Genome size varies by many orders of magnitude across plants and animals, but resolving the most important evolutionary forces driving this variation remains challenging. Since eukaryotic genome size variation is not associated with complexity, genetic drift of the amount of noncoding DNA could dominate, implicating population and species history as key drivers of shifts in DNA content. Alternatively, directional selection could be acting on DNA content, but if so, it has not been resolved which level of selection is most important. Since the predominant component of many eukaryotic genomes is comprised of selfish genetic elements such as transposable elements (TEs) and regions subject to meiotic drive, factors that influence their differential success across populations and species could account for much of the variation in genome size. However, DNA content can also have important effects on organismal phenotype that could be under directional selection. Genome size may often be an important determinant of cell size and division rate and the subject of selection via its effects on developmental and metabolic phenotypes [ 1 , 2 ]. Supporting this view, correlations of genome size with invasive potential and growth rate [ 3 ], regional abundance and seed size [ 4 ], and even metabolic intensity in flying birds [ 5 ], may suggest an adaptive role. In this issue, Bilinski et al. [ 6 ] present evidence for this organismal adaptation view of genome size evolution by providing an explicit test for natural selection on genome size and repeat abundance across multiple altitudinal clines in maize and its wild relatives and identifying the underlying physiological mechanism. Bilinski et al. [ 6 ] capitalize on the remarkable genome size variation in maize and its wild relatives, which differ by 40%–70% within and between subspecies. It is estimated that 85% of the maize genome is composed of TEs, B chromosomes, and heterochromatic knobs subject to meiotic drive [ 7 , 8 ], highlighting the success of selfish genetic elements in this lineage. Nevertheless, clines of genome size along with phenotypic and environmental variables in Zea mays spp. have been well described, with a number of studies showing evidence of genome reductions, including the loss of knobs and B chromosomes, in regions of high altitude and latitude [ 9 – 13 ]. While these parallel clines are suggestive of an adaptive process, it has been difficult to definitively demonstrate this and fully reject a role for neutral population history. Bilinski et al. [ 6 ] add to this rich literature by using a quantitative genetics framework to conduct a test of local adaptation, recognizing that genome size is a trait governed by an immense number of small-effect loci. Moreover, it can be thought of as a quantitative trait under complete genetic control, since the variation in genome size is expected to be a simple function of the net number of insertion and deletion alleles individuals have across the genome. Under this framework, a neutral model predicts that genome size differences across a geographic region are a function of the relatedness and population structure [ 14 ] and thus determined by the extent of correlated allele frequencies between a given pair of individuals. It follows that if genome size is subject to selection, it should be more strongly correlated with altitude than expected from relatedness alone. The authors use low-coverage whole genome sequence data from three altitudinal clines to obtain detailed information not only about the kinship and structure of their samples but also about the contribution of each type of repeat to overall genome size. Using this approach to test for local adaptation, the authors are able to reject the predictions of the neutral model, concluding that genome size differences along altitudinal clines are too extreme to be explained solely by drift ( Fig 1 ). When considering individual repeat types, both TEs and knob repeat abundance are significantly correlated with altitude. They also find that one type of knob repeat, known as TR1, shows the strongest over-differentiation, and the signal of altitudinal adaptation on TR1 abundance remains significant even when controlling for genome size. With megabase-long heterochromatic knobs accounting for up to 10% of maize genome size variation [ 7 , 15 ], knobs seem to be acting as large-effect loci for genome size but, in some cases, may also be under additional selection pressures independent of their effects on genome size. Although TEs do not show signals of adaptation after controlling for genome size, the strong correlation of TE copy number with genome size and altitude implies that environmental adaptation could also be an important determinant of TE abundance mediated through its effects on genome size. 10.1371/journal.pgen.1007249.g001 Fig 1 Altitudinal clines in maize and teosinte. Clines in heterochromatic knobs and genome size in Zea mays spp. are significan
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