Lewontin's paradox — the much larger variation in species abundance than in genetic diversity — is closer to being explained.
The reproductive strategy of species has an impact on genome-wide diversity, providing a connection between population dynamic processes and the long-term effective population size (Ne).
Selection at linked sites also affects genome-wide diversity, but not to an extent that it is sufficient alone to explain Lewontin's paradox.
Selection and demography, among other factors, contribute to variation in Ne within genomes and leads to variation in diversity in different genomic regions of the same species.
Genetic polymorphism varies among species and within genomes, and has important implications for the evolution and conservation of species. The determinants of this variation have been poorly understood, but population genomic data from a wide range of organisms now make it possible to delineate the underlying evolutionary processes, notably how variation in the effective population size (Ne) governs genetic diversity. Comparative population genomics is on its way to providing a solution to 'Lewontin's paradox' — the discrepancy between the many orders of magnitude of variation in population size and the much narrower distribution of diversity levels. It seems that linked selection plays an important part both in the overall genetic diversity of a species and in the variation in diversity within the genome. Genetic diversity also seems to be predictable from the life history of a species.
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This work was supported by Swedish Research Council grants (2010–5650 and 2013–8271), a European Research Council grant (AdG 249976) and the Knut and Alice Wallenberg Foundation to H.E., and by a European Research Council grant (AdG 232971) and a French National Research Agency grant (ANR-10-BINF-01-01) to N.G. The authors thank N. Bierne, S. Glemin and M. Lascoux for comments on the manuscript.
The authors declare no competing financial interests.
- Genetic diversity
(Also known as genetic polymorphism). Variation in a DNA sequence between distinct individuals (or chromosomes) of a given species (or population).
Allelic variants of proteins that can be separated by electrophoresis based on differences in charge or structure.
The complete spread of a mutation in the population such that it replaces all other alleles at a site.
- Genetic drift
Fluctuation of allele frequency among generations in a population owing to the randomness of survival and reproduction of individuals, irrespective of selective pressures.
- Effective population size
(Ne). The number of breeding individuals in an idealized population that would show the same amount of genetic drift (or inbreeding, or any other variable of interest) as the population under consideration.
- Census population size
(Nc).The number of individuals in a population.
- Frequency-dependent selection
A form of selection in which the selective advantage or disadvantage of a genotype is dependent on its frequency relative to other genotypes.
A sharp and rapid reduction in the size of a population.
The probability that two randomly sampled gene copies in a population carry distinct alleles; a measure of the genetic diversity.
- Drift-barrier hypothesis
The idea, based on the concept of diminishing returns, that selection can only improve a trait up to a point at which the next incremental improvement will be overwhelmed by the power of genetic drift.
- Coalescent theory
A retrospective model of the distribution of gene divergence in a genealogy.
- Identity-by-descent segments
Chromosomal segments carried by two or more individuals that are identical because they have been inherited from a common ancestor, without recombination.
A form of genome evolution in which the number of sets of chromosomes increases.
- Linkage disequilibrium
The non-random association of alleles at two loci, often but not always due to physical linkage on the same chromosome.
- Selective sweep
Elimination or reduction of genetic diversity in the neighbourhood of a beneficial allele that increases in frequency in the population, typically after an environmental change.
- Hard sweeps
Selective sweeps in which the beneficial allele corresponds to a single, new mutation appearing after an environmental change.
- Soft sweeps
Selective sweeps in which the beneficial allele exists before an environmental change (thus representing standing variation) and is initially neutral or even slightly deleterious, or appears several times independently.
- Genetic draft
Pervasive reduction of genetic diversity owing to recurrent selective sweeps.
- Background selection
Reduction of genetic diversity owing to selection against deleterious mutations at linked loci.
New alleles entering the population by hybridization with members of a differentiated population or even a different species.
The change in allele frequency at a locus that itself is not necessarily affected by selection but is genetically linked to a locus that is.
- Allele frequency spectrum
The distribution of the frequency of variants across biallelic loci in a population sample.
A mating system in which males mate with more than one female.
A mating system in which females mate with more than one male.
When an organism of a particular sex carries two different types of sex chromosomes: that is, males of many animals and plants and females of birds, some fish and lizards, butterflies, and others.
The situation when there is only one chromosome copy in an individual of a diploid species, as for the X chromosome in males of many species.
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Ellegren, H., Galtier, N. Determinants of genetic diversity. Nat Rev Genet 17, 422–433 (2016). https://doi.org/10.1038/nrg.2016.58
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