Historical divergence and gene flow in the genus Zea

Abstract

Gene flow plays a fundamental role in plant evolutionary history, yet its role in population divergence--and ultimately speciation--remains poorly understood. We investigated gene flow and the modalities of divergence in the domesticated Zea mays ssp. mays and three wild Zea taxa using sequence polymorphism data from 26 nuclear loci. We described diversity across loci and assessed evidence for adaptive and purifying selection at nonsynonymous sites. For each of three divergence events in the history of these taxa, we used approximate Bayesian simulation to estimate population sizes and divergence times and explicitly compare among alternative models of divergence. Our estimates of divergence times are surprisingly consistent with previous data from other markers and suggest rapid diversification of lineages within Zea in the last approximately 150,000 years. We found widespread evidence of historical gene flow, including evidence for divergence in the face of gene flow. We speculate that cultivated maize may serve as a bridge for gene flow among otherwise allopatric wild taxa.

Figure 1.—

Geographical distribution of Zea luxurians and the wild subspecies of Z. mays. Circles represent collection locations from herbarium specimens in the Missouri Botanical Garden and approximate the geographic range of these taxa.

Figure 2.—

Schematic representation of the four divergence models tested for each comparison. See text for description of parameters. (A) Isolation. (B) Island. (C) Sympatry. (D) Allopatry.

Figure 3.—

Maximum-likelihood estimates of the population mutation rate θ in four taxa of Zea. Ninety-five percent C.I.'s can be approximated by the intersection of each curve with the horizontal shaded bar at −2.

Figure 4.—

Divergence in Zea. (A) Distribution of pairwise F_ST values between Zea taxa studied. (B) Comparison of proportions of shared (S_S), fixed (S_F), and unique (S_X1 and S_X2) silent sites among pairwise comparisons. MA, maize; ME, mexicana; PA, parviglumis; LU, luxurians.

Figure 5.—

Estimates of γ = 2Ns, based on MKPRF analyses. Solid squares represent point estimates, with shaded bars showing the 95% C.I. of each estimate. A black vertical dashed line represents γ = 0 and gray dashed lines show the interval −1 < γ < 1. Loci adh1 and wx1 had too few sites in luxurians to estimate γ.

Figure 6.—

Site frequency spectra of synonymous and nonsynonymous variants in each taxon. Frequency data have been binned into 10% intervals for plotting.

Figure 7.—

Parameter estimates of the most likely model for each of the three divergence comparisons to parviglumis. Posterior probability distributions are shaded and prior probability distributions are open. The mode of each parameter is given along with its conversion into N or years. Estimates are from the island model for parviglumis–mexicana and from the sympatric model for parviglumis–luxurians and parviglumis–maize (see Table 5).