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Mortier, F.

Publications and source records attributed to Mortier, F..

12 recordsLinked to original sources

Highly repeatable phenotypic consequences of whole genome duplication in Spirodela polyrhiza

Whole-genome duplication (WGD) is widespread in plants, yet the extent to which it yields predictable phenotypic outcomes remains unclear. Here we show that the phenotypic consequences of genome doubling in a duckweed model system, Spirodela polyrhiza, are highly repeatable and largely deterministic. We previously generated three independent colchicine-induced autotetraploids from each of nine globally distributed diploid genotypes and, here, quantified growth and morphology across a salt gradient. In benign conditions, diploids grew faster, whereas tetraploids had larger, thicker fronds; with increasing salinity, the diploid advantage diminished and tetraploids often matched or exceeded diploid growth. Variance partitioning revealed that ploidy per se explains more phenotypic variation, including salt tolerance, than genotypic background, with rare within-genotype stochasticity. These results indicate that the shifts in morphology and stress tolerance from genome doubling are predictable and can outweigh the phenotypic effect from genetic sequence diversity.

evolutionary biology↗

Additive effects of environmental and demographic variation shape the repeatability of evolution across replicated experiments

The repeatability of evolution is fundamentally important for understanding the origin and diversification of life as well as for developing evolutionary forecasting tools. Repeatability is limited by stochasticity, here defined as changes that are independent of genotypic fitness effects. Over short timescales, the two main sources of stochasticity of evolutionary change are environmental stochasticity and demographic (life-history) stochasticity. Quantifying the relative importance of these two sources of stochasticity in driving fitness outcomes is crucially important for predicting evolutionary responses. To gain insights in the effects of stochasticity, five institutes replicated an evolutionary experiment exposing Caenorhabditis elegans to novel rearing conditions. Replication across the institutes led to variation in selective environments, e.g. through divergent microbiomes among institutes. Replication within institutes was done across demographic treatments that influence the potential for population-size dependent fluctuations in allele frequencies (drift) and genetic hitchhiking (draft). We found high among-institute variation in fitness outcomes, which was partially explained by variation in microbiota. Whereas lab-specific effects explained most of the variance in mean fitness, the repeatability of fitness outcomes depended more on demographic heterogeneity. Specifically, population bottlenecks resulted in high among-replicate variation in fitness. When combined, environmental and demographic stochasticity additively reduced repeatability, underlining their additive importance in developing evolutionary forecasting tools. These results further highlight the importance of statistically integrating heterogeneity in experimental evolution to identify factors constraining outcome repeatability and study replicability.

evolutionary biology↗

Polyploid - diploid coexistence in the greater duckweed Spirodela polyrhiza

Polyploidy, resulting from whole-genome duplication (WGD), is widespread among plants and originates in sympatry with their lower-ploidy progenitors. New polyploids can only succeed when they overcome the competitive disadvantage against their progenitors or through sufficient niche differentiation as resulting in a negative frequency dependent growth. Because polyploidy is frequently associated with cold, dry, and saline environments, stress is anticipated to be the key to polyploid success. We examined the invasion of neotetraploid duckweed (Spirodela polyrhiza) strains in populations of their direct diploid progenitors, in control and salt stress conditions in replicated microcosms. We also tested the reverse scenario, that is, the invasion of diploids in neotetraploid populations, to determine if the initial proportion of tetraploids affects the outcome of competition. Our results showed that the proportion of tetraploids declined in all tetraploid and all diploid invasions and it did so at a different rate than expected from only differences in intrinsic growth rate. Salt stress affected the decline in tetraploid proportion differently across strains. We also found evidence for negative frequency dependent growth that, nonetheless, was insufficient to overcome competitive disadvantages of neopolyploids towards their diploid progenitor. We showcase a robust quantitative pipeline from flow cytometry of mixed-ploidy populations to population model fitting. In doing so, we demonstrate the important effect of competition and frequency dependency on neopolyploid establishment. Therefore, we caution for inferring neopolyploid success from intrinsic growth rates alone.

plant biology↗

Interspecific transfer of genetic information through polyploid bridges

Many organisms have more than two sets of chromosomes, due to whole genome duplication (WGD), and are thus polyploid. Despite usually being an ephemeral state in the history of life, polyploidy is widely recognized as an important source of genetic novelty over macroevolutionary scales. More recently, polyploidy has also been shown to facilitate interspecific gene flow, circumventing reproductive barriers between their diploid ancestors. Yet, the implications of WGD-linked introgression on community-level evolutionary dynamics remain unknown. Here, we develop a model of cytotype dynamics within mixed-ploidy populations to demonstrate that polyploidy can in fact serve as a bridge for gene flow between diploid lineages, where introgression is fully or partially hampered by the species barrier. Polyploid bridges emerge in the presence of triploid organisms, which despite critically low levels of viability, can still allow the transfer of alleles between diploid states of independently evolving mixed-ploidy species. Notably, while marked genetic divergence prevents WGD-mediated interspecific gene flow, we show that increased recombination rates can offset these evolutionary constraints, which allows a more efficient sorting of alleles at higher-ploidy levels before introgression into diploid gene pools. Additionally, we derive an analytical approximation for the rate of gene flow at the tetraploid level necessary to supersede introgression between diploids with non-zero introgression rates, which is especially relevant for plant species complexes, where interspecific gene flow is ubiquitous. Altogether, our results illustrate the potential impact of polyploid bridges on evolutionary change within and between mixed-ploidy populations.

evolutionary biology↗

A metabolic perspective on polyploid invasion and the emergence of life histories: insights from a mechanistic model

Whole genome duplication (WGD, polyploidization), the fusion of unreduced gametes, has been identified as a driver of genetic and phenotypic novelty. Unreduced gamete formation is common in a wide range of species, but surprisingly, few polyploidization events have shown to be ecologically successful. Positive density dependence, by minority cytotype exclusion, and niche shifts are currently considered the most important drivers behind ecological failure or success. Genome doubling also results in increased cell sizes and metabolic expenses which, on their own may be sufficient to drive polyploid establishment in stable environments where their simple ancestors thrive. We developed a mechanistic model, motivated by data from natural plant polyploid species, to test whether realistic changes in size and metabolic efficiency allow polyploids to coexist with, or even invade, their original diploid population. Central to the model is metabolic efficiency, a functional trait that determines how energy gained from size-dependent photosynthetic metabolism is allocated to basal metabolism, somatic growth and reproductive growth. Polyploid invasion was observed across a wide range of metabolic efficiency differences between polyploids and their ancestors. Higher metabolic efficiency facilitates polyploid invasion, but even with minor deficits, establishment was facilitated by recurrent formation in these settings of high competition for nutrients. Interestingly, a long-term coexistence with the diploid ancestor was found to be possible only within a narrow range of this parameter space. Perenniality of the plants did not qualitatively affect these insights. Feedbacks between size-dependent metabolism and allocation of gained energy generated eventually size and age differences, resulting in intra- and intercytotype competition for nutrients as the major force for population dynamics. We thus demonstrate that changes in metabolic efficiency on their own are sufficient to impose establishment, but these advantages do not need to be substantial.

ecology↗

Interacting host modifier systems control Wolbachia-induced cytoplasmic incompatibility in a haplodiploid mite

Many reproductive parasites such as Wolbachia spread within host populations by inducing cytoplasmic incompatibility (CI). CI occurs when parasite-modified sperm fertilizes uninfected eggs. In haplodiploid hosts, CI can lead to different phenotypes depending on whether the fertilized eggs die or develop into males. Genetic conflict theories predict the evolution of host modulation of CI, which in turn strongly influences the stability of reproductive parasitism. Yet, despite the ubiquity of CI-inducing parasites in nature, there is no conclusive evidence for strong intraspecific host modulation of CI strength and phenotype. Here, we tested for intraspecific host modulation of Wolbachia-induced CI in haplodiploid Tetranychus spider mites. Using a single CI-inducing Wolbachia variant and mitochondrion, a Tetranychus urticae nuclear panel was created that consisted of infected and cured near-isogenic lines. We performed a highly replicated age-synchronized full diallel cross comprised of incompatible and compatible control crosses. We uncovered host modifier systems that strongly suppress CI strength when carried by infected T. urticae males. Interspecific crosses showed that the male modifier systems suppress CI strength across species boundaries. We also observed a continuum of CI phenotypes in our crosses and identified strong intraspecific female modulation of CI phenotype when paired with a specific male genotype. Crosses established a recessive genetic basis for the maternal effect and were consistent with polygenic Mendelian inheritance. Our findings identify spermatogenesis as an important target of selection for host suppression of CI strength and underscore the importance of maternal genetic effects for the CI phenotype. Both mechanisms interacted with the genotype of the mating partner, revealing that intraspecific host modulation of CI strength and phenotype is underpinned by complex genetic architectures.

evolutionary biology↗

Honest cues contribute to male choice for female guarding in a herbivorous spider mite.

Mate choice is a wide-spread phenomenon with important effects on ecological and evolutionary dynamics of successive generations. Increasing evidence shows that males can choose females if females vary in quality and these mating choices can strongly impact fitness. In the herbivorous spider mite Tetranychus urticae males engage in precopulatory mate guarding of quiescent females, and it is known that females vary in their time to sexual maturity and fecundity. However, our understanding of how males maximize their reproductive success and which female phenotypic traits are important cues for their mating decisions are still limited. In many arthropod species, female body size and pheromones are well known proxies for fecundity. These traits--and thus possibly male mating decisions--are however sensitive to environmental (dietary) stress. By allowing males to freely choose amongst many (synchronized) females in a controlled semi natural environment, we found that guarded females have a higher fecundity and are closer to sexual maturity than non-guarded females. Despite the fact that female body size was positively correlated with fecundity and significantly influenced by the environment, males did not discriminate on body size nor did we find evidence that they used other cues like cuticular pheromones or copying behavior (social cues). In conclusion we were able to show male mate preference for females that are closer to sexual maturity and have higher fecundity, but we were unable to identify the female traits that signal this information

animal behavior and cognition↗

Genetically diverse populations spread faster in benign but not in challenging environments

Population spread from a limited pool of founding propagules is at the basis of biological invasions. The size and genetic variation of these propagules eventually affect whether the invasion is successful or not. The inevitable bottleneck at introduction decreases genetic diversity, and therefore should affect population growth and spread. However, many heavily bottlenecked invasive populations have been successful in nature. These negative effects of a genetic bottleneck are typically considered to be relaxed in benign environments because of a release from stress. Despite its relevance to understand and predict invasions, empirical evidence on the role of genetic diversity in relation to habitat quality is largely lacking. We use the mite Tetranychus urticae Koch as a model to experimentally assess spread rate and the size of genetically depleted inbred populations and enriched mixed populations. This was assessed in replicated linear patch systems consisting of benign (bean), challenging (tomato) or a gradient (bean to tomato) habitat. We find that genetic diversity increased population spread rates in the benign but not in the challenging habitat. Additionally, variance in spread was consistently higher in genetically poor populations and highest in the challenging habitat. Our experiment challenges the general view that a bottleneck in genetic variation decreases invasion success in challenging, but not in benign environments.

evolutionary biology↗

Individual heterogeneity and its importance for metapopulation dynamics.

Landscape connectedness shapes the exchange of individuals among patches, and hence metapopulation connectivity and dynamics. Connectedness, and its resulting effects on connectivity are therefore rightfully central in conservation biology. However, besides determining demographic fluxes of individuals between patches, connectedness also generates phenotypic sorting and thus impacts local and regional eco-evolutionary dynamics. Despite the central role of connectedness, its effects on individual phenotypic heterogeneity and spatial organization are so far neglected in theory and applications. Through experimental metapopulations of Tetranychus urticae (two-spotted spider mite) with three levels of landscape connectedness and by regularly removing phenotypic structure in a subset of these populations, we tested how regional and local population dynamics are determined both by network connectedness and phenotypic spatial organization. We find that the self-organizing phenotypic spatial structure increases local equilibrium population sizes and variability. It in contrast dampens the effects of imposed connectedness differences on population sizes and is therefore anticipated to improve metapopulation persistence. Contrary to theoretical expectations, the most locally connected patches within the network showed an overall reduced local population size, possibly originating from a faster depletion of resources from immigrants or transiting individuals. This experiment shows how metapopulation dynamics can significantly deviate from theoretical expectations due to individual heterogeneity. This potential rescue effect stemming from phenotypical self-organization in space is a key point to consider for conservation actions, especially based on translocations.

ecology↗

Evolutionary history determines population spread rate in a stochastic, rather than in a deterministic way

Fragmentation of natural landscapes results in habitat and connectedness loss, making it one of the most impactful avenues of anthropogenic environmental degradation. Populations living in a fragmented landscape can adapt to this context, as witnessed in changing dispersal strategies, levels of local adaptation and changing life-history traits. This evolution, however, can have ecological consequences beyond a fragmented range. Since invasive dynamics are driven by the same traits affected by fragmentation, the question arises whether fragmented populations evolve to be successful invaders. In this study we assess population spread during three generations of two-spotted spider mite (Tetranychus urticae) population in a replicated experiment. Experimental populations evolved independently in replicated experimental metapopulations differing only in the level of habitat connectedness as determined by the inter-patch distance. We find that habitat connectedness did not meaningfully explain variation in population spread rate. Rather, variation within experimental populations that shared the same level of connectedness during evolution was larger than the one across these levels. Therefore, we conclude that experimental populations evolved different population spread capacities as a result of their specific evolutionary background independent but of the connectedness of the landscape. While population spread capacities may be strongly affected by aspects of a populations evolutionary history, predicting it from identifiable aspects of the evolutionary history may be hard to achieve.

ecology↗

Performance in a novel environment subject to ghost competition.

BackgroundA central tenet of the evolutionary theory of communities is that competition impacts evolutionary processes such as local adaptation. Species in a community exert a selection pressure on other species and may drive them to extinction. We know, however, very little about the influence of unsuccessful or ghost species on the evolutionary dynamics within the community.\n\nMethodsHere, we studied the long-term influence of a ghost competitor on the performance of a more successful species using experimental evolution. We transferred the spider mite Tetranychus urticae onto a novel host plant under initial presence or absence of a competing species, the congeneric mite T. ludeni.\n\nResultsThe latter species unintentionally went extinct soon after the start of the experiment, but we nevertheless completed the experiment and found that the initial density of this ghost competitor positively affected the performance (i.e. fecundity) of the more successful species.\n\nThis effect on T. urticae even lasted for at least 25 generations.\n\nDiscussionOur study supports the hypothesis that early experienced selection pressures can exert a persistent evolutionary signal on species performance in novel environments.

evolutionary biology↗

Habitat choice stabilizes metapopulation dynamics through increased ecological specialisation.

Dispersal is a key trait responsible for the spread of individuals and genes among local populations, thereby generating eco-evolutionary interactions. Especially in heterogeneous metapopulations, a tight coupling between dispersal, population dynamics and the evolution of local adaptation is expected. In this respect, current theory predicts dispersal to counteract ecological specialisation by redistributing locally selected phenotypes (i.e. migration load). However, in nature we observe that some specialists exhibit a strong dispersal capacity.\n\nHabitat choice following informed dispersal decisions, provides a possible mechanism for individuals to match the environment to their phenotype, thereby enabling the persistence of evolved ecological specialisation. How such informed decisions affect the evolution of dispersal and ecological specialisation and how these, in turn, influence metapopulation dynamics is yet to be determined.\n\nBy means of individual-based modelling, we show that informed decisions on both departure and settlement decouples the evolution of dispersal and generalism, favouring highly dispersive specialists. Choice at settlement decouples dispersal from ecological specialisation most effectively. Additionally, habitat choice stabilizes local and metapopulation demography because of the maintenance of ecological specialisation at all levels of dispersal propensity.\n\nWe advocate considering habitat choice in spatially structured ecological models to improve demographic predictions in the face of environmental change.

evolutionary biology↗