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Abstract
Many insect species are host-obligate specialists. The evolutionary mechanism driving the adaptation of a species to a toxic host is, however, intriguing. We analyzed the tight association of Drosophila sechellia to its sole host, the fruit of Morinda citrifolia, which is toxic to other members of the melanogaster species group. Molecular polymorphisms in the dopamine regulatory protein Catsup cause infertility in D. sechellia due to maternal arrest of oogenesis. In its natural host, the fruit compensates for the impaired maternal dopamine metabolism with the precursor l-DOPA, resuming oogenesis and stimulating egg production. l-DOPA present in morinda additionally increases the size of D. sechellia eggs, what in turn enhances early fitness. We argue that the need of l-DOPA for successful reproduction has driven D. sechellia to become an M. citrifolia obligate specialist. This study illustrates how an insect's dopaminergic system can sustain ecological adaptations by modulating ontogenesis and development.
Highlights
Morinda citrifolia fruit is the sole host of Drosophila sechellia (Tsacas and Baechli, 1981), a close relative of Drosophila melanogaster and endemic to the Seychelles archipelago (Louis and David, 1986)
We first examined the influence of chemicals found in morinda on the reproductive system of D. sechellia by testing the effect of diet on egg production
In agreement with previous reports, D. sechellia raised on standard diet produced few eggs compared to D. melanogaster wild-type Berlin and D. melanogaster Canton-S (Figure 1A and Figure 1—figure supplement 1), raised on the same media
Summary
Morinda citrifolia fruit (morinda) is the sole host of Drosophila sechellia (Tsacas and Baechli, 1981), a close relative of Drosophila melanogaster and endemic to the Seychelles archipelago (Louis and David, 1986). A peculiar aspect of the specialization is that morinda fruits are toxic to all other drosophilids (Legal et al, 1992). The toxicity stems from a high content of carboxylic acids (primarily octanoic and hexanoic acid) (Legal et al, 1994), to which D. sechellia appears to be resistant (Farine et al, 1996). The chemosensory system of D. sechellia is specialized in detecting and coding key volatiles produced by morinda (Dekker et al, 2006) while devoid of the repellence towards the acids (Matsuo et al, 2007). Morinda stimulates egg production (R'kha et al, 1997), and D. sechellia clearly prefers to oviposit in medium containing morinda carboxylic acids (Amlou et al, 1998). We here examined the dependence of Drosophila sechellia on morinda, for optimal reproduction
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