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Title: Transcriptional changes associated with lack of lipid synthesis in parasitoids

Author
item VISSER, BERTANNE - University Of Amsterdam
item ROELOFS, DICK - University Of Amsterdam
item HAHN, DANIEL - University Of Florida
item Teal, Peter
item MARIEN, JANINE - University Of Amsterdam
item ELLERS, JACINTHA - University Of Amsterdam

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/16/2012
Publication Date: 9/1/2012
Citation: Visser, B., Roelofs, D., Hahn, D.A., Teal, P.E., Marien, J., Ellers, J. 2012. Transcriptional changes associated with lack of lipid synthesis in parasitoids. Genome Biology and Evolution. 752-762.

Interpretive Summary: When we think about evolution, we usually consider novel traits that have arisen, even though the loss of traits can also affect evolutionary processes. Scientists at the Center for Medical Agricultural and Veterinary Entomology, USDA-ARS in Gainesville Florida along with colleagues from Section Animal Ecology, Department of Ecological Science, Amsterdam Global Change Institute, VU University Amsterdam, the Netherlands and the Department of Entomology and Nematology, University of Florida, used an emerging model organism to study the loss of lipid synthesis in parasitic insects. The majority of parasitic insects do not synthesize lipids in their adult life-stage, because they can take over valuable lipid stores from the host on which they develop as larvae. The parasitic lifestyle provides these insects with sufficient lipid reserves, making lipid synthesis redundant and susceptible to the degradation of underlying genetic pathways. So far, however, the genetic mechanisms underlying the loss of lipid synthesis remain to be elucidated. Their research showed that the extraordinary lifestyle adopted by these insects has led to altered transcription of fatty acid synthase (fas), the key gene involved in lipid synthesis, as well as other genes that have become unresponsive to sugar, which would normally induce lipogenesis. The findings are particularly important, because we have gained important insights into why and how traits are lost and we suggest that mechanisms involved in gaining new traits might prove similar to those involved in trait loss.

Technical Abstract: Loss of redundant morphological, behavioral or physiological traits is a common process contributing to evolutionary dynamics, but studies linking the evolutionary loss of redundant traits to the molecular decay in the genome are rare. The majority of parasitic insects have lost the ability for lipid synthesis in their adult life-stage, probably because exploitive host manipulation during larval development renders lipid synthesis redundant. Manipulation of the host’s physiology allows parasitoids to acquire lipids directly from their hosts, leaving metabolic pathways involved in parasitoid lipid synthesis prone to phenotypic regression. Here, we study transcriptional changes associated with loss of lipogenesis in the parasitic wasp Nasonia vitripennis. We first confirmed the lack of lipogenesis in N. vitripennis by showing a reduction in lipid reserves despite ingestion of dietary sugar, and a lack of incorporation of isotopic labels into lipid reserves when fed deuterated sugar solution. Second, we investigated transcriptional patterns of 28 genes involved in major nutrient metabolic pathways in short- and long-term sugar-fed females relative to starved females of N. vitripennis. Numerous genes involved in carbohydrate metabolism had a lower transcription in fed than in starved females. Sugar-feeding did not induce transcription of fatty acid synthase (fas), the key gene involved in the lipid biosynthesis pathway. We further compare our findings to gene expression of orthologous genes in Drosophila melanogaster, a species that actively synthesizes lipids. Our results reveal that N. vitripennis gene transcription involved in sugar and lipid pathways deviates severely from that of Drosophila, mainly through unresponsiveness of fas to dietary sugar in N. vitripennis. This study is the first to identify major changes in gene transcription that underlie the loss of lipogenesis in parasitic insects and provides new insight in the molecular mechanisms underlying trait loss.