Ancient and Modern Genomes Reveal Microsatellites Maintain a Dynamic Equilibrium Through Deep Time

Abstract

Microsatellites are widely used in population genetics, but their evolutionary dynamics remain poorly understood. It is unclear whether microsatellite loci drift in length over time. This is important because the mutation processes that underlie these important genetic markers are central to the evolutionary models that employ microsatellites. We identify more than 27 million microsatellites using a novel and unique dataset of modern and ancient Adélie penguin genomes along with data from 63 published chordate genomes. We investigate microsatellite evolutionary dynamics over 2 timescales: one based on Adélie penguin samples dating to ∼46.5 ka and the other dating to the diversification of chordates aged more than 500 Ma. We show that the process of microsatellite allele length evolution is at dynamic equilibrium; while there is length polymorphism among individuals, the length distribution for a given locus remains stable. Many microsatellites persist over very long timescales, particularly in exons and regulatory sequences. These often retain length variability, suggesting that they may play a role in maintaining phenotypic variation within populations.

Keywords: Adélie penguin; ancient DNA; microsatellite evolution.

Fig. 1.

Densities of microsatellite loci of different ages in intergenic, intron, exon, and regulatory sequences in the Adélie penguin genome. a) Densities of loci inferred to have arisen on the branches labeled on the tree in b), in extant loci per megabase of sequence per million years. Edge lengths are not drawn to scale.

Fig. 2.

Distributions of allele lengths for loci of different ages in different types of surrounding sequences. Distributions of mean allele lengths (in nucleotides) of pure and impure microsatellite loci present in Adélie penguin and conserved across 6 age brackets for loci with periods 2 to 6 in intergenic, intron, exon, and regulatory sequences. The 6 age brackets in each cluster correspond to loci that arose most recently on the branch leading to Adélie penguin; on the branch leading to penguins; within Neoaves or on the branch leading to Neoaves; on the branch leading to Neognathae; on the branch leading to birds; outside Sauria (note that no pure exonic microsatellites of period 5 are inferred to have arisen outside Sauria). Each box extends from the lower to upper quartiles of the length distribution, and the interior line indicates the median. The whiskers extend to the most extreme points within 1.5 × interquartile range of the quartiles.