SEARCH · Search bioRxiv

Results for “Evolutionary Biology”

Search indexed bioRxiv preprints in genomics, neuroscience, cell biology and bioinformatics. Read source abstracts and check manuscript versions; preprints are not peer reviewed.

Quote a phrase for an exact phrase match. Source license links do not imply unrestricted reuse.

At least 307 records · Page 17Linked to original sources

bioRxiv2024

Escherichia coli adaptation under prolonged resource exhaustion is characterized by extreme parallelism and frequent historical contingency

Like many other non-sporulating bacterial species, Escherichia coli is able to survive prolonged periods of resource exhaustion, by entering a state of growth called long-term stationary phase (LTSP). In July 2015, we initiated a set of evolutionary experiments aimed at characterizing the dynamics of E. coli adaptation under LTSP. In these experiments populations of E. coli were allowed to initially grow on fresh rich media, but where not provided with any new external growth resources since their establishment. Utilizing whole genome sequencing data obtained for hundreds of clones sampled at 12 time points spanning the first six years of these experiments, we reveal several novel aspects of the dynamics of adaptation. First, we show that E. coli continuously adapts genetically, up to six years under resource exhaustion, through the highly convergent accumulation of mutations. We further show that upon entry into LTSP, long-lasting lineages are established. This lineage structure is in itself convergent, with similar lineages arising across independently evolving populations. The high parallelism with which adaptations occur under LTSP, combined with the LTSP populations lineage structure, enable us to screen for pairs of loci displaying a significant association in the occurrence of mutations, suggestive of a historical contingency. We find that such associations are highly frequent and that a third of convergently mutated loci are involved in at least one such association. Combined our results demonstrate that LTSP adaptation is characterized by remarkably high parallelism and frequent historical contingency. Author summaryCharacterizing the dynamics by which adaptation occurs is a major aim of evolutionary biology. Here, we study these dynamics in five populations of Escherichia coli, independently evolving over six years under conditions of resource exhaustion. We show that even under very prolonged resource exhaustion bacteria continuously genetically adapt. Within our populations long lasting lineages are established, each of which undergoes independent and continuous adaptation. We demonstrate that bacterial adaptation under resource exhaustion is both highly convergent - meaning that same adaptive mutations occur across independently evolving populations and lineages, and frequently historically contingent - meaning that the adaptive nature of many of the adaptations we see depends on the previous occurrence of other adaptations.

evolutionary biology↗

bioRxiv2025

Adaptive Dynamics of Quantitative Traits in a SteadilyChanging Environment

Understanding the adaptation of quantitative traits to changing environments is a central challenge in evolutionary biology. However, the precise roles of the speed of environmental change and trait architecture in adaptive dynamics remain unclear. Here, we investigate their roles through an adaptive walk model and individual-based polygenic simulations within a moving-soptimum framework. We introduce a dimensionless parameter, the effective selection strength, to characterize quantitative traits in both models. We show that adapting populations attain a stationary state below a critical speed of environmental change. Properties of the stationary state are compared between the two approaches, and it is shown that the adaptive walk model provides a good approximation for long-term polygenic adaptation. Additionally, in the adaptive walk model, we derive an explicit formula for the logarithmic divergence of the stationary phenotypic gap upon approaching the critical speed. To elucidate population extinction in biologically realistic terms, we define a fitness-threshold-based critical speed and reveal its power-law dependence on the effective selection strength in both models. Finally, results of our polygenic simulations show how the genetic architecture in the stationary regime is shaped by a dynamic equilibrium between the influx of de novo mutations and their loss through fixation and extinction constrained by the rate of phenotypic change enforced by the optimum speed. Taken together, our study advances the understanding of polygenic adaptation and provides insights to simplify analytical work and computational simulations for future studies.

evolutionary biology↗

bioRxiv2021

Origin of electroneutrality in living system

Identifying the first chemical transformations, from which life emerged is a central problem in the theories of lifes origins. These reactions would likely have been self-sustaining and self-reproductive before the advent of complex biochemical pathways found in modern organisms to synthesize lipid membranes, enzymes, or nucleic acids. Without lipid membranes and enzymes, exceedingly low concentrations of the organic intermediates of early metabolic cycles in protocells would have significantly hindered evolvability. To address this problem, we propose a mechanism, where a positive membrane potential elevates the concentration of the organic intermediates. In this mechanism, positively charged surfaces of protocell membranes due to accumulation of transition metals generate positive membrane potentials. We compute steady-state ion distributions and determine their stability in a protocell model to identify the key factors constraining achievable membrane potentials. We find that (i) violation of electroneutrality is necessary to induce nonzero membrane potentials; (ii) strategies that generate larger membrane potentials can destabilize ion distributions; and (iii) violation of electroneutrality enhances osmotic pressure and diminishes reaction efficiency, thereby driving the evolution of lipid membranes, specialized ion channels, and active transport systems. SignificanceThe building blocks of life are constantly synthesized and broken down through concurrent cycles of chemical transformations. Tracing these reactions back 4 billion years to their origins has been a long-standing goal of evolutionary biology. The first metabolic cycles at the origin of life must have overcome several obstacles to spontaneously start and sustain their nonequilibrium states. Notably, maintaining the concentration of organic intermediates at high levels needed to support their continued operation and subsequent evolution would have been particularly challenging in primitive cells lacking evolutionarily tuned lipid membranes and enzymes. Here, we propose a mechanism, in which the concentration of organic intermediates could have been elevated to drive early metabolic cycles forward in primitive cells with ion-permeable porous membranes under prebiotic conditions and demonstrate its feasibility in a protocell model from first principles.

evolutionary biology↗

bioRxiv2022

Wavelet characterization of spatial pattern in allele frequency

Characterizing spatial patterns in allele frequencies is fundamental to evolutionary biology because these patterns contain evidence of underlying processes. However, the spatial scales at which gene flow, changing selection, and drift act are often unknown. Many of these processes can operate inconsistently across space, causing non-stationary patterns. We present a wavelet approach to characterize spatial pattern in allele frequency that helps solve these problems. We show how our approach can characterize spatial patterns in relatedness at multiple spatial scales, i.e. a multi-locus wavelet genetic dissimilarity. We also develop wavelet tests of spatial differentiation in allele frequency and quantitative trait loci (QTL). With simulation we illustrate these methods under different scenarios. We also apply our approach to natural populations of Arabidopsis thaliana to characterize population structure and identify locally-adapted loci across scales. We find, for example, that Arabidopsis flowering time QTL show significantly elevated genetic differentiation at 300 to 1300 km scales. Wavelet transforms of allele frequencies offer a flexible way to reveal geographic patterns and underlying evolutionary processes.

evolutionary biology↗

bioRxiv2019

The evolution of multicellular complexity: the role of relatedness and environmental constraints

A major challenge in evolutionary biology has been to explain the variation in multicellularity across the many independently evolved multicellular lineages, from slime moulds to humans. Social evolution theory has highlighted the key role of relatedness in determining multicellular complexity and obligateness, however there is a need to extend this to a broader perspective incorporating the role of the environment. In this paper, we formally test Bonners 1998 hypothesis that the environment is crucial in determining the course of multicellular evolution, with aggregative multicellularity evolving more frequently on land and clonal multicellularity more frequently in water. Using a combination of scaling theory and phylogenetic comparative analyses, we describe multicellular organisational complexity across 139 species spanning 14 independent transitions to multicellularity and investigate the role of the environment in determining multicellular group formation and in imposing constraints on multicellular evolution. Our results, showing that the physical environment has impacted the way in which multicellular groups form, could shed light on the role of the environment for other major evolutionary transitions.

evolutionary biology↗

bioRxiv2024

A Newborn F-box Gene Blocks Gene Flow by Selectively Degrading Phosphoglucomutase in Species Hybrids

The establishment of reproductive barriers such as postzygotic hybrid incompatibility (HI) remains the key to speciation. Gene duplication followed by differential functionalization has long been proposed as a major model underlying HI, but few supporting evidence exists. Here, we demonstrate that a new-born F-box gene, Cni-neib-1, of the nematode Caenorhabditis nigoni specifically inactivates an essential phosphoglucomutase encoded by Cbr-shls-1 in its sister species C. briggsae and their hybrids. Zygotic expression of Cni-neib-1 specifically depletes Cbr-SHLS-1, but not Cni-SHLS-1, in approximately 40 minutes starting from gastrulation, causing embryonic death. Cni-neib-1 is one of thirty-three paralogues emerging from a recent surge in F-box gene duplication events within C. nigoni, all of which are evolving under positive selection. Cni-neib-1 undergoes turnover even among C. nigoni populations. Differential expansion of F-box genes between the two species could reflect their distinctive innate immune responses. Collectively, we demonstrate how recent duplication of genes involved in protein degradation can cause unintended destruction of targets in hybrids that leads to HI, providing an invaluable insight into mechanisms of speciation. Significance statementUnderstanding how reproductive isolation forms and triggers speciation remains a central topic in evolutionary biology. In this study, the authors reveal a novel molecular mechanism that obstructs gene flow between the nematodes Caenorhabditis briggsae and C. nigoni. A recently evolved, species-specific F-box gene in C. nigoni selectively depletes an essential phosphoglucomutase enzyme in C. briggsae, leading to embryonic lethality in hybrids. This mechanism effectively prevents gene flow from C. nigoni to C. briggsae. This discovery underscores how a newborn gene, arising from recent gene duplication, can contribute to reproductive isolation by inadvertently disrupting a functionally important protein in hybrid offspring.

evolutionary biology↗

bioRxiv2020

Selection for reducing energy cost of protein production drives the GC content and amino acid composition bias in gene transfer agents

Gene transfer agents (GTAs) are virus-like elements integrated into bacterial genomes, particularly, those of Alphaproteobacteria. The GTAs can be induced under nutritional stress, incorporate random fragments of bacterial DNA into mini-phage particles, lyse the host cells and infect neighboring bacteria, thus enhancing horizontal gene transfer. We show that the GTA genes evolve under pronounced positive selection for the reduction of the energy cost of protein production as shown by comparison of the amino acid compositions with both homologous viral genes and host genes. The energy saving in GTA genes is comparable to or even more pronounced than that in the genes encoding the most abundant, essential bacterial proteins. In cases when viruses acquire genes from GTAs, the bias in amino acid composition disappears in the course of evolution, showing that reduction of the energy cost of protein is an important factor of evolution of GTAs but not bacterial viruses. These findings strongly suggest that GTAs are bacterial adaptations rather than selfish, virus-like elements. Because GTA production kills the host cell and does not propagate the GTA genome, it appears likely that the GTAs are retained in the course of evolution via kin or group selection. Therefore, we hypothesize that GTA facilitate the survival of bacterial populations under energy-limiting conditions through the spread of metabolic and transport capabilities via horizontal gene transfer and increase of nutrient availability resulting from the altruistic suicide of GTA-producing cells. ImportanceKin and group selection remain controversial topics in evolutionary biology. We argue that these types of selection are likely to operate in bacterial populations by showing that bacterial Gene Transfer Agents (GTAs), but not related viruses, evolve under positive selection for the reduction of the energy cost of a GTA particle production. We hypothesize that GTAs are dedicated devices for the survival of bacteria under the conditions of nutrient limitation. The benefits conferred by GTAs under nutritional stress appear to include horizontal dissemination of genes that could provide bacteria with enhanced capabilities for nutrient utilization and the increase of nutrient availability through the lysis of GTA-producing bacteria.

evolutionary biology↗

bioRxiv2025

Phylogeny, systematics and evolution of mimicry patterns in Neotropical limenitidine butterflies

The Neotropical butterfly genus Adelpha Hubner exhibits remarkable species diversity and striking convergence in wing colour patterns potentially explained by mimicry, making it an exceptional model for exploring trait evolution and its relationship with speciation. To date, unresolved phylogenetic relationships hinder a comprehensive understanding of the evolutionary biology of the genus. Using a novel multi-marker dataset combining one mitochondrial and 15 nuclear gene fragments, we generate the most comprehensive phylogeny of the genus Adelpha to revisit its systematics and investigate the evolution of mimicry colour patterns. Our data set encompasses 83 of the 87 known extant species and six Limenitis species that were recently excluded from Adelpha (134 of c. 160 subspecies in total), collectively displaying 14 distinct mimicry patterns. We provide conclusive evidence that corroborates previous work on the polyphyly of Adelpha as historically conceived, and describe the genus Adelphina Paez & Willmott n. gen. to stabilize the nomenclature, both genera representing Neotropical limenitidines. The comprehensive phylogeny provided in this study lays a solid foundation for future research into the processes driving diversification within these species interacting through mimicry. Ancestral character state reconstruction reveals gradual evolution of mimicry pattern. The more common mimicry pattern IPHICLUS (forewing with orange subapical spot and white band) is inferred as ancestral, but repeated convergent evolution is also recovered. Evolutionary convergence is also observed for the second most abundant mimicry pattern, COCALA (orange-white banded). Increased rates of mimicry pattern evolution are also found toward the equator. These results underscore the complexity of mimicry evolution in the Neotropical limenitidines i.e., Adelpha and Adelphina, emphasizing the need to explore its interplay with other biotic and abiotic factors.

evolutionary biology↗

bioRxiv2024

Comparative Single Cell Analysis of Transcriptional Bursting Reveals the Role of Genome Organization on de novo Transcript Origination

Spermatogenesis is a key developmental process underlying the origination of newly evolved genes. However, rapid cell type-specific transcriptomic divergence of the Drosophila germline has posed a significant technical barrier for comparative single-cell RNA-sequencing (scRNA-Seq) studies. By quantifying a surprisingly strong correlation between species- and cell type-specific divergence in three closely related Drosophila species, we apply a new statistical procedure to identify a core set of 198 genes that are highly predictive of cell type identity while remaining robust to species-specific differences that span over 25-30 million years of evolution. We then utilize cell type classifications based on the 198-gene set to show how transcriptional divergence in cell type increases throughout spermatogenic developmental time. After validating these cross-species cell type classifications using RNA fluorescence in situ hybridization (FISH) and imaging, we then investigate the influence of genome organization on the molecular evolution of spermatogenesis vis-a-vis transcriptional bursting. We first show altering transcriptional burst size contributes to pre-meiotic transcription and altering bursting frequency contributes to post-meiotic expression. We then report global differences in autosomal vs. X chromosomal transcription may arise in a developmental stage preceding full testis organogenesis by showing evolutionarily conserved decreases in X-linked transcription bursting kinetics in all examined somatic and germline cell types. Finally, we provide evidence supporting the cultivator model of de novo gene origination by demonstrating how the appearance of newly evolved testis-specific transcripts potentially provides short-range regulation of neighboring genes transcriptional bursting properties during key stages of spermatogenesis. Significance StatementUnderstanding the divergence and evolution of novel genes and expression is an essential question in evolutionary biology. However, rapid transcriptomic divergence in tissues such as testis has significantly hindered comparative single-cell RNA-Seq studies and understanding of the rapidly evolving components of the cell types. Here, we provide a novel strategy that does not rely on preexisting marker genes for cell type identity to overcome the challenge. We found that genome organization affects expressional evolution through transcriptional bursting dynamics. Our results also support the cultivator model of de novo gene origination--a model emphasizing the genomic environment in shaping novel gene origination--by illustrating how newly evolved transcripts alter the transcriptional bursting kinetics of neighboring genes.

evolutionary biology↗

bioRxiv2022

The evolution of cooperation in the unidirectional linear division of labour of finite roles

Evolution of cooperation is a puzzle in evolutionary biology and social sciences. Previous studies assumed that players are equal and have symmetric relationships. In our society, players are in different roles, have an asymmetric relationship, and cooperate together. We focused on the linear division of labour in a unidirectional chain that has finite roles, each of which is assigned to one group with cooperators and defectors. A cooperator in an upstream group produces and modifies a product, paying a cost of cooperation, and hands it to a player in a downstream group who obtains the benefit from the product. If players in all roles cooperate, a final product can be completed. However, if a player in a group chooses defection, the division of labour stops, the final product cannot be completed, and all players in all roles suffer damage. By using the replicator equations of the asymmetric game, we investigate which sanction system promotes the evolution of cooperation in the division of labour. We find that not the benefit of the product but the cost of cooperation matters to the evolutionary dynamics and that the probability of finding a defector determines which sanction system promotes the evolution of cooperation.

evolutionary biology↗

bioRxiv2019

The effect of autopolyploidy on population genetic signals of hard sweeps

Searching for population genomic signals left behind by positive selection is a major focus of evolutionary biology, particularly as sequencing technologies develop and costs decline. The effect of the number of chromosome copies (i.e. ploidy) on the manifestation of these signals remains an outstanding question, despite a wide appreciation of ploidy being a fundamental parameter governing numerous biological processes. We clarify the principal forces governing the differential manifestation and persistence of the signal of selection by separating the effects of polyploidy on rates of fixation versus rates of diversity (i.e. mutation and recombination) with a set of coalescent simulations. We explore what the major consequences of polyploidy, such as a more localized signal, greater dependence on dominance, and longer persistence of the signal following fixation, mean for within- and across-ploidy inference on the strength and prevalence of selective sweeps. As genomic advances continue to open doors for interrogating natural systems, studies such as this aid our ability to anticipate, interpret, and compare data across ploidy levels.

evolutionary biology↗

bioRxiv2019

Phenotypic determinism and contingency in the evolution of hypothetical tree-like organisms

Whether evolutionary history is mostly contingent or deterministic has been given much focus in the field of evolutionary biology. Studies addressing this issue have been conducted theoretically, based on models, and experimentally, based on microcosms. It has been argued that the shape of the adaptive landscape and mutation rate are major determinants of replicated phenotypic evolution. In the present study, to incorporate the effects of phenotypic plasticity, we constructed a model using tree-like organisms. In this model, the basic rules used to develop trees are genetically determined, but tree shape (described by the number and aspect ratio of the branches) is determined by both genetic components and plasticity. The results of the simulation show that the tree shapes become more deterministic under higher mutation rates. However, the tree shape became most contingent and diverse at the lower mutation rate. In this situation, the variances of the genetically determinant characters were low, but the variance of the tree shape is rather high, suggesting that phenotypic plasticity results in this contingency and diversity of tree shape. The present findings suggest that plasticity cannot be ignored as a factor that increases contingency and diversity of evolutionary outcomes.

evolutionary biology↗

bioRxiv2021

Sex, amitosis, and evolvability in the ciliate Tetrahymena thermophila

Understanding the mechanisms that generate genetic variation, and thus contribute to the process of adaptation, is a major goal of evolutionary biology. Mutation and genetic exchange have been well studied as mechanisms to generate genetic variation. However, there are additional processes that may also generate substantial genetic variation in some populations and the extent to which these variation generating mechanisms are themselves shaped by natural selection is still an open question. Tetrahymena thermophila is a ciliate with an unusual mechanism of nuclear division, called amitosis, which can generate genetic variation among the asexual descendants of a newly produced sexual progeny. We hypothesize that amitosis thus increases the evolvability of newly produced sexual progeny relative to species that undergo mitosis. To test this hypothesis, we used experimental evolution and simulations to compare the rate of adaptation in T. thermophila populations founded by a single sexual progeny to parental populations that had not had sex in many generations. The populations founded by a sexual progeny adapted more quickly than parental populations in both laboratory populations and simulated populations. This suggests that the additional genetic variation generated by amitosis of a heterozygote can increase the rate of adaptation following sex and may help explain the evolutionary success of the unusual genetic architecture of Tetrahymena and ciliates more generally.

evolutionary biology↗

bioRxiv2021

Host-associated microbial diversity in New Zealand cicadas uncovers elevational structure and replacement of obligate bacterial endosymbionts by Ophiocordyceps fungal pathogens

Host-microbe interactions influence eukaryotic evolution, particularly in the sap-sucking insects that often rely on obligate microbial symbionts to provision deficient nutrients in their diets. Cicadas (Hemiptera: Auchenorrhyncha: Cicadidae) specialize on xylem fluid and derive many essential amino acids and vitamins from intracellular bacteria or fungi (Hodgkinia, Sulcia, and Ophiocordyceps) that are propagated via transmission from mothers to offspring. Despite the beneficial role of these symbionts in nutrient provisioning, they are generally not considered to function within the gut where microbiota may play an important dietary role during insect diversification. Here, we investigate the relative impact of host phylogeny and ecology on gut microbial diversity in cicadas by sequencing 16S ribosomal RNA gene amplicons from 197 wild-collected cicadas and new mitochondrial genomes across 38 New Zealand cicada species, including natural hybrids between one species pair. We find a lack of phylogenetic structure and hybrid effects but a significant role of elevation in explaining variation in gut microbiota. Additionally, we provide evidence of Hodgkinia loss with gains of Ophiocordyceps fungal pathogens in all New Zealand cicadas examined that suggests convergent domestications of fungal pathogens. This highlights the macroevolutionary instability of obligate symbiosis and the relative importance of ecology rather than phylogeny for structuring gut microbial diversity in cicadas. ImportanceAn unresolved question in evolutionary biology is how beneficial associations between eukaryotes and microbes impact macroevolutionary patterns. We report substantial data from natural populations that suggest the absence of macroevolutionary impacts from gut microbiota in cicadas. Instead, gut microbial diversity is better explained by elevational variation across an island landscape. Cicadas, like many insects, have obligate nutritional associations with bacteria housed in organs outside of the gut, but we show that these associations seem also to be unstable at macroevolutionary scales. We report evidence for unexpected and widespread replacement of obligate bacteria by a domesticated and formerly pathogenic Ophiocordyceps fungus representing an evolutionarily convergent pattern across the cicada phylogeny.

evolutionary biology↗

bioRxiv2025

Learning the Shape of Evolutionary Landscapes: Geometric Deep Learning Reveals Hidden Structure in Phenotype-to-Fitness Maps

Elucidating the complex relationships between genotypes, phenotypes, and fitness remains one of the fundamental challenges in evolutionary biology. Part of the difficulty arises from the enormous number of possible genotypes and the lack of understanding of the underlying phenotypic differences driving adaptation. Here, we present a computational method that takes advantage of modern high-throughput fitness measurements to learn a map from high-dimensional fitness profiles to a low-dimensional latent space in a geometry-informed manner. We demonstrate that our approach using a Riemannian Hamiltonian Variational Autoencoder (RHVAE) outperforms traditional linear dimensionality reduction techniques by capturing the nonlinear structure of the phenotype-fitness map. When applied to simulated adaptive dynamics, we show that the learned latent space retains information about the underlying adaptive phenotypic space and accurately reconstructs complex fitness landscapes. We then apply this method to a dataset of high-throughput fitness measurements of E. coli under different antibiotic pressures and demonstrate superior predictive power for out-of-sample data compared to linear approaches. Our work provides a data-driven implementation of Fishers geometric model of adaptation, transforming it from a theoretical framework into an empirically grounded approach for understanding evolutionary dynamics using modern deep learning methods.

evolutionary biology↗

bioRxiv2022

Phylogenomic comparative methods: accurate evolutionary inferences in the presence of gene tree discordance

Phylogenetic comparative methods have long been a mainstay of evolutionary biology, allowing for inferences of the tempo and mode of trait evolution across species while accounting for their common ancestry. These analyses typically assume a single, bifurcating phylogenetic tree that describes the shared history among species. However, modern phylogenomic analyses have shown that genomes are often composed of a mosaic of different histories that can disagree both with the species tree and with each other--so-called discordant gene trees. These gene trees describe shared histories that are not captured by the species tree, and therefore that are unaccounted for in classic comparative approaches. The application of standard phylogenetic comparative methods to species histories containing discordance leads to incorrect inferences about the timing, direction, and rate of evolution. Here, we develop two approaches for incorporating gene tree histories into comparative methods: one involves constructing a fuller phylogenetic variance-covariance matrix that includes relationships not found in the species tree, and another that applies Felsensteins pruning algorithm over a set of gene trees to calculate trait histories and likelihoods. Both approaches are agnostic to the biological causes of gene tree discordance, which may include incomplete lineage sorting and introgression. Using simulation, we demonstrate that our new approaches generate much more accurate estimates of tree-wide rates of trait evolution than standard methods. We apply our methods to two clades of the wild tomato genus Solanum with varying rates of discordance, demonstrating the contribution of gene tree discordance to variation in a set of floral traits and the ability of our approaches to provide more accurate inferences. Our new approaches have the potential to be applied to a broad range of classic inference problems in phylogenetics, including ancestral state reconstruction and the inference of lineage-specific rate shifts.

evolutionary biology↗

bioRxiv2024

Testing for the genomic footprint of conflict between life stages in an angiosperm and a moss species

The maintenance of genetic variation by balancing selection is of considerable interest to evolutionary biologists. An important but understudied potential driver of balancing selection is antagonistic pleiotropy between diploid and haploid stages of the plant life cycle. Despite sharing a common genome, sporophytes (2n) and gametophytes (n) may undergo differential or even opposing selection. Theoretical work suggests the antagonistic pleiotropy between life stages can generate balancing selection and maintain genetic variation. Despite the potential for far-reaching consequences of gametophytic selection, empirical tests of its pleiotropic effects (neutral, synergistic, or antagonistic) on sporophytes are generally lacking. Here, we examined the population genomic signals of selection across life stages in the angiosperm Rumex hastatulus and the moss Ceratodon purpureus. We compared gene expression among life stages and between sexes, combined with neutral diversity statistics and the analysis of the distribution of fitness effects. In contrast to what would be predicted under balancing selection due to antagonistic pleiotropy, we found that unbiased genes between life stages were under stronger purifying selection, likely explained by a predominance of synergistic pleiotropy between life stages and strong purifying selection on broadly expressed genes. In addition, we found that 30% of candidate genes under balancing selection in R. hastatulus were located within inversion polymorphisms. Our findings provide novel insights into the genome-wide characteristics and consequences of plant gametophytic selection. SignificanceThe genome-wide importance of balancing selection has been a key question in evolutionary biology. Despite theoretical support for the potential of balancing selection generated by antagonistic pleiotropy between plant life stages, to our knowledge no empirical studies have systematically investigated this on a genome-wide scale. Our results revealed genome-wide patterns more consistent with synergistic pleiotropy, with gametophyte-biased genes more likely to be under relaxed purifying selection in both the angiosperm and moss species we investigated. In addition, our study suggests gene expression level and breadth has a greater effect on selection efficacy than differences between ploidy levels in different life stages.

evolutionary biology↗

bioRxiv2025

Distinct, asynchronous processes underlie cultural and genetic variation in a bird species with a complex song repertoire

Dialects in birdsongs represent population clusters and cultural diversity. Cultural and genetic variation in animals, however, do not always evolve along the same trajectory. Few studies have tested this in a wild songbird with a continuous learning strategy. Songbirds (oscine Passeriformes) with a continual learning window exhibit great song diversity and may show cultural differentiation that outpaces genetic divergence. We investigate cultural and genetic variation in a tropical endemic songbird in a topographically and climatically complex sky-island landscape of the Western Ghats of India. We combine fine-scale acoustic, behavioural, and genetic data: from 90 individuals (10,816 songs), analysed using frequency-temporal parameters and a linguistic method for syntax; a playback experiment with 136 trials to compare behavioural responses to local and non-local songs; and blood samples from 242 individuals (10,638 SNPs) to infer genetic population structure. We find no difference in songs across locations and individuals in the time-frequency domain, but only in syntax. One-third of notes, the smallest vocal units, are widely shared across all individuals in their distribution. Longer note combinations result in greater individual differences within populations, but only form small differences between populations. Geographic distance strongly predicts genetic but not song syntactic differences, and playback experiments show equal responses to local and non-local songs. Thus, strong individual signatures but weak local-level dialects are generated by a shared note repertoire and associated combinatorial syntax. We highlight that cultural transmission may operate at fine social scales, decoupled from genetic structure, which is strongly driven by isolation-by-distance. Significance statementWhether learned behaviours exhibit patterns similar to those of inherited genes remains a long-standing question in evolutionary biology. Birdsong has a strong cultural component paralleling human language, yet most knowledge comes from birds with a narrow learning window. Open-ended learners, who acquire new songs throughout life like humans, are poorly documented in the wild. We studied such a songbird restricted to the tropical cloud montane forests of southern India. Songs appear acoustically similar across populations but differ in how basic units are ordered (syntax), while individuals are more distinct from each other in longer note combinations than populations are. Genetic similarity decreased with geographic distance. Culturally learned traits can thus evolve independently of genetic structure, showing how learning decouples behaviour from geography-driven genetic ancestry.

evolutionary biology↗