The Evolutionary Dynamics of Genetic Incompatibilities Introduced by Duplicated Genes in Arabidopsis thaliana

Abstract

Although gene duplications provide genetic backup and allow genomic changes under relaxed selection, they may potentially limit gene flow. When different copies of a duplicated gene are pseudo-functionalized in different genotypes, genetic incompatibilities can arise in their hybrid offspring. While such cases have been reported after manual crosses, it remains unclear whether they occur in nature and how they affect natural populations. Here we identified four duplicated-gene based incompatibilities including one previously not reported within an artificial Arabidopsis intercross population. Unexpectedly, however, for each of the genetic incompatibilities we also identified the incompatible alleles in natural populations based on the genomes of 1,135 Arabidopsis accessions published by the 1001 Genomes Project. Using the presence of incompatible allele combinations as phenotypes for GWAS, we mapped genomic regions that included additional gene copies which likely rescue the genetic incompatibility. Reconstructing the geographic origins and evolutionary trajectories of the individual alleles suggested that incompatible alleles frequently co-exist, even in geographically closed regions, and that their effects can be overcome by additional gene copies collectively shaping the evolutionary dynamics of duplicated genes during population history.

On the impermanence of species: The collapse of genetic incompatibilities in hybridizing populations

“…In Mimulus , duplicated genes with reciprocal pseudogenization in each species create pseudogene–pseudogene incompatibilities (Zuellig & Sweigart, 2018a ), a special case of the Dobzhansky–Muller model that will typically be unstable to hybridization (Bank et al., 2012 ). In Arabidopsis thaliana , the existence of additional gene copies as rescuers of a known pseudogene–pseudogene incompatibility further increases redundancy and two pseudogenes can co‐exist at arbitrary frequencies within a population (Jiao et al., 2021 ). In other populations of A. thaliana , first‐generation hybrid necrosis was mapped to a large array of dominantly interacting immune‐response genes, which arise via multiple cycles of gene duplication and gene loss (Chae et al., 2014 ).…”

Homozygosity at its Limit: Inbreeding Depression in WildArabidopsis arenosaPopulations

“…In the A. arenosa congener A. thaliana, hybrid necrosis is by far the most common F1 hybrid weakness phenotype observed under laboratory conditions, usually resulting from crosses between individuals from different populations 4 , but other incompatibilities have been observed as well, including single-locus F1 39 , two-locus F1 40 , or two-locus F2 incompatibilities [41][42][43][44][45] . We have found the incidence of abnormal phenotypes in A. arenosa material collected from the wild, and raised in the lab, to be relatively high.…”

A comprehensive benchmark of graph-based genetic variant genotyping algorithms on plant genomes for creating an accurate ensemble pipeline

“…Genetic variants are typically divided into single nucleotide polymorphism (SNP), insertion or deletion (indels, 1–49 bp), and structural variation (SV, ≥ 50 bp, including insertion, deletion, inversion, duplication, translocation, and complex rearrangements) based on their size and type [ 1 , 2 ]. With the advances of high-throughput sequencing technologies, studies such as the 1000 Genomes Project and the Rice 3K Genomes Project have released large amounts of genetic variations, which contribute to the studies of pan-genomes, genome-wide associations, population genetics, and domestication [ 3 – 6 ]. One of the essential requirements for these studies is the rapid and correct genotyping (determination of genotypes) of millions of genetic variations for hundreds or thousands of individuals [ 3 – 6 ].…”