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Genomic quantification of inbreeding depression in wild vertebrate populations

Inbreeding depression is a critical driver of extinction risk in fragmented populations, yet its magnitude in the wild has historically been estimated using sparse pedigrees or low-resolution molecular markers. The transition to genomic metrics of inbreeding offers unprecedented precision in quantifying realized homozygosity and its fitness costs. We conducted a systematic review and multi-level meta-analysis of 91 effect sizes from 20 wild vertebrate populations to provide a global benchmark for genomic inbreeding depression. Our results confirm a pervasive and significant negative relationship between fitness and genomic inbreeding. Males exhibited significantly stronger inbreeding depression than females. Fitness costs were consistent across life stages (developmental, adult and lifetime) and across types of fitness traits (survival vs. reproduction). We found no significant association between the magnitude of inbreeding depression and IUCN conservation status or historical isolation (discretely measured as "isolated" or "non-isolated"). As we enter a genomics era that will provide realised estimates of inbreeding, future studies can be added to this meta-analysis to provide a more comprehensive view of inbreeding depression and potentially identify patterns pertinent to evolutionary biology and conservation science.

evolutionary biology↗

Cost of resistance: an unreasonably expensive concept

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (https://doi.org/10.24072/pci.evolbiol.100052). The cost of resistance, or the fitness effect of resistance mutation in absence of the drug, is a very widepsread concept in evolutionary genetics and beyond. It has represented an important addition to the simplistic view that resistance mutations should solely be considered as beneficial mutations. Yet, this concept also entails a series of serious difficulties in its definition, interpretation and current usage. In many cases, it may be simpler, clearer, and more insightful to study, measure and analyze the fitness effects of mutations across environments and to better distinguish those effects from pleiotropic effects of those mutations.

evolutionary biology↗

On the feasibility of saltational evolution

One of the key tenets of Darwins theory that was inherited by the Modern Synthesis of evolutionary biology is gradualism, that is, the notion that evolution proceeds gradually, via accumulation of \"infinitesimally small\" heritable changes 1,2. However, some of the most consequential evolutionary changes, such as, for example, the emergence of major taxa, seem to occur abruptly rather than gradually, as captured in the concepts of punctuated equilibrium 3,4 and evolutionary transitions 5,6. We examine a mathematical model of an evolutionary process on a rugged fitness landscape 7,8 and obtain analytic solutions for the probability of multi-mutational leaps, that is, several mutations occurring simultaneously, within a single generation in one genome, and being fixed all together in the evolving population. The results indicate that, for typical, empirically observed combinations of the parameters of the evolutionary process, namely, effective population size, mutation rate, and distribution of selection coefficients of mutations, the probability of a multi-mutational leap is low, and accordingly, their contribution to the evolutionary process is minor at best. However, such leaps could become an important factor of evolution in situations of population bottlenecks and elevated mutation rates, such as stress-induced mutagenesis in microbes or tumor progression, as well as major evolutionary transitions and evolution of primordial replicators.

evolutionary biology↗

Accelerated simulation of evolutionary trajectories in origin-fixation models

We present an accelerated algorithm to forward-simulate origin--fixation models. Our algorithm requires on average only about two fitness evaluations per fixed mutation, whereas traditional algorithms require, per one fixed mutation, a number of fitness evaluations on the order of the effective population size Ne. Our accelerated algorithm yields the exact same steady state as the original algorithm but produces a different order of fixed mutations. By comparing several relevant evolutionary metrics, such as the distribution of fixed selection coefficients and the probability of reversion, we find that the two algorithms behave equivalently in many respects. However, the accelerated algorithm yields less variance in fixed selection coefficients. Notably, we are able to recover the expected amount of variance by rescaling population size, and we find a linear relationship between the rescaled population size and the population size used by the original algorithm. Considering the widespread usage of origin--fixation simulations across many areas of evolutionary biology, we introduce our accelerated algorithm as a useful tool for increasing the computational complexity of fitness functions without sacrificing much in terms of accuracy of the evolutionary simulation.

evolutionary biology↗

Evolutionary adaptability linked to length variation in short genic tandem repeats

Intrinsically disordered protein regions are of high importance for temperature sensing and immune responses in plants. Tracts of identical amino acids accumulate in these regions and can vary in length over generations due to expansions and retractions of short tandem repeats at the genomic level. However, little attention has been paid to what extent length variation is shaped by natural selection. By environmental association analysis on 2,514 length variable tracts in 770 whole-genome sequenced wild Arabidopsis thaliana we show that length variation in glutamine and asparagine amino acid homopolymers, as well as in interaction hotspots, correlate with local bio-climatic habitat. We determined experimentally that the promoter activity of a light-stress gene depended on polyglutamine length variants in a disordered transcription factor. Our results show that length variations impact protein function and are substantially shaped by natural selection. Length variants modulating protein function at a global genomic scale has implications for understanding protein evolution and eco-evolutionary biology.

evolutionary biology↗

Antagonism in Evolutionary Opportunities Results in Non-Monotonic Evolution Across an Environmental Gradient

Establishing reliable frameworks for predicting unknown outcomes from empirical observations is of great interest to ecologists and evolutionary biologists. Strong predictability in evolutionary responses has been previously demonstrated by the repeated observation of similar phenotypes or genotypes across multiple natural or experimental populations in analogous environments. However, the degree to which evolutionary outcomes can be predicted across environmental gradients, or in fluctuating environments, remains largely unexplored. Presumably, the phenotypic evolution in an intermediate environment could be interpolated from the evolved phenotypes observed in two extreme environments, but this assumption remains to be fully tested. Here, we report on the experimental evolution of Escherichia coli under three nutritional transfer periods: every day, every 10 days, and every 100 days, representing increasing severity in feast/famine cycles. After 900 days of experimental evolution, populations experiencing intermediate durations of starvation had evolved longer times to reach maximum growth rate, smaller colony sizes, higher biofilm formation, and higher mutation rates than populations evolving in the other environmental extremes. Because the intermediately starved populations exhibit significantly high molecular parallelism, these distinct phenotypes are likely due to non-monotonic deterministic forces instead of increased stochastic forces commonly associated with fluctuating environments. Our results demonstrate novel complexities associated with evolutionary predictability across environmental gradients and highlight the risk of using interpolation in evolutionary biology.

evolutionary biology↗

Dude, Everyone Wants Pattern Analysis Tools (DEWPAT): Tools for measuring visual pattern diversity from digital images

O_LIExploring the diversity and function of complex colour patterns is a fundamental interest in ecology and evolutionary biology, but progress on many questions is limited by our ability to quantify diverse visual patterns. We address this problem by introducing Dude, Everyone Wants Colour Pattern Analysis Tools (DEWPAT), a Python package for characterizing multidimensional pattern complexity. C_LIO_LIDEWPAT is a flexible framework designed to extract a diversity of components of visual pattern complexity from standard RGB and multispectral images, including entropy (information content), average gradient magnitude (edge content), high frequency content (detail granularity), generalized variance (heterogeneity), and patch dissimilarity. DEWPAT offers optional image transformation functionality, including blurring to model receiver acuity and segmentation to reduce noise. C_LIO_LIFunctions in this package return both quantitative measurements and graphical representations of color and pattern diversity. We demonstrate DEWPATs key functions and applications with three empirical examples (longhorn beetles, anole lizards, and flowers). C_LIO_LIDEWPAT has the potential to quantitatively characterize previously intractable pattern phenotypes in ways that make their features available for biological analysis. C_LI

evolutionary biology↗

Lifespan-extending downregulation of insulin signalling reduces germline mutation load

Reduced insulin/IGF-1 signalling (IIS) robustly extends lifespan and enhances somatic stress resistance across taxa, yet its consequences for germline genome integrity remain unclear. Here we combine multigenerational mutation accumulation with whole-genome sequencing in C. elegans to test whether adulthood-only IIS downregulation can simultaneously promote somatic maintenance and limit germline mutational burden. We reduced IIS by adult-onset daf-2 RNAi in wild-type and heritable RNAi-deficient (hrde-1) backgrounds, allowing either spontaneous or UV-induced germline mutations to accumulate over multiple generations. In wild-type animals, reduced IIS lowered germline single-nucleotide mutation rates by up to [~]50% and prevented the UV-induced elevation in mutation rate, without detectable costs to fecundity or lineage persistence. By contrast, in hrde-1 mutants the same intervention increased both point mutations and transposable-element-driven insertions under UV exposure, accelerating lineage extinction. Thus, the genome-protective effect of reduced IIS critically requires the germline nuclear Argonaute HRDE-1, which mediates small-RNA-guided epigenetic silencing. Functional annotation of germline variants revealed enrichment in pathways linked to development, cellular maintenance and conserved longevity regulators, including IIS and mTOR, and identified high-impact mutations in genes with human orthologs implicated in neurodegeneration and cancer. Our findings show that IIS can coordinate somatic and germline maintenance in concert, rather than in competition, through an HRDE-1-dependent epigenetic pathway. This work positions nutrient-sensing IIS as a central regulator of germline genome stability and suggests that IIS downregulation can reduce germline mutation load while extending lifespan, with broad implications for biogerontology and evolutionary biology.

evolutionary biology↗

Information theory and the phenotypic complexity of evolutionary adaptations and innovations

Two main lines of research link information theory to evolutionary biology. The first focuses on organismal phenotypes, and on the information that organisms acquire about their environment. The second connects information-theoretic concepts to genotypic change. The genotypic and phenotypic level can be linked by experimental high-throughput genotyping and computational models of genotype-phenotype relationships. I here use a simple information-theoretic framework to compute a phenotypes information content (its phenotypic complexity), and the information gain or change that comes with a new phenotype. I apply this framework to experimental data on DNA-binding phenotypes of multiple transcription factors. Low phenotypic complexity is associated with a biological systems ability to discover novel phenotypes in evolution. I show that DNA duplications lower phenotypic complexity, which illustrates how information theory can help explain why gene duplications accelerate evolutionary adaptation. I also demonstrate that with the right experimental design, sequencing data can be used to infer the information gain associated with novel evolutionary adaptations, for example in laboratory evolution experiments. Information theory can help quantify the evolutionary progress embodied in the discovery of novel adaptive phenotypes.

Evolutionary Biology↗

Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat

Mammalian olfactory receptors (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoires is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of more specialized OR repertoires has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed leaf-nosed bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous versus duplicated receptors among Carollia species, and identified orthologous receptors and associated paralogs to explore the diversity and redundancy of the receptor gene repertoire. The most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two more generalist species (sowelli, perspicillata), but we discovered a few unique sets of ORs within C. castanea with exceptional redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants to an extent that the other species cannot. C. perspicillata, the species with the most generalist diet, had a larger diversity of functional receptors, suggesting the ability to detect a wider range of odorant molecules. The variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication plays a role in dietary adaptations and underlies patterns of ecological interactions between bats and plants. Impact Statement--though it asks for 3-4 sentencesThe sense of smell is essential to how many animals detect food, yet few studies have demonstrated how dietary evolution has shaped olfactory receptor genes, which encode proteins that bind to environmental scent cues, including food odorants. We compared the evolutionary history of olfactory receptor repertoires in three co-occurring neotropical bat species along a spectrum of dietary specialization on the fruits of Piper plants. We found the more generalist species possessed a more diverse olfactory receptor profile, potentially reflecting an ability to detect more diverse arrays of fruit scent compounds, while the specialist had a narrower profile that demonstrated more redundancy. By introducing creative approaches to measure diversity in large gene families and connecting diet specialization and molecular diversity, this study makes an unprecedented contribution to evolutionary biology.

evolutionary biology↗

Inferring Species Trees Using Integrative Models of Species Evolution

Evolutionary models account for either population- or species-level processes, but usually not both. We introduce a new model, the FBD-MSC, which makes it possible for the first time to integrate both the genealogical and fossilization phenomena, by means of the multispecies coalescent (MSC) and the fossilized birth-death (FBD) processes. Using this model, we reconstruct the phylogeny representing all extant and many fossil Caninae, recovering both the relative and absolute time of speciation events. We quantify known inaccuracy issues with divergence time estimates using the popular strategy of concatenating molecular alignments, and show that the FBD-MSC solves them. Our new integrative method and empirical results advance the paradigm and practice of probabilistic total evidence analyses in evolutionary biology.

evolutionary biology↗

Evolutionary macroecology: Incorporating phylogenetic information more explicitly into process-based, forward time, simulation models

AO_SCPLOWBSTRACTC_SCPLOWA conceptual and mechanistic approach for bridging the fields of macroecology (ecological biogeography) and historical biogeography has been a long-term aim in Evolutionary Biology. Such a bridge could increase our understanding on the processes governing the spatial and temporal generation of biodiversity distribution patterns. This aim has been recently approached from the perspective of evolutionary biogeographic inferential statistical models, within a maximum likelihood or Bayesian framework, which incorporates the contribution of environmental factors as scaling parameters. Here, we describe a new approach that builds on a spatially-explicit, forward-time, computer simulation ("automat") model. The model sets a series of rules by which speciation, extinction, and dispersal of lineages are governed within an environmentally heterogeneous, two-dimensional gridded landscape. Unlike some previous approaches, niche conservatism is assumed but the model allows for environmental conditions to vary both spatially and temporally, by letting the model run over three time-series of actual palaeoclimate data, spanning the last 20 million years of geological history. Speciation is governed by a global speciation rate, whereas the background extinction rate is made dependent on abiotic (palaeoenvironmental conditions) and biotic (species density per grid cell) factors, hence giving a local background extinction rate. Also, we propose a novel mechanistic approach in which species are not the result of unique, independent events but linked through evolutionary history from a single evolutionary origin. We set different rules to generate the resulting phylogenies to test different factors (time, environment) that govern the inheritance of range distributions. Dispersal follows a simple Poisson kernel model, with higher probability of migration to contiguous grid cells and rare long-distance movements to distant cells. We also describe ways in which the presence of temporal dispersal barriers could modify the resultant spatial patterns. Evaluation of model accuracy and fit is based on comparison of simulated spatial patterns with observed, empirical ones. We use statistic dependent variables such as the spatial distribution of species in the landscape, species geographic range size and location, and the shape of the resultant phylogenies. Finally, we propose that this spatially-explicit simulation model could be used to evaluate the role played by niche conservatism, ecological vicariance and climatic-driven extinction in the generation of disjunct continental patterns, such as the presence of sister-lineages in numerous families of angiosperms forming a ring in the continental margins of the African continent, the Rand Flora pattern.

evolutionary biology↗

Optimised control of adaptive evolution with competing selective pressures

The development of methods to understand and control the population dynamics of microbial evolution remains an outstanding question in synthetic biology and biotechnology more broadly. Due to the stochastic nature of evolution, its limited observability, and complex intra-population dynamics, this presents a significant challenge. In this paper, we explore techniques to control the evolutionary dynamics of a population, based on manipulation of one or two orthogonal selective pressures, which may in turn be coupled to mutagenesis. Our approach builds on past research in evolutionary biology that developed frameworks to study intra-population variant competition during asexual adaptive processes (i.e. clonal interference). Extending this theory, we design optimal control strategies for one (or more) selective pressures that can be used to maximise the rate of adaptation across a population as a whole. We introduce a theoretical modelling framework for this process, which we support with both simulations and preliminary experimental data, providing a concrete basis for emerging control approaches to directed evolution and evolution-aware design.

evolutionary biology↗

Neutral Drift and Threshold Selection Promote Phenotypic Variation

Phenotypic variations within a population exist on different scales of biological organization and play a central role in evolution by providing adaptive capacity at the population-level. Thus, the question of how evolution generates phenotypic variation within an evolving population is fundamental in evolutionary biology. Here we address this question by performing experimental evolution of an antibiotic resistance gene, VIM-2 {beta}-lactamase, combined with diverse biochemical assays and population genetics. We found that neutral drift, i.e., evolution under a static environment, with a low antibiotic concentration can promote and maintain significant phenotypic variation within the population with >100-fold differences in resistance strength. We developed a model based on the phenotype-environment-fitness landscape generated with >5,000 VIM-2 variants, and demonstrated that the combination of "mutation-selection balance" and "threshold-like fitness-phenotype relationship" is sufficient to explain the generation of large phenotypic variation within the evolving population. Importantly, high-resistance conferring variants can emerge during neutral drift, without being a product of adaptation. Our findings provide a novel and simple mechanistic explanation for why most genes in nature, and by extension, systems and organisms, inherently exhibit phenotypic variation, and thus, population-level evolvability.

evolutionary biology↗

Reconstruction of body mass evolution in the Cetartiodactyla and mammals using phylogenomic data.

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100042).\n\nReconstructing ancestral characters on a phylogeny is an arduous task because the observed states at the tips of the tree correspond to a single realization of the underlying evolutionary process. Recently, it was proposed that ancestral traits can be indirectly estimated with the help of molecular data, based on the fact that life history traits influence substitution rates. Here we challenge these new approaches in the Cetartiodactyla, a clade of large mammals which, according to paleontology, derive from small ancestors. Analysing transcriptome data in 41 species, of which 22 were newly sequenced, we provide a dated phylogeny of the Cetartiodactyla and report a significant effect of body mass on the overall substitution rate, the synonymous vs. non-synonymous substitution rate and the dynamics of GC-content. Our molecular comparative analysis points toward relatively small Cetartiodactyla ancestors, in agreement with the fossil record, even though our data set almost exclusively consists of large species. This analysis demonstrates the potential of phylogenomic methods for ancestral trait reconstruction and gives credit to recent suggestions that the ancestor to placental mammals was a relatively large and long-lived animal.

evolutionary biology↗

Experimental evolution reveals competing selective forces during an early pollinator shift in monkeyflowers

Understanding how complex multi-trait adaptations arise in nature remains a fundamental challenge in evolutionary biology. A classic example of this adaptation is the pollination syndrome, where integrated suites of floral characteristics co-evolve to attract specific pollinators. While transitions between pollination syndromes occur frequently, the underlying evolutionary trajectories traversed by adapting populations remain largely opaque. Here, we used an experimental evolution approach to track real-time phenotypic and genomic changes during a pollinator switch, leveraging the novel attraction to bumblebees exhibited by hybrids between the hummingbird-pollinated Mimulus cardinalis and the self-pollinating M. parishii. Within only three generations of bumblebee selection, we observed remarkably rapid shifts in floral traits, genotypes, and fitness. Our findings demonstrate that pollinator shifts are likely shaped by a complex interplay of selection, genomic conflict, and pleiotropic constraints that cannot be predicted simply by the genetic architecture of floral traits alone.

evolutionary biology↗

Does mother know best? Range-wide narrowing of host preference in Aricia agestis confers fitness benefits but may incur long-term costs

Biological communities are responding to changes in climate through a combination of range shifts and evolution in situ. However, even in systems where we have genomic and phenotypic evidence of recent adaptation, the ecological and fitness consequences of such evolutionary change remain underexplored, especially in terms of consequences for interactions between species. European Lepidoptera are excellent systems for understanding such shifts, given our exceptional knowledge of their ecology, natural history, and past distributions. The UK Brown Argus butterfly (Aricia agestis) has expanded rapidly northward in response to climate change. This expansion has been associated with evolutionary shifts in maternal host preference, from the chalkland restricted but locally common perennial Rockrose (Helianthemum nummularium) to more broadly distributed, but locally rare annual Geraniums (Geraniaceae). Such a rapid range shift offers an excellent opportunity to test how the evolution of novel biotic interactions associated with climate adaptation affects individual fitness and population resilience. Using common garden assays of host preference on females sampled across the UK in 2013 and 2023, we show for the first time that female preference for Geranium molle or Rockrose hosts vary among individuals within as well as among sites and to different extents at different locations. This variation is consistent with genomic signals of recent selective sweeps on these traits. In particular, we show that in 2013, females in the new part of the range are more likely to oviposit on the locally dominant host, while females from the ancestral range will use both hosts, regardless of the locally dominant host. We also demonstrate a significant temporal shift in behaviour, with a narrowing of host preference towards Geranium molle recorded in A.agestis ancestral range in 2023. To evaluate the fitness consequences of these shifts in biotic interactions, we assessed larval performance of 1412 larvae from 49 families on both host plants. Irrespective of maternal preference, feeding on Geranium molle hosts conferred higher survival, faster development and larger adult body size under laboratory conditions. These fitness outcomes are likely linked to Geranium molles significantly higher protein: carbohydrate ratio when compared to Rockrose. Moreover, we also found that larvae fed Geranium molle produced adults with elevated mass-independent resting metabolic rates, a rare demonstration that larval diet has lasting metabolic consequences in a wild butterfly. Crucially, we found no evidence of trade-offs between preference and performance: even offspring of females that laid exclusively on Rockrose also performed better on Geranium molle. These results suggest that Geranium molle confers a general performance advantage, enhancing traits likely to promote population persistence where Geranium molle is reliably available. However, despite selection favouring Geranium molle in warming climates, we also show that a narrowing of host preference towards these more widespread host plants throughout the UK range is likely to make A.agestis populations more vulnerable under future warmer, drier conditions, when compared to Rockrose. Together these findings highlight a central challenge in evolutionary biology: what happens when traits that are adaptive in the short term spread rapidly through populations, but are likely to become maladaptive as environmental conditions continue to change?

evolutionary biology↗

Rare variation in malaria parasites biases population-genetic inference

Understanding how pathogens evolve is fundamental to disease control and is a basic question in evolutionary biology, yet pathogens with complex life cycles violate assumptions of classic evolutionary models. Genetic analyses of the malaria parasite Plasmodium falciparum have shown multiple surprising patterns. For example, empirical analyses produce effective population size estimates that vary by orders of magnitude depending on the method and an excess of genes with elevated nonsynonymous variation (measured as{pi} N /{pi}S). Here, reanalyzing genomic data from 18 worldwide populations, I show that these observations directly follow from distributions of genetic variation enriched for rare variants. Multiple potential mechanisms may increase the proportion of rare variants, including host expansions, lifecycle dynamics, population structure, or selection. The observed genealogies are more consistent with a multiple-merger coalescent than a Kingman coalescent, causing common summary statistics to be biased in predictable directions. In particular, the abundance of rare variants interacts with the mathematical properties of ratio statistics to systematically inflate gene-level{pi} N /{pi}S estimates even in the absence of selection. Notably, filtering this rare variation reveals previously masked candidates for selection, including well-characterized antigens such as merozoite surface proteins. This framework provides a foundation for interpreting genomic data in pathogens with high variance in reproductive success. Significance StatementPathogen genomics increasingly guides public health decisions, yet organisms with complex life cycles can produce genealogies that violate assumptions of standard population genetic methods. Here I show that the malaria parasite Plasmodium falciparum has an excess of rare variation, perhaps produced from overdispersed distributions of reproductive success. These genealogies generate systematic biases in commonly reported statistics arising from the interaction between rare variation and the mathematical properties of the statistics themselves, not from biological processes often invoked to explain anomalous patterns. Correcting for this bias reveals signatures of selection in well-characterized vaccine candidates that were previously masked, demonstrating that appropriate null models are essential for identifying targets of intervention and inferring evolutionary history in pathogens and other systems with reproductive skew.

evolutionary biology↗