So, We Meet Again…Gene Expression in Recurrent Origins of the Allopolyploid Fern Polypodium hesperium

Allopolyploid formation is a common mode of speciation in ferns, with many taxa having formed recurrently from multiple, distinct hybridization events between the same parent species. Each hybridization event marks the union of divergent parental gene copies, or homeologs, and the formation of a novel, independently-derived lineage of an allopolyploid taxon.  Little is known about the effects of recurrent origins on genomic composition, phenotypic diversity, and, ultimately, the evolutionary success of allopolyploid ferns.  As an initial attempt to address these questions, we have adopted the allotetraploid fern Polypodium hesperium, derived from the diploid species P. glycyrrhiza and P. amorphum, as a natural model system for investigating gene expression patterns between two independently-derived lineages. Polypodium hesperium has at least two reciprocally-derived lineages, each with disjunct geographic distributions in western North America. We used Illumina sequencing to construct a de novo reference transcriptome and quantify gene expression for three biological replicates of each reciprocal lineage of P. hesperium that we grew in common garden conditions. By surveying the gene expression levels for 19000 genes and homeolog-specific expression for 2000 genes, we discovered that gene expression in both reciprocal lineages of P. hesperium broadly reflects gene expression in P. amorphum—both by mirroring expression levels of P. amorphum and preferentially expressing homeologs derived from P. amorphum. However, despite similar gene expression patterns across the genome, we recovered substantial variation between the two reciprocal lineages in expression levels and homeolog-expression bias of individual genes. Our results suggest that general “rules” may dictate gene expression patterns in allopolyploids, but recurrent origins impart substantial expression, or phenotypic, variation to an allopolyploid taxon.