Transposable element abundance subtly contributes to lower fitness in maize

Abstract

Transposable elements (TEs) have long been shown to have deleterious effects on the survival and reproduction of their host organism. As TEs are mobile DNA that jump to new positions, this deleterious cost can occur directly, by inserting into genes and regulatory sequences. Classical population genetic theory suggests copy-number dependent selection against TEs is necessary to prevent TEs from expanding so much they take over a genome. Such models have been difficult to interpret when applied to large genomes like maize, where there are hundreds of thousands of TE insertions that collectively make up 85% of the genome. Here, we use nearly 5000 inbred lines from maize mapping populations and a pan-genomic imputation approach to measure TE content. Segregating TE content gives rise to 100 Mb differences between individuals, and populations often show transgressive segregation in TE content. We use replicated phenotypes measured in hybrids across numerous years and environments to empirically measure the fitness costs of TEs. For an annual plant like maize, grain yield is not only a key agronomic phenotype, but also a direct measure of reproductive output. We find weak negative effects of TE accumulation on grain yield, nearing the limit of the efficacy of natural selection in maize. This results in a loss of one kernel ({approx}0.1% of average per-plant yield) for every additional 14 Mb of TE content. This deleterious load is enriched in TEs within 1 kilobase of genes and young TE insertions. Together, we provide rare empirical measurements of the fitness costs of TEs, and suggest that the TEs we see today in the genome have been filtered by selection against their deleterious consequences on maize fitness.