Deleterious Mutations Accumulate Faster in Allopolyploid Than Diploid Cotton (Gossypium) and Unequally between Subgenomes

Abstract

Whole genome duplication (polyploidization) is among the most dramatic mutational processes in nature, so understanding how natural selection differs in polyploids relative to diploids is an important goal. Population genetics theory predicts that recessive deleterious mutations accumulate faster in allopolyploids than diploids due to the masking effect of redundant gene copies, but this prediction is hitherto unconfirmed. Here, we use the cotton genus (Gossypium), which contains seven allopolyploids derived from a single polyploidization event 1-2 million years ago, to investigate deleterious mutation accumulation. We use two methods of identifying deleterious mutations at the nucleotide and amino acid level, along with whole-genome resequencing of 43 individuals spanning six allopolyploid species and their two diploid progenitors, to demonstrate that deleterious mutations accumulate faster in allopolyploids than in their diploid progenitors. We find that, unlike what would be expected under models of demographic changes alone, strongly deleterious mutations show the biggest difference between ploidy levels, and this effect diminishes for moderately and mildly deleterious mutations. We further show that the proportion of nonsynonymous mutations that are deleterious differs between the two co-resident subgenomes in the allopolyploids, suggesting that homoeologous masking acts unequally between subgenomes. Our results provide a genome-wide perspective on classic notions of the significance of gene duplication that likely are broadly applicable to allopolyploids, with implications for our understanding of the evolutionary fate of deleterious mutations. Finally, we note that some measures of selection (e.g. dN/dS, πN/πS) may be biased when species of different ploidy levels are compared.

Global Patterns of Subgenome Evolution in Organelle-Targeted Genes of Six Allotetraploid Angiosperms

“…This is especially true for the older allopolyploids (i.e., cotton, wheat, and quinoa). Importantly, we expected that the subgenome with the more closely related diploid model (i.e., lower d S ) would exhibit artificially inflated d N (and therefore ω ) relative to the other subgenome due to the persistence of slightly deleterious changes, as well as the masking effect acting on recessive deleterious changes in the allopolyploids ( Conover and Wendel 2021 ). This is indeed the case for wheat, cotton, and tobacco, in which the subgenome with the more closely related diploid progenitor ( fig.…”

“…6 ). This potentially indicates that the species of higher ploidy may inherently have higher ω due to mutations at phylogenetically conserved sites accumulating more rapidly in the polyploid subgenomes as a result of mutational masking ( Conover and Wendel 2021 ). The extent to which the evolutionary trajectory of polyploid lineages is affected by the accelerated accumulation of deleterious mutations, therefore, represents an important open question in plant biology.…”

Retrieving a disrupted gene encoding phospholipase A for fibre enhancement in allotetraploid cultivated cotton

“…Notably, after polyploidization/ whole-genome duplication (WGD), some of the redundant genes were lost over the course of a few million years (Lynch and Conery, 2000). The most recent evolutionary analysis on the Gossypium genus reported that disrupted genes, also termed genes with deleterious mutations, have accumulated faster in allotetraploid cotton than in diploid species (Conover and Wendel, 2022). However, the precise effects of these disrupted genes on fibre traits have yet to be elucidated.…”

Evolutionary origin and establishment of a dioecious diploid‐tetraploid complex

“…For the diploid W1 and E, the difference in diversity could be the results of refugia preservation during past repeated glaciations in the western mountains and degraded habitat in the east. Higher diversity in W2 may be due to genome duplication because tetraploids can have up to four alleles and hence a greater capacity to mask recessive mutations than diploid populations, and also to accumulate more neutral mutations (Bever & Felber, 1992; Conover & Wendel, 2022; Hill, 1970). Gene exchange with other species could also contributed to its diversity (Figure 3a; Figure S9).…”