Current evolutionary theory

The nomenclature of “Modern synthesis” and “Population genetics” can be seen as two sides of the same coin, with the first one representing the theoretical framework and the latter the mathematical implementation of our current evolutionary theory. In the most recent version of one of the classic modern textbooks, the basic principles of the MS, i.e., the basic mechanisms driving evolution, were listed by and are summarized in Box1.

Box 1: Evolutionary mechanisms

Natural selection: This is the key process at the base of the modern synthesis. It refers to the differential survival and reproduction rate of individuals as a consequence of their individual phenotype. In a nutshell, individuals with higher fitness for a specific environment, have higher chances of survival and reproduction. Their genes, providing the higher fitness features, will be passed on to the next generation at a higher frequency.

Genetic drift: Genetic drift is a change in allele frequencies due to the random sampling of alleles for the next generation (Masel 2011). It results in random allele frequency changes and depends on population size. The smaller the population, the more likely alleles will be lost compared to the originally larger genepool due to stochasticity. A conceptual example is given in figure 1.

Figure 1: Schematic example of genetic drift. Simply by chance, in generation 1 only four individuals produce progeny and only one of them carries the blue allele. Consequently, in generation 2 only a minority of individuals carry the blue allele.

Genetic hitchhiking: Genetic hitchhiking occurs when an allele changes in frequency not for being under selection itself but for being in linkage with another allele which is under selection. An extreme case of genetic hitchhiking was observed in the model plant Arabidopsis thaliana: a glyphosate resistance mutation occurred in the chloroplast genome causing an increase in the occurrence of the entire nuclear genome associated with the mutation (Flood et al. 2016). The stronger the selection and the quicker it acts, the less recombination events will occur between the positive mutation and the rest of the genome, extending the hitchhiking to normally unlinked parts of the genome.

Epistasis: Epistasis occurs when a locus A is interfering with the phenotypic effect of another locus B. Selection on locus B will therefore be dependent on the allele present at locus A. A straightforward example is eye colour in many animals. For example, in the parasitic wasp Nasonia vitripennis, the compound determining eye colour is synthesized through a biosynthetic pathway. The last steps of the pathway are catalysed by two enzymes that define the eye colour depending on the alleles present on the loci coding the enzymes, which we will call A and B for simplicity (Figure 2).

Figure 2: Example of epistasis. Nasonia vitripennis is a wasp with diploid females and haploid males. This species has Wild Type (WT) individuals with dark eyes, but loss of function mutations (a and b) exist for two genes (A and B) acting at the end of the biosynthetic pathway responsible for a compound of the eye color. As gene B variation produces phenotypic variation only when a functional copy of gene A is present, gene A has an epistatic effect on gene B.

Recessive loss of function mutations exist for both genes A and B. While in the presence of a functional copy of Enzyme A, enzyme B variation produces phenotypic variation (dark eyes if a functional copy of B is present, red eyes otherwise), this is not the case when there are no functional copies of enzyme A (grey eyes regardless of locus B variation).

Pleiotropic effects: Pleiotropic effects are present when a single gene has multiple phenotypic effects. Natural selection on that gene will therefore pass through selection of multiple phenotypes. When one of the phenotypes is selected for, the other affected phenotypes will also change their occurrence in the next generations, even though they are not directly under selection.

Population bottleneck: A population bottleneck refers to a drastic reduction of population size due to environmental events (such as drought, flood, fires, pest attacks…). Such events drastically reduce the genetic variation of the population. Population bottleneck can result in genetic drift when the surviving individuals are selected randomly. Alternatively, a bottleneck can result in an extreme form of natural selection when the surviving individuals are the most fit to overcome the stress event.

Founder effect: Founder effect refers to the low genetic variation observed in new colonizing populations originated from few individuals that naturally poorly represent the gene-pool of the larger population from which they originate. Founder effects are closely related to bottlenecks but involve the colonization of new space for the species. Like in bottlenecks, mostly genetic drift and but also natural selection are the main evolutionary mechanisms at work.

Gene flow: Gene flow or Genetic migration refers to the transfer of genetic material from one population to another. When two populations have a really high gene flow and their genetic material is exchanged without limit, they may be considered a single population.

The discipline of population genetics describes, in mathematical terms, how the mechanisms in Box 1 cause changes in allele frequencies. To do so, the starting point is the null hypothesis in which no changes is allele frequencies are acting on a population and there is random mating and consequently random combination of alleles (individuals carrying allele A have the same chance to mate with individuals carrying allele A and B). In this theoretical null hypothesis, the population reaches the Hardy-Weinberg Equilibrium and there is no variation in allele frequencies between generations. So, in a locus with two alleles A and a, where we indicate the allele frequencies with f = p and f = q respectively, the corresponding genotype frequencies can be represented in a Punnett square (Figure 3) and they will be:

Freq(AA) = p2 Freq(aa) = q2 Freq(Aa) = 2pq

Figure 3: Punnett Square representing allele and genotype (AA, aa, Aa) frequencies in a population harbouring two alleles (A and a) at locus A. Allele frequencies (p and q) are represented by the length of the arrows, genotype frequencies (f(…)) by the area of the squares.

When the population is in HWE, the allele frequencies in the next generation will remain equal and can be calculated as:

p’ = (p2 + 2pq * 1⁄2) = p2 + pq = p(p+q) = p

q’ = (q2 + 2pq * 1⁄2) = q2 + pq = q(p+q) = q

In natural populations, it is possible to test for deviation from the HWE, i.e. to test whether a specific locus is under selection. To do so, it is necessary to measure genetic variation in two subsequent generations and compare genotype frequencies between these. Deviation from the HWE can be tested through a χ2 (chi-square) test.

Population genetics and genomics allow to draw a variety of information from the genetic variability measured in populations and species. In contrast, quantitative genetics focuses on the study of complex quantitative traits controlled by several genes. The name of this discipline refers to the sometimes-miniscule phenotypic differences among individuals that are quantified and utilized in order to unravel the nature of the trait’s genetic basis. More information and examples on the field of population genetics can be found on quantitative genetics in Falconer & Mackay (1996). A technical report of the most recent analysis available in quantitative genetics can be found on chapter “Differential Methylation”.