Population genetic evidence for rapid changes in intraspecific diversity and allelic cycling of a specialist defense gene in Zea

Abstract

Two patterns of plant defense gene evolution are emerging from molecular population genetic surveys. One is that specialist defenses experience stronger selection than generalist defenses. The second is that specialist defenses are more likely to be subject to balancing selection, i.e., evolve in a manner consistent with balanced-polymorphism or trench-warfare models of host-parasite coevolution. Because most of the data of specialist defenses come from Arabidopsis thaliana, we examined the genetic diversity and evolutionary history of three defense genes in two outcrossing species, the autotetraploid Zea perennis and its most closely related extant relative the diploid Z. diploperennis. Intraspecific diversity at two generalist defenses, the protease inhibitors wip1 and mpi, were consistent with a neutral model. Like previously studied genes in these taxa, wip1 and mpi harbored similar levels of diversity in Z. diploperennis and Z. perennis. In contrast, the specialist defense hm2 showed strong although distinctly different departures from a neutral model in the two species. Z. diploperennis appears to have experienced a strong and recent selective sweep. Using a rejection-sampling coalescent method, we estimate the strength of selection on Z. diploperennis hm2 to be approximately 3.0%, which is approximately equal to the strength of selection on tb1 during maize domestication. Z. perennis hm2 harbors three highly diverged alleles, two of which are found at high frequency. The distinctly different patterns of diversity may be due to differences in the phase of host-parasite coevolutionary cycles, although higher hm2 diversity in Z. perennis may also reflect reduced efficacy of selection in the autotetraploid relative to its diploid relative.

Figure 1.—

Maximum likelihood estimates of θ, derived from apparently neutrally evolving genes in Z. diploperennis and Z. perennis. Arrows indicate the estimates of θ at Hm2, which was not used in making the likelihood estimates. The horizontal line marks the 95% credibility interval. hm2 (red) was calculated after removing the per7b sequence from the Z. perennis data.

Figure 2.—

The hm2 exon-intron structure and sequences from Z. diploperennis and Z. perennis. The shaded regions represent exons, the position of polymorphic sites is shown at the top, and dashes indicate indels.

Figure 3.—

Results of selective sweep simulations and rejection sampling. (A) Sample from the posterior distribution of T, the time of the fixation event, based on hm2 and adh1 data (based on 10,000 and 6781 simulations, respectively). (B) The joint posterior distribution of T and the selection coefficient s of the favored allele. Shading represents the frequency of simulated data sets; black > 1.0% data sets, 1.0% > dark gray > 0.5%, 0.5% > light gray > 0.0%, white = 0.0%.

Figure 4.—

Hypothetical dynamics of three defense alleles coevolving with parasite avirulence alleles (after Seger 1990). Hm2 may exhibit very low diversity in Z. diploperrenis because it has been the object of a recent selective sweep (up arrow). Two common alleles may be present in Z. perennis because each has recently increased in frequency (down arrows).