Habitat avoidance and speciation for phytophagous insect specialists

1. Models of sympatric speciation via host shifting for phytophagous insect specialists are based on a synergistic feedback between habitat-specific mating and performance genes. Under these models, insects are presumed to choose host plants based on the cumulative, additive effects of attraction alleles at one or several host preference loci. 2. Host choice for insects may not be based solely on attraction genes, however. Habitat avoidance may also play an important role in host use and the evolutionary implications of avoidance may differ from attraction. Insects that are heterozygous for avoidance alleles to alternate host plants may be behaviourally conflicted and have difficulty accepting any suitable host to feed, mate or oviposit on in a timely manner. 3. Here, we perform computer simulations of a three locus, epistatic model for ecological specialization involving host attraction, avoidance and performance genes. We show that the role habitat avoidance potentially plays in sympatric speciation is predicated on the strength of host-specific mating and fitness trade-offs. 4. When host discrimination and performance trade-offs are relatively strong, avoidance alleles that reduce the host-finding ability of hybrids (heterozygotes) can be favoured by selection and drive sympatric divergence to completion. The effect is similar to reinforcement, except that habitat avoidance not only strengthens pre-zygotic barriers to gene flow, but also causes post-zygotic isolation due to the behavioural sterility of hybrids. 5. In contrast, when host discrimination and performance trade-offs are weak, avoidance alleles with negative fitness effects in hybrids tend to be eliminated from populations. Habitat avoidance genes under these conditions are therefore akin to attraction alleles, increasing in frequency only if they have minimal or no detrimental effects on hybrids.