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- Rapid Experimental Evolution of Pesticide Resistance in C. elegans Entails No Costs and Affects the Mating SystemPublication . Lopes, PC; Sucena, E; Santos, ME; Magalhães, SPesticide resistance is a major concern in natural populations and a model trait to study adaptation. Despite the importance of this trait, the dynamics of its evolution and of its ecological consequences remain largely unstudied. To fill this gap, we performed experimental evolution with replicated populations of Caenorhabditis elegans exposed to the pesticide Levamisole during 20 generations. Exposure to Levamisole resulted in decreased survival, fecundity and male frequency, which declined from 30% to zero. This was not due to differential susceptibility of males. Rather, the drug affected mobility, resulting in fewer encounters, probably leading to reduced outcrossing rates. Adaptation, i.e., increased survival and fecundity, occurred within 10 and 20 generations, respectively. Male frequency also increased by generation 20. Adaptation costs were undetected in the ancestral environment and in presence of Ivermectin, another widely-used pesticide with an opposite physiological effect. Our results demonstrate that pesticide resistance can evolve at an extremely rapid pace. Furthermore, we unravel the effects of behaviour on life-history traits and test the environmental dependence of adaptation costs. This study establishes experimental evolution as a powerful tool to tackle pesticide resistance, and paves the way to further investigations manipulating environmental and/or genetic factors underlying adaptation to pesticides.
- Cognitive and motivational requirements for the emergence of cooperation in a rat social gamePublication . Viana, DS; Gordo, I; Sucena, E; Moita, MABackground: Game theory and the Prisoner's Dilemma (PD) game in particular, which captures the paradox of cooperative interactions that lead to benefits but entail costs to the interacting individuals, have constituted a powerful tool in the study of the mechanisms of reciprocity. However, in non-human animals most tests of reciprocity in PD games have resulted in sustained defection strategies. As a consequence, it has been suggested that under such stringent conditions as the PD game humans alone have evolved the necessary cognitive abilities to engage in reciprocity, namely, numerical discrimination, memory and control of temporal discounting. Methodology/Principal Findings: We use an iterated PD game to test rats (Rattus norvegicus) for the presence of such cognitive abilities by manipulating the strategy of the opponent, Tit-for-Tat and Pseudo-Random, or the relative size of the temptation to defect. We found that rats shape their behaviour according to the opponent's strategy and the relative outcome resulting from cooperative or defective moves. Finally, we show that the behaviour of rats is contingent upon their motivational state (hungry versus sated). Conclusions/Significance: Here we show that rats understand the payoff matrix of the PD game and the strategy of the opponent. Importantly, our findings reveal that rats possess the necessary cognitive capacities for reciprocity-based cooperation to emerge in the context of a prisoner's dilemma. Finally, the validation of the rat as a model to study reciprocity-based cooperation during the PD game opens new avenues of research in experimental neuroscience.
- Co-option of a coordinate system defined by the EGFr and Dpp pathways in the evolution of a morphological noveltyPublication . Vreede, Barbara MI; Lynch, Jeremy A; Roth, Siegfried; Sucena, ÉlioMorphological innovation is an elusive and fascinating concept in evolutionary biology. A novel structure may open up an array of possibilities for adaptation, and thus is fundamental to the evolution of complex multicellular life. We use the respiratory appendages on the dorsal-anterior side of the Drosophila eggshell as a model system for morphological novelty. To study the co-option of genetic pathways in the evolution of this novelty we have compared oogenesis and eggshell patterning in Drosophila melanogaster with Ceratitis capitata, a dipteran whose eggs do not bear dorsal appendages.
- Evolution of mir-92a Underlies Natural Morphological Variation in Drosophila melanogasterPublication . Arif, Saad; Murat, Sophie; Almudi, Isabel; Nunes, Maria D.S.; Bortolamiol-Becet, Diane; McGregor, Naomi S.; Currie, James M.S.; Hughes, Harri; Ronshaugen, Matthew; Sucena, Élio; Lai, Eric C.; Schlötterer, Christian; McGregor, Alistair P.Identifying the genetic mechanisms underlying phenotypic change is essential to understanding how gene regulatory networks and ultimately the genotype-to-phenotype map evolve. It is recognized that microRNAs (miRNAs) have the potential to facilitate evolutionary change [1-3]; however, there are no known examples of natural morphological variation caused by evolutionary changes in miRNA expression. Therefore, the contribution of miRNAs to evolutionary change remains unknown [1, 4]. Drosophila melanogaster subgroup species display a portion of trichome-free cuticle on the femur of the second leg called the "naked valley." It was previously shown that Ultrabithorax (Ubx) is involved in naked valley variation between D. melanogaster and D. simulans [5, 6]. However, naked valley size also varies among populations of D. melanogaster, ranging from 1,000 up to 30,000 μm(2). We investigated the genetic basis of intraspecific differences in the naked valley in D. melanogaster and found that neither Ubx nor shavenbaby (svb) [7, 8] contributes to this morphological difference. Instead, we show that changes in mir-92a expression underlie the evolution of naked valley size in D. melanogaster through repression of shavenoid (sha) [9]. Therefore, our results reveal a novel mechanism for morphological evolution and suggest that modulation of the expression of miRNAs potentially plays a prominent role in generating organismal diversity.
- Filling the gaps of dinosaur eggshell phylogeny: Late Jurassic Theropod clutch with embryos from PortugalPublication . Araújo, Ricardo; Castanhinha, Rui; Martins, Rui M. S.; Mateus, Octávio; Hendrickx, Christophe; Beckmann, F.; Schell, N.; Alves, L. C.The non-avian saurischians that have associated eggshells and embryos are represented only by the sauropodomorph Massospondylus and Coelurosauria (derived theropods), thus missing the basal theropod representatives. We report a dinosaur clutch containing several crushed eggs and embryonic material ascribed to the megalosaurid theropod Torvosaurus. It represents the first associated eggshells and embryos of megalosauroids, thus filling an important phylogenetic gap between two distantly related groups of saurischians. These fossils represent the only unequivocal basal theropod embryos found to date. The assemblage was found in early Tithonian fluvial overbank deposits of the Lourinhã Formation in West Portugal. The morphological, microstructural and chemical characterization results of the eggshell fragments indicate very mild diagenesis. Furthermore, these fossils allow unambiguous association of basal theropod osteology with a specific and unique new eggshell morphology.
- Host Adaptation Is Contingent upon the Infection Route Taken by PathogensPublication . Martins, Nelson E.; Faria, Vitor G.; Teixeira, Luis; Magalhães, Sara; Sucena, ÉlioEvolution of pathogen virulence is affected by the route of infection. Also, alternate infection routes trigger different physiological responses on hosts, impinging on host adaptation and on its interaction with pathogens. Yet, how route of infection may shape adaptation to pathogens has not received much attention at the experimental level. We addressed this question through the experimental evolution of an outbred Drosophila melanogaster population infected by two different routes (oral and systemic) with Pseudomonas entomophila. The two selection regimes led to markedly different evolutionary trajectories. Adaptation to infection through one route did not protect from infection through the alternate route, indicating distinct genetic bases. Finally, relatively to the control population, evolved flies were not more resistant to bacteria other than Pseudomonas and showed higher susceptibility to viral infections. These specificities and trade-offs may contribute to the maintenance of genetic variation for resistance in natural populations. Our data shows that the infection route affects host adaptation and thus, must be considered in studies of host-pathogen interaction.
- Steroid Hormone Signaling Is Essential to Regulate Innate Immune Cells and Fight Bacterial Infection in DrosophilaPublication . Regan, Jennifer C.; Brandão, Ana S.; Leitão, Alexandre B.; Mantas Dias, Ângela Raquel; Sucena, Élio; Jacinto, António; Zaidman-Rémy, AnnaCoupling immunity and development is essential to ensure survival despite changing internal conditions in the organism. Drosophila metamorphosis represents a striking example of drastic and systemic physiological changes that need to be integrated with the innate immune system. However, nothing is known about the mechanisms that coordinate development and immune cell activity in the transition from larva to adult. Here, we reveal that regulation of macrophage-like cells (hemocytes) by the steroid hormone ecdysone is essential for an effective innate immune response over metamorphosis. Although it is generally accepted that steroid hormones impact immunity in mammals, their action on monocytes (e.g. macrophages and neutrophils) is still not well understood. Here in a simpler model system, we used an approach that allows in vivo, cell autonomous analysis of hormonal regulation of innate immune cells, by combining genetic manipulation with flow cytometry, high-resolution time-lapse imaging and tissue-specific transcriptomic analysis. We show that in response to ecdysone, hemocytes rapidly upregulate actin dynamics, motility and phagocytosis of apoptotic corpses, and acquire the ability to chemotax to damaged epithelia. Most importantly, individuals lacking ecdysone-activated hemocytes are defective in bacterial phagocytosis and are fatally susceptible to infection by bacteria ingested at larval stages, despite the normal systemic and local production of antimicrobial peptides. This decrease in survival is comparable to the one observed in pupae lacking immune cells altogether, indicating that ecdysone-regulation is essential for hemocyte immune functions and survival after infection. Microarray analysis of hemocytes revealed a large set of genes regulated at metamorphosis by EcR signaling, among which many are known to function in cell motility, cell shape or phagocytosis. This study demonstrates an important role for steroid hormone regulation of immunity in vivo in Drosophila, and paves the way for genetic dissection of the mechanisms at work behind steroid regulation of innate immune cells.
- A Discrete Model of Drosophila Eggshell Patterning Reveals Cell-Autonomous and Juxtacrine EffectsPublication . Fauré, Adrien; Vreede, Barbara M. I.; Sucena, Élio; Chaouiya, ClaudineThe Drosophila eggshell constitutes a remarkable system for the study of epithelial patterning, both experimentally and through computational modeling. Dorsal eggshell appendages arise from specific regions in the anterior follicular epithelium that covers the oocyte: two groups of cells expressing broad (roof cells) bordered by rhomboid expressing cells (floor cells). Despite the large number of genes known to participate in defining these domains and the important modeling efforts put into this developmental system, key patterning events still lack a proper mechanistic understanding and/or genetic basis, and the literature appears to conflict on some crucial points. We tackle these issues with an original, discrete framework that considers single-cell models that are integrated to construct epithelial models. We first build a phenomenological model that reproduces wild type follicular epithelial patterns, confirming EGF and BMP signaling input as sufficient to establish the major features of this patterning system within the anterior domain. Importantly, this simple model predicts an instructive juxtacrine signal linking the roof and floor domains. To explore this prediction, we define a mechanistic model that integrates the combined effects of cellular genetic networks, cell communication and network adjustment through developmental events. Moreover, we focus on the anterior competence region, and postulate that early BMP signaling participates with early EGF signaling in its specification. This model accurately simulates wild type pattern formation and is able to reproduce, with unprecedented level of precision and completeness, various published gain-of-function and loss-of-function experiments, including perturbations of the BMP pathway previously seen as conflicting results. The result is a coherent model built upon rules that may be generalized to other epithelia and developmental systems.
- Host adaptation to viruses relies on few genes with different cross-resistance propertiesPublication . Martins, N. E.; Faria, V. G.; Nolte, V.; Schlotterer, C.; Teixeira, L.; Sucena, E.; Magalhaes, S.Host adaptation to one parasite may affect its response to others. However, the genetics of these direct and correlated responses remains poorly studied. The overlap between these responses is instrumental for the understanding of host evolution in multiparasite environments. We determined the genetic and phenotypic changes underlying adaptation of Drosophila melanogaster to Drosophila C virus (DCV). Within 20 generations, flies selected with DCV showed increased survival after DCV infection, but also after cricket paralysis virus (CrPV) and flock house virus (FHV) infection. Whole-genome sequencing identified two regions of significant differentiation among treatments, from which candidate genes were functionally tested with RNAi. Three genes were validated--pastrel, a known DCV-response gene, and two other loci, Ubc-E2H and CG8492. Knockdown of Ubc-E2H and pastrel also led to increased sensitivity to CrPV, whereas knockdown of CG8492 increased susceptibility to FHV infection. Therefore, Drosophila adaptation to DCV relies on few major genes, each with different cross-resistance properties, conferring host resistance to several parasites.
- Reversion of developmental mode in insects: evolution from long germband to short germband in the polyembrionic wasp Macrocentrus cingulum BrischkePublication . Sucena, Élio; Vanderberghe, Koen; Zhurov, Vladimir; Grbić, MiodragGermband size in insects has played a central role in our understanding of insect patterning mechanisms and their evolution. The polarity of evolutionary change in insect patterning has been viewed so far as the unidirectional shift from the ancestral short germband patterning of basal hemimetabolous insects to the long germband patterning observed in most modern Holometabola. However, some orders of holometabolic insects display both short and long germband development, though the absence of a clear phylogenetic context does not permit definite conclusions on the polarity of change. Derived hymenoptera, that is, bees and wasps, represent a classical textbook example of long germband development. Yet, in some wasps putative short germband development has been described correlating with lifestyle changes, namely with evolution of endoparasitism and polyembryony. To address the potential reversion from long to short germband, we focused on the family Braconidae, which displays ancestral long germband development, and examined the derived polyembryonic braconid Macrocentrus cingulum. Using SEM analysis of M. cingulum embryogenesis coupled with analyses of embryonic patterning markers, we show that this wasp evolved short germband embryogenesis secondarily, in a way that is reminiscent of embryogenesis in the beetle Tribolium castaneum. This work shows that the evolution of germband size in insects is a reversible process that may correlate with other life-history traits and suggests broader implications on the mechanisms and evolvability of insect development.