The evolution of intron size in amniotes: a role for powered flight?

Abstract

Intronic DNA is a major component of eukaryotic genes and genomes and can be subject to selective constraint and have functions in gene regulation. Intron size is of particular interest given that it is thought to be the target of a variety of evolutionary forces and has been suggested to be linked ultimately to various phenotypic traits, such as powered flight. Using whole-genome analyses and comparative approaches that account for phylogenetic nonindependence, we examined interspecific variation in intron size variation in three data sets encompassing from 12 to 30 amniotes genomes and allowing for different levels of genome coverage. In addition to confirming that intron size is negatively associated with intron position and correlates with genome size, we found that on average mammals have longer introns than birds and nonavian reptiles, a trend that is correlated with the proliferation of repetitive elements in mammals. Two independent comparisons between flying and nonflying sister groups both showed a reduction of intron size in volant species, supporting an association between powered flight, or possibly the high metabolic rates associated with flight, and reduced intron/genome size. Small intron size in volant lineages is less easily explained as a neutral consequence of large effective population size. In conclusion, we found that the evolution of intron size in amniotes appears to be non-neutral, is correlated with genome size, and is likely influenced by powered flight and associated high metabolic rates.

Fig. 1.—

Distribution of intron median size in 11 species used in data set A. “Other introns” include all other introns after the fourth intron. (A) Introns identified in data set A. (B) Introns from genes with at least five introns in each species.

Fig. 2.—

Intron size distributions in different data sets. Boxplot is used to display the logarithmized size distribution of introns in each data set. Species names in black represent mammals, names in red represent reptiles/birds, and names in dark green represent amphibians. (A) Data set A; (B) data set B; and (C) data set C.

Fig. 3.—

The influence of greater taxon sampling on the significance of PGLS-based t-tests. We generated four larger phylogenetic trees with more bird species (A03 and A12 derived from data set A and B12 and B23 derived from data set B). Then we used the median size of a specific intron class in each species as node values in a phylogenetic tree and performed PGLS analysis. For newly added bird species, node values were generated by normal distribution (see text for details). To get a hypothetical distribution, this procedure was repeated 5,000 times. In each diagram, the red line denotes the P value from PGLS analysis in the original data set, and the blue and green bars denote the 5,000-time simulation of such P value in two simulated data sets derived from a same original data set. (A) Simulation based on the median size of first introns in data set A. (B) Simulation based on the median size of first introns in data set B.

Fig. 4.—

Correlation between genome size and intron size. Light-blue lines indicate regression lines derived from normal linear regression model; and brown lines indicate regression lines derived from PGLS model, which accounts for nonindependence among data points. (A) Median size of first introns in data set A; (B) median size of other introns (introns except first introns) in data set A; (C) median size of first introns in data set B; and (D) median size of other introns (introns except first introns) in data set B.

Fig. 5.—

Correlations between the proportion of repetitive elements in introns and genomes. Brown lines indicate regression lines from normal linear regression model. (A) Data from data set A and (B) data from data set B.