Genetics, experience, and host-plant preference in Eurosta solidaginis: Implications for host shifts and speciation

Host-associated mating is crucial in maintaining the partial reproductive isolation between the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and S. gigantea. (We refer to flies reared from S. gigantea as gigantea flies and those reared from S. altissima as altissima flies.) We measured the host preference of males and females of both host races, F₁ hybrids between the host races, F₂, and backcrosses to both host races. Male and female altissima flies and female gigantea flies had high host fidelity, whereas male gigantea flies had low host fidelity. This result suggests that3 1, 4tive mating that occurs when male gigantea mate with altissima females on S. altissima. This indicates assortative-mating mechanisms in addition to host-associated mating are required to produce the partial reproductive isolation between the host races that has been observed. Nongenetic factors had no influence on host preference. Larval conditioning did not influence host preference: reciprocal F₁ hybrids reared in S. altissima and S. gigantea both preferred S. gigantea. Adult experience had no impact on host preference: females preferred their natal host plant regardless of which host they encountered first as an adult. The hypothesis that maternal effects influence preferences was rejected because male and female flies did not show a consistent preference for the host plant of their mother. We also found no evidence that preference was a sex-linked trait because F₁ and backcrosses to the host races with different combinations of X chromosomes from the two host races preferred S. gigantea. Our results indicate that host preference is not determined by a large number of genes because preference of hybrids did not correspond to the proportion of the genome derived from each host race. The strength of the ovipuncture preference for S. gigantea by gigantea females, the females of both reciprocal F₁ hybrids, the backcross to gigantea, and F₂s indicates that preference is inherited nonadditively at a limited number of loci. The F₁ female hybrids, however, had a weaker host preference for S. gigantea than the pure gigantea host race, indicating that there may be incomplete dominance or modifier loci. Males had different host preference patterns than females, with individual male gigantea and male F₁ hybrids usually exhibiting preference exclusively for S. gigantea or S. altissima. One hypothesis explaining the difference in host preference between males and females is that the same gene influences both female and male host preference, but it is a sex-influenced gene. Thus, males carrying the gene for S. gigantea preference have an intermediate host preference, whereas females have a strong host preference to S. gigantea. In summary, we found that the host preference that produces host-associated mating is inherited nonadditively at a relatively small number of loci on autosomal genes. This mode of inheritance meets the assumptions of models of sympatric speciation, indicating that the host races could have evolved in sympatry.