The Stabilizing Effect Of Intraspecific Genetic Variation On Population Dynamics In Novel And Ancestral Habitats

Recent studies show that intraspecific genetic variation in asexual species may have large effects on community and ecosystem functions, increasing their stability, productivity, and species richness. However, major questions regarding its population-level impact remain empirically unanswered: (a) How does intraspecific genetic diversity affect the ecological characteristics of sexual species, in which recombination can alter the outcome of causal mechanisms such as selection and niche diversification? (b) Does genetic diversity increase population dynamic stability? (c) Is the impact of genetic diversity dependent on the selective environment? To answer these questions, I founded replicate flour beetle (Tribolium castaneum) populations with different degrees of ecologically relevant, heritable trait variation and monitored their dynamics for approximately eight generations. I show that population stability and persistence increased with greater genetic variation but that the stabilizing effect was independent of the selective habitat (different proportions of ancestral and novel resources). Alleles from a single founding strain underwent a selective sweep in the homogeneous ancestral habitat but not in a novel heterogeneous habitat. These results expand current understanding of the ecological impacts of genetic diversity by showing that genetically more diverse sexual populations persist longer and are more stable but that the selective environment determines the mechanistic basis of increased stability.Integrative Biolog

Intraspecific competition reduces niche width in experimental populations

Intraspecific competition is believed to drive niche expansion, because otherwise suboptimal resources can provide a refuge from competition for preferred resources. Competitive niche expansion is well supported by empirical observations, experiments, and theory, and is often invoked to explain phenotypic diversification within populations, some forms of speciation, and adaptive radiation. However, some foraging models predict the opposite outcome, and it therefore remains unclear whether competition will promote or inhibit niche expansion. We conducted experiments to test whether competition changes the fitness landscape to favor niche expansion, and if competition indeed drives niche expansion as expected. Using Tribolium castaneum flour beetles fed either wheat (their ancestral resource), corn (a novel resource) or mixtures of both resources, we show that fitness is maximized on a mixed diet. Next, we show that at higher population density, the optimal diet shifts toward greater use of corn, favoring niche expansion. In stark contrast, when beetles were given a choice of resources, we found that competition caused niche contraction onto the ancestral resource. This presents a puzzling mismatch between how competition alters the fitness landscape, versus competition's effects on resource use. We discuss several explanations for this mismatch, highlighting potential reasons why optimality models might be misleading

Novel candidate genes underlying extreme trophic specialization in Caribbean pupfishes

The genetic changes responsible for evolutionary transitions from generalist to specialist phenotypes are poorly understood. Here we examine the genetic basis of craniofacial traits enabling novel trophic specialization in a sympatric radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. This recent radiation consists of a generalist species and two novel specialists: a small-jawed "snail-eater" and a large-jawed "scale-eater." We genotyped 12 million single nucleotide polymorphisms (SNPs) by whole-genome resequencing of 37 individuals of all three species from nine populations and integrated genome-wide divergence scans with association mapping to identify divergent regions containing putatively causal SNPs affecting jaw size-the most rapidly diversifying trait in this radiation. A mere 22 fixed variants accompanied extreme ecological divergence between generalist and scale-eater species. We identified 31 regions (20 kb) containing variants fixed between specialists that were significantly associated with variation in jaw size which contained 11 genes annotated for skeletal system effects and 18 novel candidate genes never previously associated with craniofacial phenotypes. Six of these 31 regions showed robust signs of hard selective sweeps after accounting for demographic history. Our data are consistent with predictions based on quantitative genetic models of adaptation, suggesting that the effect sizes of regions influencing jaw phenotypes are positively correlated with distance between fitness peaks on a complex adaptive landscape

Good Codons, Bad Transcript: Large Reductions in Gene Expression and Fitness Arising from Synonymous Mutations in a Key Enzyme

Biased codon usage in protein-coding genes is pervasive, whereby amino acids are largely encoded by a specific subset of possible codons. Within individual genes, codon bias is stronger at evolutionarily conserved residues, favoring codons recognized by abundant tRNAs. Although this observation suggests an overall pattern of selection for translation speed and/or accuracy, other work indicates that transcript structure or binding motifs drive codon usage. However, our understanding of codon bias evolution is constrained by limited experimental data on the fitness effects of altering codons in functional genes. To bridge this gap, we generated synonymous variants of a key enzyme-coding gene in Methylobacterium extorquens. We found that mutant gene expression, enzyme production, enzyme activity, and fitness were all significantly lower than wild-type. Surprisingly, encoding the gene using only rare codons decreased fitness by 40%, whereas an allele coded entirely by frequent codons decreased fitness by more than 90%. Increasing gene expression restored mutant fitness to varying degrees, demonstrating that the fitness disadvantage of synonymous mutants arose from a lack of beneficial protein rather than costs of protein production. Protein production was negatively correlated with the frequency of motifs with high affinity for the anti-Shine-Dalgarno sequence, suggesting ribosome pausing as the dominant cause of low mutant fitness. Together, our data support the idea that, although a particular set of codons are favored on average across a genome, in an individual gene selection can either act for or against codons depending on their local context.Organismic and Evolutionary Biolog

The road not taken: Could stress-specific mutations lead to different evolutionary paths?

Organisms often encounter stressful conditions, some of which damage their DNA. In response, some organisms show a high expression of error-prone DNA repair machinery, causing a temporary increase in the genome-wide mutation rate. Although we now have a detailed map of the molecular mechanisms underlying such stress-induced mutagenesis (SIM), it has been hotly debated whether SIM alters evolutionary dynamics. Key to this controversy is our poor understanding about which stresses increase mutagenesis and their long-term consequences for adaptation. In a new study with Escherichia coli, Maharjan and Ferenci show that while only some nutritional stresses (phosphorous and carbon limitation) increase total mutation rates, each stress generates a unique spectrum of mutations. Their results suggest the potential for specific stresses to shape evolutionary dynamics and highlight the necessity for explicit tests of the long-term evolutionary impacts of SIM

Consequences of intraspecific genetic variation for population dynamics and niche expansion

textIntraspecific genetic diversity is an important attribute of natural populations and is deemed critical for their adaptive potential and persistence. However, we have limited empirical understanding of the impact of genetic diversity on population performance under different conditions. For my dissertation, I conducted long-term laboratory experiments with populations of the flour beetle Tribolium castaneum to test the consequences of genetic variation for population dynamic stability and niche evolution. In Chapter 1, I show that genetic variation prevented population extinction in a novel habitat. In addition, genetically diverse populations were more stable, both in a novel heterogeneous habitat and in their ancestral habitat. In the ancestral habitat, alleles from a single founding lineage dominated the dynamics, leading to increased stability of genetically diverse populations. However, such as selective effect was not observed in the novel heterogeneous habitat. Therefore, while genetic variation within populations increased their stability and persistence, the magnitude of the impact and its mechanism depended on the selective habitat. In Chapter 2, I ask whether genetic variation also facilitates resource niche expansion, i.e., use of a novel resource. Using stable carbon isotopes, I analyzed diets of beetles sampled from the above experiment and quantified the rate of change in resource use. Contrary to theoretical predictions, I found that genetic variation for resource use had no effect on the rate of niche evolution. Furthermore, behavioral niche expansion accounted for most of the adaptation to the novel resource, and the behavioral change hindered subsequent evolutionary change in resource use. It is thus apparent that in the short term, behavioral plasticity in niche use may impose far greater constraints on niche evolution than the amount of standing genetic variation. Mathematical models predict that intraspecific competition generates selection for niche evolution, and that genetic variation increases the response to selection. Therefore, I hypothesized that the impact of genetic variation on resource niche evolution may depend on the degree of intraspecific competition. In the final chapter of this thesis, I describe results of an experiment to test this hypothesis. I found that genetic variation and competition indeed interacted to increase the rate of niche expansion in T. castaneum, but that their impacts were temporally variable. Furthermore, the two factors acted on different components of niche evolution: while competition only affected the degree of niche expansion, genetic variation also promoted maintenance of individual variation in resource use. In summary, my thesis describes experiments to test for the ecological and evolutionary impacts of intraspecific genetic variation; and its interaction with behavioral plasticity, intraspecific competition, and resource availability. Genetic diversity and behavioral plasticity are common features of living organisms, and therefore it is vital to understand their combined consequences for population ecological and evolutionary dynamics. In addition, natural populations often face intense competition for limited resources. Hence the experimental results presented here can help us to better understand how populations overcome these resource constraints, given their specific genetic composition. Biologists are increasingly aware that the intricate connection between ecological and evolutionary dynamics is important to gain a more complete understanding of population biology. The work described here represents one of the few experiments providing such detailed mechanistic understanding of the interactions between- and consequences of - key ecological and evolutionary parameters. Finally, the results have important implications for conservation biology, because they show that the effects of genetic diversity can vary greatly depending on a number of population and environmental parameters.Ecology, Evolution and Behavio

The red flour beetle Tribolium castaneum: A model for host-microbiome interactions.

A large body of ongoing research focuses on understanding the mechanisms and processes underlying host-microbiome interactions, and predicting their ecological and evolutionary outcomes. To draw general conclusions about such interactions and understand how they are established, we must synthesize information from a diverse set of species. We analysed the microbiome of an important insect model-the red flour beetle Tribolium castaneum-which is a widespread generalist pest of stored cereals. The beetles complete their entire life cycle in flour, which thus serves multiple functions: habitat, food, and a source of microbes. We determined key factors that shape the T. castaneum microbiome, established protocols to manipulate it, and tested its consequences for host fitness. We show that the T. castaneum microbiome is derived from flour-acquired microbes, and varies as a function of (flour) resource and beetle density. Beetles gain multiple fitness benefits from their microbiome, such as higher fecundity, egg survival, and lifespan; and reduced cannibalism. In contrast, the microbiome has a limited effect on development rate, and does not enhance pathogen resistance. Importantly, the benefits are derived only from microbes in the ancestral resource (wheat flour), and not from novel resources such as finger millet, sorghum, and corn. Notably, the microbiome is not essential for beetle survival and development under any of the tested conditions. Thus, the red flour beetle is a tractable model system to understand the ecology, evolution and mechanisms of host-microbiome interactions, while closely mimicking the host species' natural niche

Data from: Experimental evolution of insect immune memory versus pathogen resistance

Under strong pathogen pressure, insects often evolve resistance to infection. Many insects are also protected via immune memory (‘immune priming’), whereby sub-lethal exposure to a pathogen enhances survival after secondary infection. Theory predicts that immune memory should evolve when the pathogen is highly virulent, or when pathogen exposure is relatively rare. However, there are no empirical tests of these hypotheses, and the adaptive benefits of immune memory relative to direct resistance against a pathogen are poorly understood. To determine the selective pressures and ecological conditions that shape immune evolution, we imposed strong pathogen selection on flour beetle (Tribolium castaneum) populations, infecting them with Bacillus thuringiensis (Bt) for 11 generations. Populations injected first with heat-killed and then live Bt each generation evolved high basal resistance against multiple Bt strains. In contrast, populations injected only with a high dose of live Bt evolved a less effective but strain-specific priming response. Control populations injected with heat-killed Bt did not evolve priming; and in the ancestor, priming was effective only against a low Bt dose. Intriguingly, one replicate population first evolved priming and subsequently evolved basal resistance, suggesting the potential for dynamic evolution of different immune strategies. Our work is the first report showing that pathogens can select for rapid modulation of insect priming ability, allowing hosts to evolve divergent immune strategies (generalized resistance vs. specific immune memory) with potentially distinct mechanisms

Data from: Dietary and developmental shifts in butterfly-associated bacterial communities

Bacterial communities associated with insects can substantially influence host ecology, evolution and behavior. Host diet is a key factor that shapes bacterial communities, but the impact of dietary transitions across insect development is poorly understood. We analyzed bacterial communities of 12 butterfly species across different development stages, using amplicon sequencing of the 16S rRNA gene. Butterfly larvae typically consume leaves of a single host plant, whereas adults are more generalist nectar feeders. Thus, we expected bacterial communities to vary substantially across butterfly development. Surprisingly,only few species showed significant dietary and developmental transitions in bacterial communities, suggesting weak impacts of dietary transitions across butterfly development. On the other hand, bacterial communities were strongly influenced by butterfly species and family identity, potentially due to dietary and physiological variation across the host phylogeny. Larvae of most butterfly species largely mirrored bacterial community composition of their diets, suggesting passive acquisition rather than active selection. Overall, our results suggest that although butterflies harbor distinct microbiomes across taxonomic groups and dietary guilds, the dramatic dietary shifts that occur during development do not impose strong selection to maintain distinct bacterial communities across all butterfly hosts