Academic journal article Genetics

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

Academic journal article Genetics

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

Article excerpt

ABSTRACT 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.

HALF of all insects interact with plants (Grimaldi and Engel 2005). Most phytophageous insects, however, use only a few plant genera for food, mating, and oviposition (Bernays and Chapman 1994). Changes in host use can result in both new species and new adaptations (Ehrlich and Raven 1964; Janz 2011). For example, the evolution of a new host specialization may have contributed to the formation of new species in pea aphids (Acyrthosiphon) among others (Via 2001; Matsubayashi et al. 2010). Adapting to a new host can drive genetic and phenotypic change that is critical for isolating nascent species. In some cases, specialization has a price: Increased performance on the new host correlates with reduced performance on other hosts (Futuyma and Moreno 1988; Jaenike 1990; Fry et al. 1996; Scheirs et al. 2005; Via and Hawthorne 2005). This scenario poses a new challenge for the nascent specialist, as it must keep together alleles for finding and selecting the appropriate host ("preference") along with those for utilizing that host ("performance," e.g., physiologically adapting to that host's secondary compounds or nutritional content; Jaenike 1990; Janz 2011). Theory suggests that a genetic correlation between the preference and performance alleles, such as caused by pleiotropy or genetic linkage, can overcome this problem and facilitate the switch to a new host (Lande 1979; Jaenike 1990; Fry et al. 1996; Janz 2011).

Until recently, evidence for this "genetic linkage" hypothesis in phytophagous insects has been mixed. Early genetic data in Drosophila by Jaenike (1986, 1987, 1989) suggested that oviposition preference and "settling" behavior are unlinked in Drosophila tripunctata, while Taylor and Condra (1983) found linkage between preference and performance in D. pseudoobscura. No linkage was found in other herbivorous species, such as Callosobruchus maculatus (southern cowpea weevil; Wasserman and Futuyma 1981), Colias philodice (butterfly; Tabashnik 1986), Papilionidae (swallowtail butterflies; Thompson 1988; Thompson et al. 1990), Chrysomelidae (leaf-feeding beetles; Keese 1996), Nilaparvata lugens (brown planthopper; Sezer and Butlin 1998a,b), and Oreina elongata (leaf beetle; Ballabeni and Rahier 2000). …

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