The immediate metabolomic effects of whole-genome duplication in the greater duckweed, Spirodela polyrhiza.

PREMISE: In plants, whole-genome duplication (WGD) is a common mutation with profound evolutionary potential. Given the costs associated with a superfluous genome copy, polyploid establishment is enigmatic. However, in the right environment, immediate phenotypic changes following WGD can facilitate establishment. Metabolite abundances are the direct output of the cell's regulatory network and determine much of the impact of environmental and genetic change on the phenotype. While it is well known that an increase in the bulk amount of genetic material can increase cell size, the impact of gene dosage multiplication on the metabolome remains largely unknown. METHODS: We used untargeted metabolomics on four genetically distinct diploid-neoautotetraploid pairs of the greater duckweed, Spirodela polyrhiza, to investigate how WGD affects metabolite abundances per cell and per biomass. RESULTS: Autopolyploidy increased metabolite levels per cell, but the response of individual metabolites varied considerably. However, the impact on metabolite level per biomass was restricted because the increased cell size reduced the metabolite concentration per cell. Nevertheless, we detected both quantitative and qualitative effects of WGD on the metabolome. Many effects were strain-specific, but some were shared by all four strains. CONCLUSIONS: The nature and impact of metabolic changes after WGD depended strongly on the genotype. Dosage effects have the potential to alter the plant metabolome qualitatively and quantitatively, but were largely balanced out by the reduction in metabolite concentration due to an increase in cell size in this species.

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

PREMISE: Whole-genome duplication (WGD, polyploidization) has been identified as a driver of genetic and phenotypic novelty, having pervasive consequences for the evolution of lineages. While polyploids are widespread, especially among plants, the long-term establishment of polyploids is exceedingly rare. Genome doubling commonly results in increased cell sizes and metabolic expenses, which may be sufficient to modulate polyploid establishment in environments where their diploid ancestors thrive. METHODS: We developed a mechanistic simulation model of photosynthetic individuals to test whether changes in size and metabolic efficiency allow autopolyploids to coexist with, or even invade, ancestral diploid populations. Central to the model is metabolic efficiency, which determines how energy obtained from size-dependent photosynthetic production is allocated to basal metabolism as opposed to somatic and reproductive growth. We expected neopolyploids to establish successfully if they have equal or higher metabolic efficiency as diploids or to adapt their life history to offset metabolic inefficiency. RESULTS: Polyploid invasion was observed across a wide range of metabolic efficiency differences between polyploids and diploids. Polyploids became established in diploid populations even when they had a lower metabolic efficiency, which was facilitated by recurrent formation. Competition for nutrients is a major driver of population dynamics in this model. Perenniality did not qualitatively affect the relative metabolic efficiency from which tetraploids tended to establish. CONCLUSIONS: Feedback between size-dependent metabolism and energy allocation generated size and age differences between plants with different ploidies. We demonstrated that even small changes in metabolic efficiency are sufficient for the establishment of polyploids.

Interspecific transfer of genetic information through polyploid bridges.

Hybridization blurs species boundaries and leads to intertwined lineages resulting in reticulate evolution. Polyploidy, the outcome of whole genome duplication (WGD), has more recently been implicated in promoting and facilitating hybridization between polyploid species, potentially leading to adaptive introgression. However, because polyploid lineages are usually ephemeral states in the evolutionary history of life it is unclear whether WGD-potentiated hybridization has any appreciable effect on their diploid counterparts. 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 fitness, can still allow the transfer of alleles between diploid states of independently evolving mixed-ploidy species. Notably, while marked genetic divergence prevents polyploid-mediated interspecific gene flow, we show that increased recombination rates can offset these evolutionary constraints, allowing 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 nonzero 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 the (re)distribution of genetic material across ecological communities during evolution, representing a potential force behind reticulation.

Neutral processes underlying the macro eco-evolutionary dynamics of mixed-ploidy systems.

Polyploidy, i.e. the occurrence of multiple sets of chromosomes, is regarded as an important phenomenon in plant ecology and evolution, with all flowering plants likely having a polyploid ancestry. Owing to genome shock, minority cytotype exclusion and reduced fertility, polyploids emerging in diploid populations are expected to face significant challenges to successful establishment. Their establishment and persistence are often explained by possible fitness or niche differences that would relieve the competitive pressure with diploid progenitors. Experimental evidence for such advantages is, however, not unambiguous, and considerable niche overlap exists among most polyploid species and their diploid counterparts. Here, we develop a neutral spatially explicit eco-evolutionary model to understand whether neutral processes can explain the eco-evolutionary patterns of polyploids. We present a general mechanism for polyploid establishment by showing that sexually reproducing organisms assemble in space in an iterative manner, reducing frequency-dependent mating disadvantages and overcoming potential reduced fertility issues. Moreover, we construct a mechanistic theoretical framework that allows us to understand the long-term evolution of mixed-ploidy populations and show that our model is remarkably consistent with recent phylogenomic estimates of species extinctions in the Brassicaceae family.

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

Reproductive parasites such as Wolbachia spread within host populations by inducing cytoplasmic incompatibility (CI). CI occurs when parasite-modified sperm fertilizes uninfected eggs and is typified by great variation in strength across biological systems. In haplodiploid hosts, CI has different phenotypic outcomes 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 influences the stability of reproductive parasitism. However, despite the ubiquity of CI-inducing parasites in nature, there is scarce evidence for intraspecific host modulation of CI strength and phenotype. Here, we tested for intraspecific host modulation of Wolbachia-induced CI in haplodiploid Tetranychus urticae mites. Using a single CI-inducing Wolbachia variant and mitochondrion, a nuclear panel was created that consisted of infected and cured near-isogenic lines. We performed a highly replicated age-synchronized full diallel cross composed of incompatible and compatible control crosses. We uncovered host modifier systems that cause striking variation in CI strength when carried by infected T. urticae males. We observed a continuum of CI phenotypes in our crosses and identified strong intraspecific female modulation of the CI phenotype. Crosses established a recessive genetic basis for the maternal effect and were consistent with polygenic Mendelian inheritance. Both male and female modulation interacted with the genotype of the mating partner. Our findings identify spermatogenesis as an important target of selection for host modulation of CI strength and underscore the importance of maternal genetic effects for the CI phenotype. Our findings reveal that intraspecific host modulation of CI is underpinned by complex genetic architectures and confirm that the evolution of reproductive parasitism is contingent on host genetics.

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. 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 size of genetically depleted inbred populations vs. enriched mixed populations. This was assessed in replicated linear patch systems consisting of benign (bean), challenging (tomato), or a gradient (bean to tomato) habitat. As expected, we found no effect of genetic diversity on population size in benign habitat but found that it increased population size in challenging habitat. However, we found that population spread rates were increased due to genetic diversity 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 benign environments.

Trapped by habitat choice: Ecological trap emerging from adaptation in an evolutionary experiment.

Individuals moving in heterogeneous environments can improve their fitness considerably by habitat choice. Induction by past exposure, genetic preference alleles and comparison of local performances can all drive this decision-making process. Despite the importance of habitat choice mechanisms for eco-evolutionary dynamics in metapopulations, we lack insights on the connection of their cue with its effect on fitness optimization. We selected a laboratory population of Tetranychus urticae Koch (two-spotted spider mite) according to three distinct host-choice selection treatments for ten generations. Additionally, we tested the presence of induced habitat choice mechanisms and quantified the adaptive value of a choice before and after ten generations of artificial selection in order to gather insight on the habitat choice mechanisms at play. Unexpectedly, we observed no evolution of habitat choice in our experimental system: the initial choice of cucumber over tomato remained. However, this choice became maladaptive as tomato ensured a higher fitness at the end of the experiment. Furthermore, a noteworthy proportion of induced habitat choice can modify this ecological trap depending on past environments. Despite abundant theory and applied relevance, we provide the first experimental evidence of an emerging trap. The maladaptive choice also illustrates the constraints habitat choice has in rescuing populations endangered by environmental challenges or in pest control.

Performance in a novel environment subject to ghost competition.

BACKGROUND: A 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. METHODS: Here we report 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. RESULTS: The competitor species, T. ludeni, unintentionally went extinct soon after the start of the experiment, but we nevertheless completed the experiment and found that the early competitive pressure of this ghost competitor positively affected the performance (i.e., fecundity) of the surviving species, T. urticae. This effect on T. urticae lasted for at least 25 generations. DISCUSSION: Our study suggests that early experienced selection pressures can exert a persistent evolutionary signal on species' performance in novel environments.

Transient local adaptation and source-sink dynamics in experimental populations experiencing spatially heterogeneous environments.

Local adaptation is determined by the strength of selection and the level of gene flow within heterogeneous landscapes. The presence of benign habitat can act as an evolutionary stepping stone for local adaptation to challenging environments by providing the necessary genetic variation. At the same time, migration load from benign habitats will hinder adaptation. In a community context, interspecific competition is expected to select against maladapted migrants, hence reducing migration load and facilitating adaptation. As the interplay between competition and spatial heterogeneity on the joint ecological and evolutionary dynamics of populations is poorly understood, we performed an evolutionary experiment using the herbivore spider mite Tetranychus urticae as a model. We studied the species's demography and local adaptation in a challenging environment that consisted of an initial sink (pepper plants) and/or a more benign environment (cucumber plants). Half of the experimental populations were exposed to a competitor, the congeneric T. ludeni. We show that while spider mites only adapted to the challenging pepper environment when it was spatially interspersed with benign cucumber habitat, this adaptation was only temporary and disappeared when the populations in the benign cucumber environment were expanding and spilling-over to the challenging pepper environment. Although the focal species outcompeted the competitor after about two months, a negative effect of competition on the focal species's performance persisted in the benign environment. Adaptation to challenging habitat in heterogeneous landscapes thus highly depends on demography and source-sink dynamics, but also on competitive interactions with other species, even if they are only present for a short time span.

Eco-evolutionary feedbacks following changes in spatial connectedness.

Humans are drastically changing the spatial configuration of habitats. The associated changes in habitat connectedness impose strong selection on dispersal, and dispersal related traits. Evolutionary responses do, however, strongly feedback on the metapopulation dynamics, by further constraining or improving connectivity and impacting local population and food web dynamics. Because these spatial eco-evolutionary interactions occur at contemporary time scales, unique evidence on its importance is especially emerging in the field of entomology as many insects have short generation times and a huge reproductive potential. We review the ecological feedbacks originating from the evolution of dispersal rate, dispersal syndromes and genetic diversity on metapopulation dynamics and range expansions. We thus close the eco-evolutionary loop for insect and arachnid spatial dynamics.