Chromosome inversions, local adaptation and speciation

Abstract

We study the evolution of inversions that capture locally adapted alleles when two populations are exchanging migrants or hybridizing. By suppressing recombination between the loci, a new inversion can spread. Neither drift nor coadaptation between the alleles (epistasis) is needed, so this local adaptation mechanism may apply to a broader range of genetic and demographic situations than alternative hypotheses that have been widely discussed. The mechanism can explain many features observed in inversion systems. It will drive an inversion to high frequency if there is no countervailing force, which could explain fixed differences observed between populations and species. An inversion can be stabilized at an intermediate frequency if it also happens to capture one or more deleterious recessive mutations, which could explain polymorphisms that are common in some species. This polymorphism can cycle in frequency with the changing selective advantage of the locally favored alleles. The mechanism can establish underdominant inversions that decrease heterokaryotype fitness by several percent if the cause of fitness loss is structural, while if the cause is genic there is no limit to the strength of underdominance that can result. The mechanism is expected to cause loci responsible for adaptive species-specific differences to map to inversions, as seen in recent QTL studies. We discuss data that support the hypothesis, review other mechanisms for inversion evolution, and suggest possible tests.

Figure 1.

Schematic for the conditions in which an inversion will invade. The vertical axis is the frequency of a haplotype through a generation, relative to its frequency in zygotes: (1) in zygotes, (2) in juveniles after migration, (3) in adults after selection, and (4) in zygotes in the following generation. (Top) The pattern for an ancestral haplotype captured by an inversion, which then spreads because it avoids the recombination load (bottom).

Figure 2.

The same as in Figure 1, but showing the specific cases in which the inversion captures the locally adapted alleles at zero, one, and two loci.

Figure 3.

Simulation of the invasion of an inversion in a cline. Two haploid loci with multiplicative fitness effects are initially at a migration–selection equilibrium in a stepping-stone population with 10 demes. At each locus, one allele has fitness 1 + s to the left of the midpoint and fitness 1 − s to the right. An inversion that captures the locally favored haplotype is introduced in the central deme at an initial frequency of 0.01. (A) The invasion of the inversion. (B) The extinction of the ancestral recombining haplotype that carries the same alleles as the inversion. (C) The extinction of recombinant haplotypes as the inversion invades. Parameters are s = 0.025, m = 0.1, and r = 0.5. Note the change in the vertical scale in C.

Figure 4.

Two scenarios for establishing the conditions that favor the spread of an underdominant inversion in parapatry. The population occupies two habitats, indicated by the stippled and open regions. Alleles A and B are deleterious in combination in both habitats. Allele A is favored in the habitat to the left and allele B in the habitat to the right. The most common genotype is shown in the top corners. Dashed curves show the frequency of Ab and solid curves the frequency of aB. Asterisks show the appearance of a new mutation that spreads by selection in one of the habitats. (Left side) One advantageous mutation appears in each of the two populations. (Right side) Both advantageous mutations appear in the right-hand population. (Both sides, bottom) An inversion appearing in either habitat that captures the most common haplotype will spread by the local adaptation mechanism.