Chromosome Evolution Model Reveals Hidden Variation in Fern Diversification Rates

Change in the haploid chromosome number commonly generates reproductive isolation between diverging species. If changes to the haploid chromosome number (karyotype) most often generate new species, variation in the rate of chromosome number evolution is expected to predict variation in diversification rates. While this correlation has been supported in some plants, we know less about how the mode and tempo of karyotype change evolve. Methods to address the evolution of diversification and chromosome number transition rates are computationally expensive and analyses are typically restricted to small clades or avoided all together. We identify and describe variation in the mode and tempo of karyotype evolution (via dysploidy and polyploidy) in the Polypodiales-a species and karyotype-rich order of ferns-by extending the Chromosome Number and Hidden State-dependent Speciation and Extinction model (ChromoHiSSE) to include whole genome duplication. Using the extended ChromoHiSSE model we estimate rates of karyotype evolution across 962 leptosporangiate ferns of the Polypodiales. We recover two hidden modes of chromosome number evolution between which the rates of karyotype evolution differ by more than an order of magnitude. Our rate estimates and the stochastic mapping of these modes across fern evolution suggests lineages with high karyotype lability are less likely to persist in the long-term. These results reinforce the theory that modern fern diversity is shaped substantially by polyploid speciation but challenge the expectation that diversification rates are enhanced by karyotype-driven reproductive isolation.