A Model for Divergent, Allopatric Speciation of Polyploid Pteridophytes Resulting from Silencing of Duplicate-Gene Expression

We present a model for allopatric speciation at the polyploid level, based on different patterns of gene silencing that would occur in geographically isolated populations. Allopatric populations of a single allotetraploid species may experience silencing of the same gene but in different genomes (reciprocal silencing). Hybrids between such genotypes would experience a reduction in viability of gametophyte progeny to 0.75n, where n is the number of reciprocally silenced homoeologous gene pairs. A minimum value of n ≥ 8, representing a maximum hybrid fertility of 0.10, is shown to be virtually certain when the proportion of genes silenced reaches 0.2. Gene silencing would also lead to genetic divergence between the populations. Silencing of regulatory genes could lead to significant interpopulational differences in morphology and other complex traits. It is predicted that the combined effect of postzygotic hybrid sterility and genetic divergence resulting from gene silencing might lead to speciation of allopatric populations even in the absence of strong selection. It is also predicted that such speciation events would be relatively rapid, because they are driven by the most frequent class of mutations, and only a fraction of the genome needs to be silenced for speciation to occur. Criteria are provided for evaluating whether this mode of speciation has occurred in nature.