Genetics of egg production in Drosophila sechellia

Abstract

Drosophila sechellia, an island endemic that specializes on a single host plant, has a lower rate of egg production than its generalist sister species D. melanogaster, D. simulans, and D. mauritiana. Earlier work showed that part of this difference in egg production was due to a reduction in the number of ovarioles in D. sechellia relative to its sister species. Here, I extend this earlier work by genetically analyzing the difference in egg production between D. sechellia and D. simulans. In all, 10 genetic markers were used in several interspecific backcrosses to identify chromosome regions that affected the rate of egg production. While previously mapped factors affecting ovariole number appear to impact the rate of egg production, new, non-ovariole factors were also identified. Overall, the difference in egg production between D. sechellia and D. simulans appears to be a polygenic trait. The relationship between these factors and genes involved the adaptation of D. sechellia to its host plant is not yet clear. The data are consistent with the hypothesis that decline in egg production is, in part, a negative pleiotropic effect of genetic changes required for host specialization in D. sechellia, although finer-scale genetic analysis of both traits is needed to truly test this hypothesis.

Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila sechellia

“…These genes are clearly functional in D. sechellia; the open reading frames of these genes are intact and loss-of-function mutations at Cp36 cause female sterility. The lower expression of these likely reflects the fewer ovarioles and lower rate of egg production in D. sechellia on standard medium ( Jones 2004;Orgogozo et al 2006).…”

“…The host preference behavior of D. sechellia has been modeled in the lab either with chemotaxis (R' Kha et al 1991;Higa and Fuyama 1993;Amlou et al 1998a;Legal et al 1999) or with oviposition-site preference experiments (R' Kha et al 1991Kha et al , 1997Jones 2004;Matsuo et al 2007). We developed both types of assay, verified that they produced comparable results, and showed a strong species difference in behavior.…”

“…As a result, most fruit flies avoid this plant. In contrast, D. sechellia responds positively to olfactory cues from Morinda; when female D. sechellia detect Morinda they increase egg production and ovipositioning (R'Kha et al 1991;Jones 2004). Field experiments suggest that D. sechellia can detect Morinda at distances up to 50 m (R' Kha et al 1991).…”

“…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 contributed to the host specialization per 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). …”

“…D. sechellia has evolved strong preference for and resistance to the toxins in Morinda (Louis and David 1986;R'Kha et al 1991;Jones 1998Jones , 2004Jones , 2005. D. simulans, on the other hand, is a human commensal that originally arose in eastern Africa (Lachaise and Silvain 2004).…”