Biology subjects

Proulx, S. R.

Publications and source records attributed to Proulx, S. R..

11 recordsLinked to original sources

bioRxiv2026

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↗

bioRxiv2025

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↗

bioRxiv2024

Ancient secretory pathways contributed to the evolutionary origin of an ecologically impactful bioluminescence system

Evolutionary innovations in chemical secretion - such as the production of secondary metabolites, pheromones, and toxins - profoundly impact ecological interactions across a broad diversity of life. These secretory innovations may involve a "legacy-plus-innovation" mode of evolution, whereby new biochemical pathways are integrated with conserved secretory processes to create novel products. Among secretory innovations, bioluminescence is important because it evolved convergently many times to influence predator-prey interactions, while often producing courtship signals linked to increased rates of speciation. However, whether or not deeply conserved secretory genes are used in secretory bioluminescence remains unexplored. Here, we show that in the ostracod Vargula tsujii, the evolutionary novel c-luciferase gene is co-expressed with many conserved genes, including those related to toxin production and high-output protein secretion. Our results demonstrate that the legacy-plus-innovation mode of secretory evolution, previously applied to sensory modalities of olfaction, gustation, and nociception, also encompasses light-producing signals generated by bioluminescent secretions. This extension broadens the paradigm of secretory diversification to include not only chemical signals but also bioluminescent light as an important medium of ecological interaction and evolutionary innovation. Significance StatementAnimals produce an enormous diversity of secreted chemical products, like toxins and pheromones, with wide-ranging impacts on ecological interactions. Although a deeply conserved toolkit of secretory genes may often underlie chemical interactions mediated through smell, taste, and sensing pain, whether or not this evolutionary mode generalizes to sensing light is unknown. Here we show that a bioluminescence secretion system, which creates light for anti-predator and courtship interactions, also uses genes of a deeply conserved secretory toolkit. Therefore, secretory innovations may act through all sensory modalities by integrating conserved genes with novel biosynthesis pathways, to serve as crucibles of evolutionary and ecological diversity.

evolutionary biology↗

bioRxiv2023

Unifying optimal offspring size and bacterial aging through resource distribution models

Models of optimal offspring size and bacterial aging share the same underlying mathematical problem: how should a parent optimally distribute limited resources among its offspring? Optimal offspring size theory has long explored the trade-off between offspring number and size in higher organisms. Meanwhile, the emerging field of bacterial aging examines whether and under what conditions cells evolve unequal sharing of old cellular components. Despite addressing similar problems, these models remain constrained by field-specific assumptions. We unify them in a generalized resource-distribution framework that yields insights and predictions unreachable by either field alone. Our central finding is that the convexity of the function relating resources to offspring survivorship determines the optimal resource distribution strategy. Furthermore, we show that these strategies evolve, characterize their robustness to fluctuating environments, and uncover the conditions that select for producing a "runt of the litter."

evolutionary biology↗

bioRxiv2022

MODELING THE METABOLIC EVOLUTION OF MIXOTROPHIC PHYTOPLANKTON IN RESPONSE TO RISING OCEAN SURFACE TEMPERATURES

BackgroundClimate change is expected to lead to warming in ocean surface temperatures which will have unequal effects on the rates of photosynthesis and heterotrophy. As a result of this changing metabolic landscape, directional phenotypic evolution will occur, with implications that cascade up to the ecosystem level. While mixotrophic phytoplankton, organisms that combine photosynthesis and heterotrophy to meet their energetic and nutritional needs, are expected to become more heterotrophic with warmer temperatures due to heterotrophy increasing at a faster rate than photosynthesis, it is unclear how evolution will influence how these organisms respond to warmer temperatures. In this study, we used adaptive dynamics to model the consequences of temperature-mediated increases in metabolic rates for the evolution of mixotrophic phytoplankton, focusing specifically on phagotrophic mixotrophs. ResultsWe find that mixotrophs tend to evolve to become more reliant on phagotrophy as temperatures rise, leading to reduced prey abundance through higher grazing rates. However, if prey abundance becomes too low, evolution favors greater reliance on photosynthesis. These responses depend upon the trade-off that mixotrophs experience between investing in photosynthesis and phagotrophy. Mixotrophs with a convex trade-off maintain mixotrophy over the greatest range of temperatures; evolution in these "generalist" mixotrophs was found to exacerbate carbon cycle impacts, with evolving mixotrophs exhibiting increased sensitivity to rising temperature. ConclusionsOur results show that mixotrophs may respond more strongly to climate change than predicted by phenotypic plasticity alone due to evolutionary shifts in metabolic investment. However, the type of metabolic trade-off experienced by mixotrophs as well as ecological feedback on prey abundance may ultimately limit the extent of evolutionary change along the heterotrophy-phototrophy spectrum.

evolutionary biology↗

bioRxiv2021

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↗

bioRxiv2020

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↗

bioRxiv2018

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↗

bioRxiv2017

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↗

bioRxiv2017

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↗

bioRxiv2017

The evolution of p53 network behavior

We study the evolution of the p53 core regulation network across the taxonomic span of humans to protozoans and nematodes. We introduce a new model for the core regulation network in mammalian cells, and conduct a formal analysis of the different network configurations that emerge in the evolutionary path to complexity. Solving the high dimensional equations associated with this model is typically challenging, and we develop a novel algorithm to overcome this problem. A key technical tool used is the representation of the distinct pathways in the core regulation networks as \"modules\", such that the behavior of the composite of two or more modules can be inferred from the characteristics of each of the individual modules. Apart from simplifying the complexity of the algorithm, this modular representation also allows us to qualitatively compare the distinct types of switching behaviors each network can exhibit. This then allows us to demonstrate how our model for the core regulation network in mammalian cells matches experimentally observed phenomena, and contrast this with the plausible behaviors admitted by the network configurations in putative primordial organisms. We show that the complexity of the p53 core regulation network in vertebrates permits a range of behaviors that can bring about distinct cell fate decisions not possible in the putative primordial organisms.\n\nSignificance StatementThe p53 protein has been protecting organisms from tumors for a billion years. We study the link between the evolution of the p53 network structure and its corresponding tumor suppression strategies. We compare the dynamical behaviors in putative primordial organisms with simple networks with the vertebrate network that contains multiple feedback loops. We show that the vertebrate network, but not the ancestral network, can both repair moderate damage and induce apoptosis if too much damage accumulates, balancing the risk of cancer with the cost of too much cell death. Moreover, the complexity of the vertebrate network allows for adaptation, for example to increase p53 network sensitivity, which is consistent with recent research on large mammals.

systems biology↗