International audienceEvolutionary 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 metabolic 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 inwhich 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

No abstract

Loss of traits can dramatically alter the fate of species. Evidence is rapidly accumulating that the prevalence of trait loss is grossly underestimated. New findings demonstrate that traits can be lost without affecting the external phenotype, provided the lost function is compensated for by species interactions. This is important because trait loss can tighten the ecological relationship between partners, affecting the maintenance of species interactions. Here, we develop a new perspective on so-called `compensated trait loss' and how this type of trait loss may affect the evolutionary dynamics between interacting organisms. We argue that: (1) the frequency of compensated trait loss is currently underestimated because it can go unnoticed as long as ecological interactions are maintained; (2) by analysing known cases of trait loss, specific factors promoting compensated trait loss can be identified and (3) genomic sequencing is a key way forwards in detecting compensated trait loss. We present a comprehensive literature survey showing that compensated trait loss is taxonomically widespread, can involve essential traits, and often occurs as replicated evolutionary events. Despite its hidden nature, compensated trait loss is important in directing evolutionary dynamics of ecological relationships and has the potential to change facultative ecological interactions into obligatory ones.

Phenotypic regression of morphological, behavioral, or physiological traits can evolve when reduced trait expression has neutral or beneficial effects on overall performance. Studies on the evolution of phenotypic degradation in animals have concentrated mostly on the evaluation of resulting phenotypes, whereas much less research has been dedicated to uncovering the molecular mechanisms that underlie phenotypic regression. The majority of parasitoids (i.e., insects that develop on or inside other arthropods), do not accumulate lipid reserves during their free-living adult life-stage and represent an excellent system to study phenotypic regression in animals. Here, we study transcriptional patterns associated with lack of lipogenesis in the parasitic wasp Nasonia vitripennis. We first confirmed that N. vitripennis does not synthesize lipids 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 responses of 28 genes involved in lipid and sugar metabolism in short- and long-term sugar-fed females relative to starved females of N. vitripennis. Sugar feeding did not induce transcription of fatty acid synthase (fas) or other key genes involved in the lipid biosynthesis pathway. Furthermore, several genes involved in carbohydrate metabolism had a lower transcription in fed than in starved females. Our results reveal that N. vitripennis gene transcription in response to dietary sugar deviates markedly from patterns typically observed in other organisms. This study is the first to identify differential gene transcription associated with lack of lipogenesis in parasitoids and provides new insights into the molecular mechanism that underlies phenotypic regression of this trait.

The diet of organisms generally provides a sufficient supply of energy and building materials for healthy growth and development, but should also contain essential nutrients. Species differ in their exogenous requirements, but it is not clear why some species are able to synthesize essential nutrients, while others are not. The unsaturated fatty acid, linoleic acid (LA; 18:2n-6) plays an important role in functions such as cell physiology, immunity, and reproduction, and is an essential nutrient in diverse organisms. LA is readily synthesized in bacteria, protozoa and plants, but it was long thought that all animals lacked the ability to synthesize LA de novo and thus required a dietary source of this fatty acid. Over the years, however, an increasing number of studies have shown active LA synthesis in animals, including insects, nematodes and pulmonates. Despite continued interest in LA metabolism, it has remained unclear why some organisms can synthesize LA while others cannot. Here, we review the mechanisms by which LA is synthesized and which biological functions LA supports in different organisms to answer the question why LA synthesis was lost and repeatedly gained during the evolution of distinct invertebrate groups. We propose several hypotheses and compile data from the available literature to identify which factors promote LA synthesis within a phylogenetic framework. We have not found a clear link between our proposed hypotheses and LA synthesis; therefore we suggest that LA synthesis may be facilitated through bifunctionality of desaturase enzymes or evolved through a combination of different selective pressures.Electronic supplementary materialThe online version of this article (doi:10.1007/s11692-017-9436-5) contains supplementary material, which is available to authorized users.

No abstract

Lipid synthesis can have a major effect on survival and reproduction, yet most insect parasitoids fail to synthesize lipids. For parasitic wasps in the genus Leptopilina, however, studies have suggested that there is intraspecific variation in the ability for lipid synthesis. These studies were performed on only few populations, and a large‐scale investigation of both lipogenic ability and population genetic structure is now needed. Here, we first examined lipogenic ability of nine Leptopilina heterotoma populations collected in 2013 and found that five of nine populations synthesized lipids. The 2013 populations could not be used to determine genetic structure; hence, we obtained another 20 populations in 2016 that were tested for lipogenic ability. Thirteen of 20 populations (all Leptopilina heterotoma) were then used to determine the level of genetic differentiation (i.e., haplotype and nucleotide diversity) by sequencing neutral mitochondrial (COI) and nuclear (ITS2) markers. None of the 2016 populations synthesized lipids, and no genetic differentiation was found. Our results did reveal a nearly twofold increase in mean wasp lipid content at emergence in populations obtained in 2016 compared to 2013. We propose that our results can be explained by plasticity in lipid synthesis, where lipogenic ability is determined by environmental factors, such as developmental temperature and/or the amount of lipids carried over from the host.

Coexistence of species sharing the same resources is often possible if species are phylogenetically divergent in resource acquisition and allocation traits, decreasing competition between them. Developmental and life-history traits related to resource use are influenced by environmental conditions such as temperature, but thermal trait responses may differ among species. An increase in ambient temperature may, therefore, affect trait divergence within a community, and potentially species coexistence. Parasitoids are interesting models to test this hypothesis, because multiple species commonly attack the same host, and employ divergent larval and adult host use strategies. In particular, development mode (arrested or continued host growth following parasitism) has been recognized as a major organiser of parasitoid life histories. Here, we used a comparative trait-based approach to determine thermal responses of development time, body mass, egg load, metabolic rate and energy use of the coexisting Drosophila parasitoids Asobara tabida, Leptopilina heterotoma, Trichopria drosophilae and Spalangia erythromera. We compared trait values between species and development modes, and calculated trait divergence in response to temperature, using functional diversity indices. Parasitoids differed in their thermal response for dry mass, metabolic rate and lipid use throughout adult life, but only teneral lipid reserves and egg load were affected by developmental mode. Species-specific trait responses to temperature were probably determined by their adaptations in resource use (e.g. lipogenesis or ectoparasitism). Overall, trait values of parasitoid species converged at the higher temperature. Our results suggest that local effects of warming could affect host resource partitioning by reducing trait diversity in communities.