A Locus in Drosophila sechellia Affecting Tolerance of a Host Plant Toxin

Many insects feed on only one or a few types of host. These host specialists often evolve a preference for chemical cues emanating from their host and develop mechanisms for circumventing their host’s defenses. Adaptations like these are central to evolutionary biology, yet our understanding of their genetics remains incomplete. Drosophila sechellia, an emerging model for the genetics of host specialization, is an island endemic that has adapted to chemical toxins present in the fruit of its host plant, Morinda citrifolia. Its sibling species, D. simulans, and many other Drosophila species do not tolerate these toxins and avoid the fruit. Earlier work found a region with a strong effect on tolerance to the major toxin, octanoic acid, on chromosome arm 3R. Using a novel assay, we narrowed this region to a small span near the centromere containing 18 genes, including three odorant binding proteins. It has been hypothesized that the evolution of host specialization is facilitated by genetic linkage between alleles contributing to host preference and alleles contributing to host usage, such as tolerance to secondary compounds. We tested this hypothesis by measuring the effect of this tolerance locus on host preference behavior. Our data were inconsistent with the linkage hypothesis, as flies bearing this tolerance region showed no increase in preference for media containing M. citrifolia toxins, which D. sechellia prefers. Thus, in contrast to some models for host preference, preference and tolerance are not tightly linked at this locus nor is increased tolerance per se sufficient to change preference. Our data are consistent with the previously proposed model that the evolution of D. sechellia as a M. citrifolia specialist occurred through a stepwise loss of aversion and gain of tolerance to M. citrifolia’s toxins

Incompatibility and Competitive Exclusion of Genomic Segments between Sibling <i>Drosophila</i> Species

The extent and nature of genetic incompatibilities between incipient races and sibling species is of fundamental importance to our view of speciation. However, with the exception of hybrid inviability and sterility factors, little is known about the extent of other, more subtle genetic incompatibilities between incipient species. Here we experimentally demonstrate the prevalence of such genetic incompatibilities between two young allopatric sibling species, Drosophila simulans and D. sechellia. Our experiments took advantage of 12 introgression lines that carried random introgressed D. sechellia segments in different parts of the D. simulans genome. First, we found that these introgression lines did not show any measurable sterility or inviability effects. To study if these sechellia introgressions in a simulans background contained other fitness consequences, we competed and genetically tracked the marked alleles within each introgression against the wild-type alleles for 20 generations. Strikingly, all marked D. sechellia introgression alleles rapidly decreased in frequency in only 6 to 7 generations. We then developed computer simulations to model our competition results. These simulations indicated that selection against D. sechellia introgression alleles was high (average s = 0.43) and that the marker alleles and the incompatible alleles did not separate in 78% of the introgressions. The latter result likely implies that most introgressions contain multiple genetic incompatibilities. Thus, this study reveals that, even at early stages of speciation, many parts of the genome diverge to a point where introducing foreign elements has detrimental fitness consequences, but which cannot be seen using standard sterility and inviability assays.</p

Summary of maximum likelihood estimates of recombination rate (<i>c</i>) and selection coefficient (<i>s</i>) parameters with different dominance (<i>h</i>).

<p>Note: Data was summarized from contour plots described in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002795#pgen.1002795.s002" target="_blank">Figure S2</a>.</p

Fertility (viability+fecundity) assays of introgression lines and the <i>simulans</i> strain.

<p>Note: Fertility was measured by the total progeny produced by three pairs of flies for 15 days (N = 10).</p>*<p>Tukey-Kramer HSD value here shows significant difference between the sim132 <i>D. simulans</i> strain and introgression strains, taking into account multiple testing. It is equal to Abs(Mean[i]-Mean[j])-LSD. The value must be positive to be significant at <i>P-value</i><0.05. NS = not significant. All analyses were performed using JMP software (SAS). 25H line was lost before it could be tested.</p

Data from: A locus in Drosophila sechellia affecting tolerance of a host plant toxin

Many insects feed on only one or a few types of host. These host specialists often evolve a preference for chemical cues emanting from their host and develop mechanisms for circumventing their host’s defenses. Adaptations like these are central to evolutionary biology, yet our understanding of their genetics remains incomplete. Drosophila sechellia, an emerging model for the genetics of host specialization, is an island endemic that has adapted to chemical toxins present in the fruit of its host plant, Morinda citrifolia. Its sibling species, D. simulans, and many other Drosophila species do not tolerate these toxins and avoid the fruit. Earlier work showed that a region with a strong effect on tolerance to the major toxin, octanoic acid, was on chromosome arm 3R. Using a novel assay we narrowed this region to a small span near the centromere containing 18 genes, including three odorant binding proteins. It has been hypothesized that the evolution of host specialization is facilitated by genetic linkage between alleles contributing to host preference and alleles contributing to host usage, such as tolerance to secondary compounds. We tested this hypothesis by measuring the effect of this tolerance locus on host preference behavior. Our data were inconsistent with the linkage hypothesis as flies bearing this tolerance region showed no increase in preference for media containing M. citrifolia toxins, which D. sechellia prefers. Thus, in contrast to some models for host preference, preference and tolerance are not tightly linked at this locus and increased tolerance per se is not sufficient to change preference. Our data are consistent with the previously proposed model that the evolution of D. sechellia as a M. citrifolia specialist occurred through a step-wise loss of aversion and gain of tolerance to M. citrifolia’s toxins

Mating success tests between each introgression line and the <i>simulans</i> strain.

<p>Note: Labels inside parentheses for each introgression line indicate the experiment performed in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002795#pgen-1002795-g001" target="_blank">Figure 1</a>. N_SS = <i>simulans</i> homotypic pairs, N_SI = <i>simulans</i> females x introgression males, N_IS = introgression females x <i>simulans</i> males, N_II = introgression homotypic pairs. 25H line (corresponding to experiment A in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1002795#pgen-1002795-g001" target="_blank">Figure 1</a>) was lost before it could be tested.</p

RawData_DRYAD_031913

All raw data, including: Morinda tolerance, OA-HA behavior, OA boundary lines, KD times, and flow rat