Polyploid evolution

Work financed by the Austrian Science Fund (FWF) project (Y661-B16) awarded to Ovidiu Paun

Allopolyploidy is an important source of phenotypic diversity and biological novelty. The molecular mechanisms that stabilize the duplicated, hybrid regulatory landscape are not fully clarified, but they shape the eco-physiological properties of allopolyploids and their adaptive success. The frequently cited biased fractionation model gives weight to interactions within and between parental subgenomes as the cause of differential usage and subsequent loss of genetic material following allopolyploid formation. Polyploids often form recurrently, and sibling allopolyploids offer excellent comparative study systems for characterizing the impact of allopolyploidy on cis and trans-regulatory patterns. We study these effects in a pair of widespread, ecologically-divergent, sibling allotetraploid marsh orchids (Dactylorhiza), estimated to have originated independently less than 2000 generations ago. The patterns uncovered in this system offer no clear support for a consistent, directional biased fractionation. However, we find that the subgenome-specific gene expression levels largely overlap between the sibling allotetraploids, reflecting major constraints despite independent origins and ecological divergence. Furthermore, the same genes appear misexpressed and rewired in both allopolyploids, but the patterns observed indicate that cis-trans compensatory regulation does not fully stabilize over thousands of generations after allopolyploidization. Transgressive gene expression, potentially linked to adaptation to non-parental habitats, is exclusively driven by compensatory misregulation that may become adaptive in the allopolyploid background. Our results demonstrate that, in the relatively short evolutionary timescale relevant for the Dactylorhiza system, the contribution of trans-acting regulation is key to individual phenotypic traits between independently-originated, sibling allopolyploids.