Chromosome Inversions, Local Adaptation and Speciation

Abstract

CHROMOSOMAL inversions are found as fixed differences between species and as polymorphisms within species in many groups of animals and plants. In some groups, speciation is associated with inversions and other changes in the karyotype (White 1978, Chap. 3). The forces responsible for establishing inversions remain obscure, however, as does their evolutionary significance. The main importance of inversions might lie in their ability to produce genetic isolation between populations and species. Inversions can create postzygotic barriers when they reduce the fecundity of heterokaryotypes (chromosomal heterozygotes) (White 1978, Chap. 6; King 1993, Chap. 6).

Alternatively, the main evolutionary importance of inversions might come from the fact that they suppress recombination in heterokaryotypes (Sturtevant 1917; Roberts 1976). This view was championed by Dobzhansky (1947, 1954,1970), who argued that inversions represent sets of coadapted alleles. His verbal arguments were followed by the development of a substantial body of theory on recombination modifiers, beginning with Nei (1967). A major conclusion from that work is that, for a single population in a constant environment, fitness interactions between loci (epistasis) will generally favor the evolution of decreased recombination (Feldmanet al. 1997). When populations are connected by migration, selection can favor loosely linked modifiers that decrease recombination between loci involved in local adaptation, even in the absence of epistasis (Charlesworth and Charlesworth 1979; Pylkovet al. 1998; Lenormand and Otto 2000). This result suggests that inversions could be established by a similar mechanism. Simulations by Trickett and Butlin (1994) show that this can indeed happen.

Inversions have two genetic features that may make them particularly favorable agents for decreasing recombination between sets of locally adapted genes. An inversion is very tightly linked to the loci whose recombination rates it changes. This means that evolutionary forces acting on inversions may be much stronger than those for unlinked modifiers of recombination. Second, an inversion's effect on recombination is underdominant: it suppresses only recombination in heterokaryotypes. Once an inversion is established in a population, recombination again occurs at substantial rates. Thus that region of the chromosome is not doomed to the deleterious effects that ensue when recombination is completely and permanently shut down (Barton and Charlesworth 1998; Charlesworth and Charlesworth 2000).

In this article we study the conditions in which an inversion will spread if it carries a set of locally adapted alleles. We see that the chance that a new inversion happens to capture an advantageous haplotype can be very high. If it does, selection will favor its invasion. The scenario applies equally to species that hybridize since, from a population genetic perspective, hybridization and immigration are equivalent.

Two aspects of the local adaptation mechanism imply that it could contribute to the evolution of inversions under quite biologically general conditions. First, no epistasis is required. The loci must to be individually adapted to local conditions, but no coadaptation between them is needed. Second, it does not depend on drift and so can operate in populations of any size. Thus it provides an alternative (or complement) to the standard hypotheses based on epistasis, drift, and/or meiotic drive (e.g., Dobzhansky 1951; White 1978; Lande 1979).

The basic idea is simple. Consider a population that is receiving immigrants carrying alleles at two or more loci that are disadvantageous under the local conditions. The population is at equilibrium. That means that each copy of a locally adapted allele leaves one descendant on average. These alleles find themselves on different genetic backgrounds, sometimes with locally adapted alleles at the other loci, but sometimes with disadvantageous migrant alleles. An inversion now appears in a chromosome that happens to be carrying only the locally favorable alleles. This new chromosome does not recombine with others. Consequently, a copy of the locally favored allele that it carries at one locus never suffers the disadvantage of being found on the same chromosome with deleterious immigrant alleles at the other loci. This gene therefore has higher fitness than competing copies of the allele at the same locus that are carried on recombining chromosomes. Consequently, the allele on the inversion spreads, and the inversion spreads with it. This scenario is plausible in light of the evidence for local adaptation of a number of inversion polymorphisms in Drosophila (Dobzhansky 1970; Krimbas and Powell 1992; Balanyàet al. 2003; Etges and Levitan 2004).

We begin by quantifying this verbal argument with a model of two haploid loci that are initially loosely linked. The results are then extended to consider other factors such as more loci, partial linkage, diploidy, the geographical setting, and underdominance. In the discussion, we put the local adaptation mechanism in perspective by reviewing alternative hypotheses, discussing the relevant data, and suggesting futher empirical tests.

Acknowledgments