The evolution of sex chromosomes is usually considered to be driven by sexually antagonistic selection in the diploid phase. However, selection during the haploid gametic phase of the lifecycle has recently received theoretical attention as possibly playing a central role in sex chromosome evolution, especially in plants where gene expression in the haploid phase is extensive. In particular, male‐specific haploid selection might favor the linkage of pollen beneficial alleles to male sex determining regions on incipient Y chromosomes. This linkage might then allow such alleles to further specialize for the haploid phase. Purifying haploid selection is also expected to slow the degeneration of Y‐linked genes expressed in the haploid phase. Here, we examine the evolution of gene expression in flower buds and pollen of two species of Rumex to test for signatures of haploid selection acting during plant sex chromosome evolution. We find that genes with high ancestral pollen expression bias occur more often on sex chromosomes than autosomes and that genes on the Y chromosome are more likely to become enriched for pollen expression bias. We also find that genes with low expression in pollen are more likely to be lost from the Y chromosome. Our results suggest that sex‐specific haploid selection during the gametophytic stage of the lifecycle may be a major contributor to several features of plant sex chromosome evolution.
Causal mutations and their frequency in agricultural fields are well-characterized for herbicide resistance. However, we still lack understanding of their evolutionary history: the extent of parallelism in the origins of target-site resistance (TSR), how long these mutations persist, how quickly they spread, and allelic interactions that mediate their selective advantage. We addressed these questions with genomic data from 18 agricultural populations of common waterhemp (Amaranthus tuberculatus), which we show to have undergone a massive expansion over the past century, with a contemporary effective population size (Ne) estimate of 8x107. We found variation at seven characterized TSR loci, two of which had multiple amino acid substitutions, and three of which were common. These three common resistance variants show parallelism in their mutational origins, with gene flow having shaped their distribution across the landscape. Allele age estimates supported a strong role of adaptation from de novo mutations, with a median allele age of 30 suggesting that most resistance alleles arose soon after the onset of herbicide use. However, resistant lineages varied in both their age and evidence for selection over two different timescales, implying considerable heterogeneity in the forces that govern their persistence. The evolutionary history of TSR has also been shaped by both intra- and inter-locus allelic interactions. We report a signal of extended haplotype competition between two common TSR alleles, and extreme linkage with genome-wide alleles with known functions in resistance adaptation. Together, this work reveals a remarkable example of spatial parallel evolution in a metapopulation, with important implications for the management of herbicide resistance.
Whether deleterious mutations affect fitness independently, or synergistically, remains an open question in evolutionary genetics. Previous work by Sohail et al. (2017) reported an abundance of negative linkage disequilibrium (LD) values among loss-of - function (LOF) mutations in several human and fruit fly datasets, a pattern the authors interpreted as evidence of negative synergistic epistasis. Here we re-visit this question in a population genomic dataset of plants (Capsella grandiflora), and a fruit fly (Drosophila melanogaster) dataset previously used by Sohail et al. When using synonymous sites as a control, as Sohail et al., we find that both species have significantly less positive LD at LOF sites than synonymous sites. However, LD is not significantly different from 0 for LOF mutations but is significantly positive for synonymous mutations in both species. We question the use of synonymous sites as an appropriate control when attempting to make inferences about LD at selected sites. We use simulations to show how admixture or mating bias towards physically proximal individuals can cause positive LD to build up among neutral mutations but has a much weaker effect on selected sites, regardless of the presence of epistasis. Finally, we use information from published biological networks to explore whether there is evidence for negative synergistic epistasis between interacting radical missense mutations. We report no significant enrichment for negative inter-network LD in C. grandiflora. However, we note a modest but significant enrichment of negative LD in D. melanogaster networks, suggestive of intra-network negative synergistic epistasis in this species.
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