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

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 betwe...

Recurrent specialization on a toxic fruit in an island Drosophila population

“…Hungate et al (19) hypothesized that olfactory attraction might have evolved first from recessive alleles segregating in the ancestral range, such as loss-of-function mutations at olfaction-related genes (7,12,15,45). Such attraction would yield strong selection for tolerance alleles, which may often be dominant (13,14) and may originate from new mutations or rare variants in the ancestral populations.…”

“…Mutations in genes affecting the ecdysteroid metabolism pathway have enhanced D. sechellia adaptation on toxic noni (20) and helped make Drosophila pachea an obligatory specialist on a toxic cactus (9). Another particularly intriguing candidate is the Osiris cluster associated with resistance to octanoic acid in D. sechellia (19). Although the exact function of these transmembrane proteins remains unknown, they are differentially expressed upon exposure to Arabidopsis glucosinolates in the herbivorous drosophilid S. flava (38) and they have expanded in herbivorous silkworm and pea aphid (50).…”

“…It contains a cluster of digestive serine proteases that have rapidly evolved in D. sechellia (34) and expanded in cactophilic Drosophila (35) and are associated with detoxification (36) and food choice (37) in D. melanogaster. Interestingly, the third-highest peak in these regions falls in the middle of a major QTL region on chromosome arm 3R that confers adult resistance against octanoic acid in D. sechellia (19). The ∼170-kb-long QTL was found from interspecific introgression mapping and contains 18 genes, with "none .…”

“…QTLs were drawn from mapping studies of noni attraction (ref. 18 and C. D. Jones, personal communication) and tolerance to noni or octanoic acid (19,21). QTL positions were obtained with respect to the D. yakuba genome.…”

“…A peculiar example is the specialization of Drosophila sechellia, which is endemic on the Seychelles islands in the Indian Ocean, on noni (Morinda citrifolia) fruits that are highly toxic to other drosophilids (13)(14)(15)(16)(17)(18)(19)(20)(21)(22). The partial reproductive isolation between D. sechellia and its close relatives from the melanogaster subgroup retaining the ancestral decaying habitat has facilitated the investigation of the genetics of some phenotypes related to herbivory (18,19,21). However, the order by which these adaptations appeared, their effect on reproductive isolation, and the reproducibility of the genetic mechanisms underlying them remain largely unclear.…”