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Teotonio, H.

Publications and source records attributed to Teotonio, H..

17 recordsLinked to original sources

Weak selection of phenotypic memory in periodic environments

Offspring can inherit a physiological or molecular state from their parents, and the carry-over in phenotypes across generations that results is often called epigenetic or phenotypic "memory''. Most theory on the evolution of such memory asks how the rate of switching between pre-existing phenotypic variants evolves in a fluctuating environment. Here we ask instead how the variants themselves originate. We model an asexual population in a periodically alternating environment in which a genotype specifies two inherited states, the phenotypic value each produces and the probability with which each is retained from parent to offspring. Starting from an ancestor that produces a single phenotype, mutations creating small differences between inherited states have no first-order selective advantage. Their spread depends on second-order selection and requires strong selection against phenotype-environment mismatch. A maternal effect of the same small size, conditioned on the maternal environment, is under first-order selection in the same model. Once phenotypes have diverged, genotypes whose retention probabilities match the duration of the environmental states are strongly favored, and the evolved strategy persists under conditions in which it could not originate. Memory is a consequence of individual selection and its origin probably follows earlier selection for cue-dependent maternal effects.

evolutionary biology↗

Self-fertilization reverses the direction of selection on recombination

The evolution of recombination is thought to be influenced by many factors, including the mating system. Here, we provide an experimental test of how self-fertilization (selfing) affects the evolution of a recombination modifier. We used experimental populations of Caenorhabditis elegans segregating for the recombination modifier rec-1, a mutant that redistributes crossovers from the genetically diverse chromosome arms toward the less diverse central regions. By evolving populations under varying selfing rates, we show that increasing selfing reverses selection acting on the rec-1 mutant, from positive to negative. Simulations show that this reversal can be explained by an expansion of the genomic region over which the modifier remains associated with the genetic combinations it creates. These results demonstrate that selfing can fundamentally alter the evolutionary fate of recombination modifiers and reveal a mechanism not predicted by previous theoretical models of recombination evolution under different mating systems, which assumed uniform recombination landscapes.

evolutionary biology↗

Cue reliability and the evolution of adaptive plasticity in maternal traits

Natural populations face challenges from multiple environmental factors, and adaptive phenotypic plasticity is expected to evolve only when these factors are strongly correlated across time. In variable environments where developing individuals cannot directly perceive future conditions, natural selection may favor the use of arbitrary but reliable cues by mothers to signal their progenys challenging environments, resulting in adaptation that otherwise could not be achieved. We performed evolution experiments with genetically-variable and predominantly selfing populations of the nematode Caenorhabditis elegans in a temporally uncorrelated anoxic selection environment, where during oogenesis and ovulation mothers received blue light pulses that either reliably or unreliably cued impending anoxic conditions in their progeny. After 60 non-overlapping generations of experimental evolution, populations reliably exposed to light evolved both a cue-dependent increase in offspring survival in anoxia following maternal light exposure, and a larger light-independent increase in survival that depended primarily on the maternal oxygen environment. Differentiation between reliable and unreliable populations in their ability to respond to light was most apparent after two generations of anoxia, with evidence of maladaptation in unreliable populations through decreased fecundity and survival in anoxia, although most fitness differentiation between reliable and unreliable populations was observed regardless of light variation, particularly when maternal generations were under normoxia. These results show that when maternal and offspring selection environments are uncorrelated, maternal traits evolve only if maternal environments provide cues predictive of offspring selection. They indicate that cue reliability can determine the evolution of adaptive plasticity in traits with maternal effects.

evolutionary biology↗

Selection can favor a recombination landscape that limits polygenic adaptation

Meiotic crossover positions are uneven along eukaryotic chromosomes, giving rise to heterogeneous recombination rate landscapes. Genetic modifiers of local and genome-wide crossover positions have been described, but the selective pressures acting on them and their potential effect on adaptation in already-recombining populations remain unclear. We performed experimental evolution using a mutant that modifies the position of crossovers along chromosomes in the nematode Caenorhabditis elegans, without any detectable direct fitness effect. Our results show that when the recombination landscape is fixed, adaptation is facilitated by the modifier allele that, on average, increases recombination rates in genomic regions containing heritable fitness variation. However, in polymorphic populations containing both the wild-type and mutant modifier alleles, the allele that facilitates adaptation tends to decrease in frequency. This is likely because the allele that reduces recombination between selected loci at the genome-wide scale increases recombination in its chromosomal vicinity, and may thus benefit from local associations it establishes with beneficial genotype combinations. These results demonstrate that indirect selection acting on a recombination modifier mainly depends on its local effect, which may be decoupled from its consequences on genome-wide polygenic adaptation.

evolutionary biology↗

rec-1 loss of function is insufficient to homogenize crossover distribution in Caenorhabditis elegans

Meiotic control of crossover (CO) position is critical for proper homologous chromosome segregation and organismal fertility, recombination of parental genotypes, and the generation of novel genetic combinations. We here characterize the recombination rate landscape of a loss of function genetic modifier of CO position in Caernorhabditis elegans. By averaging CO position across hermaphrodite and male meioses and by genotyping 203 single-nucleotide variants covering about 95% of the genome, we find that the characteristic chromosomal arm-center recombination rate domain structure is lost in a loss of function rec-1 mutant. The rec-1 loss of function mutant smooths the recombination rate landscape but is insufficient to eliminate the non-uniform position of CO. We further find that the rec-1 mutant is of little consequence for organismal fertility and embryo hatchability and thus for rates of autosomal non-disjunction. However, it specifically increases X chromosome non-disjunction rates and males appearance. Our findings question the maintenance of genetic diversity among C. elegans natural populations, and they further suggest that manipulating genetic modifiers of CO position will help map quantitative trait loci in low-recombining genomic regions.

genetics↗

Variation in mutational (co)variances

1Because of pleiotropy, mutations affect the expression and inheritance of multiple traits and are expected to determine the structure of standing genetic variation and phenotypic evolution. It is thus important to find if the M matrix, describing mutational (co)variances between traits, varies between genotypes. We here estimate the M matrix for six locomotion behavior traits in two genotypes of the nematode Caenorhabditis elegans. We find significant mutational variance along at least one phenotypic dimension of the M matrix, but its size and orientation was similar between genotypes. We then tested if the M matrices were similar to one G matrix describing the standing genetic (co)variances of a domesticated population derived by the hybridization of several genotypes and adapted to a lab defined environment for 140 generations. M and G are different in part because the genetic covariances caused by mutational pleiotropy in the two genotypes are smaller than those caused by standing linkage disequilibrium in the lab population. If generalized to other genotypes, these observations indicate that selection is unlikely to shape the evolution of the M matrix for locomotion behavior and suggests that the genetic restructuring due to the hybridization of C. elegans genotypes allows for selection in the lab on new phenotypic dimensions of locomotion behavior, phenotypic dimensions which are inaccessible to natural populations.

evolutionary biology↗

Selection and the direction of phenotypic evolution

1Predicting phenotypic evolution on the short-term of tens to hundreds of generations, particularly in changing environments and under finite population sizes, is an important theoretical goal. Because organisms are not simply collections of independent traits, making headway into this goal requires understanding if the phenotypic plasticity of ancestral populations aligns with the phenotypic dimensions that contain more genetic variation for selection to be effective and eventually feedback on the maintenance of genetic variation and promote adaptation or rescue from extinction. By performing 50 generations of experimental evolution in a changing environment we show that ancestral phenotypic plasticity for locomotion behavior in the partially-outcrossing nematode Caenorhabditis elegans is nonadaptive because it does not align with the phenotypic dimension encompassing most genetic variance in the ancestral population and is of no consequence to future phenotypic divergence. Despite evolution of the genetic structure of locomotion behavior we are able to predict the direction of phenotypic divergence, but not the magnitude, based on the genetic covariances between the component traits of locomotion behavior and fitness of the ancestral population. We further demonstrate that indirect selection on the component traits of locomotion behavior with unobserved trait(s) is responsible for the observed phenotypic divergence on them. Our findings indicate that selection theory can predict the direction of short-term adaptive phenotypic evolution.

evolutionary biology↗

Phenotypic stasis with genetic divergence

1Whether or not genetic divergence on the short-term of tens to hundreds of generations is compatible with phenotypic stasis remains a relatively unexplored problem. We evolved predominantly outcrossing, genetically diverse populations of the nematode Caenorhabditis elegans under a constant and homogeneous environment for 240 generations, and followed individual locomotion behavior. Although founders of lab populations show highly diverse locomotion behavior, during lab evolution the component traits of locomotion behavior - defined as the transition rates in activity and direction - did not show divergence from the ancestral population. In contrast, transition rates genetic (co)variance structure showed a marked divergence from the ancestral state and differentiation among replicate populations during the final 100 generations and after most adaptation had been achieved. We observe that genetic differentiation is a transient pattern during the loss of genetic variance along phenotypic dimensions under drift during the last 100 generations of lab evolution. These results suggest that short-term stasis of locomotion behavior is maintained because of stabilizing selection, while the genetic structuring of component traits is contingent upon drift history.

evolutionary biology↗

The relative strength of selection on modifiers of genetic architecture under migration load

Gene flow between populations adapting to differing local environmental conditions might be costly because individuals can disperse to habitats where their survival is low or because they can reproduce with locally maladapted individuals. The amount by which the mean relative population fitness is kept below one creates an opportunity for modifiers of the genetic architecture to spread due to selection. Prior work that separately considered modifiers changing dispersal, recombination rates, or altering dominance or epistasis, has typically focused on the direction of selection rather than its absolute magnitude. We here develop methods to determine the strength of selection on modifiers of the genetic architecture, including modifiers of the dispersal rate, in populations that have previously evolved local adaptation. We consider scenarios with up to five loci contributing to local adaptation and derive a new model for the deterministic spread of modifiers. We find that selection for modifiers of epistasis and dominance is stronger than selection for decreased recombination, and that selection for partial reductions in recombination are extremely weak, regardless of the number of loci contributing to local adaptation. The spread of modifiers that reduce dispersal depends on the number of loci, epistasis and extent of local adaptation in the ancestral population. We identify a novel effect, that modifiers of dominance are more strongly selected when they are unlinked to the locus that they modify. These findings help explain population differentiation and reproductive isolation and provide a benchmark to compare selection on modifiers under finite population sizes and demographic stochasticity. Author SummaryWhen populations of a species are spread over different habitats the populations can adapt to their local conditions, provided dispersal between habitats is low enough. Natural selection allows the populations to maintain local adaptation, but dispersal and gene flow create a cost called the migration load. The migration load measures how much fitness is lost because of dispersal between different habitats, and also creates an opportunity for selection to act on the arrangement and interaction between genes that are involved in local adaptation. Modifier genes can spread in these linked populations and cause functional, local adaptation genes, to become more closely linked on a chromosome, or change the way that these genes are expressed so that the locally adapted gene copy becomes dominant. We modeled this process and found that selection on modifiers that create tighter linkage between locally adapted genes is generally weak, and modifiers that cause gene interactions are more strongly selected. Even after these gene interactions have begun to evolve, further selection for increased gene interaction is still strong. Our results show that populations are more likely to adapt to local conditions by evolving new gene interactions than by evolving tightly linked gene clusters.

evolutionary biology↗

A single nucleotide change underlies the genetic assimilation of a plastic trait

Genetic assimilation - the evolutionary process by which an ancestral environmentally sensitive phenotype is made constitutive - is a fundamental concept in biology. Its evolutionary relevance is debated, and our understanding of its prevalence, and underlying genetics and molecular mechanisms, is poor. Matricidal hatching is an extreme form of maternal provisioning induced by adverse conditions, which varies among Caenorhabditis elegans populations. We identified wild isolates, sampled from natural populations across multiple years and locations, that express a derived state of near-constitutive matricidal hatching. A single amino acid change in kcnl-1, encoding a small-conductance calcium-activated potassium channel subunit, explains most of this variation. A gain-of-function mutation altering the S6 transmembrane domain causes inappropriate activation of the K+ channel, leading to reduced vulval muscle excitability, and thus reduced expulsion of embryos, irrespective of environment. Using reciprocal allelic replacements, we show that this amino acid change is sufficient to induce constitutive matricidal hatching whilst re-establishing the ancestral protein abolishes matricidal hatching and restores egg-laying, thereby doubling lifetime reproductive fitness under benign conditions. While highly deleterious in the laboratory, experimental evolution showed that KNCL-1(V530L) is maintained under fluctuating resource availability. Selection on a single point mutation can therefore underlie the genetic assimilation of an ancestrally plastic trait with drastic life-history consequences.

evolutionary biology↗

Testing the adaptive value of sporulation in budding yeast using experimental evolution

Saccharomyces yeast can grow through mitotic vegetative cell division while they convert resources in their environment into biomass. When cells encounter specific low nutrient environments, sporulation may be initiated and meiotic division produces 4 haploid cells contained inside a protective ascus. The protected spore state does not acquire new resources but is partially protected from desiccation, heat, and caustic chemicals. Because cells cannot both be protected and acquire resources simultaneously, committing to sporulation represents a trade-off between current and future reproduction. Recent work has suggested that one of the major environmental factors that select for the formation of spores is passaging through insect guts, as this also represents a major way that yeasts are vectored to new food sources. We subjected replicate populations of a panel of 5 yeast strains to repeated, predictable passaging through insects by feeding them to fruit flies (Drosopila melanogaster) and then allowing surviving yeast cell growth in defined media for a fixed period of time. We also evolved control populations using the same predictable growth environments but without being exposed to flies. We assayed populations for their sporulation rate, as measured by the percentage of cells that had sporulated after resource depletion. We found that the strains varied in their ancestral sporulation rate such that domesticated strains had lower sporulation. During evolution, all strains evolved increased sporulation in response to passaging through flies, but domesticated strains evolved to lower final levels of sporulation. We also found that exposure to flies led to an evolved change in the timing of the sporulation response relative to controls, with a more rapid shift to sporulation, and that wild-derived strains showed a more extreme response. We conclude that strains that have lost the ability to access genetic variation for total sporulation rate and the ability to respond to cues in the environment that favor sporulation due to genetic canalization during domestication.

evolutionary biology↗

Selection and drift determine phenotypic stasis despite genetic divergence

1Evolutionary theory suggests that phenotypic stasis is explained by natural selection and genetic drift, or by constraints imposed by mutation and recombination of standing genetic variation. We performed experimental evolution from standing genetic variation with the nematode Caenorhabditis elegans, measuring individual locomotion in outcrossing populations for 240 generations. We find that, in our constant environment, locomotion bias shows no directional divergence, due to both stabilizing and disruptive selection on specific combinations of component traits. Despite phenotypic stasis, the genetic variance-covariance structure between component traits shows clear divergence from the ancestral state and extensive differentiation among replicated populations facing the same environment. Analysis of mutation accumulation experiments and genome-sequenced recombinant inbred lines from the experimental populations indicates that the evolution of the genetic variance-covariance structure is independent of de novo mutation or major effect QTL; being instead explained by the joint action of selection and drift in generating subtle linkage disequilibrium differences between small effect QTL among replicate populations. These findings indicate that phenotypic evolution is repeatable because of selection, even if the genetic structuring of component traits within lineages is mostly contingent upon drift history.

evolutionary biology↗

Gene-level quantitative trait mapping in an expanded C. elegans multiparent experimental evolution panel

The Caenorhabditis elegans multiparental experimental evolution (CeMEE) panel is a collection of genome-sequenced, cryopreserved recombinant inbred lines useful for mapping the genetic basis and evolution of quantitative traits. We have expanded the resource with new lines and new populations, and here report updated additive and epistatic mapping simulations and the genetic and haplotypic composition of CeMEE version 2. Additive QTL explaining 3% of trait variance are detected with >80% power, and the median detection interval is around the length of a single gene on the highly recombinant chromosome arms. Although CeMEE populations are derived from a long-term evolution experiment, genetic structure is dominated by variation present in the ancestral population and is not obviously associated with phenotypic differentiation. C. elegans provides exceptional experimental advantages for the study of phenotypic evolution.

evolutionary biology↗

How differing modes of transgenerational inheritance affect population viability in fluctuating environments

1Different modes of transgenerational inheritance are expected to affect population persistence in fluctuating environments. We here analyze Caenorhabiditis elegans density-independent per capita growth rate time series on 36 populations experiencing 6 controlled sequences of challenging oxygen level fluctuations across 60 generations, and parameterize competing models of transgenerational inheritance that do not involve genetic changes in order to explain observed dynamics. Our analysis shows that phenotypic plasticity and anticipatory maternal effects are sufficient to explain growth rate dynamics, but that a carryover model where epigenetic memory is imperfectly transmitted and might be reset at each generation is a better fit to the data. After validating the models, we use the fitted transgenerational inheritance parameters to forecast population growth rates and find that it is negatively related to the degree of environmental autocorrelation.

ecology↗

Partial selfing eliminates inbreeding depression while maintaining genetic diversity

Classical theory on the origin and evolution of selfing and outcrossing relies on the role of inbreeding depression created by unlinked partially-deleterious recessive alleles to predict that individuals from natural populations predominantly self or outcross. Comparative data indicates, however, that maintenance of partial selfing and outcrossing at intermediate frequencies is common in nature. In part to explain the presence of mixed reproductive modes within populations, several hypotheses regarding the evolution of inbreeding depression have been put forward based on the complex interaction of linkage and identity disequilibrium among fitness loci, together with Hill-Robertson effects. We here ask what is the genetic basis of inbreeding depression so that populations with intermediate selfing rates can eliminate it while maintain potentially adaptive genetic diversity. For this, we use experimental evolution in the nematode C. elegans under partial selfing and compare it to the experimental evolution of populations evolved under exclusive selfing and predominant outcrossing. We find that the ancestral risk of extinction upon enforced inbreeding by selfing is maintained when populations evolve under predominant outcrossing, but reduced when populations evolve under partial or exclusive selfing. Analysis of genome-wide single-nucleotide polymorphism (SNP) during experimental evolution and after enforced inbreeding suggests that, under partial selfing, populations were purged of unlinked deleterious recessive alleles that segregate in the ancestral population, which in turn allowed the expression of unlinked overdominant fitness loci. Taken together, these observations indicate that populations evolving under partial selfing gain the short-term benefits of selfing, in purging deleterious recessive alleles, but also the long-term benefits of outcrossing, in maintaining genetic diversity that may important for future adaptation.

evolutionary biology↗

Slower environmental change hinders adaptation from standing genetic variation

Evolutionary responses to environmental change depend on the time available for adaptation before environmental degradation leads to extinction. Explicit tests of this relationship are limited to microbes where adaptation depends on the order of mutation accumulation, excluding standing genetic variation which is key for most natural species. When adaptation is determined by the amount of heritable genotype-by-environment fitness variance then genetic drift and/or maintenance of similarly fit genotypes may deter adaptation to slower the environmental changes. To address this hypothesis, we perform experimental evolution with self-fertilizing populations of the nematode Caenorhabditis elegans and develop a new inference model that follows pre-existing genotypes to describe natural selection in changing environments. Under an abrupt change, we find that selection rapidly increases the frequency of genotypes with high fitness in the most extreme environment. In contrast, under slower environmental change selection favors those genotypes that are worse at the most extreme environment. We further demonstrate with a second set of evolution experiments that, as a consequence of slower environmental change, population bottlenecks and small population sizes lead to the loss of beneficial genotypes, while maintenance of polymorphism impedes their fixation in large populations. Taken together, these results indicate that standing variation for genotype-by-environment fitness interactions alters the pace and outcome of adaptation under environmental change.

evolutionary biology↗

Polygenicity And Epistasis Underlie Fitness-Proximal Traits In The Caenorhabditis elegans Multiparental Experimental Evolution (CeMEE) Panel

Understanding the genetic basis of complex traits remains a major challenge in biology. Polygenicity, phenotypic plasticity and epistasis contribute to phenotypic variance in ways that are rarely clear. This uncertainty is problematic for estimating heritability, for predicting individual phenotypes from genomic data, and for parameterizing models of phenotypic evolution. Here we report a recombinant inbred line (RIL) quantitative trait locus (QTL) mapping panel for the hermaphroditic nematode Caenorhabditis elegans, the C. elegans multiparental experimental evolution (CeMEE) panel. The CeMEE panel, comprising 507 RILs, was created by hybridization of 16 wild isolates, experimental evolution at moderate population sizes and predominant outcrossing for 140-190 generations, and inbreeding by selfing for 13-16 generations. The panel contains 22% of single nucleotide polymorphisms known to segregate in natural populations, and complements existing mapping resources for C. elegans by providing high nucleotide diversity across >95% of the genome. We apply it to study the genetic basis of two fitness components, fertility and hermaphrodite body size at time of reproduction, with high broad sense heritability in the CeMEE. While simulations show we should detect common alleles with additive effects as small as 5%, at gene-level resolution, the genetic architectures of these traits does not feature such alleles. We instead find that a significant fraction of trait variance, particularly for fertility, can be explained by sign epistasis with weak main effects. In congruence, phenotype prediction, while generally poor (r2 < 10%), requires modeling epistasis for optimal accuracy, with most variance attributed to the highly recombinant, rapidly evolving chromosome arms.

evolutionary biology↗