The probability of genetic parallelism and convergence in natural populations

Abstract

Genomic and genetic methods allow investigation of how frequently the same genes are used by different populations during adaptive evolution, yielding insights into the predictability of evolution at the genetic level. We estimated the probability of gene reuse in parallel and convergent phenotypic evolution in nature using data from published studies. The estimates are surprisingly high, with mean probabilities of 0.32 for genetic mapping studies and 0.55 for candidate gene studies. The probability declines with increasing age of the common ancestor of compared taxa, from about 0.8 for young nodes to 0.1-0.4 for the oldest nodes in our study. Probability of gene reuse is higher when populations begin from the same ancestor (genetic parallelism) than when they begin from divergent ancestors (genetic convergence). Our estimates are broadly consistent with genomic estimates of gene reuse during repeated adaptation to similar environments, but most genomic studies lack data on phenotypic traits affected. Frequent reuse of the same genes during repeated phenotypic evolution suggests that strong biases and constraints affect adaptive evolution, resulting in changes at a relatively small subset of available genes. Declines in the probability of gene reuse with increasing age suggest that these biases diverge with time.

Figure 1.

Hypothetical example to illustrate calculation of proportional similarity (PS) to measure probability of gene reuse between sister taxa. A, B, and C represent species having one or more populations that independently evolved a similar change in phenotype (open circles) compared with an ancestral phenotype (filled circles). Bar graph above each derived population indicates the relative contributions of each gene i to the phenotype (here, i is 1, 2 or 3). PS is calculated between a pair of taxa as PS = Σ_i min(p_i1, p_i2), where p_i1 and p_i2 are the proportional contributions of gene i in the two taxa. Within a species, PS is measured between all pairs of derived populations and averaged. Relative contributions of genes are then averaged among populations (illustrated for species A by the bar graph immediately below node A). PS_A–B compares the relative contributions of the three genes in species B with the average for species A (PS = 0.6 + 0 + 0 = 0.6). PS_AB-C compares the relative contributions of the three genes in species C with the average of A and B, shown in the bar graph below the node connecting A and B (PS = 0 + 0.2 + 0 = 0.2).

Figure 2.

Measurements of the probability of gene reuse based on (a) data from genetic crosses and (b) candidate gene data. Open symbols represent average of PS between all pairs of derived populations within the same species (i.e. parallel evolution). Filled symbols represent similarity measurements between sister taxa at deeper nodes in the phylogenetic trees (i.e. convergent evolution). Curves are best-fit logistic regressions to the data.