterns of both phenotypic and genomic evolution, highlighting the multidimensional nature of the evolution of plant diversity across geological timescales. 

Chloroplasts and mitochondria each contain their own genomes, which have historically been and continue to be important sources of information for inferring the phylogenetic relationships among land plants. The organelles are predominantly inherited from the same parent, and therefore should exhibit phylogenetic concordance. In this study, we examine the mitochondrion and chloroplast genomes of 226 land plants to infer the degree of similarity between the organelles’ evolutionary histories. Our results show largely concordant topologies are inferred between the organelles, aside from four well-supported conflicting relationships that warrant further investigation. Despite broad patterns of topological concordance, our findings suggest that the chloroplast and mitochondrial genomes evolved with significant differences in molecular evolution. The differences result in the genes from the chloroplast and the mitochondrion preferentially clustering with other genes from their respective organelles by a program that automates selection of evolutionary model partitions for sequence alignments. Further investigation showed that changes in compositional heterogeneity are not always uniform across divergences in the land plant tree of life. These results indicate that although the chloroplast and mitochondrial genomes have coexisted for over 1 billion years, phylogenetically, they are still evolving sufficiently independently to warrant separate models of evolution. As genome sequencing becomes more accessible, research into these organelles’ evolution will continue revealing insight into the ancient cellular events that shaped not only their history, but the history of plants as a whole. 

Evolutionary biologists have long been fascinated with the episodes of rapid phenotypic innovation that underlie the emergence of major lineages. Although our understanding of the environmental and ecological contexts of such episodes has steadily increased, it has remained unclear how population processes contribute to emergent macroevolutionary patterns. One insight gleaned from phylogenomics is that gene-tree conflict, frequently caused by population-level processes, is often rampant during the origin of major lineages. With the understanding that phylogenomic conflict is often driven by complex population processes, we hypothesized that there may be a direct correspondence between instances of high conflict and elevated rates of phenotypic innovation if both patterns result from the same processes. We evaluated this hypothesis in six clades spanning vertebrates and plants. We found that the most conflict-rich regions of these six clades also tended to experience the highest rates of phenotypic innovation, suggesting that population processes shaping both phenotypic and genomic evolution may leave signatures at deep timescales. Closer examination of the biological significance of phylogenomic conflict may yield improved connections between micro- and macroevolution and increase our understanding of the processes that shape the origin of major lineages across the Tree of Life.