Meghan Joanne Brady

Meiotic drivers are selfish genetic elements that gain transmission advantages by distorting equal, Mendelian segregation. For decades, biologists have considered meiotic drivers as interesting, albeit esoteric, case studies. It is now clear, however, that meiotic drive is more common and phylogenetically widespread than previously supposed. Indeed, intensive study of a few well-known cases has begun to reveal the evolutionary genomic consequences of meiotic drive. We argue here that many features of genome evolution, content, and organization that are seemingly inexplicable by organismal adaptation or nearly neutral processes are instead best accounted for by recurrent histories of meiotic drive. We review how meiotic drive can affect the evolution of sequences, gene copy numbers, genes with functions in meiosis and gametogenesis, signatures of “selection,” chromosome rearrangements, and karyotype evolution. We also explore the interactions of meiotic drive elements with other classes of selfish genetic elements, including satellite DNAs, transposable elements, and with the endogenous host genes involved in drive suppression. Finally, we argue that some aspects of drive-mediated genome evolution are now sufficiently well established that we might reverse the direction of discovery—rather than ask how drive affects genome evolution, we can use genome data to discover new putative drive elements.

Meiotic drive elements are regions of the genome that are transmitted to progeny at frequencies that exceed Mendelian expectations, often to the detriment of the organism. In maize there are three prevalent chromosomal drive elements known as Abnormal chromosome 10 (Ab10), K10L2, and the B chromosome. There has been much speculation about how these drivers might interact with each other and the environment in traditional maize landraces and their teosinte ancestors. Here we used genotype-by-sequencing data to score more than 10,000 maize and teosinte lines for the presence or absence of each driver. Fewer than ~0.5% of modern inbred lines carry chromosomal drivers. In contrast, among individuals from 5331 open-pollinated landraces, 6.32% carried Ab10, 5.16% carried K10L2, and 12.28% carried at least one B chromosome. These frequencies are consistent with those reported in previous studies. Using a GWAS approach we identified unlinked loci that associate with the presence or absence of the selfish genetic elements. Many significant SNPs are positively associated with the drivers, suggesting that there may have been selection for alleles that ameliorate their negative fitness consequences. We then assessed the contributions of population structure, associated loci, and the environment on the distribution of each chromosomal driver. There was no significant relationship between any chromosomal driver and altitude, contrary to conclusions based on smaller studies. Our data suggest that the distribution of the major chromosomal drivers is primarily influenced by neutral processes and the deleterious fitness consequences of the drivers themselves. While each driver has a unique relationship to genetic background and the environment, they are largely unconstrained by either.

Meiotic drive elements are regions of the genome that are transmitted to progeny at frequencies that exceed Mendelian expectations, often to the detriment of the organism. In maize there are three prevalent chromosomal drive elements known as Abnormal chromosome 10 (Ab10), K10L2, and the B chromosome. There has been much speculation about how these drivers might interact with each other and the environment in traditional maize landraces and their teosinte ancestors. Here we used genotype-by-sequencing data to score more than 10,000 maize and teosinte lines for the presence or absence of each driver. Less than ∼0.5% of modern inbred lines carry chromosomal drivers. Among individuals from 5331 open-pollinated landraces, 6.32% carried Ab10, 5.16% carried K10L2, and 12.28% carried at least one B chromosome. Using a GWAS approach we identified unlinked loci that associate with the presence or absence of the selfish genetic elements. Many genetic modifiers are positively associated with the drivers, suggesting that there may have been selection for alleles that ameliorate their negative fitness consequences. We then assessed the contributions of population structure, associated loci, and the environment on the distribution of each chromosomal driver. There was no significant relationship between any chromosomal driver and altitude, contrary to conclusions based on smaller studies. Our data suggest that the distribution of the major chromosomal drivers is primarily influenced by neutral processes and the deleterious fitness consequences of the drivers themselves. While each driver has a unique relationship to genetic background and the environment, they are largely unconstrained by either. AUTHOR SUMMARY Meiotic drivers are selfish genetic elements that are transmitted to progeny at frequencies that exceed what is expected by chance. There are three such meiotic drivers in maize known as Ab10, K10L2 and the B chromosome. Prior data indicate that each driver lowers plant fitness to some degree, partially explaining the fact that they are usually observed at low frequencies, but the impact of environment and genetic modifiers has not been investigated. Here we identified the presence or absence of each driver using low coverage sequencing data from over 10,000 maize inbreds, open pollinated landraces, and accessions of teosinte -- the grass-like ancestor of maize. We found that they exist at 5-12% frequencies in open pollinated varieties, but are rare in modern inbreds. We went on to use location data to assess the impact of environmental variables on their distribution, and applied genome-wide association methods to look for genetic modifiers that might contribute to their prevalence. We found that neither the environment nor genetic modifiers have strong influences on the distribution of the three meiotic drive elements, suggesting that their low but consistent frequencies are determined primarily by the fitness consequences of the drivers themselves.

Maize s triate leaves2 ( sr2 ) is a mutant that causes white stripes on leaves that has been used in mapping studies for decades, though the underlying gene has not been identified. The sr2 locus has been previously mapped to small regions of the normal chromosome 10 (N10) and a rearranged variant called Abnormal Chromosome 10 (Ab10). A comparison of assembled genomes carrying N10 and Ab10 revealed only five candidate sr2 genes. Analysis of a stock carrying the sr2 reference allele ( sr2-ref ) showed that one of the five genes has a transposon insertion that disrupts its protein sequence and has a severe reduction in mRNA. An independent Mutator transposon insertion in the gene ( sr2-Mu ) failed to complement the sr2-ref mutation, and plants homozygous for sr2-Mu showed white striped leaf margins. The sr2 gene encodes a DUF3732 protein with strong homology to a rice gene with a similar mutant phenotype called young seedling stripe1 ( yss1 ). These and other published data suggest that sr2 may have a function in plastid gene expression.