Divergent population structure and climate associations of a chromosomal inversion polymorphism across the Mimulus guttatus species complex

Abstract

Chromosomal rearrangement polymorphisms are common and increasingly found to be associated with adaptive ecological divergence and speciation. Rearrangements, such as inversions, reduce recombination in heterozygous individuals and thus can protect favourable allelic combinations at linked loci, facilitating their spread in the presence of gene flow. Recently, we identified a chromosomal inversion polymorphism that contributes to ecological adaptation and reproductive isolation between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus. Here we evaluate the population genetic structure of this inverted region in comparison with the collinear regions of the genome across the M. guttatus species complex. We tested whether annual and perennial M. guttatus exhibit different patterns of divergence for loci in the inverted and noninverted regions of the genome. We then evaluated whether there are contrasting climate associations with these genomic regions through redundancy analysis. We found that the inversion exhibits broadly different patterns of divergence among annual and perennial M. guttatus and is associated with environmental variation across population accessions. This study is the first widespread population genetic survey of the diversity of the M. guttatus species complex. Our findings contribute to a greater understanding of morphological, ecological, and genetic evolutionary divergence across this highly diverse group of closely related ecotypes and species. Finally, understanding species relationships among M. guttatus sp. has hitherto been stymied by accumulated evidence of substantial gene flow among populations as well as designated species. Nevertheless, our results shed light on these relationships and provide insight into adaptation in life history traits within the complex.

Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus

“…Nevertheless, M. guttatus and M. nudatus are strongly reproductively isolated. Field experiments, as well as microsatellite and genomic sequencing data suggest that introgression between these species is rare (Gardner & Macnair, 2000; Oneal et al ., 2014; L. Flagel, unpublished data). Few if any seeds of round appearance are produced from crosses between M. guttatus and M. nudatus .…”

“…Seed inviability is a common outcome of crosses between members of the M. guttatus species complex, a highly diverse group of populations, ecotypes and species distributed across western North America (Vickery, 1966, 1978). M. guttatus , also a diploid, is the most geographically widespread and genetically diverse member of the complex (Wu et al ., 2007; Oneal et al ., 2014), and exhibits varying interfertility with other members of the complex (Vickery, 1978; Wu et al ., 2007), however, hybridization between closely related species within the complex is frequently accompanied by varying levels of hybrid seed failure (Vickery, 1978). …”

“…While the diploid, edaphic endemic M. nudatus is likely recently derived from a M. guttatus -like ancestor (Oneal et al ., 2014), this species pair exhibits the highest level of sequence divergence of any within the M. guttatus sp. complex (~3% genomic sequence divergence; L. Flagel, pers.…”

Genomics of invasion: diversity and selection in introduced populations of monkeyflowers (Mimulus guttatus)

“…Instead, these selective sweeps are located near or at a known inversion region of ~6 Mb in length (Oneal et al . ). This inversion ( DIV1 ) is polymorphic in the native range and is associated with a number of morphological and life history differences between annual and perennial ecotypes (Lowry & Willis ).…”

“…Previous molecular analyses of M. guttatus have demonstrated that a scattered sampling design, with one individual per population, is sufficient to capture regional differentiation and can avoid clustering biases resulting from sampling multiple individuals from fewer populations (Oneal et al . ). In total, we analysed genome data from 27 populations: 12 M. guttatus populations in the native range, 10 UK M. guttatus and five out‐groups.…”