Speciation and introgression between Mimulus nasutus and Mimulus guttatus

Abstract

Mimulus guttatus and M. nasutus are an evolutionary and ecological model sister species pair differentiated by ecology, mating system, and partial reproductive isolation. Despite extensive research on this system, the history of divergence and differentiation in this sister pair is unclear. We present and analyze a population genomic data set which shows that M. nasutus budded from a central Californian M. guttatus population within the last 200 to 500 thousand years. In this time, the M. nasutus genome has accrued genomic signatures of the transition to predominant selfing, including an elevated proportion of nonsynonymous variants, an accumulation of premature stop codons, and extended levels of linkage disequilibrium. Despite clear biological differentiation, we document genomic signatures of ongoing, bidirectional introgression. We observe a negative relationship between the recombination rate and divergence between M. nasutus and sympatric M. guttatus samples, suggesting that selection acts against M. nasutus ancestry in M. guttatus.

Figure 1. Relationships among Mimulus samples.

A) A map of all samples with identity and species denoted by population code and color, respectively. M. guttatus individuals are colored in blues and purples, and M. nasutus is colored in oranges and reds. Approximate species distribution boundaries are shown for M. guttatus with the purple dashed line and for M. nasutus with the solid pink line. Sympatric samples are marked by lines originating in the same location. B) A neighbor-joining tree for all samples rooted by M. dentilobous. Sample and species colors are identical to those in 1A. The consensus tree was constructed from the pairwise distance matrix described in the main text with the nj function in the R package, ape, and smoothed with the function, chronopl, with λ = 1, an implementation of Sanderson's nonparametric rate smoothing program, r8s . The distribution of trees is plotted using densitree as implemented in the R package, phangorn . Each of the one thousand trees is a resampling of the 14,000 SNPs with replacement. All of the 14,000 trees support a strong split between northern and southern groups. The one exception is LMC, a California sample that clusters with southern and northern M. guttatus in 542 and 458 of the 1,000 bootstrapped trees, respectively. C) A principle component analysis of these data, excluding M. dentilobus. D) The mean number of pairwise sequence differences per fourfold degenerate site (π_S) within and among Mimulus species and populations, including uncertainty via a block bootstrap. E) Demographic history as inferred by the PSMC. Inferred population size through time is shown for pairwise combinations of haploid genomes of M. guttatus and/or M. nasutus individuals. Black/gray = interspecific comparisons with allopatric M. guttatus. Blue and violet = intraspecific M. guttatus comparisons. Red = intraspecific M. nasutus. For each pair-wise comparison, the thick dark line represents the point inference and each lighter-colored, thin line represents 1 of 100 bootstraps (see Text S1).

Figure 2. Genomic consequences of the transition to selfing.

A) A histogram of pairwise sequence diversity (π) within and between species in overlapping 5 kb windows. For interspecific comparisons we focus only on allopatric M. guttatus populations. The dotted line denotes π_S<0.5% or 170 ky of divergence. B) Moving along a part of chromosome two, for all M. nasutus samples, we color genomic regions in which the focal individual (y-label) and another M. nasutus sample, indicated by color, recently coalesce (π_S≤0.5%). White regions coalesce more distantly in the past (π_S>0.5%) and gray regions indicate insufficient density of informative sites. Major tick-marks on the x-axis indicate 1 megabase. C) Linkage disequilibrium (measured as r²) within M. nasutus (red) and M. guttatus (blue), as a function of physical distance. D) The number of premature stop codons observed in one, two, three, or four M. nasutus (red) and M. guttatus (blue) samples.

Figure 3. Introgression of M. nasutus material into M. guttatus.

A) Treemix suggests introgression from M. nasutus in to sympatric M. guttatus samples. B) A histogram of interspecific pairwise sequence divergence in 5 kb windows for each M. guttatus sample. C) Introgression across a chromosome - Moving along a part of chromosome two for all M. guttatus samples, we color genomic regions in which the focal individual (y-label) and a M. nasutus sample, indicated by color, recently coalesce (π_S≤0.5%). White regions coalesce more distantly in the past (π_S>0.5%) and gray regions indicate insufficient density of informative sites. Major tick marks on the x-axis indicate 1 megabase. Purple bars above each focal individual denote greater than a 95% posterior probability of M. nasutus ancestry as inferred from our HMM. D) Admixture block length distribution - The number of admixed blocks, as inferred by a greater than 95% posterior probability of M. nasutus ancestry from our HMM, longer than x. The expected exponential distribution is marked with a dotted line.