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bioRxiv2019

Viral host-range evolvability changes in response to fluctuating selection

The concept of evolvability (the capacity of populations to evolve) has deep historical roots in evolutionary biology. Interest in the subject has been renewed recently by innovations in microbiology that permit direct tests of the causes of evolvability, and with the acknowledgement that evolvability of pathogens has important implications for human health. Here, we investigate how fluctuating selection on the virus, Bacteriophage {lambda}, affects its evolvability. We imposed dynamic selection by altering the expression of two host outer membrane receptors. This, in turn, selected phage to alternately infect the host via a single, or multiple, receptors. Our selection regime resulted in two orthogonal evolutionary behaviors, namely enhanced or reduced evolvability. Strains with enhanced evolvability readily evolved between receptors, losing and gaining the ability to bind multiple receptors more quickly than the ancestral {lambda}. This suggests the receptor-binding protein retained a genetic memory of past states and that evolutionary history can be used to predict future adaptation. Strains with reduced evolvability were refractory to re-specialization and remained generalists on both receptors. Consistent with this behavior, unevolvable strains had reduced rates of molecular evolution in the receptor-binding protein compared to their evolvable counterparts. We found a single mutation in the receptor-binding protein was sufficient to render these strains resistant to evolution and did so by counteracting a receptor-binding trade-off associated with generalism. In this way, cost-free generalization allowed for reduced evolution and evolvability while maximizing success in both environments. Our results suggest the response to fluctuating selection is contingent and can lead to distinct differences in evolvability. These findings contribute to a growing understanding of the causes and consequences of evolvability and have important implications for infectious disease management.

evolutionary biology↗

bioRxiv2025

scoup: Simulate Codon Sequences with Darwinian Selection Incorporated as an Ornstein-Uhlenbeck Process

Genetic analyses of natural selection within and between populations have increasingly developed along separate paths. The two important genres of evolutionary biology (i.e. phylogenetics and population genetics) borne from the split can only benefit from research that seeks to bridge the gap. Simulation algorithms that combine fundamental concepts from both genres are important to achieve such unifying objective. We introduce scoup, a codon sequence simulator that is implemented in R and hosted on the Bioconductor platform. There is hardly any other simulator dedicated to genetic sequence generation for natural selection analyses on the platform. Concepts from the Halpern-Bruno mutation-selection model and the Ornstein-Uhlenbeck (OU) evolutionary algorithm were creatively fused such that the end-product is a novelty with respect to computational genetic simulation. Users are able to seamlessly adjust the model parameters to mimic complex evolutionary procedures that may have been otherwise infeasible. For example, it is possible to explicitly interrogate the concepts of static and changing fitness landscapes with regards to Darwinian natural selection in the context of codon sequences from multiple populations.

evolutionary biology↗

bioRxiv2019

Differential gene expression and gene variants drive color and pattern development in divergent color morphs of a mimetic poison frog

A common goal in evolutionary biology is to discern the mechanisms that produce the astounding diversity of morphologies seen across the tree of life. Aposematic species, those with a conspicuous phenotype coupled with some form of defense, are excellent models to understand the link between vivid color pattern variations, the natural selection shaping it, and the underlying genetic mechanisms underpinning this variation. Mimicry systems in which multiple species share the same conspicuous phenotype can provide an even better model for understanding the mechanisms of color production in aposematic species, especially if comimics have divergent evolutionary histories. Here we investigate the genetic mechanisms by which vivid color and pattern are produced in a Mullerian mimicry complex of poison frogs. We did this by first assembling a high-quality de novo genome assembly for the mimic poison frog Ranitomeya imitator. This assembled genome is 6.8 Gbp in size, with a contig N50 of 300 Kbp and 93% of expected tetrapod genes. We then leveraged this genome to conduct gene expression analyses throughout development of four color morphs of R. imitator and two color morphs from both R. fantastica and R. variabilis which R. imitator mimics. We identified a large number of pigmentation and patterning genes that are differentially expressed throughout development, many of them related to melanocyte development, melanin synthesis, iridophore development, and guanine synthesis. In addition, we identify the pteridine synthesis pathway (including genes such as qdpr and xdh) as a key driver of the variation in color between morphs of these species. Finally, we hypothesize that genes in the keratin family are important for producing different structural colors within these frogs.

evolutionary biology↗

bioRxiv2017

Stags, hawks, and doves: Social evolution theory and individual variation in cooperation

One of the triumphs of evolutionary biology is the discovery of robust mechanisms that promote the evolution of cooperative behaviors even when those behaviors reduce the fertility or survival of cooperators. Though these mechanisms, kin selection, reciprocity, and nonlinear payoffs to cooperation, have been extensively studied separately, investigating their joint effect on the evolution of cooperation has been more difficult. Moreover, how these mechanisms shape variation in cooperation is not well known. Such variation is crucial for understanding the evolution of behavioral syndromes and animal personality. Here, I use the tools of kin selection theory and evolutionary game theory to build a framework that integrates these mechanisms for pairwise social interactions. Using relatedness as a measure of the strength of kin selection, responsiveness as a measure of reciprocity, and synergy as a measure of payoff nonlinearity, I show how different combinations of these three parameters produce directional selection for or against cooperation or variation in levels of cooperation via balancing or diversifying selection. Moreover, each of these outcomes maps uniquely to one of four classic games from evolutionary game theory, which means that modulating relatedness, responsiveness, and synergy effectively transforms the payoff matrix from one the evolutionary game to another. Assuming that cooperation exacts a fertility cost on cooperators and provides a fertility benefit to social partners, a prisoners dilemma game and directional selection against cooperation occur when relatedness and responsiveness are low and synergy is not too positive. Enough positive synergy in these conditions generates a stag-hunt game and diversifying selection. High levels of relatedness or responsiveness turn cooperation from a fitness cost into a fitness benefit, which produces a mutualism game and directional selection for cooperation when synergy is not too negative. Sufficiently negative synergy in this case creates a hawk-dove game and balancing selection for cooperation. I extend the results with relatedness and synergy to larger social groups and show that how group size changes the effect of relatedness and synergy on selection for cooperation depends on how the per capita benefit of cooperation changes with group size. Together, these results provide a general framework with which to generate comparative predictions that can be tested using quantitative genetic techniques and experimental techniques that manipulate investment in cooperation. These predictions will help us understand both interspecific variation in cooperation as well as within-population and within-group variation in cooperation related to behavioral syndromes.

evolutionary biology↗

bioRxiv2020

Fly wing evolution explained by a neutral model with mutational pleiotropy

To what extent the speed of mutational production of phenotypic variation determines the rate of long-term phenotypic evolution is a central question in evolutionary biology. In a recent study, Houle et al. addressed this question by studying the mutational variation, microevolution, and macroevolution of locations of vein intersections on fly wings, reporting very slow phenotypic evolution relative to the rates of mutational input, high phylogenetic signals of these traits, and a strong, linear correlation between the mutational variance of a trait and its rate of evolution. Houle et al. examined multiple models of phenotypic evolution but found none consistent with all these observations. Here we demonstrate that the purported linear correlation between mutational variance and evolutionary divergence is an artifact. More importantly, patterns of fly wing evolution are explainable by a simple model in which the wing traits are neutral or neutral within a range of phenotypic values but their evolutionary rates are reduced because most mutations affecting these traits are purged owing to their pleiotropic effects on other traits that are under stabilizing selection. We conclude that the evolutionary patterns of fly wing morphologies are explainable under the existing theoretical framework of phenotypic evolution.

evolutionary biology↗

bioRxiv2026

Pleistocene climatic oscillations impact the diversification of deer mice (Peromyscus maniculatus) and the independent evolution of ecotypes

A central question in evolutionary biology is whether local adaptation is predictable when a species repeatedly encounters similar environments. The deer mouse, Peromyscus maniculatus, has a range of over 13 million km2 in North America and may be found in nearly every terrestrial habitat. Because of their abundance and wide habitat preference, deer mice and closely related Peromyscus, which we refer to as the P. maniculatus species complex, are at the forefront of studies of biogeography and local adaptation. Here, we undertake a comprehensive survey of genome-wide and phenotypic diversity to characterize the recent evolutionary history of this group. We sequenced whole genomes from 232 individuals across their range, representing the most thorough genetic sampling of the P. maniculatus species complex to date. We identify six geographically delineated clades, several of which encompass both classically recognized P. maniculatus subspecies as well as other recognized species. Ecological niche modelling suggests that this geographic structure resulted from rapid post-LGM range expansion and adaptation to emerging habitats. Our morphological measurements of 979 specimens and field data compiled from over 28,000 museum records show that deer mice in forests across the range consistently have longer tails, larger feet, bigger ears, and elongated whiskers. These traits constitute an arboreal ecotype that has evolved at least three times independently, and was likely lost in other parts of the range as populations moved out of forested habitat. Altogether, these results suggest that post-LGM increases in forested habitat drove the parallel evolution of arboreal ecotypes across the deer mouse range.

evolutionary biology↗

bioRxiv2020

Linking genomic signatures of selection to expression variation and direct evidence of local adaptation

Understanding how genomic and expression variation is linked to adaptation of plants to local environments is fundamental to the fields of evolutionary biology and species conservation. Using locally adapted Arabidopsis thaliana Italy and Sweden populations, we examine how variation in gene expression under control and cold acclimation conditions, is linked to allele frequency differentiation (AFD); linkage disequilibrium (LD); selective constraint at nonsynonymous sites; and genetic-tradeoff quantitative trait loci (GT-QTL). Our results indicate that contrary to genes showing a main effect in environment (E), expression genotype by environment interactions (GxE) show significantly higher AFD along cis-regulatory and nonsynonymous sites than the neutral expectation; and interestingly, highly differentiated GxE genes show higher expression and inter-species selective constraint than the rest of the genes. When examining the association between genomic signatures of selection along GxE/E genes and GT-QTL, we find that GxE genes showing a high AFD and LD, display a significant and much higher enrichment along GT-QTL than the genome-wide/E set of genes. Nonetheless, E genes show a higher enrichment than the genome-wide control. In summary, our results suggest, that these highly expressed and selectively constrained GxE genes, may have been part of a cold-responsive regulon of E genes that experienced recent selection when migrating to new environments. Candidate GxE genes underlying GT-QTL reveal interesting biological processes that may underlie local adaptation to temperature, including flowering time, light-dependent cold acclimation, freezing tolerance, and response to hypoxia. Finally, we find no evidence linking lower expression of the CBF-dependent freezing tolerance pathway to genetic-tradeoffs and adaptation to warmer climates.

evolutionary biology↗

bioRxiv2021

Ecological correlates of gene family size: the draft genome of the redheaded pine sawfly Neodiprion lecontei

A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a non-eusocial hymenopteran and exemplar of a pine-specialized lineage evolved from angiosperm-feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions and characterized their genomic distributions and evolutionary history. Our results suggest that expansions of bitter gustatory receptor (GR), clan 3 cytochrome P450 (CYP3), and antimicrobial peptide (AMP) subfamilies may have contributed to pine adaptation. By contrast, there was no evidence of recent gene family contraction via pseudogenization. Next, we compared the number of genes in these same families across insect taxa that vary in diet, dietary specialization, and social behavior. In Hymenoptera, herbivory was associated with small GR and olfactory receptor (OR) families, eusociality was associated with large OR and small AMP families, and--unlike investigations in more closely related taxa--ecological specialization was not related to gene family size. Overall, our results suggest that gene families that mediate ecological interactions may expand and contract predictably in response to particular selection pressures, however, the ecological drivers and temporal pace of gene gain and loss likely varies considerably across gene families.

evolutionary biology↗

bioRxiv2024

Predicting species invasiveness with genomic data: is Genomic Offset related to establishment probability?

Predicting the risk of establishment and spread of populations outside their native range represents a major challenge in evolutionary biology. Various methods have recently been developed to estimate population (mal)adaptation to a new environment with genomic data via so-called Genomic Offset (GO) statistics. These approaches are particularly promising for studying invasive species, but have still rarely been used in this context. Here, we evaluated the relationship between GO and the estab-lishment probability of a population in a new environment using both in silico and empirical data. First, we designed invasion simulations to evaluate the ability to predict establishment probability of two GO computation methods (Geometric GO and Gradient Forest) under several conditions. Additionally, we aimed to evaluate the interpretability of absolute Geometric GO values, which the-oretically represent the adaptive genetic distance between populations from distinct environments. Second, utilizing public real data from the crop pest species Bactrocera tryoni, a fruit fly native from Northern Australia, we computed GO between "source" populations and a diverse range of locations within invaded areas. This practical application of GO within the context of a biological invasion underscores its potential in providing insights and guiding recommendations for future invasion risk assessment. Overall, our results suggest that GO statistics represent good predictors of the estab-lishment probability and may thus inform invasion risk, although the influence of several factors on prediction performance (e.g. propagule pressure or admixture) will need further investigation.

evolutionary biology↗

bioRxiv2024

Measuring heritability in messy prebiotic chemical systems

A key question in origins-of-life research, is whether heritability, and thus evolution, could have preceded genes. Out-of-equilibrium chemical reaction networks with multiple autocatalytic motifs may provide chemical "memory" and serve as units of heritability, but experimental validation is lacking. We established conditions that may be conducive to the emergence of heritable variation and developed methods to search for heritability and autocatalysis. We prepared a food set (FS) of three organic species, three inorganic salts and pyrite. We conducted a serial dilution experiment where FS was incubated for 24 hours, after which a 20% fraction was transferred into freshly prepared FS that went through the same procedure, repeated for 10 generations. To serve as controls, we also incubated the fresh solutions in each generation. We compared the chemical composition of transfer vials and no-transfer controls using liquid chromatography-mass spectrometry (LCMS), with metrics adapted from ecology and evolutionary biology. While variability was high, focusing on a subset of chemicals with more consistent patterns revealed evidence of heritable variation among vials. Using rule-based chemical reaction network inference, constrained by the LCMS data, we identified a plausible FS-driven chemical reaction network that was found to contain numerous autocatalytic cycles.

evolutionary biology↗

bioRxiv2016

Happens in the best of subfamilies: Replacement and internalisation of co-obligate Serratia endosymbionts in Lachninae aphids

Virtually all aphids maintain an obligate mutualistic symbiosis with bacteria from the Buchnera genus, which produce essential nutrients for their aphid hosts. Most aphids from the Lachninae subfamily have been consistently found to house additional endosymbionts, mainly Serratia symbiotica. This apparent dependence on secondary endosymbionts was proposed to have been triggered by the loss of the riboflavin biosynthetic capability by Buchnera in the Lachninae last common ancestor. However, an integral large-scale analysis of secondary endosymbionts in the Lachninae is still missing, hampering the interpretation of the evolutionary and genomic analyses of these endosymbionts. Here, we analysed the endosymbionts of selected representatives from seven different Lachninae genera and nineteen species, spanning four tribes, both by FISH (exploring the symbionts morphology and tissue tropism) and 16S rRNA gene sequencing. We demonstrate that all analysed aphids possess dual symbiotic systems, and while most harbour S. symbiotica, some have undergone symbiont replacement by other phylogenetically-distinct bacterial taxa. We found that these secondary associates display contrasting cell shapes and tissue tropism, and some appear to be lineage-specific. a scenario for symbiont establishment in the Lachninae, followed by changes in the symbionts tissue tropism and symbiont replacement events, thereby highlighting the extraordinary versatility of host-symbiont interactions.\n\nOriginality-Significance StatementA key question in evolutionary biology is that of how mutualism evolves. One way to approach this problem is to investigate recently-established mutualistic associations, particularly by comparing various symbiotic systems in closely related hosts. Here, we present a most comprehensive study to investigate co-obligate symbioses in aphids, focusing in the Lachninae subfamily. While most aphids keep an obligate vertically-transmitted association with intracellular Buchnera bacteria, some, such as members of the Lachninae subfamily, host an additional putative co-obligate symbiont. Thus, the Lachninae dual symbiotic systems offer a unique opportunity to understand the evolutionary dynamics of host-symbiont associations, in particularly how secondary symbionts become obligate and eventually may be replaced. Through genome sequencing of three aphid species belonging to distantly related tribes within the subfamily, we have previously corroborated that they have indeed established co-obligate mutualistic associations with the S. symbiotica secondary endosymbiotic bacterium. This was putatively facilitated by an ancient pseudogenisation of the riboflavin biosynthetic pathway in Buchnera, rendering it unable to provide the essential vitamin to the host. However, not all Lachninae members harbour S. symbiotica, some species being associated to at least four different bacterial taxa. To correctly interpret the genomic data and to understand the evolutionary dynamics of these symbiotic associations, a wide-range analysis of both the phylogenetic relations as well as of the secondary symbionts localisation within the bacteriome is needed. To tackle this, we have combined phylogenetic analyses of the symbionts 16S rRNA gene sequences and FISH microscopy, to understand the symbionts identity as well as the morphological characteristics and tissue tropism. The phylogenetic affinities and patterns of co-divergence of the symbionts, in combination with previously published genomic data, have enabled us to build an evolutionary scenario for the establishment, changes in tissue tropism such as \"stable\" internalisation into bacteriocytes, and replacements of the putative \"ancient\" secondary endosymbiont from the Lachninae last common ancestor. Also, we were able to determine through phylogenetic analyses that some putative co-obligate endosymbionts may have evolved from once facultative ones. The evolutionary framework presented here reveals a dynamic pattern for the more recent evolutionary history of these symbioses, including replacement and novel acquisition of phylogenetically different co-obligate symbionts. This study opens new research avenues on this symbiont-diverse subfamily, providing insight into how mutualism in endosymbiotic associations can evolve, and the role these bacteria have played in the species adaptation and even in the speciation process.

Evolutionary Biology↗

bioRxiv2017

Identifying drivers of parallel evolution: A regression model approach

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100045). Parallel evolution, defined as identical changes arising in independent populations, is often attributed to similar selective pressures favoring the fixation of identical genetic changes. However, some level of parallel evolution is also expected if mutation rates are heterogeneous across regions of the genome. Theory suggests that mutation and selection can have equal impacts on patterns of parallel evolution, however empirical studies have yet to jointly quantify the importance of these two processes. Here, we introduce several statistical models to examine the contributions of mutation and selection heterogeneity to shaping parallel evolutionary changes at the gene-level. Using this framework we analyze published data from forty experimentally evolved Saccharomyces cerevisiae populations. We can partition the effects of a number of genomic variables into those affecting patterns of parallel evolution via effects on the rate of arising mutations, and those affecting the retention versus loss of the arising mutations (i.e. selection). Our results suggest that gene-to-gene heterogeneity in both mutation and selection, associated with gene length, recombination rate, and number of protein domains drive parallel evolution at both synonymous and nonsynonymous sites. While there are still a number of parallel changes that are not well described, we show that allowing for heterogeneous rates of mutation and selection can provide improved predictions of the prevalence and degree of parallel evolution.\n\nData archival locationDryad, doi to be included later

evolutionary biology↗

bioRxiv2022

Frequencies and Features of Frameshift Mutations in Microevolution and Macroevolution of Viruses

Some nucleotide insertions or deletions (indels) in open reading frames of virus genes lead to frameshift mutations (FSMs), which can drastically change amino acid sequences. Most FSMs are deleterious and inhibited by natural selection, but some FSMs could aid viruses in adapting to new hosts, escaping immunity, or changing viral pathogenicity or transmissibility. Surprisingly, various fundamental aspects of FSMs in virus evolution remain unknown. In this report, we identified 679 FSMs in the genomes of viruses from 13 randomly selected animal virus families using randomly selected sequences. The 679 FSMs were formed with 1-5 indels, and most (89.4%) FSMs were fixed through the compensatory mechanism with two indels. Each FSM changed 3-209 (mean=15.4, median=13) amino acid residues. FSM frequencies were usually higher in viral sequences with lower sequence identities and steeply increased when sequence identities declined to 60.0%-69.9% or 70.0%-79.9%. This suggests that FSMs are more important to the macroevolution (i.e., inter-species evolution, including speciation) than to the microevolution (i.e., intra-species evolution) of viruses. This study provided novel evidence for the hopeful monster hypothesis in evolutionary biology. Furthermore, we found that FSMs occurred at different frequencies among genes in the same virus genomes and among virus families. Collectively, this study revealed multiple fundamental features of FSMs in virus evolution for the first time and provided novel insights into the mechanisms of macroevolution and speciation.

evolutionary biology↗

bioRxiv2020

Chromosomal arrangement of synthetic lethal gene pairs: repulsion or attraction?

Synthetic lethal interactions are of paramount importance both in biology and in medicine, and hence increasing efforts have been devoted to their systematic identification. Our previous computational analysis revealed that in prokaryotic species, synthetic lethal genes tend to be further away in chromosomes than random (i.e. repulsion), which was shown to provide bacterial genomes with greater robustness to large-scale DNA deletions. To test the generalizability of this observation in eukaryotic genomes, we leveraged the wealth of experimentally determined synthetic lethal genetic interactions of yeast that are curated in the BioGRID (Biological General Repository for Interaction Datasets) database. We observed an opposite trend that is the genomic proximity of synthetic lethal gene pairs both on the 2D and 3D chromosomal space of the yeast genome (i.e. 2D and 3D attraction). To gain mechanistic insights into the origin of the attraction of synthetic lethal gene pairs in S. cerevisiae, we characterized four classes of genes, in which synthetic lethal interactions are enriched and partly explain the observed patterns of genomic attraction: i) gene pairs operating on the same pathways, 2) co-expressed genes, 3) gene pairs whose protein products physically interact and 4) the paralogs. However, our analysis revealed that the contribution of these four types of genes is not sufficient to fully explain the observed 2D and 3D attraction of synthetic lethal gene pairs and hence its evolutionary origin still remains as an open question. Significance statementUnravelling the organizing principles underlying gene arrangements is one of the fundamental questions of research in evolutionary biology. One understudied aspect of this organization is the relative chromosomal arrangement of synthetic lethal gene pairs. In this study, by analyzing a wealth of synthetic lethality data in yeast, we provide evidence that synthetic lethal gene pairs tend to be attracted to each other both on 2D and 3D chromosomal space of the yeast genome. This observation is in sharp contrast with the repulsion of synthetic lethal (metabolic) gene pairs that we observed previously in bacterial genomes. Characterizing the evolutionary forces underlying this genomic pattern in yeast can open the door towards an evolutionary theory of genome organization in eukaryotes.

evolutionary biology↗

bioRxiv2025

Rapid and repeated evolution of the pigmentation patterns in reef fishes

Pigmentation patterns are integral to animal biology1-3 and uncovering the mechanisms driving their diversification is essential for determining the evolutionary principles that shape this fundamental aspect of biodiversity4-7. Coral reef fishes are particularly notable for their extraordinary pattern diversity, ranging from simple spots and stripes to intricate, maze-like designs. Despite over a century of investigation, the evolutionary processes that govern the diversification of these pigmentation patterns remain one of the most persistent unresolved questions in evolutionary biology. Here, we investigate the relationship between pattern diversity, species richness, and geography across six iconic families of pattern-diverse coral reef fishes. Utilizing time-calibrated phylogenies, we reveal constant disparity of pigmentation patterns across globally variable reef fish communities8. We find strong evidence for a positive correlation between pattern diversity and species richness, with a high divergence of pigmentation patterns in sympatry that highlights the role of these patterns in speciation and phenotypic differentiation. Moreover, our findings support the stages model of adaptive radiation9, revealing that most pigmentation pattern diversity has emerged in evolutionary history. These results demonstrate that the evolutionary history of pigmentation patterns in reef fishes is characterized by a combination of rapid and constrained phenotypic diversification that has likely played a crucial role in their speciation dynamics.

evolutionary biology↗

bioRxiv2014

Bias and measurement error in comparative analyses: a case study with the Ornstein Uhlenbeck model

Phylogenetic comparative methods are increasingly used to give new insight into variation, causes and consequences of trait variation among species. The foundation of these methods is a suite of models that attempt to capture evolutionary patterns by extending the Brownian constant variance model. However, the parameters of these models have been hypothesised to be biased and only asymptotically behave in a statistically predictable way as datasets become large. This does not seem to be widely appreciated. We show that a commonly used model in evolutionary biology (the Ornstein-Uhlenbeck model) is biased over a wide range of conditions. Many studies fitting this model use datasets that are small and prone to substantial biases. Our results suggest that simulating fitted models and comparing with empirical results is critical when fitting OU and other extensions of the Brownian model.

Evolutionary Biology↗

bioRxiv2019

Adaptive and maladaptive genetic diversity in small populations; insights from the Brook Charr (Salvelinus fontinalis) case study

Investigating the relative importance of neutral versus selective processes governing the accumulation of genetic variants is a key goal in evolutionary biology. This is particularly true in the context of small populations, where genetic drift can counteract the effect of selection. In this study, we investigated the accumulation of putatively beneficial and harmful variations using 7,950 high-quality filtered SNPs among 36 lacustrine, seven riverine and seven anadromous Brook Charr (Salvelinus fontinalis) populations (n = 1,193) from Quebec, Canada. Using the Provean algorithm, we observed an accumulation of deleterious mutations that tend to be more prevalent in isolated lacustrine and riverine populations than the more connected anadromous populations. In addition, the absence of correlation between the occurrence of putative beneficial nor deleterious mutations and local recombination rate supports the hypothesis that genetic drift might be the main driver of the accumulation of such variants. Despite the effect of pronounced genetic drift and limited gene flow in non-anadromous populations, several loci representing biological functions of potential adaptive significance were associated with environmental variables, and particularly with temperature. We also identified genomic regions associated with anadromy. We also observed an overrepresentation of transposable elements associated with variation in environmental variables, thus supporting the importance of transposable elements in adaptation.

evolutionary biology↗

bioRxiv2025

Friend or foe: A mosquito parasite with mixed transmission mode displays mutualistic traits promoting oogenesis.

Mutualism is often selected in vertically transmitted symbionts due to their fitness interdependence with hosts. However, the evolution of mutualism remains unclear in symbionts using both vertical and horizontal transmission. In this study, we show that Ascogregarina taiwanensis, previously known as a weak horizontally transmitted parasite of the Asian tiger mosquito (Aedes albopictus), exhibits mutualistic traits that enhance mosquito reproduction. The symbiont improves embryogenesis and extends the egg-laying period while most females are pseudo-vertically transmitting symbiont oocysts to their progeny at oviposition sites. Dual transcriptomic analyses reveal that early oogenesis in infected females involves increased nitrogen metabolism in both partners, enhanced detoxification of blood waste, and activation of egg development pathways. These changes lead to improved assimilation of blood proteins essential for egg production. Our findings provide rare empirical evidence of a symbiont displaying both parasitic and mutualistic traits, offering new insights into the evolutionary dynamics of mixed-mode transmission symbioses. Significance StatementHow mutualism evolves from parasitism remains a central question in evolutionary biology, particularly for symbionts that combine vertical and horizontal transmission. We show that Ascogregarina taiwanensis, an Apicomplexan parasite previously known to be costly for developing Aedes albopictus mosquitoes, is also pseudo-vertically transmitted: most females release oocysts into the water during oviposition, exposing their offspring. Surprisingly, infection enhances host reproduction by promoting oogenesis through protein assimilation, leading to the production of larger larvae. Dual transcriptomic analyses reveal coordinated shifts in host and parasite metabolism, especially in nitrogen assimilation. Our findings provide rare evidence that mutualistic traits can emerge in a symbiont with mixed-mode transmission, offering new insights into the evolutionary transitions shaping host-microbe interactions.

evolutionary biology↗