Genomics of evolutionary novelty in hybrids and polyploids

It has long been recognized that hybridization and polyploidy are prominent processes in plant evolution. Although classically recognized as significant in speciation and adaptation, recognition of the importance of interspecific gene flow has dramatically increased during the genomics era, concomitant with an unending flood of empirical examples, with or without genome doubling. Interspecific gene flow is thus increasingly thought to lead to evolutionary innovation and diversification, via adaptive introgression, homoploid hybrid speciation and allopolyploid speciation. Less well understood, however, are the suite of genetic and genomic mechanisms set in motion by the merger of differentiated genomes, and the temporal scale over which recombinational complexity mediated by gene flow might be expressed and exposed to natural selection. We focus on these issues here, considering the types of molecular genetic and genomic processes that might be set in motion by the saltational event of genome merger between two diverged species, either with or without genome doubling, and how these various processes can contribute to novel phenotypes. Genetic mechanisms include the infusion of new alleles and the genesis of novel structural variation including translocations and inversions, homoeologous exchanges, transposable element mobilization and novel insertional effects, presence-absence variation and copy number variation. Polyploidy generates massive transcriptomic and regulatory alteration, presumably set in motion by disrupted stoichiometries of regulatory factors, small RNAs and other genome interactions that cascade from single-gene expression change up through entire networks of transformed regulatory modules. We highlight both these novel combinatorial possibilities and the range of temporal scales over which such complexity might be generated, and thus exposed to natural selection and drift.This study was supported by the grants CGL2017-88500-P (AEI/FEDER, EU) to GN and AGL2016-78992-R to JC from the Spanish Ministry of Economy and Competitivity, as well as Severo Ochoa Program for Centers of Excellence in R&D 2016–2020 (SEV-2015-0533) to JC, and by grants from the National Science Foundation to JW.Peer reviewe