The genetics of speciation by reinforcement

Abstract

Reinforcement occurs when natural selection strengthens behavioral discrimination to prevent costly interspecies matings, such as when matings produce sterile hybrids. This evolutionary process can complete speciation, thereby providing a direct link between Darwin's theory of natural selection and the origin of new species. Here, by examining a case of speciation by reinforcement in Drosophila,we present the first high-resolution genetic study of variation within species for female mating discrimination that is enhanced by natural selection. We show that reinforced mating discrimination is inherited as a dominant trait, exhibits variability within species, and may be influenced by a known set of candidate genes involved in olfaction. Our results show that the genetics of reinforced mating discrimination is different from the genetics of mating discrimination between species, suggesting that overall mating discrimination might be a composite phenomenon, which in Drosophila could involve both auditory and olfactory cues. Examining the genetics of reinforcement provides a unique opportunity for both understanding the origin of new species in the face of gene flow and identifying the genetic basis of adaptive female species preferences, two major gaps in our understanding of speciation.

Figure 1. Experimental Design to Substitute Chromosomes or Chromosomal Regions Derived from Sympatry into an Allopatric Background and Measure Their Effect on Mating Discrimination

F₁ male-parent backcrosses (A) allow measurements of whole chromosome effects, while F₁ female-parent backcrosses (B) measure specific chromosomal region effects. Curved arrow represents the reciprocal backcross of the one shown.

Figure 2. Mean Square Chromosomal Effects on Mating Discrimination

(A) Male-parent backcross 1 shows the effects of substituting chromosomes derived from Mather, California (sympatry), into a background derived from Flagstaff, Arizona (allopatry). (B) Male-parent backcross 2 shows the effects of substituting chromosomes derived from Mt. St. Helena, California (sympatry), into a background derived from Mesa Verde, Colorado (allopatry). *, p < 0.005; **, p < 0.001; ***, p < 0.0001. (C) Combined chromosomal contributions to female mating discrimination. Small bars on the left represent chromosomes (X, 2, 3, and 4), while long bars on the right show the frequency of matings of backcross females with D. persimilis.

Figure 3. QTLs and Candidate Genes for Reinforced Mating Discrimination

Each panel shows CIM estimations of chromosomal region effects on mating discrimination. Arrows point to major QTL locations and are named after their candidate genes. The direction of the chromosomal region effect on mating discrimination is shown in parentheses. The y-axis, LR, is the ratio of the likelihood value under the null hypothesis of no QTL to the likelihood value under the hypothesis that there is a QTL in a given interval of adjacent markers. The likelihood ratio significance threshold reflecting a Type I error of 0.05 is 11.5 s. The indicated inversion is a fixed chromosomal inversion differentiating D. pseudoobscura and D. persimilis.

Figure 4. Genomic Distribution of Genetic Factors Preventing Gene Flow between D. pseudoobscura and D. persimilis

Gray boxes denote fixed chromosomal inversions separating D. pseudoobscura and D. persimilis. Black boxes denote the genomic locations of QTLs for reinforced mating discrimination. Note that the third chromosome also conferrs high discrimination in sympatry, but no particular QTLs have been identified for this chromosome.