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Over onsFaculty of Science and EngineeringOnderzoekFSE research themesAdaptive LifeKey Research

Research Projects II

The second round of integrative projects within the scope of the Adaptive Life programme comprises of 15 PhD projects that will start between July and December 2017.

Three-spined sticklebacks

The eco-evo-devo of migration syndromes
PhD candidate: Aparajitha Ramesh
PIs: Marion Nicolaus, Franjo Weissing & Ton Groothuis

Mouse
Obese and normal mouse
Winter moth
Mosquito
Gut microbiome

Eco-evolutionary dynamics and control of the gut microbiome
PhD candidate: Kevin Kort
PIs: Sander van Doorn, Hermie Harmsen & Franjo Weissing

Spotted-winged Drosophila

The role of microbial symbionts in the niche shift of Drososphila suzukii
PhD candidate: Kiran Gurung
PIs: Bregje Wertheim, Joana Falcao Salles & Jean-Christophe Billeter

Edible dormouse
Mediterranean drylands

Facilitation - A novel mechanism of adaptive capacity
PhD candidate: Megan Korte
PIs: Chris Smit, Rampal Etienne & Louis van de Zande

Potato field
Zebra finches

Parsing developmental plasticity of personality in zebra finches
PhD candidate: Yoran Gerritsma
PIs: Simon Verhulst & Sietse de Boer

Mosquitoes

Adaptive diversity and eco-evolutionary dynamics
PhD candidate: Raphaël Scherrer
PIs: Rampal Etienne, Sander van Doorn & Michael Fontaine

Thorn-tailed rayadito
Apples

The evolutionary impact of habitat-dependent reproductive decisions - Comparing apples and grapes
PhD candidate: Xiaocui Wang
PIs: Jean-Christophe Billeter & Martine Maan


The eco-evo-devo of migration syndromes
Three-spined sticklebacks

The existence of animal personality (consistent individual differences in behaviours across contexts) and behavioural syndromes (correlations among personality traits) is intriguing, since one would expect that more flexible behaviour is selectively favoured. Understanding syndromes is therefore important. An excellent example is the migration syndrome found in many species. In many animal populations individuals differ considerably in their migration tendency. The extreme case is ‘partial migration,’ where only a fraction of the population migrates. Migrants often represent a non-random subset of the population that differ consistently in sets of phenotypic features (morphology, physiology, behaviour). Individual differences in this ‘migration syndrome’ are ideal to study the emergence of individual variation from both a mechanistic and an evolutionary perspective. By a combination of theoretical modelling and empirical studies, we will address the following questions:

  • Under which conditions of spatiotemporal variation and predictability of the environment should we predict partial migration?
  • Which factors determine differences in migration tendency between populations?
  • Which individuals in a partially migrating population migrate and which individuals stay?
  • When is the migration decision taken (early in development vs later in life) and by whom (the migrant itself vs parental effects)?
  • What are the eco-evolutionary implications of partial migration?

We will use three-spined sticklebacks (Gasterosteus aculeatus) as our study system, because they inhabit ecologically diverse conditions, have populations exhibiting no, partial or full migration. In two field studies, encompassing a spectrum of populations and seasons, we will quantify the within- and between-population variation in migration tendency and the corresponding syndrome. In two lab experiments, we will investigate the emergence of the migration syndrome and possibility for parental programming. The empirical studies will be complemented by theoretical modelling to derive testable predictions and to provide a framework for interpreting the empirical results. Together this will provide a deeper understanding of three intriguing basic biological phenomena: individual differences, behavioural syndromes and partial migration.

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The role of the microbiome in disease–associated mental and behavioral problems - The case of phenylketonuria (PKU)
Mouse

The microbiota has been implicated in the evolution of social behavior and developmental programming of the brain, affecting social and cognitive behaviors. It has been demonstrated that strain-specific behavioral profiles could be transplanted by interchanging microbiota between strains. This is interesting as recent PKU research in our facility has demonstrated that identical mutations in the liver enzyme phenylalaninehydroxylase – leading to highly elevated Phenylalanine-levels in blood and brain that correlate with the severity of behavioral deficits in PKU patients – generate strain-specific behavioral consequences. Surprisingly, one strain (C57Bl/6) does not show the expected PKU-specific behavioral deficits whereas the other strain (BTBR) does. Considering the similarities between behaviors, neurotrophins and synaptic proteins affected by altered microbiota and PKU, we hypothesize that the microbiome could be a determining factor for the different consequences of PKU found between these strains.

In this proposal we will address the following research questions: 1) How does the PKU environment influence the gut microbiota in PKU mice of both strains? 2) To what degree does the gut microbiota influence behavior in the PKU mice of both strains? and 3) Can manipulation of the gut microbiota (e.g. by diet or transplantations) normalize the PKU-specific behavioral deficits? In collaboration with the UMCG we will also analyse the microbiota of PKU patients, to further substantiate the potential decisive role of microbiota in PKU. This research could provide 1) new insights in the link between the composition of the microbiota and behavior in general and more specifically in the PKU mice and 2) new therapeutic approaches to prevent cognitive and emotional malfunctioning of PKU patients. Within GELIFES, this proposal is anticipated to be a starting point of a long-term research topic on the microbiome, the gut-brain axis determining behavior, and its relevance to health and disease.

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Fitness and reproductive success - Developmental plasticity as tools for adaptation
Obese and normal mouse

The perinatal milieu may provide a forecast about the future conditions of the external world that an individual will subsequently inhabit, which often underlies a predictive adaptive response (PAR). If this forecast does not materialize, however, the PAR may turn out to become maladaptive. A noticeable example is the increased incidence of adults with cardiometabolic diseases in affluent societies, who have been set out during the perinatal stage for a poor nutritional future. While such a mismatch (i.e. from nutritionally poor during the perinatal stage to nutritionally rich during adulthood) may have impeding health consequences later in life, the effect on fitness (the ability to reproduce and contribute to future generations) may be relatively small. The opposite case (i.e. from nutritionally rich to poor) may be more deleterious in terms of maintenance of sustainable health and fitness. In this proposal, we will directly test the PAR hypothesis in mice (C57BL6/J - Mus Musculus) by exposing breeding pairs of mice to either a diet ad libitum or calorie-restricted (80%), from which the offspring will then be exposed to either high, medium, or low nutritional conditions by manipulating litter size. Manipulation of litter size has been shown to cause differences in energy transfer from parents to offspring. We will then subject offspring after weaning to nutritionally matching or mismatching conditions and investigate various sustainable health and fitness parameters as well as their reproductive success in this generation, as well as in their descendants. Matching/mismatching effects on sustainable health, fitness, and reproduction in subsequent generations can be anticipated because parents (of which the individual variation in body structure, physiology and behavior has been caused by their perinatal condition) are the environmental interface for the next generation. Studying this under controlled laboratory conditions offers a unique insight into the origin on phenotypic variation.

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Evolutionary dynamics to understand the mechanisms of adaptation to changing ecological conditions in the winter moth
Winter moth

Winter moths are one of the few species that have been shown to rapidly adapt to selection pressures altered by climate change. Over the past decades, they have delayed their seasonal timing of egg-hatching as they evolved a reduced temperature sensitivity during egg development. This has led to a better match with the phenology of the oak bud burst on which the caterpillars critically depend for their food. In this proposal, I aim to reveal the feedback between the trait variation and population dynamics, to elucidate the mechanisms of the winter moths' adaptive response to its changing environment. Firstly, I will sequence genomes of winter moths stored over the past 20 years, specifically those collected at the start and end of this time course, and from a few selected periods after strong population declines. By identifying ‘signatures of selection’ across the whole genome, I will identify loci that were affected strongly by population decline. This unbiased approach provides insight in which parts of the genome have been altered due to changing selection pressures. Secondly, I will investigate the genes that are involved in temperature (in)sensitivity during development. For this, I will first characterize embryonic development under different temperature regimes, defining threshold temperature and the rate of development. I will then use this information to measure gene-expression in the eggs of split-brood experiments, transferred to different temperatures at key moments during development. Thirdly, I will track allele changes in these previously determined genomic regions throughout periods of increasing selection pressure and explain changes based on two ecological processes: the annual phenological match between the winter moth and the oak, and the winter moth population numbers. In this way, I can link ecological and evolutionary processes as they act on the genomic bases of a key life-history trait.

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How species of malaria vector mosquitoes emerged and evolved in the Anopheles gambiae complex in face of widespread introgressive hybridization - Theoretical and empirical approaches
Mosquito

Evidence of introgressive hybridization is widespread in the tree of life, occurring especially among closely related species in various clades such as hominids, Anopheline mosquitoes and Heliconius butterflies. High-resolution genomic-data have recently been produced and enabled scientists to perform in-depth investigation of the extent and evolutionary consequences of introgression on the adaptation and speciation processes. However, major challenges remain to redefine key biological concepts and our understating of speciation: How can species diverge and adapt to distinct ecological niches if their reproductive barriers are porous? What genomic features and processes keep species as separate entities if their genomes are a blend of private genomic sequences that have evolved within the species and genomic information borrowed from related organisms but with an independent evolutionary past? What are the adaptive implications of introgression and how to quantify them? This project explores the genetic architecture of divergence, adaptation and speciation with gene-flow in the medically important A. gambiae species complex, mosquito vectors of the deadly Plasmodium sp. parasite causing malaria. We will use state-of-the-art population genetic approaches to analyse mosquitoes’ genetic diversity using new comprehensive genomic data about the species complex. From a theoretical perspective, we will use mechanistic models to simulate conditions under which species of A. gambiae complex diverged and specialize ecologically in face of gene flow; we will also simulate introgression occurring between individuals to analyse the resilience of allele networks occurring in nature and, using agent-based models, we will aim to understand how patterns of gene flow can become established and be affected by changes in the environment. Finally, we will try to integrate the results produced in the previous three approaches in a definitive theory of speciation that incorporates the concept of gene exchange and porous reproductive barriers.

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Eco-evolutionary dynamics and control of the gut microbiome
Gut microbiome

The intestinal tracts of human and other animals hosts a highly diverse, dynamic and personalised community of microbes that plays a vital role in regulating digestion, immunity and health. Recent next-generation metagenomic sequencing efforts have provided an unprecedented view of the species composition of the gut microbiota, its development over life, and the way it adjusts in response to changes in diet or lifestyle. Moreover, abnormal microbiota have been associated with several diseases, including cancer, chronic inflammatory bowel diseases and psychiatric disorders. Currently, however, we lack a mechanistic understanding of the processes that shape the diversity and ecological interactions within the microbial community, which makes it difficult to intervene in a targeted way to improve the function of the gut microbiota by means of pre- or probiotics. Here we propose a research project aimed at developing a computational eco-evolutionary framework for modelling the microbiome. This framework builds on genome-scale models of microbial metabolism to quantify the fluxes of metabolites between microbial species, the gut environment, and the host, in order to reconstruct the ecological interactions within the microbial community. We will characterise the ecological assembly rules of the microbial community, investigate whether the feedback between metabolic fluxes and community assembly can explain the presence of alternative stable community states, and study how to induce transitions between such alternative stable states. We will also investigate the process of coevolution between microbial species, study under what conditions evolution of the microbiota aligns with the interests of the hosts and explore mechanisms to direct evolution towards an improved ecosystem functioning. Insights from these ecological and evolutionary analysis will be applied to a model of microbial imbalance in patients suffering from inflammatory bowel disease, with the aim of identifying novel targets for pre- and probiotic treatment.

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The role of microbial symbionts in the niche shift of Drososphila suzukii
Spotted-winged Drosophila

Insects are associated with microbes that have demonstrable effects on the insect metabolism and performance. For pest insects, it is especially important to understand these associations, as these can be causal to their pest status, and it can provide targets for pest management approaches. The insect-microbe associations are often vital for the fitness of the host. Drosophila suzukii, an invasive pest, attacks a variety of unripe fruits, unlike the other members of Drosophilidae, which feed on rotten fruits.

What is the role of microbial symbionts of D. suzukii for its niche shift from rotting to fresh ripening fruits, and its ability to feed on a wide variety of fruits? Importantly, larvae of Drosophila critically depend on yeasts and other microorganisms for the uptake of essential nutrients for body-tissue construction. The abundance and composition of microbial communities differ vastly in the new niche to which D. suzukii adapted. I want to examine the role of bacterial symbionts and yeasts on D. suzukii development, fitness and behaviour. The metabolism, longevity and pheromone production of the sibling species D. melanogaster have all been shown to depend on microbiome composition predicting a similar function of the microbiome in D. suzukii.

I hypothesize that the ecological niche shift and the polyphagous nature of D. suzukii is due to its associations with microbial symbionts. I will first examine the diversity, the co-occurrence patterns and infection rates of the associated microbes of D. suzukii in a range of fruits. I will further dissect the functional roles of microbial symbionts on their hosts' development and behaviour. Additionally, I will study their effect on chemical communication by analysing how the pheromones of D. suzukii are influenced by their symbionts. This will reveal whether and how microbes may have contributed to the ecological niche shift of this invasive pest species.

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What doesn`t kill you, makes you stronger - Increased lifespan in hibernators despite DNA damage
Edible dormouse

Hibernation is an adaptation to cope with harsh environmental conditions through gross reduction of metabolism (torpor). In line with the rate of living hypothesis, hibernators show increased longevity. During hibernation, periods of torpor are alternated with short periods of high metabolism and euthermic body temperatures (arousals). Remarkably, extended DNA damage was found to accumulate during torpor and rapidly normalized during arousals in hibernating hamster. This DNA damage/repair during torpor and arousal cycles, may lead to genomic instability, which cannot be reconciled with the hibernators’ extended lifespan and absence of tumor genesis. Consequently, we hypothesize that hibernators have developed an evolutionary adaptive mechanism to deal with DNA breaks, either by deploying superior repair mechanisms or by clearing of damaged cells. This adaptive mechanism will be the main objective of this research in combination with its effects on longevity and senescence. Inducing torpor in mice (Mus musculus) has shown to increase DNA damage in a pilot study. One of the key challenges is to confirm that daily torpor induced by the work-for-food paradigm will induce similar DNA damage/repair mechanisms in mice, allowing for a wide range of molecular techniques. These results will be compared with an obligatory deep hibernator, the edible dormouse (Glis glis). This species is a record holder for hibernation and torpor duration. It allows us to experimentally assess the role of torpor and arousals in DNA damage/repair mechanisms and compare these results with the effects of daily torpor in the house mouse. These two animal models allow us to use a well-established molecular toolbox in the house mouse to find relevant and potentially novel modes of DNA repair as well as the possibility to find long term consequences of DNA damage during hibernation.

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Facilitation - A novel mechanism of adaptive capacity
Mediterranean drylands

One of today’s largest concerns is the worldwide rapid degradation of ecosystems due to human-induced environmental change. If these environmental changes occur too fast for species to adapt, biodiversity will further decline, with negative impacts for ecosystem functioning and human wellbeing. Hence, it is of crucial importance to understand which mechanisms allow species to timely adapt. Interspecific plant facilitation (positive species interactions) may be one of these mechanisms. Facilitation plays an important role in upholding plant species diversity, especially in drylands that are particularly vulnerable to climate change. However, the role of interspecific facilitation for the adaptive diversity and eco-evolutionary dynamics in plant communities has so far received little attention. In this project, we hypothesize that interspecific facilitation can act as a mechanism of adaptive capacity: facilitation by nurse plants may conserve genetic variation in beneficiary species that promotes their adaptive capacity to new environmental conditions. To test this novel hypothesis, we propose a combination of reciprocal experiments, greenhouse studies, molecular analyses, and dynamic modelling. As a study system we will use Brachypodium distachyon, a model grass with a sequenced genome that has been intensively studied by the agricultural community. In a field study in southern Spain, we will compare B. distachyon populations with and without facilitating nurse plants (bunch grass Stipa tenacissima) in terms of physiological traits (photosynthesis, gas exchange, water use efficiency, stomatal conductance, transpiration, phenology, growth rate, biomass) and genetic variation using recently developed microsatellites (simple sequence repeat: SSR). In a reciprocal sowing experiment, we will sow seeds from facilitated populations into bare patches, and seeds from unfacilitated populations under the canopy of S. tenacissima, and follow plant performance and ecophysiological traits. In a supplementary greenhouse study, we will grow plants from facilitated and unfacilitated populations, as well as their crossbred line, and subject plants to a combination of drought and temperature treatments for multiple generations. We will select for plants with the highest fitness (e.g. reproductive traits) and test for evolved adaptive capacity and fitness to elevated drought and temperature. In parallel with the empirical studies, we will develop a simulation model to predict how the adaptive diversity and eco-evolutionary dynamics of beneficiary plants evolve over time under different environmental scenarios. Our project will lead to an improved understanding of facilitation for the adaptive diversity and evolutionary dynamics of beneficiary plants, a potential novel mechanism for plant species to cope with ongoing environmental change.

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Identification of salt tolerant endophytic fungi from Solanaceae plants and evaluation of molecular mechanisms associated with endophytic fungi-induced stress tolerance
Potato field

Plant-microbe interactions are integral part of any ecosystem. During the long period of co-existence, different relationships have evolved between endophytic fungi and their host plants and they can be categorized as: (i) mutualistic, (ii) antagonistic (pathogenic), and (iii) neutralistic (commensalistic). Fungus-host plant relationships should be regarded as flexible interaction, whose directionality is determined by slight differences in fungal gene expression in response to the host reaction, or conversely, by host recognition and response to the fungi. Hence, slight genetic differences in the genomes of both partners control the outcome of the symbiosis. The genetic background, nutrient level and ecological habitats of the host plants are considered as the important-choice factors on the population structure of the endophytic fungi that, in turn, confer benefits to the plant, such as stimulated growth, increased resistance to biotic and abiotic stresses, as well as accumulation of bioactive components. In this context, discovering how endophytic microbes collaborate to improve the hardiness of plants is a key to sustainable agriculture that can help to meet increasing food demands.

Amongst the major environmental stresses affecting crop productivity, salinity and drought are the major ones. Theses stresses induce a range of physiological and biochemical responses in plants. There are many research findings to indicate the beneficial effect of endophytic fungi in imparting tolerance to abiotic stresses. However, the exact mechanisms of the acclimation response are not well studied. In this proposal it is envisaged to examine the ecological significance of endophytic fungi-induced stress tolerance in Solanaceae plants. We propose to identify abiotic stress tolerant fungi from salt adapted Solanaceae plants and evaluate their ability in imparting stress tolerance to sensitive plants. Since many plant processes involved in stress acclimation have been attributed to endophytic fungal association, attempts would be made to examine the molecular mechanisms of plant-fungal association.

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Parsing developmental plasticity of personality in zebra finches
Zebra finches

In wildlife, human, and laboratory animal populations, considerable variability exists among individuals in their trait-like patterns of behavioural and physiological responses to salient environmental challenges and opportunities. This individual variation in so-called personalities (also temperament or coping style) has important functional consequences in terms of fitness of the individual. It remains largely unknown how plastic certain personality traits are during an individual’s lifetime and we aim to understand the proximate neuromolecular determinants of personality differences.
In the proposed project we will investigate the effect of early developmental environment manipulations on (1) avian personality traits including sociality in adulthood and (2) selective neuromolecular mechanisms underlying the behavioural expressions of personality.

This project builds on a recently started Adaptive Life project on zebra finches housed in outdoor aviaries, with either ‘easy’ or ‘hard’ foraging conditions. We thereby influence the developmental conditions of the offspring, as there is less parental care in hard foraging conditions. Recent findings indicate that variation in developmental conditions causes differences in certain aspects of personality, e.g. sociality, flexibility and aggressiveness. Avian personality will be assessed using a wide array of behavioural tests covering different personality dimensions, including tests of dominance, boldness, reversal learning and sociality and we will determine the relationships between these different behavioural facets of personality.
In the same animals, we will study the putative neuromolecular mechanisms that give rise to developmentally induced behavioural changes. These include measures of serotonin, dopamine and nonapeptide (the vasopressin- and oxytocin-like neuropeptides) signalling in key nodes of the brain’s social decision–making network. These neuromolecular mechanisms will provide us with a first insight in the causative chain from developmental conditions to personality.
The proposed project, by integrating behavioural biology, neurobiology and ontogeny, will critically advance our understanding of the causes of consistent individual differences.

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Adaptive diversity and eco-evolutionary dynamics
Mosquitoes

While the genetic basis of more and more traits is being unravelled, the complexity of the genome has remained underappreciated in making theories on one of the most important questions in evolution, how do species form? Most of the models of speciation make simplistic assumptions with respect to the genomic basis of potential traits under disruptive selection, or leading to reproductive isolation. We know recombination is heterogeneous across the genome (linkage blocks are often present, separated by hot spots of recombination) and it is likely that most genes act in epistasis (the effect of an allele depends on its genetic background) in their contribution to individual fitness. These two fundamental properties are likely interacting with natural or sexual selection regimes to lead to divergence between populations and speciation, but their relative influence on the divergence process is unknown. In this study, we propose tackling the question of the relationship between genome structure and eco-evolutionary divergence using individual-based models to simulate speciation under various scenarios of genomic complexity and ecological interactions and investigate their impact on diversification, and diversity. We will empirically test the link between recombination and divergence across the genome in a case study of malaria mosquitoes Anopheles gambiae showing putative ecological speciation mediated by reduced recombination. This project will help build a more integrative theory of speciation as well as in enhancing further research in research on malaria vectors.

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Do parental effects mediate adaptation to climate differences? - A study in a bird species breeding at different latitudes
Thorn-tailed rayadito

To what extent and how organisms adapt to changing or extreme environments has become an urgent biological question. One effective parental response to extreme climatic differences (i.e. breeding season length mediated by temperature and food availability) is altering offspring developmental time through parental effects. I will test how parents adjust pre- and postnatal investment responding to such environmental variation in thorn-tailed rayaditos, Aphrastura spinicauda. This songbird breeds along a wide latitudinal gradient with extreme climatic variation (long to short food peaks, extreme warm to extreme cold environments). I will measure parental adjustment of offspring development in three populations. I expect the high-latitude population (cold environment, short food peaks) to have greater incubation attendance (hypothesis 1) and higher yolk testosterone and thyroid hormones deposition (hypothesis 2), accelerating embryo development. More hormones may increase nestling competitiveness and begging, parental provisioning, and nestling growth (hypothesis 3). First, I will test whether populations differ in egg quality, incubation patterns, nestling begging and fitness, and parental provisioning. Subsequently, I will test the hypotheses as follows:
H1: I will mimic increased incubation attendance using incubators to accelerate embryo developmental time. After relocating hatchlings, I expect higher fledging weight and survival of faster hatching nestlings, interacting with origin.
H2: I will manipulate yolk testosterone and thyroid hormones levels, incubate and hatch the eggs in incubators, revealing whether prenatal maternal effects influence embryo development and fitness, and whether this differs between populations.
H3: Hatchlings from hormone-manipulated, control and untreated eggs will be relocated (incubator to nests) and subjected to standard begging tests. I expect that nestlings from hormonally-augmented eggs will beg more, resulting in accelerated nestling development, higher fledging weight and survival.
The results will show to what extent and how evolution has shaped pre-and postnatal parental effects and phenotypic plasticity for adaptation to different environments.

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The evolutionary impact of habitat-dependent reproductive decisions - Comparing apples and grapes
Apples

Food is important! Food availability is a major factor influencing reproduction because of the high nutritional demand of gamete production and offspring rearing. Most food resources are spatially and temporally heterogeneous requiring finely tuned sensory perception for optimal foraging. The same holds true for the detection and evaluation of potential mates. The evolution of different sensory abilities, favoured by different environments but also affecting sexual communication, is the basis of the sensory drive hypothesis. This theory provides a potential mechanism for the evolution of pre-mating isolation between populations exploiting different food resources or habitats. To date, evidence for this evolutionary mechanism comes mostly from visual communication in aquatic species living in different light environments. Here, I propose to combine our unique expertise in evolutionary ecology and neurogenetics to explore the role of sensory divergence in reducing gene flow between populations that exploit alternative food resources in Drosophila melanogaster. I will characterize phenotypic and genetic differences of natural D. melanogaster populations (‘ecotypes’) exploiting alternative food resources. Using transcriptomics, I will identify the chemosensory receptors underlying the sensory response of different ecotypes to their food habitats and causally link them to changes in habitat and mate preference. Through a reciprocal transplant experiment, I will establish the contributions of genetic adaptation and phenotypic plasticity to viability, food preference and mate choice. Finally, I will assess whether differences between ecotypes actually translate into gene flow reduction under natural reproductive conditions, including multiple matings and different food environments. Thus, by integrating proximate and ultimate aspects of food-associated population divergence, we will advance our understanding of the role of sensory divergence in reducing gene flow between populations at the single gene level, providing much needed candidate genes and neuronal mechanisms for adaptation and speciation.

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Laatst gewijzigd:19 september 2017 10:52