The field of genomics has ushered in new methods for studying molecular-genetic variation in natural populations. However, most population-genomic studies still rely on small sample sizes (typically, <100 individuals) from single time points, leaving considerable uncertainties with respect to the behavior of relatively young (and rare) alleles and, owing to the large sampling variance of measures of variation, to the specific gene targets of unusually strong selection. Genomic sequences of ∼1,700 haplotypes distributed over a 10-year period from a natural population of the microcrustacean Daphnia pulex reveal evolutionary-genomic features at a refined scale, including previously hidden information on the behavior of rare alleles predicted by recent theory. Background selection, resulting from the recurrent introduction of deleterious alleles, appears to strongly influence the dynamics of neutral alleles, inducing indirect negative selection on rare variants and positive selection on common variants. Temporally fluctuating selection increases the persistence of nonsynonymous alleles with intermediate frequencies, while reducing standing levels of variation at linked silent sites. Combined with the results from an equally large metapopulation survey of the study species, classes of genes that are under strong positive selection can now be confidently identified in this key model organism. Most notable among rapidly evolving Daphnia genes are those associated with ribosomes, mitochondrial functions, sensory systems, and lifespan determination.
Evolutionary Genomics of a Subdivided Species
The ways in which genetic variation is distributed within and among populations is a key determinant of the evolutionary
features of a species. However, most comprehensive studies of these features have been restricted to studies
of subdivision in settings known to have been driven by local adaptation, leaving our understanding of the natural
dispersion of allelic variation less than ideal. Here, we present a geographic population-genomic analysis of 10 populations
of the freshwater microcrustacean Daphnia pulex, an emerging model system in evolutionary genomics.
These populations exhibit a pattern of moderate isolation-by-distance, with an average migration rate of 0.6 individuals
per generation, and average effective population sizes of ∼650,000 individuals. Most populations contain numerous
private alleles, and genomic scans highlight the presence of islands of excessively high population subdivision
for more common alleles. A large fraction of such islands of population divergence likely reflect historical neutral
changes, including rare stochastic migration and hybridization events. The data do point to local adaptive divergence,
although the precise nature of the relevant variation is diffuse and cannot be associated with particular
loci, despite the very large sample sizes involved in this study. In contrast, an analysis of between-species divergence
highlights positive selection operating on a large set of genes with functions nearly nonoverlapping with those involved
in local adaptation, in particular ribosome structure, mitochondrial bioenergetics, light reception and response,
detoxification, and gene regulation. These results set the stage for using D. pulex as a model for
understanding the relationship between molecular and cellular evolution in the context of natural environments.
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- Award ID(s):
- 1922914
- NSF-PAR ID:
- 10382922
- Date Published:
- Journal Name:
- Molecular biology and evolution
- Volume:
- 39
- Issue:
- 8
- ISSN:
- 0737-4038
- Page Range / eLocation ID:
- 1-22
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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