Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila Sechellia
Dworkin, Ian, Jones, Corbin D., Genetics
Changes in host specialization contribute to the diversification of phytophagous insects. When shifting to a new host, insects evolve new physiological, morphological, and behavioral adaptations. Our understanding of the genetic changes responsible for these adaptations is limited. For instance, we do not know how often host shifts involve gain-of-function vs. loss-of-function alleles. Recent work suggests that some genes involved in odor recognition are lost in specialists. Here we show that genes involved in detoxification and metabolism, as well as those affecting olfaction, have reduced gene expression in Drosophila sechellia-a specialist on the fruit of Morinda citrifolia. We screened for genes that differ in expression between D. sechellia and its generalist sister species, D. simulans. We also screened for genes that are differentially expressed in D. sechellia when these flies chose their preferred host vs. when they were forced onto other food. D. sechellia increases expression of genes involved with oogenesis and fatty acid metabolism when on its host. The majority of differentially expressed genes, however, appear downregulated in D. sechellia. For several functionally related genes, this decrease in expression is associated with apparent loss-of-function alleles. For example, the D. sechellia allele of Odorant binding protein 56e (Obp56e) harbors a premature stop codon. We show that knockdown of Obp56e activity significantly reduces the avoidance response of D. melanogaster toward M. citrifolia. We argue that apparent loss-of-function alleles like Obp56e potentially contributed to the initial adaptation of D. sechellia to its host. Our results suggest that a subset of genes reduce or lose function as a consequence of host specialization, which may explain why, in general, specialist insects tend to shift to chemically similar hosts.
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HALF of known insect species feed primarily on plants (Jolivet 1992; Bernays and Chapman 1994), with 90% of these phytophagous insects specializing on one or a few host plant families (Bernays and Graham 1988; Jolivet 1992; Bernays and Chapman 1994). Specialists often evolve host-specific adaptations suchas resistancetoplant secondarycompounds, changes inmorphology,andnewpreferencebehaviors.Anunderstanding of the genetic basis of traits such as these is critical to knowing how host specialization evolves (Jaenike 1987; Via 1990; Futuyma 1991; Jaenike and Holt 1991; Hawthorne and Via 2001).
Recent work has uncovered genes and genetic regions affecting host specialization (Via 1990; Sheck and Gould 1993, 1995; Cleland et al. 1996; Jones 1998; Hawthorne and Via 2001; Carsten et al. 2005; Dambroski et al. 2005; Jones 2005; Nylin et al. 2005; Matsuo et al. 2007; Kopp et al. 2008). For example, in several cactophillicDrosophila species cytochrome P450s have been implicated in detoxification of host secondary compounds (Frank and Fogleman 1992; Barker et al. 1994; Danielson and Fogleman 1997; Danielson et al. 1997; Fogleman et al. 1997, 1998; Matzkin et al. 2006). Most of these genetic studies, however, concentrated on one or a few traits. Moreover, these earlier trait-specific studies could not distinguish between genetic changes that were a consequence of host specialization vs. those that directly contributedtothehost specializationper se (Bono et al. 2008; Matzkin 2008; but see Sucena and Stern 2000; Jones 2004; Orgogozo et al. 2006;McBride 2007; McGregor et al. 2007).
On its native islands, the Seychelles, Drosophila sechellia almost exclusively uses the fruit of Morinda citrifolia (Morinda), a plant common around the Indian Ocean and Polynesia (Louis and David 1986; Jones 2005). D. sechellia has evolved strong preference for and resistance to the toxins in Morinda (Louis and David 1986; R'Kha et al. 1991; Jones 1998, 2004, 2005). D. simulans, on the otherhand, is ahumancommensal that originally arose in eastern Africa (Lachaise and Silvain 2004). …