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. 2010 May 11;107(19):8677-82.
doi: 10.1073/pnas.1001744107. Epub 2010 Apr 26.

Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle

Bertanne Visser  1 , Cécile Le Lann, Frank J den Blanken, Jeffrey A Harvey, Jacques J M van Alphen, Jacintha Ellers
Affiliations

Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle

Bertanne Visser et al. Proc Natl Acad Sci U S A. .

Abstract

Evolutionary loss of traits can result from negative selection on a specific phenotype, or if the trait is selectively neutral, because the phenotype associated with the trait has become redundant. Even essential traits may be lost, however, if the resulting phenotypic deficiencies can be compensated for by the environment or a symbiotic partner. Here we demonstrate that loss of an essential me-tabolic trait in parasitic wasps has evolved through environmental compensation. We tested 24 species for the ability to synthesize lipids de novo and collected additional data from the literature. We found the majority of adult parasitoid species to be incapable of synthesizing lipids, and phylogenetic analyses showed that the evolution of lack of lipogenesis is concurrent with that of parasitism in insects. Exploitive host manipulation, in which the host is forced to synthesize lipids to the benefit of the parasitoid, presumably facilitates loss of lipogenesis through environmental compensation. Lipogenesis re-evolved in a small number of parasitoid species, particularly host generalists. The wide range of host species in which generalists are able to develop may impede effective host manipulation and could have resulted in regaining of lipogenic ability in generalist parasitoids. As trait loss through environmental compensation is unnoticed at the phenotypic level, it may be more common than currently anticipated, especially in species involved in intricate symbiotic relationships with other species.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Difference in mean lipid content (%) between emerged and fed individuals as measured in the feeding experiments. Asterisks indicate significant differences between emerged and fed individuals: *P < 0.05; **P < 0.01; ***P < 0.001; ns, not significant. Sample sizes for each treatment and species are listed in Table S1.
Fig. 2.
Fig. 2.
Phylogeny based on morphological and molecular data, showing inferred gains (formula image) and losses (formula image) in parasitic lifestyle. Character tracing for lipogenic ability is shown, in which dark gray branches refer to an ability to accumulate lipids, whereas light gray branches refer to a lack of lipid accumulation in adults. In this phylogeny, Ichneumonoidea and Proctotrupomorpha are considered sister groups.
Fig. 3.
Fig. 3.
Phylogeny showing inferred character states for host range (specialist/generalist) for hymenopteran parasitoids, in which gains (formula image) in lipogenic ability are shown. In this phylogeny, Ichneumonoidea and Proctotrupomorpha are regarded as sister groups.
See this image and copyright information in PMC

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