Eric Wajnberg

Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga

Loss of sexual reproduction is considered an evolutionary dead end for metazoans, but bdelloid rotifers challenge this view as they appear to have persisted asexually for millions of years. Neither male sex organs nor meiosis have ever been observed in these microscopic animals: oocytes are formed through mitotic divisions, with no reduction of chromosome number and no indication of chromosome pairing. However, current evidence does not exclude that they may engage in sex on rare, cryptic occasions. Here we report the genome of a bdelloid rotifer, Adineta vaga (Davis, 1873), and show that its structure is incompatible with conventional meiosis. At gene scale, the genome of A. vaga is tetraploid and comprises both anciently duplicated segments and less divergent allelic regions. However, in contrast to sexual species, the allelic regions are rearranged and sometimes even found on the same chromosome. Such structure does not allow meiotic pairing; instead, we find abundant evidence of gene conversion, which may limit the accumulation of deleterious mutations in the absence of meiosis. Gene families involved in resistance to oxidation, carbohydrate metabolism and defence against transposons are significantly expanded, which may explain why transposable elements cover only 3% of the assembled sequence. Furthermore, 8% of the genes are likely to be of non-metazoan origin and were probably acquired horizontally. This apparent convergence between bdelloids and prokaryotes sheds new light on the evolutionary significance of sex.

Venom gland extract is not required for successful parasitism in the polydnavirus-associated endoparasitoid Hyposoter didymator (Hym. Ichneumonidae) despite the presence of numerous novel and conserved venom proteins

The venom gland is a conserved organ in Hymenoptera that shows adaptations associated with life-style diversification. Few studies have investigated venom components and function in the highly diverse parasitic wasps and all suggest that the venom regulates host physiology. We explored the venom of the endoparasitoid Hyposoter didymator (Campopleginae), a species with an associated polydnavirus produced in the ovarian tissue. We investigated the effects of the H.xa0didymator venom on two physiological traits of the host Spodoptera frugiperda (Noctuidae): encapsulation response and growth rate. We found that H.xa0didymator venom had no significant effect on host cellular immunity or development, suggesting that it does not contribute to parasitism success. The host physiology seemed to be modified essentially by the ovarian fluid containing the symbiotic polydnaviruses. Proteomic analyses indicated that the H.xa0didymator venom gland produces a large variety of proteins, consistent with the classical hymenopteran venom protein signature, including: reprolysin-like, dipeptidyl peptidase IV, hyaluronidase, arginine kinase or allergen proteins. The venom extracts also contained novel proteins, encoded by venom genes conserved in Campopleginae ichneumonids, and proteins with similarities to active molecules identified in other parasitoid species, such as calreticulin, reprolysin, superoxide dismutase and serpin. However, some of these proteins appear to be produced only in small amounts or to not be secreted. Possibly, in Campopleginae carrying polydnaviruses, the host-modifying activities of venom became redundant following the acquisition of polydnaviruses by the lineage.

Contribution of Lateral Gene Transfers to the Genome Composition and Parasitic Ability of Root-Knot Nematodes

Lateral gene transfers (LGT), species to species transmission of genes by means other than direct inheritance from a common ancestor, have played significant role in shaping prokaryotic genomes and are involved in gain or transfer of important biological processes. Whether LGT significantly contributed to the composition of an animal genome is currently unclear. In nematodes, multiple LGT are suspected to have favored emergence of plant-parasitism. With the availability of whole genome sequences it is now possible to assess whether LGT have significantly contributed to the composition of an animal genome and to establish a comprehensive list of these events. We generated clusters of homologous genes and automated phylogenetic inference, to detect LGT in the genomes of root-knot nematodes and found that up to 3.34% of the genes originate from LGT of non-metazoan origin. After their acquisition, the majority of genes underwent series of duplications. Compared to the rest of the genes in these species, several predicted functional categories showed a skewed distribution in the set of genes acquired via LGT. Interestingly, functions related to metabolism, degradation or modification of carbohydrates or proteins were substantially more frequent. This suggests that genes involved in these processes, related to a parasitic lifestyle, have been more frequently fixed in these parasites after their acquisition. Genes from soil bacteria, including plant-pathogens were the most frequent closest relatives, suggesting donors were preferentially bacteria from the rhizosphere. Several of these bacterial genes are plasmid-borne, pointing to a possible role of these mobile genetic elements in the transfer mechanism. Our analysis provides the first comprehensive description of the ensemble of genes of non-metazoan origin in an animal genome. Besides being involved in important processes regarding plant-parasitism, genes acquired via LGT now constitute a substantial proportion of protein-coding genes in these nematode genomes.

Specific versus Non-Specific Immune Responses in an Invertebrate Species Evidenced by a Comparative de novo Sequencing Study

Our present understanding of the functioning and evolutionary history of invertebrate innate immunity derives mostly from studies on a few model species belonging to ecdysozoa. In particular, the characterization of signaling pathways dedicated to specific responses towards fungi and Gram-positive or Gram-negative bacteria in Drosophila melanogaster challenged our original view of a non-specific immunity in invertebrates. However, much remains to be elucidated from lophotrochozoan species. To investigate the global specificity of the immune response in the fresh-water snail Biomphalaria glabrata, we used massive Illumina sequencing of 5′-end cDNAs to compare expression profiles after challenge by Gram-positive or Gram-negative bacteria or after a yeast challenge. 5′-end cDNA sequencing of the libraries yielded over 12 millions high quality reads. To link these short reads to expressed genes, we prepared a reference transcriptomic database through automatic assembly and annotation of the 758,510 redundant sequences (ESTs, mRNAs) of B. glabrata available in public databases. Computational analysis of Illumina reads followed by multivariate analyses allowed identification of 1685 candidate transcripts differentially expressed after an immune challenge, with a two fold ratio between transcripts showing a challenge-specific expression versus a lower or non-specific differential expression. Differential expression has been validated using quantitative PCR for a subset of randomly selected candidates. Predicted functions of annotated candidates (approx. 700 unisequences) belonged to a large extend to similar functional categories or protein types. This work significantly expands upon previous gene discovery and expression studies on B. glabrata and suggests that responses to various pathogens may involve similar immune processes or signaling pathways but different genes belonging to multigenic families. These results raise the question of the importance of gene duplication and acquisition of paralog functional diversity in the evolution of specific invertebrate immune responses.

Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses

The Polydnaviridae is a family of double-stranded DNA viruses that are symbionts of parasitoid wasps. The family is currently divided into two genera, the Ichnovirus (IV) and Bracovirus (BV), which are associated with wasps in the families Ichneumonidae and Braconidae, respectively. IVs and BVs have similar immunosuppressive and developmental effects on parasitized hosts but their encapsidated genomes largely encode different genes. To assess whether IV and BV infection has similar or disparate effects on the transcriptome of shared hosts, we characterized the effects of Hyposoter didymator Ichnovirus (HdIV) and Microplitis demolitor Bracovirus (MdBV) on the fat body and hemocyte transcriptome of Spodoptera frugiperda (Lepidoptera: Noctuidae). Our results indicated that HdIV and MdBV infection alters the abundance of a relatively low proportion of S.xa0frugiperda transcripts at 24xa0h post-infection. Axa0majority of the transcripts affected by infection also differed between MdBV and HdIV. However, we did identify some host transcripts that were similarly affected by both viruses. A majority of these genes were transcribed in the fat body and most belonged to functional classes with roles in immunity, detoxification, or cell structure. Particularly prominent in this suite of transcripts were genes encoding for predicted motor-related and collagen IV-like proteins. Overall, our data suggest that the broadly similar effects that HdIV and MdBV have on host growth and immunity are not due to these viruses inducing profound changes in host gene expression. Given though that IVs and BVs encode few shared genes, the host transcripts that are similarly affected by HdIV and MdBV could indicate convergence by each virus to target a few processes at the level of transcription that are important for successful parasitism of hosts by H.xa0didymator and M.xa0demolitor.

Effect of plant nitrogen and water status on the foraging behavior and fitness of an omnivorous arthropod

Abstract Omnivorous arthropods make dietary choices according to the environment in which they forage, mainly availability/quality of plant and/or prey resources. Such decisions and their subsequent impacts on life‐history traits may be affected by the availability of nutrients and water to plants, that is, through bottom‐up forces. By setting up arenas for feeding behavior observation as well as glasshouse cages for plant preference assessment, we studied effects of the presence of prey (Lepidoptera eggs) and nitrogen/water availability to host tomato plants on the foraging behavior and life‐history traits in the omnivorous predator Macrolophus pygmaeus (Heteroptera: Miridae). In the absence of prey, the predator fed equally on the plants treated with various levels of nitrogen and water. In the presence of prey, however, the feeding rate on plants decreased when the plant received low water input. The feeding rate on prey was positively correlated with feeding rate on plants; that is, prey feeding increased with plant feeding when the plants received high water input. Moreover, plants receiving high water input attracted more M. pygmaeus adults compared with those receiving low water input. For M. pygmaeus fitness, the presence of prey enhanced its fertility and longevity, but the longevity decreased when plants received low compared with high water input. In conclusion, the omnivorous predator may be obliged to feed on plants to obtain water, and plant water status may be a limiting factor for the foraging behavior and fitness of the omnivorous predator.

Host kairomone learning and foraging success in an egg parasitoid: a simulation model

Abstract 1.u2002Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) is an egg parasitoid that recognises chemical residues left by its host the green stink bug Nezara viridula (L.) (Heteroptera: Pentatomidae) as kairomone signals, enabling it to find egg masses in which to lay eggs.

Does Plant Cultivar Difference Modify the Bottom-Up Effects of Resource Limitation on Plant-Insect Herbivore Interactions?

Variation in resource input to plants triggers bottom-up effects on plant-insect herbivore interactions. However, variation in plant intrinsic traits in response to resource availability may modify the bottom-up effects. Furthermore, the consequences also may depend on the feeding strategy of insect herbivores belonging to different feeding guilds. We evaluated the performance of two insect herbivores from distinct feeding guilds, the leaf miner Tuta absoluta and the phloem feeder Bemisia tabaci. We offered the insects two tomato cultivars growing under optimal nitrogen input vs. nitrogen limitation, or under optimal water input vs. water limitation. We found that: (i) the two cultivars differed in their responses to nitrogen and water limitation by regulating primary (leaf-gas exchange related parameters, leaf nitrogen content, and leaf C/N ratio) and secondary metabolism (main defensive compounds: glycoalkaloids); (ii) for both plant cultivars, nitrogen or water limitation significantly affected T. absoluta survival and development, while B. tabaci survival was affected only by nitrogen limitation; and surprisingly (iii) plant cultivar differences did not modify the negative bottom-up effects of resource limitation on the two insect herbivores. In conclusion, the negative effects of resource limitation cascaded up to insect herbivores even though plant cultivars exhibited various adaptive traits to resource limitation.

Hyposoter didymator uses a combination of passive and active strategies to escape from the Spodoptera frugiperda cellular immune response

An endoparasitic life style is widespread among Hymenoptera, and various different strategies allowing parasitoids to escape from the host encapsulation response have been reported. Species carrying polydnaviruses (PDVs), such as the ichneumonid Hyposoter didymator, generally rely on the viral symbionts to evade host immune responses. In this work, we show that H. didymator eggs can evade encapsulation by the host in the absence of calyx fluid (containing the viral particles), whereas protection of the larvae requires the presence of calyx fluid. This evasion by the eggs depends on proteins associated with the exochorion. This type of local passive strategy has been described for a few species carrying PDVs. Immune evasion by braconid eggs appears to be related to PDVs or proteins synthesized in the oviducts being associated with the egg. We report that in H. didymator, by contrast, proteins already present in the ovarian follicles are responsible for the eggs avoiding encapsulation. Mass spectrometry analysis of the egg surface proteins revealed the presence of host immune-related proteins, including one with similarities with apolipophorin-III, and also the presence of three viral proteins encoded by IVSPERs (Ichnovirus Structural Protein Encoding Regions).

How optimal foragers should respond to habitat changes: a reanalysis of the Marginal Value Theorem

The Marginal Value Theorem (MVT) is a cornerstone of biological theory. It connects the quality and distribution of patches in a fragmented habitat to the optimal time an individual should spend exploiting them, and thus its optimal rate of movement. However, predictions regarding how habitat alterations should impact optimal strategies have remained elusive, with heavy reliance on graphical arguments. Here we derive the sensitivity of realized fitness and optimal residence times to general habitat attributes, for homogeneous and heterogeneous habitats, retaining the level of generality of the MVT. We provide new predictions on how altering travel times, patch qualities and/or relative abundances should affect optimal strategies, and study the consequences of habitat heterogeneity. We show that knowledge of average characteristics is in general not sufficient to predict the change in the average rate of movement. We apply our results to examine the conditions under which the optimal strategies are invariant to scaling. We prove a previously conjectured form of invariance in homogeneous habitats, but show that invariances to scaling are not generic in heterogeneous habitats. We also consider the relative exploitation of patches that differ in quality, clarifying the conditions under which it is adaptive to stay longer on poorer patches.