Conditions for mutation-order speciation

Abstract

Two models for speciation via selection have been proposed. In the well-known model of 'ecological speciation', divergent natural selection between environments drives the evolution of reproductive isolation. In a second 'mutation-order' model, different, incompatible mutations (alleles) fix in different populations adapting to the same selective pressure. How to demonstrate mutation-order speciation has been unclear, although it has been argued that it can be ruled out when gene flow occurs because the same, most advantageous allele will fix in all populations. However, quantitative examination of the interaction of factors influencing the likelihood of mutation-order speciation is lacking. We used simulation models to study how gene flow, hybrid incompatibility, selective advantage, timing of origination of new mutations and an initial period of allopatric differentiation affect population divergence via the mutation-order process. We find that at least some population divergence can occur under a reasonably wide range of conditions, even with moderate gene flow. However, strong divergence (e.g. fixation of different alleles in different populations) requires very low gene flow, and is promoted when (i) incompatible mutations have similar fitness advantages, (ii) less fit mutations arise slightly earlier in evolutionary time than more fit alternatives, and (iii) allopatric divergence occurs prior to secondary contact.

Figure 1.

A schematic representation of the epistasis model. There are two patches, 1 and 2, that experience uniform selection for the same optimum. Symmetrical migration between patches occurs at rate m. Each patch is initially fixed for the ancestral alleles a and b. During the course of the simulations, two new mutations arise, denoted as A and B. Both new mutations confer a selective advantage over the ancestral genotype. A is the most favoured allele, and B is more favoured than b, but less favoured than A (table 1). ‘Hybrid’ individuals carrying both A and B exhibit reduced fitness because these two alleles are incompatible. Mutations may arise simultaneously or in staggered fashion such that mutation B arises first in patch 1, reaches a frequency q_thresh in at least one of the patches, following which mutation A arises in patch 2. Scenarios of initial allopatric divergence were also examined by setting m initially to zero for t_contact generations.

Figure 2.

The effects of migration rate and relative fitnesses on mutation-order divergence when the novel alleles arise at different loci (epistasis model). Squares with continuous line show the frequency of allele A in patch 1 (P₁); circles with dashed lines show the frequency of allele A in patch 2 (P₂). In panels (a,b), the mutations (alleles A and B) arise simultaneously. In panels (c–l), allele B reaches a frequency q_thresh in at least one patch before allele A arises in patch 2. In all panels, there is no allopatric divergence period (i.e. t_contact = 0). Strong population divergence (i.e. p₁ ≈ 0 and p₂ ≈ 1) via the mutation-order process occurs when there is no migration (all panels) or when the migration rate is low and fitnesses are relatively similar (right-hand panels). Note that while the frequencies of allele B are not shown, by the end of a simulation, we have q_i ≈ 1 − p_i (i.e. either A or B becomes common in a patch by the end).

Figure 3.

Outcomes of simulations from the epistasis model as influenced by migration rate, the ratio (w_AAbb/w_aaBB) of fitnesses of the two favoured alleles, and the fitness w_AABB (=w_AaBB = w_AABb = w_AaBb) of genotypes having at least one copy of each of the two incompatible alleles. Each panel represents outcomes from 10 000 simulations for varying combinations of the fitness ratio (w_AAbb/w_aaBB) and the migration rate. In all panels, there is no allopatric divergence period (i.e. t_contact = 0). Outcome classifications are according to the shading as detailed in (e) and as explained in the text. (a) no lag, w_AABB = 0.9; (b) q_thresh = 0.01, w_AABB = 0.9; (c) q_thresh = 0.333, w_AABB = 0.9; (d) no lag, w_AABB = 0.001; (e) q_thresh = 0.01, w_AABB = 0.001; (f) q_thresh = 0.333, w_AABB = 0.001.

Figure 4.

The role of a period of t_contact generations of allopatric divergence on the outcome of mutation-order divergence in the epistasis model. Shading as for figure 3; top row: parameter values as in figure 3a; bottom row: parameters values as in figure 3f. (a,e) t_contact = 10 generations; (b,f) 25 generations; (c,g) 40 generations; (d,h) 75 generations.