Nederlandse Zo÷logieprijs 2013
2013 Dutch Zoology Prize

The winner of the 2013 Dutch Zoology Prize is Dr. Bertanne Visser.

The prize was presented by Dr. Jan Kammenga (president of the Royal Dutch Zoological Society) at a symposium organised by the recepient and the KNDV.

Parasitism and the Evolutionary Loss of Lipogenesis: Symbiosis fuels evolutionary change

    Much research in evolutionary biology has been devoted to evolutionary novelties and trait acquisition. The reverse process, i.e.: that of trait loss has received considerably less attention, even though trait loss can also affect the evolutionary trajectories of lineages.

Use it, lose it, or outsource it

Olm, or proteus (Proteus anguinus)

    Traits can be lost when a phenotypic function is unused, such as eyes in cave-dwelling organisms, or when a phenotypic function is deleterious in a novel environment. Another type of trait loss is one in which the lost phenotypic function is still required for successful reproduction and survival of the organism, but is compensated for by symbiotic interactions. Here a symbiotic partner provides a function that is subsequently lost in the receiving organism, termed compensated trait loss.

    Using parasitoids as model organisms, Bertanne showed that evolution of the parasitoid lifestyle led to the loss of lipid synthesis, a trait typically expressed by all animals. The loss of lipid synthesis is associated with the absence of transcription of the key gene involved in lipid synthesis. This led to the conceptualization of compensated trait loss, where symbiotic interactions drive the loss of traits and evolutionary change.

What can be learned from parasites

Caterpillar with parasites

    It has been known for about fifteen years that certain insects showed an atypical metabolic response to feeding. These individual cases all described how parasitoids failed to increase their lipid reserves after feeding on sugar, something that is common in many other species, including man.

    Unlike predatory or herbivorous insects, parasitoids (species that spend part of their development as parasites) develop on or in a single host insect, ultimately killing their host upon entering their free-living adult life-stage. Lacking lipid synthesis is a remarkable deviation from typical nutrient metabolism, because core nutrient metabolic pathways are highly conserved and lipid synthesis is essential for key traits, such as growth, survival, and reproduction. Based on these earlier findings Bertanne hypothesized that evolution of the parasitoid lifestyle preceded or coincided with lack of lipogenesis, i.e. only parasitoids have lost lipid synthesis.

    Using a comparative approach, Bertanne tested the hypothesis of concurrent evolution between the parasitoid lifestyle and loss of lipogenesis. She was able to show that lipogenesis was lost at least three times in parallel in parasitoid flies, beetles and wasps. She further found that some parasitoids had reverted their strategy to active lipogenesis. Although the vast majority of parasitoids lack lipid synthesis, active lipid synthesis predominates in generalist parasitoids that adopt a wide host range. Bertanne's work was the first to show correlated evolution between lipogenesis and the parasitoid lifestyle. The re-evolution of this trait highlights the rapidity with which major evolutionary transitions can take place. This is particularly interesting because it directly contradicts deep-rooted views in evolutionary biology on the irreversibility of evolution (Visser et al., 2010).

Loss of fatty genes

Nasonia vitripennis

    Following the key finding that lipogenesis was lost in the majority of parasitoid lineages, the question remains which mechanisms underlie regressed lipid synthesis. Sugar feeding typically leads to up regulation of a suite of genes involved in carbohydrate and lipid metabolism, such as the prime gene necessary for lipid synthesis, fatty acid synthase. Contrary to findings in other animals, the transcriptional response to feeding of the parasitoid Nasonia vitripennis did not reveal up regulation of fatty acid synthase. Furthermore, numerous genes involved in sugar metabolism were down regulated rather than up regulated. By integrating physiological and functional genomic data, this study was the first to link phenotypic regression of lipid synthesis to a deviating transcriptional response (Visser et al., 2012).

Fruiteating primate

    Parasitoids provide an excellent example and model system for studying compensated trait loss. There is a difference between the loss of unwanted or unnecessary traits, and compensated trait loss in which the lost phenotypic function is still critical for the organism's fitness. Compensated trait loss is much more common than currently appreciated. Many distinct taxa, including bacteria, plants and humans, exhibit compensated trait loss in one or both interacting partners through mutualistic or parasitic interactions, such as the loss of photosynthesis in parasitic plants or the loss of vitamin C synthesis in fruit-eating primates and other mammals. Of critical importance is further that compensated trait loss severely tightens the dependence of interacting organisms; hence compensated trait loss may direct symbiotic interactions by preventing partners from splitting up (Ellers et al., 2012).

New concepts, novel insights

Jan Kammenga presents the 2013 Dutch Zoology Prize to Bertanne Visser

    Bertanne's integrative approach towards studying the evolutionary loss of lipogenesis has yielded valuable insights into the dynamic nature of trait evolution. Her work was the first to reveal why parallel evolutionary loss of essential lipid synthesis occurred, as well as uncovering the first molecular underpinnings. It also yielded comprehensive results revealing the potential for rapid evolutionary change and reverse evolution. And it further propelled the development of a new concept in evolutionary biology, compensated trait loss, which reaches beyond the realm of physiology to include morphological and behavioural trait degradation and loss in interacting organisms ranging from bacteria to humans.

Having worked as a post-doctoral researcher at the Netherlands Institute of Ecology (the Netherlands) and the University of Florida (USA), Bertanne now obtained funding from three competitive sources to work on the ecological conditions that fuelled re-evolution of lipogenesis in parasitoids at the University of Tours (France).