Parallel altitudinal clines reveal trends in adaptive evolution of genome size in domesticated maize (Zea mays)

GENOME SIZE varies by several orders of magnitude across species, due to both changes in ploidy (number of sets of homologous chromosomes that make up the genome of a cell or an organism) as well as haploid DNA content (one-half of the diploid genome, i.e. no chromosome pairs such as one sees in egg or sperm). Early hypotheses for this variation had suggested that genome size might be linked to complexity of the organism, because more complex organisms “should require a larger number of genes”. Empirical studies, however, then revealed instead –– that most variation in genome size is due to noncoding repetitive sequence (which makes up ~45% of an organism’s genome) and that gene content is relatively constant (i.e. 1.0 to 1.2% of the genome).

Although this discovery resolved “the lack of correlation between genome size and complexity”, we still know relatively little about the make-up of many eukaryote (organisms containing chromosome pairs) genomes, the impact of genome size on phenotype (i.e. what traits are expressed by genes), or the processes that govern variation in repetitive DNA and genome size among taxa (groups of populations of an organism or organisms, as identified by taxonomists to form units).

Many theories have been offered to explain variation in genome size among taxa. Across deep evolutionary time, genome size appears to correlate with estimates of effective population size –– leading to suggestions that genetic drift permits maladaptive expansion (i.e. not providing adequate or appropriate adjustment to environmental signals or pressures) or contraction (smaller size) of genomes across species. Other models propose that variation may be due to differences in rates of insertions and deletions (indels) or a consequence of changes in modes of reproduction. While each of these models finds limited empirical support, counter-examples are common.

In addition to these neutral models, many authors have proposed adaptive explanations for genome size variation. Numerous correlations between genome size and physiologically or ecologically relevant phenotypes have been observed –– including size of nucleus, size of plant cell, size of seed, size of body, and growth rate. Adaptive models of genome-size evolution suggest that positive selection drives genome size towards an optimum due to selection on these, or other, traits, and that stabilizing selection prevents expansions and contractions away from the optimum. In most of these models, however, the mechanistic link between genome size and phenotype continues to remain obscure.

Authors [see attached] investigated parallel changes in intraspecific genome size and DNA-repeat content of domesticated maize (Zea mays) land-races versus their wild relative, teosinte, across altitudinal gradients in Mesoamerica and South America. They combined genotyping, low-coverage whole-genome-sequence data, and flow cytometry –– to test for evidence of selection on genome size and individual DNA-repeat abundance. They found that population structure alone cannot explain the observed variation, implying that clinal patterns of genome size are maintained by natural selection. To better understand the phenotypes driving selection on genome size, authors conducted a growth chamber experiment using a population of highland teosinte exhibiting extensive variation in genome size. They found weak support for a positive correlation between genome size and cell size, but stronger support for a negative correlation between genome size and rate of cell production.

Reanalyzing published data of cell counts in maize-shoot apical meristems, authors then identified a negative correlation between cell production rate and flowering time. Together, these findings suggest a model in which variation in genome size is driven by natural selection on flowering time across clines living at different altitudes –– connecting intraspecific variation in repetitive-DNA sequence to important differences in phenotypes (traits) adapting to such signals as altitude.


PLoS Genet May 2o18; 14: e1007162

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