Ecological Adaptation and Speciation: The Evolutionary Significance of Habitat Avoidance as a Postzygotic Reproductive Barrier to Gene Flow

Table 1

Three models for how genetically based behavioral incompatibilities due to conflicting habitat avoidance can evolve during speciation-with-gene-flow that cause postzygotic isolation in hybrids (see Figures 1–3).

Model 1: intermediate null allele (o)
Step 1: 𝑎^+ state in ancestral population for a habitat choice locus with a recessive null (o) allele also segregating as low a frequency polymorphism that confers no habitat preference.
Step 2: new habitat becomes available and o/o genotypes from ancestral population shift and adapt to novel habitat.
Step 3: new avoidance mutation to ancestral habitat (𝑎^−) arises and elevates to high frequency in primarily 𝑜 null allele initial genetic background of novel habitat population.
Step 4: new avoidance mutation to novel habitat (𝑛^−) arises that confers even greater fidelity to ancestarl habitat than 𝑎^+ allele and elevates to high frequency in the ancestral habitat population.
Step 5: behavioral inviability/sterility in hybrids when individuals move between novel and ancestral habitat and cross mate producing 𝑛^−/𝑎^− heterozygotes at habitat choice locus.
Model 2: epistasis between habitat preference and avoidance loci
Step 1: initial 𝑎^+ state exists for ancestral habitat preference at habitat preference locus in ancestral population and initial 𝑛^− state for novel habitat avoidance at habitat avoidance locus.
Step 2: new habitat becomes available and new preference mutation for novel habitat (𝑛^+) arises and elevates to high frequency in novel habitat population.
Step 3: new avoidance mutation to ancestral habitat (𝑎^−) arises at avoidance locus and elevates to high frequency in novel habitat population because negative effects of 𝑛^−/𝑎^− heterozygosity at avoidance locus are not expressed in 𝑛^+/𝑛^+ genetic background at the preference locus in the novel habitat.
Step 4: behavioral inviability/sterility in hybrids when individuals move between novel and ancestral habitat and cross mate producing 𝑛^−/𝑎^− heterozygotes at habitat avoidance locus in 𝑛^+/𝑎^+ genetic background of hybrids at the preference locus.
Model 3: epistasis between ancestral and novel habitat loci with preference and avoidance alleles
Step 1: initial 𝑎^+ state exists for ancestral habitat preference at ancestral habitat choice locus in ancestral population and initial 𝑛^− state for novel habitat avoidance at novel habitat locus.
Step 2: new habitat becomes available and new preference mutation for novel habitat (𝑛^+) arises at novel habitat choice locus and elevates to high frequency in novel habitat population.
Step 3: new avoidance mutation to ancestral habitat (𝑎^−) arises at ancestral habitat choice locus and elevates to high frequency in 𝑛^+/𝑛^+ genetic background at the novel habitat locus in the novel habitat population.
Step 4: behavioral inviability/sterility in hybrids when individuals move between novel and ancestral habitat and cross mate producing 𝑎^+/𝑎^− heterozygotes at ancestral habitat locus in 𝑛^+/𝑛^− genetic background of hybrids at the novel habitat locus.