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Evolutionary Rescue Over A Fitness Landscape

Evolutionary rescue describes a situation where adaptive evolution prevents the extinction of a population facing a stressing environment. Models of evolutionary rescue could in principle be used to predict the level of stress beyond which extinction becomes likely for species of conservation concern, or conversely the treatment levels most likely to limit the emergence of resistant pests or pathogens. Stress levels are known to affect both the rate of population decline (demographic effect) and the speed of adaptation (evolutionary effect), but the latter aspect has received less attention. Here, we address this issue using Fishers Geometric Model of adaptation. In this model, the fitness effects of mutations depend both on the genotype and the environment in which they arise. In particular, the model introduces a dependence between the level of stress, the proportion of rescue mutants, and their costs before the onset of stress. We obtain analytic results under a strong-selection-weak-mutation regime, which we compare to simulations. We show that the effect of the environment on evolutionary rescue can be summarized into a single composite parameter quantifying the effective stress level, which is amenable to empirical measurement. We describe a narrow characteristic stress window over which the rescue probability drops from very likely to very unlikely as the level of stress increases. This drop is sharper than in previous models, as a result of the decreasing proportion of stress-resistant mutations as stress increases. We discuss how to test these predictions with rescue experiments across gradients of stress.

evolutionary biology

Comparative Genomics Of Apomictic Root-Knot Nematodes: Hybridization, Ploidy, And Dynamic Genome Change

The Root-Knot Nematodes (RKN; genus Meloidogyne) are important plant parasites causing substantial agricultural losses. The Meloidogyne incognita group (MIG) of species, most of which are obligatory apomicts (mitotic parthenogens), are extremely polyphagous and important problems for global agriculture. While understanding the genomic basis for their variable success on different crops could benefit future agriculture, analyses of their genomes pose challenges due to complex evolutionary histories that may incorporate hybridization, ploidy changes, and chromosomal fragmentation. Here we sequence 19 genomes, representing five species of key RKN collected from different geographic origins. We show that a hybrid origin that predated speciation within the MIG has resulted in each species possessing two divergent genomic copies. Additionally, the MIG apomicts are hypotriploids, with a proportion of one genome present in a second copy, and this proportion varies among species. The evolutionary history of the MIG genomes is revealed to be very dynamic, with non-crossover recombination both homogenising the genomic copies, and acting as a mechanism for generating divergence between species. Interestingly, the automictic MIG species M. floridensis differs from the apomict species in that it has become homozygous throughout much of its genome.

evolutionary biology

Evolution Of Pre-Copulatory And Post-Copulatory Strategies Of Inbreeding Avoidance And Associated Polyandry

Inbreeding depression is widely hypothesised to drive adaptive evolution of pre-copulatory and post-copulatory mechanisms of inbreeding avoidance, which in turn are hypothesised to affect evolution of polyandry (i.e., female multiple mating). However, surprisingly little theory or modelling critically examines selection for pre-copulatory or post-copulatory inbreeding avoidance, or both strategies, given evolutionary constraints and direct costs, or examines how evolution of inbreeding avoidance strategies might feed back to affect evolution of polyandry. Selection for post-copulatory inbreeding avoidance, but not for pre-copulatory inbreeding avoidance, requires polyandry, while interactions between pre-copulatory and post-copulatory inbreeding avoidance might cause functional redundancy (i.e., degeneracy) potentially generating complex evolutionary dynamics among inbreeding strategies and polyandry. We used individual-based modelling to quantify evolution of interacting pre-copulatory and post-copulatory inbreeding avoidance and associated polyandry given strong inbreeding depression and different evolutionary constraints and direct costs. We found that evolution of post-copulatory inbreeding avoidance increased selection for initially rare polyandry, and that evolution of a costly inbreeding avoidance strategy became negligible over time given a lower cost alternative strategy. Further, fixed pre-copulatory inbreeding avoidance often completely precluded evolution of polyandry and hence post-copulatory inbreeding avoidance, but fixed post-copulatory inbreeding avoidance did not preclude evolution of pre-copulatory inbreeding avoidance. Evolution of inbreeding avoidance phenotypes and associated polyandry are therefore affected by evolutionary feedbacks and degeneracy. All else being equal, evolution of pre-copulatory inbreeding avoidance and resulting low polyandry is more likely when post-copulatory inbreeding avoidance is precluded or costly, and evolution of post-copulatory inbreeding avoidance greatly facilitates evolution of costly polyandry.

evolutionary biology

Evolutionary Processes Shaping Diversity Across The Homo Lineage

Recent fossil finds have highlighted extensive morphological diversity within our genus, Homo, and the co-existence of a number of species. However, little is known about the evolutionary processes responsible for producing this diversity. Understanding the action of these processes can provide insight into how and why our lineage evolved and diversified. Here, we examine cranial and mandibular variation and diversification from the earliest emergence of our genus at 2.8 Ma until the Late Pleistocene (0.126-0.0117 Ma), using statistical tests developed from quantitative genetics theory to evaluate whether stochastic (genetic drift) versus non-stochastic (selection) processes were responsible for the observed variation. Results show that random processes can account for species diversification for most traits, including neurocranial diversification, and across all time periods. Where selection was found to shape diversification, we show that: 1) adaptation was important in the earliest migration of Homo out of Africa; 2) selection played a role in shaping mandibular and maxillary diversity among Homo groups, possibly due to dietary differences; and 3) Homo rudolfensis is adaptively different from other early Homo taxa, including the earliest known Homo specimen. These results show that genetic drift, and likely small population sizes, were important factors shaping the evolution of Homo and many of its novel traits, but that selection played an essential role in driving adaptation to new contexts.

evolutionary biology

Excretion Through Digestive Tissues Predates The Evolution Of Excretory Organs

Most bilaterian animals excrete toxic metabolites through specialized organs, such as nephridia and kidneys, which share morphological and functional correspondences. In contrast, the excretory mechanisms in non-nephrozoans are largely unknown, and therefore the reconstruction of ancestral excretory mechanisms is problematic. Here, we investigated the excretory mode of members of the Xenacoelomorpha, the sister group to Nephrozoa, and Cnidaria, the sister group to Bilateria. By combining gene expression, inhibitor experiments and exposure to varying environmental ammonia conditions we show that both, Xenacoelomorpha and Cnidaria, are able to excrete across digestive-associated tissues. Based on these results we propose that digestive-associated tissues functioned as excretory sites before the evolution of specialized organs in nephrozoans. We conclude that diffusion was likely the ancestral mode of excretion, whilst the emergence of a compact, multiple-layered bilaterian body plan necessitated the evolution of active transport excretory mechanisms that was later recruited into the specialized excretory organs.

evolutionary biology

Selection-Driven Cost-Efficiency Optimisation Of Transcript Sequences Determines The Rate Of Gene Sequence Evolution In Bacteria

BackgroundMost amino acids are encoded by multiple synonymous codons. However synonymous codons are not used equally and this biased codon use varies between different organisms. It has previously been shown that both selection acting to increase codon translational efficiency and selection acting to decrease codon biosynthetic cost contribute to differences in codon bias. However, it is unknown how these two factors interact or how they affect molecular sequence evolution.\n\nResultsThrough analysis of 1,320 bacterial genomes we show that bacterial genes are subject to multi-objective selection-driven optimisation of codon use. Here, selection acts to simultaneously decrease transcript biosynthetic cost and increase transcript translational efficiency, with highly expressed genes under the greatest selection. This optimisation is not simply a consequence of the more translationally efficient codons being less expensive to synthesise. Instead, we show that tRNA gene copy number alters the cost-efficiency trade-off of synonymous codons such that for many species such that selection acting on transcript biosynthetic cost and translational efficiency act in opposition. Finally, we show that genes highly optimised to reduce cost and increase efficiency show reduced rates of synonymous and non-synonymous mutation.\n\nConclusionsThis analysis provides a simple mechanistic explanation for variation in evolutionary rate between genes that depends on selection-driven cost-efficiency optimisation of the transcript. These findings reveal how optimisation of resource allocation to mRNA synthesis is a critical factor that determines both the evolution and composition of genes.

evolutionary biology

Detecting Molecular Basis Of Phenotypic Convergence

Convergence is the process by which several species independently evolve similar traits. This evolutionary process is not only strongly related to fundamental questions such as the predictability of evolution and the role of adaptation, its study also may provide new insights about genes involved in the convergent character. We focus on this latter question and aim to detect molecular basis of a given phenotypic convergence. After pointing out a number of concerns about detection methods based on ancestral reconstruction, we propose a novel approach combining an original measure of the extent to which a site supports a phenotypic convergence, with a statistical framework for selecting genes from the measure of their sites. First, our measure of \"convergence level\" outperforms two previous ones in distinguishing simulated convergent sites from non-convergent ones. Second, by applying our detection approach to the well-studied case of convergent echolocation between dolphins and bats, we identified a set of genes which is very significantly annotated with audition-related GO-terms. This result constitutes an indirect evidence that genes involved in a phenotypic convergence can be identified with a genome-wide approach, a point which was highly debated, notably in the echolocation case (the latest articles published on this topic were quite pessimistic). Our approach opens the way to systematic studies of numerous examples of convergent evolution in order to link (convergent) phenotype to genotype.

evolutionary biology

Estimation Of Universal And Taxon-Specific Parameters Of Prokaryotic Genome Evolution

Our recent study on mathematical modeling of microbial genome evolution indicated that, on average, genomes of bacteria and archaea evolve in the regime of mutation-selection balance defined by positive selection coefficients associated with gene acquisition that is counter-acted by the intrinsic deletion bias. This analysis was based on the strong assumption that parameters of genome evolution are universal across the diversity of bacteria and archaea, and yielded extremely low values of the selection coefficient. Here we further refine the modeling approach by taking into account evolutionary factors specific for individual groups of microbes using two independent fitting strategies, an ad hoc hard fitting scheme and an hierarchical Bayesian model. The resulting estimate of the mean selection coefficient of s[~]10-10 associated with the gain of one gene implies that, on average, acquisition of a gene is beneficial, and that microbial genomes typically evolve under a weak selection regime that might transition to strong selection in highly abundant organisms with large effective population sizes. The apparent selective pressure towards larger genomes is balanced by the deletion bias, which is estimated to be consistently greater than unity for all analyzed groups of microbes. The estimated values of s are more realistic than the lower values obtained previously, indicating that global and group-specific evolutionary factors synergistically affect microbial genome evolution that seems to be driven primarily by adaptation to existence in diverse niches.

evolutionary biology

Role Of Competition In The Strain Structure Of Rotavirus Under Invasion And Reassortment

The role of competitive interactions in the formation and coexistence of viral strains remains unresolved. Neglected aspects of existing strain theory are that viral pathogens are repeatedly introduced from animal sources and readily exchange their genes. The combined effect of introduction and reassortment opposes strain structure, in particular the predicted stable coexistence of antigenically differentiated strains under strong frequency-dependent selection mediated by cross-immunity. Here we use a stochastic model motivated by rotavirus, the most common cause of childhood diarrheal mortality, to investigate serotype structure under these conditions. We describe a regime in which the transient coexistence of distinct strains emerges despite only weak cross-immunity, but is disturbed by invasions of new antigenic segments that reassort into existing backgrounds. We find support for this behavior in global rotavirus sequence data and present evidence for the displacement of new strains towards open antigenic niches. Our work extends previous work to bacterial and viral pathogens that share these rotavirus-like characteristics, with important implications for the effects of interventions such as vaccination on strain composition, and for the understanding of the factors promoting emergence of new subtypes.

evolutionary biology

Experimental Evolution Of Insect Immune Memory Vs. 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. To understand the evolution and consequences of these immune responses, we imposed strong pathogen selection on flour beetles (Tribolium castaneum), 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, all populations injected only with a high dose of live Bt evolved 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. Thus, pathogens can select for rapid modulation of insect priming ability, leading to divergent immune strategies (generalized resistance vs. specific immune priming) with distinct mechanisms and adaptive benefits.

evolutionary biology

A Balance Between Regulatory Constraints And Pathogen Pressure Shapes The Evolution Of Innate Immunity

As the first line of defence against pathogens, cells mount an innate immune response, which is highly variable from cell to cell. The response must be potent yet carefully controlled to avoid self-damage. How these constraints have shaped the evolution of innate immunity remains poorly understood. Here, we characterise this programmes transcriptional divergence between species and expression variability across cells. Using bulk and single-cell transcriptomics in primate and rodent fibroblasts challenged with an immune stimulus, we reveal a striking architecture of the innate immune response. Rapidly diverging genes, including cytokines and chemokines, also vary across cells and have distinct promoter structures. Conversely, genes involved in response regulation, such as transcription factors and kinases, are conserved between species and display low cell-to-cell variability. We suggest that this unique expression pattern, observed across species and conditions, has evolved as a mechanism for fine-tuned regulation, to achieve an effective but balanced response.

evolutionary biology

Predicting Drug Resistance Evolution: Antimicrobial Peptides Vs. Antibiotics

Antibiotic resistance constitutes one of the most pressing public health concerns. Antimicrobial peptides of multicellular organisms are considered part of a solution to this problem, and AMPs produced by bacteria such as colistin are last resort drugs. Importantly, antimicrobial peptides differ from many antibiotics in their pharmacodynamic characteristics. Here we implement these differences within a theoretical framework to predict the evolution of resistance against antimicrobial peptides and compare it to antibiotic resistance. Our analysis of resistance evolution finds that pharmacodynamic differences all combine to produce a much lower probability that resistance will evolve against antimicrobial peptides. The finding can be generalized to all drugs with pharmacodynamics similar to AMPs. Pharmacodynamic concepts are familiar to most practitioners of medical microbiology, and data can be easily obtained for any drug or drug combination. Our theoretical and conceptual framework is therefore widely applicable and can help avoid resistance evolution if implemented in antibiotic stewardship schemes or the rational choice of new drug candidates.

evolutionary biology

Mitochondrial Genetic Effects On Reproductive Success: Signatures Of Positive Intra-Sexual, But Negative Inter-Sexual Pleiotropy

Mitochondria contain their own DNA, and numerous studies have reported that genetic variation in this (mt)DNA sequence modifies the expression of life-history phenotypes. Maternal inheritance of mitochondria adds a layer of complexity to trajectories of mtDNA evolution, because theory predicts the accumulation of mtDNA mutations that are male-biased in effect. While it is clear that mitochondrial genomes routinely harbor genetic variation that affects components of reproductive performance, the extent to which this variation is sex-biased, or even sex-specific in effect, remains elusive. This is because nearly all previous studies have failed to examine mitochondrial genetic effects on both male and female reproductive performance within the one-and-the-same study. Here, we show that variation across naturally-occurring mitochondrial haplotypes affects components of reproductive success in both sexes, in Drosophila melanogaster. However, while we uncovered evidence for positive pleiotropy, across haplotypes, in effects on separate components of reproductive success when measured within the same sex, such patterns were not evident across sexes. Rather, we found a pattern of sexual antagonism across haplotypes on some reproductive parameters. This suggests the pool of polymorphisms that delineate global mtDNA haplotypes is likely to have been partly shaped by maternal transmission of mtDNA and its evolutionary consequences.

evolutionary biology

A Maladaptive Combination Of Traits Contributes To The Maintenance Of A Stable Hybrid Zone Between Two Divergent Species Of Drosophila

Geographical areas where two species come into contact and hybridize serve as natural laboratories for assessing mechanisms that limit gene flow between species. The ranges of about half of all closely related Drosophila species overlap, and the genomes of several pairs reveal signatures of past introgression. However, only two contemporary hybrid zones have been characterized in the genus, and both are recently diverged sister species (D. simulans-D. sechellia, Ks = 0.05; D. yakuba-D. santomea, Ks = 0.048). Here we present evidence of a new hybrid zone, and the ecological mechanisms that maintain it, between two highly divergent Drosophila species (Ks = 0.11). On the island of Bioko in west Africa, D. teissieri occupies mostly forests, D. yakuba occupies mostly open agricultural areas, and recently, we discovered that hybrids between these species occur near the interface of these habitats. Genome sequencing revealed that all field-sampled hybrids are F1 progeny of D. yakuba females and D. teissieri males. We found no evidence for either advanced-generation hybrids or F1 hybrids produced by D. teissieri females and D.yakuba males. The lack of advanced-generation hybrids on Bioko is consistent with mark-recapture and laboratory experiments that we conducted, which indicate hybrids have a maladaptive combination of traits. Like D. yakuba, hybrids behaviorally prefer open habitat that is relatively warm and dry, but like D. teissieri, hybrids have low desiccation tolerance, which we predict leaves them physiologically ill-equipped to cope with their preferred habitat. These observations are consistent with recent findings of limited introgression in the D. yakuba clade and identify an ecological mechanism for limiting gene flow between D. yakuba and D. teissieri; namely, selection against hybrids that we have documented, in combination with hybrid male sterility, contributes to the maintenance of this narrow (~30m), stable hybrid zone centered on the forest-open habitat ecotone. Our results show how a deleterious combination of parental traits can result in unfit or maladapted hybrids.

evolutionary biology

Migration Harshness Drives Habitat Choice And Local Adaptation In Anadromous Arctic Char: Evidence From Integrating Population Genomics And Acoustic Telemetry

Migration is a ubiquitous life history trait with profound evolutionary and ecological consequences. Recent developments in telemetry and genomics, when combined, can bring significant insights on the migratory ecology of non-model organisms in the wild. Here, we used this integrative approach to document dispersal, gene flow and potential for local adaptation in anadromous Arctic Char from six rivers in the Canadian Arctic. Acoustic telemetry data from 124 tracked individuals indicated asymmetric dispersal, with a large proportion of fish (72%) tagged in three different rivers migrating up the same short river in the fall. Population genomics data from 6,136 SNP markers revealed weak, albeit significant, population differentiation (average pairwise FST = 0.011) and asymmetric dispersal was also revealed by population assignments. Approximate Bayesian Computation simulations suggested the presence of asymmetric gene flow, although in the opposite direction to that observed from the telemetry data, suggesting that dispersal does not necessarily lead to gene flow. These observations suggested that Arctic Char home to their natal river to spawn, but may overwinter in rivers with the shortest migratory route to minimize the costs of migration in non-breeding years. Genome scans and genetic-environment associations identified 90 outlier markers putatively under selection, 23 of which were in or near a gene. Of these, at least four were involved in muscle and cardiac function, consistent with the hypothesis that migratory harshness could drive local adaptation. Our study illustrates the power of integrating genomics and telemetry to study migrations in non-model organisms in logistically challenging environments such as the Arctic.

evolutionary biology

On The Advantages Of Evolutionary Passivity In Fluctuating Environments: Could Sex Be The Preadaptation For The Stability-Based Sorting?

The ability of organisms to adaptively respond to environmental changes (evolvability) is usually considered to be an important advantage in interspecific competition. It has been suggested, however, that evolvability could be a double-edged sword that could present a serious handicap in fluctuating environments. The authors of this counterintuitive idea have published only verbal models to support their claims.\n\nHere we present the results of individual-based stochastic modelling of competition between two asexual species differing only by their evolvability. They show that, in changeable environments, less evolvable species could outperform their more evolvable competitors in a broad area of a parameter space, regardless of whether the conditions fluctuated periodically or aperiodically. Highly evolvable species prospered better nearly all the time; however, they sustained a higher probability of extinction during rare events of the rapid transient change of conditions.\n\nOur results offer an explanation of why sexually reproducing species, with their reduced capacity to respond adaptively to local or temporal environmental changes, prevail in most eukaryotic taxa in nearly all biotopes on the surface of Earth. These species may suffer several important disadvantages in direct competitive battles with asexual species; however, they might win in changeable environments in the more important sorting-according-to-stability war.

evolutionary biology

Fine-mapping the Favored Mutation in a Positive Selective Sweep

Methods to identify signatures of selective sweeps in population genomics data have been actively developed, but mostly do not identify the specific mutation favored by the selective sweep. We present a method, iSAFE, that uses a statistic derived solely from population genetics signals to pinpoint the favored mutation even when the signature of selection extends to 5Mbp. iSAFE was tested extensively on simulated data and in human populations from the 1000 Genomes Project, at 22 loci with previously characterized selective sweeps. For 14 of the 22 loci, iSAFE ranked the previously characterized candidate mutation among the 13 highest scoring (out of [~] 21, 000 variants). Three loci did not show a strong signal. For the remaining loci, iSAFE identified previously unreported mutations as being favored. In these regions, all of which involve pigmentation related genes, iSAFE identified identical selected mutations in multiple non-African populations suggesting an out-of-Africa onset of selection. The iSAFE software can be downloaded from https://github.com/alek0991/iSAFE.

evolutionary biology

Health Status By Gender, Hair Color, And Eye Color: Red-Haired Women Are The Most Divergent

BackgroundRed hair is associated with pain sensitivity, and more so in women than in men. Hair redness may thus interact with a female-specific factor. We tested this hypothesis on a large sample of Czech and Slovak respondents. They were asked about the natural redness and darkness of their hair, their natural eye color, their physical and mental health (24 categories), and other personal attributes (height, weight, number of children, lifelong number of sexual partners, frequency of smoking).\n\nResultsWe found that red-haired women did worse than other women in ten health categories and better in only three. In particular, they were more prone to colorectal, cervical, uterine, and ovarian cancer. Cancer risk increased steadily with increasing hair redness except for the reddest shade. Red-haired men showed a balanced pattern of health effects, doing better than other men in three categories and worse in three. Number of children was the only category where both male and female redheads did better than other respondents. We also confirmed earlier findings that red hair is naturally more frequent in women than in men.\n\nConclusionRed-haired women had higher fecundity and sexual attractiveness, but this selective advantage seems offset by worse health outcomes and therefore lower viability. The resulting equilibrium between these two counterbalancing forces might explain why red hair has remained less common than other hair and eye colors. Of the new hair and eye colors, red hair diverges the most from the ancestral state of black hair and brown eyes. It is the most sexually dimorphic variant, not only in population frequency but also in health outcomes. This sexual dimorphism seems to have resulted from a selection pressure that acted primarily on early European women and which led to a general and apparently rapid diversification of hair and eye colors.

evolutionary biology