Abstract
While the vast majority of genome size variation in plants is due to differences in repetitive sequence, we know little about how selection acts on repeat content in natural populations. Here we investigate parallel changes in intraspecific genome size and repeat content of domesticated maize (Zea mays) landraces and their wild relative teosinte across altitudinal gradients in Mesoamerica and South America. We combine genotyping, low coverage whole-genome sequence data, and flow cytometry to test for evidence of selection on genome size and individual repeat abundance. We find that population structure alone cannot explain the observed variation, implying that clinal patterns of genome size are maintained by natural selection. Our modeling additionally provides evidence of selection on individual heterochromatic knob repeats, likely due to their large individual contribution to genome size. To better understand the phenotypes driving selection on genome size, we conducted a growth chamber experiment using a population of highland teosinte exhibiting extensive variation in genome size. We find weak support for a positive correlation between genome size and cell size, but stronger support for a negative correlation between genome size and the rate of cell production. Reanalyzing published data of cell counts in maize shoot apical meristems, we then identify a negative correlation between cell production rate and flowering time. Together, our data suggest a model in which variation in genome size is driven by natural selection on flowering time across altitudinal clines, connecting intraspecific variation in repetitive sequence to important differences in adaptive phenotypes.
Highlights
Genome size varies many orders of magnitude across species, due to both changes in ploidy as well as haploid DNA content [1, 2]
We used low-coverage whole-genome sequencing mapped to reference repeat libraries to estimate the abundance of repetitive sequences in each individual with estimated genome size, and validated this approach by comparing sequence-based estimates of heterochromatic knob abundance to fluorescence in situ hybridization (FISH) data from mexicana populations (Fig 2 and S4 Fig; see Methods for details)
In support of the hypothesis that smaller genomes may enable more rapid development, our leaf elongation model indicates a negative correlation between genome size and cell production rate in our highland teosinte population. Though these results showed strong prior sensitivity, the sign of the relationship between genome size and cell production rate did not change for prior mean values of leaf elongation rate within the range of those published for maize, all equal to or larger than the rates observed in our experiment
Summary
Genome size varies many orders of magnitude across species, due to both changes in ploidy as well as haploid DNA content [1, 2] Hypotheses for this variation proposed that genome size was linked to organismal complexity, as more complex organisms should require a larger number of genes. Other models propose that variation may be due to differences in the rates of insertions and deletions [8] or a consequence of changes in modes of reproduction [9, 10] While each of these models find limited empirical support [11, 12], counterexamples are common [9, 10, 13, 14]. In most of these models, the mechanistic link between genome size and phenotype remains unclear [21]
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