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Results for “Evolutionary Biology”

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bioRxiv2025

The evolution of gene expression in seasonal environments

The biological activities of organisms are closely linked to seasonality. Phenology, the temporal orchestration of biological activities, is governed by gene expression, yet the evolutionary dynamics underlying seasonal gene expression remain unclear. To investigate these dynamics, we compared genome-wide expression dynamics (molecular phenology) in four dominant evergreen Fagaceae species in Asia (Quercus glauca, Q. acuta, Lithocarpus edulis, and L. glaber), using leaf and bud tissues over two seasonal cycles. We assembled high-quality reference genomes, identifying 11749 single-copy orthologous genes. Seasonal transcriptomic profiling of these orthologous genes revealed highly conserved gene expression across species in winter when temperatures fall below [~]10{degrees}C. Rhythmic gene expression with significant periodic oscillations was more prevalent in buds (51.9%) than in leaves (40.6%), with most rhythmic genes (78.4-92.0%) exhibiting annual periodicity, while a smaller fraction (1.2-11.9%) followed half-annual cycles. The seasonal peaks of rhythmic genes were highly synchronized across species in winter but diverged during the growing season, reflecting species-specific timing of leaf flushing and flowering. These findings suggest that the four species share a common molecular calendar in winter, which constrains the evolution of gene expression under seasonal environments. Impact StatementA comparative analysis of genome-wide seasonal gene expression dynamics across four forest tree species revealed that a shared "molecular calendar" emerges in winter, constraining gene expression evolution and potentially limiting temporal niche partitioning and species divergence in seasonal environments.

evolutionary biology↗

bioRxiv2025

Ecological inheritance facilitates the coexistence of environmental helpers and free-riders

Variation in social traits and behaviours is widespread in nature and can be maintained by selection. Many social traits influence fitness indirectly by modifying shared environments that are transmitted across generations, a process known as ecological inheritance. Here, we investigate how variation in environmentally mediated social behaviour, such as helping to improve shared resources, can emerge and persist in spatially subdivided populations where locally modified environments are transmitted across generations. Using mathematical and computational modelling, we show that ecological inheritance, when combined with limited dispersal, readily leads to the stable coexistence of two types with opposite environmental legacies: helpers, who improve the local environment for the future at a personal cost, and environmental free-riders, who benefit without contributing to the detriment of future generations. In turn, this polymorphism generates lasting spatial heterogeneity in environmental quality and, consequently, in survival and reproduction--particularly under isolation-by-distance, creating stable clusters of high- and low-quality habitats across an otherwise homogeneous landscape. These findings reveal how ecological inheritance and spatial structure interact to stabilise polymorphism, potentially driving long-term behavioural, ecological, and fitness variation across diverse biological systems.

evolutionary biology↗

bioRxiv2025

Generalists link peaks in the shifting adaptive landscape of Australia's dragon lizards

The adaptive landscape is a flexible concept in biology which helps map entities onto an eco-evolutionary topography. A common practice is clustering species to identify adaptive peaks but the pathways that allow movement into new adaptive zones remain poorly understood. Here we integrate new sequence-capture (>5,000 nuclear markers) and multivariate morphological data to investigate the adaptive landscape of Amphibolurinae dragon lizards (Agamidae). Our well-supported, time-calibrated phylogeny includes over 360 specimens from 176 species, including iconic taxa such as the frilled-neck lizard, thorny devil, and bearded dragon. We show that arrival in Australia was followed by rapid expansion of morphological diversity facilitated by generalist habitat use. Ancestral dragons were likely arboreal, but species with broad niche breadths and intermediate morphologies provided pathways to subsequent specialization. These findings reveal an evolutionary pathway for adaptive diversification in a major continental radiation.

evolutionary biology↗

bioRxiv2025

Non-ergodicity in ecology and evolution

Stochasticity plays an important role in all biological systems. The standard way to deal with stochasticity involves averaging over an ensemble of independent realizations. However, such mean statistics need not accurately reflect the typical outcomes in any finite sample unless the system satisfies the property of ergodicity, which guarantees that each trajectory will over time experience the same statistics as the entire ensemble. Here, we argue that, in contrast, non-ergodicity might instead be the rule rather than exception in real biological systems and investigate its implications for eco-evolutionary dynamics through three case-studies. First, we show how demographic stochasticity leads to ergodicity breaking where the asymptotic growth rate carries a signature of the initial condition. This motivates us to define a mutant establishment threshold, which quantifies a critical population size above which the typical mutant population starts to grow. Second, we consider environmental stochasticity and demonstrate that autocorrelated environmental variation does not average out in time, which has the important consequence that the fitness of a genotype cannot be simply averaged over the environments. Finally, we show how in a metapopulation structure the evolutionary dynamics within a typical subpopulation can deviate from the ensemble dynamics in the entire metapopulation, which is sufficient to explain the evolution and persistence of cooperation despite a fitness cost.

evolutionary biology↗

bioRxiv2019

Floral signals evolve in a predictable way under artificial and pollinator selection in Brassica rapa using a G-matrix

BackgroundAngiosperms employ an astonishing variety of visual and olfactory floral signals that are generally thought to evolve under natural selection. Those morphological and chemical traits can form highly correlated sets of traits. It is not always clear which of these are used by pollinators as primary targets of selection and which would be indirectly selected by being linked to those primary targets. Quantitative genetics tools for predicting multiple traits response to selection have been developed since long and have advanced our understanding of evolution of genetically correlated traits in various biological systems. We use these tools to predict the evolutionary trajectories of floral traits and understand the selection pressures acting on them. ResultsWe used data from an artificial and a pollinator (bumblebee, hoverfly) selection experiment with fast cycling Brassica rapa plants to predict evolutionary changes of 12 floral volatiles and 4 morphological floral traits in response to selection. Using the observed selection gradients and the genetic variance-covariance matrix (G-matrix) of the traits, we showed that the responses of most floral traits including volatiles were predicted in the right direction in artificial- and bumblebee-selection experiment, revealing direct and indirect targets of bumblebee selection. Genetic covariance had a mix of constraining and facilitating effects on evolutionary responses. We further revealed how G-matrices evolved in the selection processes. ConclusionsOverall, our integrative study shows that floral signals, and especially volatiles, evolve under selection in a mostly predictable way, at least during short term evolution. Evolutionary constraints stemming from genetic covariance affected traits evolutionary trajectories and thus it is important to include genetic covariance for predicting the evolutionary changes of a comprehensive suite of traits. Other processes such as resource limitation and selfing also needs to be considered for a better understanding of floral trait evolution.

evolutionary biology↗

bioRxiv2019

Relaxed constraint and functional divergence of the progesterone receptor (PGR) in the human stem-lineage

The steroid hormone progesterone, acting through the progesterone receptor (PR), a ligand-activated DNA-binding transcription factor, plays an essential role in regulating nearly every aspect of female reproductive biology. While many reproductive traits regulated by PR are conserved in mammals, Catarrhine primates evolved several derived traits including spontaneous decidualization, menstruation, and a divergent (and unknown) parturition signal, suggesting that PR may also have evolved divergent functions in Catarrhines. There is conflicting evidence, however, whether the progesterone receptor gene (PGR) was positively selected in the human lineage. Here we show that PGR evolved rapidly in the human stem-lineage (as well as other Catarrhine primates), which likely reflects an episode of relaxed selection intensity rather than positive selection. Coincident with the episode of relaxed selection intensity, ancestral sequence resurrection and functional tests indicate that the major human PR isoforms (PR-A and PR-B) evolved divergent functions in the human stem-lineage. These results suggest that the regulation of progesterone signaling by PR-A and PR-B may also have diverged in the human lineage and that non-human animal models of progesterone signaling may not faithfully recapitulate human biology.

evolutionary biology↗

bioRxiv2016

Detection of pathways affected by positive selection in primate lineages ancestral to humans

Gene set enrichment approaches have been increasingly successful in finding signals of recent polygenic selection in the human genome. In this study, we aim at detecting biological pathways affected by positive selection in more ancient human evolutionary history. Focusing on four branches of the primate tree that lead to modern humans, we tested all available protein coding gene trees of the Primates clade for signals of adaptation in these branches, using the likelihood-based branch site test of positive selection. The results of these locus-specific tests were then used as input for a gene set enrichment test, where whole pathways are globally scored for a signal of positive selection, instead of focusing only on outlier \"significant\" genes. We identified signals of positive selection in several pathways that are mainly involved in immune response, sensory perception, metabolism, and energy production. These pathway-level results are highly significant, even though there is no functional enrichment when only focusing on top scoring genes. Interestingly, several gene sets are found significant at multiple levels in the phylogeny, but different genes are responsible for the selection signal in the different branches. This suggests that the same function has been optimized in different ways at different times in primate evolution.

Evolutionary Biology↗

bioRxiv2016

A positive association between population genetic differentiation and speciation rates in New World birds

Although an implicit assumption of speciation biology is that population differentiation is an important stage of evolutionary diversification, its true significance remains largely untested. If population differentiation within a species is related to its speciation rate over evolutionary time, the causes of differentiation could also be driving dynamics of organismal diversity across time and space. Alternatively, geographic variants might be short-lived entities with rates of formation that are unlinked to speciation rates, in which case the causes of differentiation would have only ephemeral impacts. Combining population genetics datasets including 17,746 individuals from 176 New World bird species with speciation rates estimated from phylogenetic data, we show that the population differentiation rates within species predict their speciation rates over long timescales. Although relatively little variance in speciation rate is explained by population differentiation rate, the relationship between the two is robust to diverse strategies of sampling and analyzing both population-level and species-level datasets. Population differentiation occurs at least three to five times faster than speciation, suggesting that most populations are ephemeral. Population differentiation and speciation rates are more tightly linked in tropical species than temperate species, consistent with a history of more stable diversification dynamics through time in the Tropics. Overall, our results suggest investigations into the processes responsible for population differentiation can reveal factors that contribute to broad-scale patterns of diversity.

evolutionary biology↗

bioRxiv2023

Introgressive descent and hypersexuality drive the evolution of sexual parasitism and morphological reduction in a fungal species complex.

Taxonomists consider species as discrete units of biological organization, which are subject to a continuous process of evolutionary change and are connected through their shared ancestry. However, the continuous nature of evolutionary change is difficult to reconcile with the discrete outcome of speciation, especially where species boundaries are permeable. A good example of this inconsistency is the lichen genus Pyrenodesmia, which shows a high morphologic and genetic diversity that that defies systematization by taxonomic or phylogenetic methods. Here we show that hybridization explains the presence of discordant morphs and that European species are interconnected through cross-mating in a single reproductive network, a syngameon, despite which species remain largely distinct and distinguishable. Whole genome data reflect the important role played by genome defense mechanisms in the genomic stabilization of fungal hybrids. The recurrence of Repeat Induced Point mutations (RIP) shapes genomes with islands of suppressed recombination and loss of gene content, which in turn generates a feedback loop reinforcing the lack of reproductive isolation through the loss of heterokaryon incompatibility and a tendency towards morphological reduction.

evolutionary biology↗

bioRxiv2023

Rapid life-history evolution reinforces competitive asymmetry between invasive and resident species

Biological invasions by phylogenetically and ecologically similar competitors pose an evolutionary challenge to native species. Cases of character displacement following invasions suggest that they can respond to this challenge by shifting their traits. However, the actual impact of such shifts on competition are seldom studied. Here, we study competition between two freshwater snails from Guadeloupe (French Antilles), the native Aplexa marmorata and the introduced Physa acuta. The former has responded to invasion by rapid life-history evolution towards earlier maturity, higher fecundity and higher juvenile survival, traits that might favor rapid population growth in a noncompetitive context, but not necessarily in a competitive one. We here observe negative impacts of competition by both species on each other, though P. acuta is dominant and over generations largely displaces A. marmorata from co-cultures. In addition, our experiments suggest that A. marmorata populations having experienced competition by P. acuta for sufficient time in nature, have evolved to become even less tolerant to it. Though apparently paradoxical, this result supports the hypothesis that rapid life-history evolution has allowed A. marmorata not to resist competition, but to avoid it by increasing its specialization into the colonizer lifestyle previously documented by long-term field surveys. This example illustrates how evolution, in accordance with metacommunity coexistence theory, sometimes takes other ways than specialization into distinct types of resources or habitats to ensure coexistence between related species inhabiting the same landscape.

evolutionary biology↗

bioRxiv2025

In Vitro and Viral Evolution Convergence Reveal the Selective Pressures Driving Omicron Emergence

In vitro protein evolution provides powerful insights into the amino acid sequences that underlie key biological functions. Here, we used this approach to explore the evolutionary trajectories of the SARS-CoV-2 spike protein receptor-binding domain (RBD) constrained to engage the human ACE2 receptor--an essential first step in viral infection. Applying mild (LSS) or stringent (HSS) selection pressures starting from the ancestral Wuhan strain, we found that HSS, but not LSS rapidly converged on mutations characteristic of the Omicron variant. HSS resulted in fewer, but dominant, non-synonymous mutations mirroring Omicron mutations and its advanced sub-lineages. Conversely, LSS produced only some Omicron-like mutations at much lower frequencies and with incomplete representation. Notably, initiating evolution from Omicron itself resulted in high-fidelity maintenance of Omicron-defining mutations under both HSS and LSS conditions. This evolutionary pattern parallels global SARS-CoV-2 mutation trends as well as in silico simulations, emphasizing the critical role of receptor-binding constraints in shaping viral adaptation, which may be a frequent driver during zoonosis. Predominantly immune evasion associated mutations not selected in vitro. Our findings demonstrate the predictive capacity of in vitro evolution, suggesting Omicrons abrupt emergence resulted from rare, high-stringency selection, superimposed on a background of broader, milder pressures, with Omicron being the humanized SARS-CoV-2.

evolutionary biology↗

bioRxiv2018

Assessing the impact of high-throughput sequencing strategy and model complexity on ABC-inferred demographic history in mussels

Genome-scale diversity data are increasingly available in a variety of biological systems, and can be used to reconstruct the past evolutionary history of species divergence. However, extracting the full demographic information from these data is not trivial, and requires inferential methods that account for the diversity of coalescent histories throughout the genome. Here, we evaluate the potential and limitations of one such approach. We reexamine a well-known system of mussel sister species, using the joint site frequency spectrum (jSFS) of synonymous mutations computed either from exome capture or RNA-seq, in an Approximate Bayesian Computation (ABC) framework. We first assess the best sampling strategy (number of: individuals, loci, and bins in the jSFS), and show that model selection is robust to variation in the number of individuals and loci. In contrast, different binning choices when summarizing the joint site frequency spectrum, strongly affect the results: including classes of low and high frequency shared polymorphisms can more effectively reveal recent migration events. We then take advantage of the flexibility of ABC to compare more realistic models of speciation, including variation in migration rates through time (i.e. periodic connectivity) and across genes (i.e. genome-wide heterogeneity in migration rates). We show that these models were consistently selected as the most probable, suggesting that mussels have experienced a complex history of gene flow during divergence and that the species boundary is semi-permeable. Our work provides a comprehensive evaluation of ABC demographic inference in mussels based on the coding site frequency spectrum, and supplies guidelines for employing different sequencing techniques and sampling strategies. We emphasize, perhaps surprisingly, that inferences are less limited by the volume of data, than by the way in which they are analyzed.

evolutionary biology↗

bioRxiv2016

An Extended Maximum Likelihood Inference of Geographic Range Evolution by Dispersal, Local Extinction and Cladogenesis

The origin and evolution of species ranges remains a central focus of historical biogeography and the advent of likelihood methods based on phylogenies has revolutionized the way in which range evolution has been studied. A decade ago, the first elements of what turned out to be a popular inference approach of ancestral ranges based on the processes of Dispersal, local Extinction and Cladogenesis (DEC) was proposed. The success of the DEC model lies in its use of a flexible statistical framework known as a Continuous Time Markov Chain and since, several conceptual and computational improvements have been proposed using this as a baseline approach. In the spirit of the original version of DEC, we introduce DEC eXtended (DECX) by accounting for rapid expansion and local extinction as possible anagenetic events on the phylogeny but without increasing model complexity (i.e. in the number of free parameters). Classical vicariance as a cladogenetic event is also incorporated by making use of temporally flexible constraints on the connectivity between any two given areas in accordance with the movement of landmasses and dispersal opportunity over time. DECX is built upon a previous implementation in C/C++ and can analyze phylogenies on the order of several thousand tips in a few minutes. We test our model extensively on Pseudo Observed Datasets and on well-curated and recently published data from various island clades and a worldwide phylogeny of Amphibians (3309 species). We also propose the very first implementation of the DEC model that can specifically account for trees with fossil tips (i.e. non-ultrametric) using the phylogeny of palpimanoid spiders as a case study. In this paper, we argue in favour of the proposed improvements, which have the advantage of being computationally efficient while toeing the line of increased biological realism.

Evolutionary Biology↗

bioRxiv2019

The successful invasion of the European earwig across North America reflects adaptations to thermal regimes but not mean temperatures

Understanding the mechanisms by which an introduced species adapt to newly encountered habitats is a major question in ecology. A key method to address this question is to collect data on introduced species that have successfully invaded a broad diversity of novel environments, and analyze how their life-history traits changed with these new constraints. Here, we present and analyze such a unique data set in the European earwig Forficula auricularia L, an insect that invaded North America during the last century. We conducted a common garden experiment, in which we measured 13 life-history traits in 4158 individuals from 19 populations across North America. Our results demonstrate that the successful invasion of this species came with changes in 10 of their life-history traits in response to thermal regimes (winter-summer and autumn-spring temperatures), but with no change in response to the overall mean temperatures of the invaded locations. Importantly, we show that some of these changes are by-products of novel thermal regimes, whereas others reflect adaptive strategies of females to these constraints. Overall, our findings reveal the importance of thermal regimes over mean temperatures in climate adaptation, and emphasize that studying adaptive capabilities is crucial to predict the limits of biological invasions.

evolutionary biology↗

bioRxiv2015

Distinguishing contemporary hybridization from past introgression with post-genomic ancestry-informative SNPs in strongly differentiated Ciona species

Biological introductions bring into contact species that can still hybridize. The evolutionary outcomes of such secondary contacts may be diverse (e.g. adaptive introgression from or into the introduced species) but are not yet well examined in the wild. The recent secondary contact between the non-native sea squirt Ciona robusta (formerly known as C. intestinalis type A) and its native congener C. intestinalis (formerly known as C. intestinalis type B), in the western English Channel, provides an excellent case study to examine. To examine contemporary hybridization between the two species, we developed a panel of 310 ancestry-informative SNPs from a population transcriptomic study. Hybridization rates were examined on 449 individuals sampled in 8 sites from the sympatric range and 5 sites from allopatric ranges. The results clearly showed an almost complete absence of contemporary hybridization between the two species in syntopic localities, with only one first generation hybrid and no other genotype compatible with recent backcrosses. Despite the almost lack of contemporary hybridization, shared polymorphisms were observed in sympatric and allopatric populations of both species. Furthermore, one allopatric population from SE Pacific exhibited a higher rate of shared polymorphisms compared to all other C. robusta populations. Altogether, these results indicate that the observed level of shared polymorphism is more probably the outcome of ancient gene flow spread afterwards at a worldwide scale. They also emphasise efficient reproductive barriers preventing hybridization between introduced and native species, which suggests hybridization should not impede too much the expansion and the establishment of the non-native species in its introduction range.

Evolutionary Biology↗

bioRxiv2023

Beauty beacon: correlated strategies for the Fisher runaway process

Suppose that females choose males based on attributes that do not signal any genetic quality that is not related to the choice itself. Can being choosy confer selective advantage in this situation? We introduce correlated strategies, which means that females, when making their choice, may take into consideration external and independent random factors that are known to be observable by all. Individual-based simulation is used to show that, in this case, choosiness can emerge against the cost of over 25% when pitted against randomly mating females. Moreover, after being established in the population, it can sustain costs of over 35% . While such costs are not biologically plausible, they demonstrate unequivocally that sexual choice is a strong evolutionary force. Thus, correlated strategies are shown to be an evolutionary tool that channels randomness from the environment into genetic diversity. In addition, it turns out that a higher number of attributes in the ornament makes the choice more advantageous, which may result in a runaway complexity of sexual traits. Implications for the evolution of (female) cognitive abilities and speciation are discussed.

evolutionary biology↗

bioRxiv2025

Rapid evolution in response to biological invasion: variation in resistance and survival of the European bitterling fish across a gradient of Sinanodonta woodiana expansion

Biological invasions impose new selective pressures on native species, prompting rapid evolutionary responses. We examined how the parasitic larvae (glochidia) of the invasive East Asian mussel Sinanodonta woodiana affect European bitterling fish (Rhodeus amarus) populations with different histories of exposure to the parasite (none, 15 years, or 40+ years). Glochidia parasitise fish fins and gills, and bitterling are especially vulnerable to parasitism due to their spawning association with mussels. We found the lowest glochidia load in bitterling from populations with the longest association with S. woodiana. While infection reduced swimming capacity proportionally to parasite load, this effect was not population-specific. However, post-infection mortality was highest in naive and lowest in long-associated populations, indicating evolved tolerance. No long-term effects on survival, growth, condition, or reproduction were observed, suggesting fitness costs are concentrated shortly after infection. These results show that novel host-parasite interactions during invasions can drive rapid adaptive change, emphasising the need to consider evolutionary dynamics in invasion management.

evolutionary biology↗

bioRxiv2020

Ontogenetic and static allometry of hind femur length in the cricket Gryllus bimaculatus (Orthoptera: Gryllidae) with implications for evo-devo of morphological scaling

The evolution of morphological allometry or scaling is a long-standing enigma in biology. Three types of allometric relationships have been defined: static, ontogenetic and evolutionary allometry. However, the theory of the interrelationship between these three types of allometry have not been tested in Orthopterans and to a lesser extent in hemimetabolous insects. Here, the ontogenetic allometry of hind femur length in the cricket Gryllus bimaculatus was observed to be slightly positive as compared with a negative allometric relationship for Orthopterans in general, while the instar-specific static allometries were highly variable. The findings give support for the size-grain hypothesis in Orthoptera and indicate that ontogenetic allometries may not predict evolutionary allometries. The current model for the developmental basis of allometry derived from holometabolous insects is extended into a phylogenetic context and the potential of G. bimaculatus and other Orthopterans for further experiments of evo-devo of morphological scaling is discussed.

evolutionary biology↗