Theory suggests adaptive divergence can proceed in the face of gene flow when adaptive alleles occur in areas of the genome, such as chromosomal inversions, that are protected from recombination, which can break up beneficial allele pairings. In their recent Evolution paper, Twyford and Friedman determine phylogeographic structure and the role of an inversion in the adaptive divergence of life history strategies in the yellow monkey flower, Mimulus guttatus, across northwest North America.
Mimulus gattatus plants employ perennial or annual life history strategies. Perennial plants tend to occur in wetter sites, invest heavily in vegetative growth, and flower later in the season while annual plants occur in drier, drought prone areas and reproduce early in the season. The two ecotypes differ in flowering and senescence time, flower size, and potential to spread clonally, but have overlapping ranges and are fully interfertile. Previous studies found adaptive traits that differ between the perennial and adaptive ecotypes map to a chromosomal inversion that contains hundreds of genes.
Twyford and Friedman used a population genomics approach to 1) clarify the evolutionary relationships between annual and perennial populations of M. guttatus, 2) test whether the chromosomal inversion or some other genomic region(s) are associated with divergence between annual and perennial M. guttatus, and 3) determine the evolutionary history of the chromosomal inversion, specifically, which orientation is derived, how old is the inversion, and how did the inversion spread?
Clustering analyses showed that variation in SNPs across the genome was partitioned according to geography but not life history (panels B and A, respectively, in the figure above, taken from Twyford and Friedman 2015). However SNPs within the chromosomal inversion clearly cluster according to life history and less so with geography (panels C and D). In testing for candidate regions underlying divergence between ecotypes, the authors found that 40% of outlier loci mapped to the inversion, although it represents just 3.5% of genome-wide SNPs (figure below).
In regards to the final aim of the paper, to determine the evolutionary history of the inversion, Twyford and Friedman conclude that it is likely ancient in origin given that sufficient time as passed for the development of a pattern of geographic subdivision within the inversion loci for both ecotypes and the presence of substantial nucleotide diversity within the inversion (i.e. the inversion is old enough to have acquired many mutations).
It seems very unlikely that the inversion is of recent origin, sweeping through existing populations. Instead it seems more likely that the inversion is old, potentially arising early in the origin of the ecotypes, and has subsequently experienced much the same demographic history as the collinear regions of the genome.
Twyford, AD and Friedman, J (2015) Adaptive divergence in the monkey flower Mimulus guttatus is maintained by a chromosomal inversion. Evolution. DOI: 10.1111/evo.12663