BMC Evolutionary Biology

Body size, through its links to various physiological traits, has often been hypothesized to influence evolutionary rates. Negative body size-rate correlations have been reported in the morphological or molecular evolution of several extant vertebrate groups, including mammals, birds, reptiles, and teleost fishes. In this study, we estimated body masses for 89 species of plesiosaurs, a clade of Mesozoic aquatic reptiles, and found that their body size evolution conforms to a three-regime Ornstein-Uhlenbeck process, indicative of constrained evolution. Rates of morphological evolution, inferred using the skyline fossilized birth-death process and the variable-rates model, show minimal support for a correlation with body size in this clade. Our results thus serve as a counterexample, suggesting that the negative body size-rate relationship is not a universal vertebrate pattern, but rather a trend restricted to certain lineages.

Evolutionary innovation is a key driver of the colonization of new environments and the adaptive radiations of major groups. Novel traits typically evolve through the modification of pre-existing characters but the genetic paths underlying their origin have been challenging to trace, and the general requirements for and relative order of different kinds of gene mutations have been difficult to assess. Here, we trace the genomic origins of four procoagulant venom toxins (factor X, factor V, group I phospholipase A2, and Kunitz-type toxins) that collectively underlie a novel, especially potent blood-clotting venom type in the recently evolved Australian brown snake and taipan clade. We discover evidence for a previously unknown fifth toxin, coagulation factor VII, and show that the toxins evolved through two distinct genetic paths. The factor X and factor V toxins evolved through the sequential de novo co-option of ancestral clotting factor proteins that entailed their heterotopic expression in the venom gland, the fixation of segmental duplications containing each locus, and subsequent gain-of-function mutations that rendered factor X and factor V constitutively active. In contrast, the phospholipase A2 and Kunitz-type toxins evolved by modifying the functions of neurotoxins that were part of the venom arsenal. Our findings support models in which innovative mutations in single-copy genes precede gene duplication in the evolution of novel proteins and offer a rare view into the genesis of a complex trait that has played a central role in a major adaptive radiation. Significance StatementThis study investigates how an entirely new blood-clotting venom type evolved during the recent radiation of Australias iconic venomous snakes. We traced the key genetic events that occurred on the evolutionary path to one of the worlds most potent venoms. We found that the novel venom activity evolved through the sequential co-option of multiple proteins of the snakes own blood-clotting system, followed by the modification of two venom neurotoxins into proteins with procoagulant activities. We suggest that these unique de novo gene co-options are seminal events that can unlock new ecological strategies, which in turn, may enable major adaptive radiations.

BackgroundSynonymous mutations, once considered neutral, can affect translation efficiency through mRNA folding and splicing, generating codon usage bias. This bias is often linked to genomic GC content, which also influences gene regulation. In the parasitoid wasp Lysiphlebus fabarum, GC content was previously shown to shift between developmental stages, with larvae showing higher GC than adults. Whether this phenomenon is widespread among insects remains unknown. ResultsTranscriptomic data from six insect species spanning Diptera, Hymenoptera, and Lepidoptera was used to compare GC content between expressed genes in larvae and adults. In five species, larval transcripts exhibited higher GC content than adult transcripts. Differential expression analysis revealed that stage-biased genes displayed consistent GC shifts, and orthologous gene families with representatives across species showed particularly GC-rich larval-biased genes in Hymenoptera and Diptera. At the genome scale, modeling in 317 insect species demonstrated an association between parasitic lifestyle and reduced mean GC content in Hymenoptera and Diptera, providing a possible ecological explanation for AT-rich genomes. ConclusionsOur results show that GC content is dynamic across developmental stages, independent of overall genome composition. Stage-specific GC enrichment may reflect adaptive codon usage optimizing translation during energetically demanding life-history stages such as larval development. Furthermore, the association between parasitism and reduced genomic GC highlights how ecological lifestyle might with genome content and evolution. Lastly, this work identifies candidate genes underlying stage-specific GC bias and provides new insights into the interplay between molecular evolution, development, and parasitic adaptation in insects.

Hearing in Lepidoptera mediates a range of ecologically important behaviours, including mate communication, predator avoidance, and acoustic signalling. In moths, the evolution of predator-prey interactions with bats has further shaped hearing through a sensory arms race, with repeated co-option of auditory organs to detect and evade echolocating predators. Despite significant prior characterization of the neurophysiology and behaviour of hearing in moths, the genetic basis of hearing is poorly understood in most insects. In this study, we identify a core set of putative auditory genes in Lepidoptera using a combination of homology-based searches from Drosophila and evolutionary rate analyses. We find 56 genes present across all species and investigate whether gene copy number varies among non-hearing and hearing lineages and among 3 different ear types. We discovered seven genes associated with ear type and one with ear presence, but did not find significant losses in gene copy number in non-hearing species. We identified three genes (btv, Dnai2, and nompB) with strong evidence of selection in hearing clades and five genes with weaker evidence of selection. We discuss the potential roles of btv, nompB, and Dnai2 in ciliary transport and the aging of hair cells, as well as the possibility of actively amplified hearing. Our study serves as a primer and resource for further gene mining and functional testing of auditory genes in moths and other insects.

Reconstructing the spatio-temporal history of human genetic lineages is fundamental to understanding human evolution and population distribution. While succinct tree sequences and maximum parsimony reconstruction methods applied to large-scale genomic data have improved our ability to trace the geographic history of genetic ancestry, they have essentially relied on Euclidean distances, which ineluctably ignore opportunity costs that have shaped human mobility patterns since the earliest human migrations and settlement formations. Here we propose an approach to incorporate realistic geographical migration costs through a human movement friction surface. Using simulated data mimicking the dispersal process of human migration out of Africa, we found that, compared to the Euclidean-based benchmark (M0), the proposed friction-based model (Mf) leads to a more accurate estimation of the geographical origin (n = 346, accuracy M0 = 0.18, f = 0.27) and genetic flux (n = 30, MSE M0 = 0.20, Mf = 0.12) through the Mandeb corridor in the Horn of Africa. We further illustrate these findings in a case study, in which our model seems to better identify plausible human migration paths from Eurasia to the Americas by accounting for geographic factors affecting migration opportunity costs, such as the Alaska Range and Rocky Mountains that represent physical barriers that constraint migration. While important migration drivers such as climate change, technological advances, social organization, and culture remain omitted here, our work highlights the importance of explicitly accounting for geographic constraints to improve our ability to reconstruct past human mobility and, ultimately, understand the evolution of human populations.

Fossil data is crucial to construct phylogenetic time trees, which serve as the basis to test a wide range of evolutionary hypotheses. While the fossil record is known to be incomplete, modern stratigraphy provides predictions of the structure of the fossil record as expressed by gap location and duration. Advances in phylogenetic model development allow us to propagate this information into Bayesian phylogenetic inference in the form of priors on time-variable fossil sampling. However, the impact and role of stratigraphic architectures on time tree inference has so far remained unexplored. We introduce a novel simulation framework that combines realistic stratigraphic forward models with phylogenetic simulations. Using this framework, we examine (1) how stratigraphically plausible model violations of fossil sampling due to gaps affect total-evidence inference under the fossilized birth-death model and (2) if stratigraphic knowledge on gap duration and timing improves inference when incorporated in priors on fossil sampling. We find that total-evidence analysis is robust to stratigraphically plausible distribution of gaps in disparate stratigraphic architectures, with results being instead dominated by the number of morphological characters. Surprisingly, incorporating information on prominent gaps in the stratigraphic record does not improve phylogenetic inference. Our results suggest that phylogenetic inference is robust to model violations introduced by stratigraphic gaps over short timescales, with results being dominated by a priori known data availability constraints such as morphological character matrix size. This research establishes the foundations for joint modeling of phylogenetic and stratigraphic processes and narrows the knowledge gap between paleontology, stratigraphy, and neontology.

Limb loss in vertebrate animals is surprisingly common despite imposing strong functional constraints. These pressures funnel species towards regions of limited ecological and phenotypic space. To date, snakes have been considered unique in having escaped this pattern. Using a new species-level phylogeny and comparative morphological and dietary datasets, we show that pygopods, a group of limbless Australo-Papuan geckos, have undergone a similar evolutionary trajectory to snakes. Our analyses provide evidence of exceptional morphological and diet evolution. This is exemplified by strong niche partitioning among genera through dietary specialization and greater than expected dietary disparity. Diversification in pygopods has also been driven by extreme phenotypic evolution, with pygopods encompassing much of the morphological space covered by all other limb-reduced lizards. Interestingly, the diversification of pygopods has resulted in only a modest number of species, emphasizing the decoupling of diversity and richness possible in adaptive radiations.

Mitochondrial loci were for long considered as markers of choice to reconstruct phylogenies. The development of high-throughput sequencing over the past two decades fostered the sequencing of mitogenomes, allowing further macroevolutionary questions to be tested. Several biological traits of birds (e.g. body mass, migration distances) have been related to mitochondrial substitution rates. Environmental parameters in ectothermics vertebrates, and potentially in endotherms, have been further suggested to impact substitution rates for specific taxa or loci. Yet, the relative importance of biological traits versus bioclimatic variables is unknown because the former were not systematically controlled for in studies that underlined the effect of the bioclimatic variables. To assess the importance of bioclimatic variables on selection regimes, we analysed the thirteen mitochondrial protein-coding genes for 176 Piciformes (toucans, honeyguides, woodpeckers), a clade with homogeneous life-history traits that can be found in diverse bioclimatic environments. Our analyses highlighted a negative relationship between temperature annual range and the non synonymous to synonymous substitutions ratio. The higher purifying selection in temperate environments may be a result of the strong constraints on maintaining an optimal metabolism in broader climatic variations. Our results further highlight that care should be taken when applying general mitochondrial clocks to estimate divergence times among avian lineages distributed in different climatic conditions.

Land-bridge islands are former mainland areas isolated by post-glacial sea-level rise (<15,000 years) and the most common island type. Because of their recurrent connectivity with continents, it is unclear whether species on land-bridge islands can undergo evolutionary changes associated with the more isolated oceanic islands ( island syndrome). Here, we test the hypothesis that the selective environment on land-bridge islands exerts predictable and consistent evolutionary shifts in morphological traits of songbirds. We apply Bayesian hierarchical models to a morphological dataset of 6,917 individuals comprising 185 species of songbirds from four land-bridge islands (Bioko, Sri Lanka, Taiwan and Trinidad) and adjacent continents. Across all 185 species, we find that occurrence on a land-bridge island has clear directional effects on five morphological traits related to beak, wing, and tarsus, as well as a general increase in body size. At the species level, 57 out of 90 tested species exhibit significant morphological divergence between land-bridge island and mainland, yet for only 20 of these are the land-bridge island populations recognised as distinct endemic subspecies. Our results show that occurrence on land-bridge islands has a detectable effect on passerine morphology consistent with the island syndrome, and suggest these islands harbour previously unrecognized unique biodiversity.

Allele frequency (AF) timeseries allow us to directly observe the dynamics of evolution at a genetic level. However, extracting useful inferences from AF timeseries has proved difficult due to the model uncertainties and noisiness inherent in AF change at fine temporal scales. Here we present three new permutation tests --- which do not assume a model of evolutionary change or a parametric statistical model --- to detect AF timeseries features of evolutionary interest. The features identified by these approaches are: 1) any evolutionary change (as opposed to apparent change due to measurement error); 2) directional selection; 3) fluctuating selection with a propensity to change sign (negative autocorrelation). We are not aware of existing tests for features 1 and 3. Feature 2 is commonly tested using standard evolutionary models such as the Wright-Fisher; we show that the permutation approach has comparable statistical power. We apply our new approaches to AF timeseries data from D. melanogaster and D. pulex.

Eusocial insects have extreme intraspecific lifespan variation, where queens are long-lived (up to 30 years) whereas workers only live for a few months or years at most. Several studies have invoked the disposable soma theory to explain the evolution of caste-specific ageing in eusocial insects, which proposes that senescence results from a resource allocation trade-off between maintenance vs. reproduction. An extension of this theory to eusocial insects is that caste-specific ageing could emerge from a resource allocation trade-off between castes. However, to date this idea has not been formalised in a theoretical model. Here, we present an individual-based model for the evolution of ageing in social insects. In our model, queens and workers die when their nutritional state becomes too low. The evolving trait in our model is the age-specific resource allocation of individual workers, who can allocate resources between themselves, other workers, and the queen. We find that lifespan differences between queens and workers emerge from the evolved resource allocation within colonies, which are within the range of empirically observed lifespans of queens and workers in monogynous eusocial insects. Caste-specific ageing evolves in our model because queens obtain large amounts of resources, which allows them to be long-lived and highly fertile, whereas workers evolve to give resources away to enhance the queens reproduction and thereby their own indirect fitness. We also observe that age polyethism emerges, where young workers nurse the brood and older workers forage. Overall, our model demonstrates that both caste-specific ageing and age-related worker division of labour emerge as a consequence of evolved within-colony resource allocation.

Evolutionary diversity in metabolic rate underlies differences in physiology, morphology, and life history across the tree of life. Cell size has been proposed as an important determinant of metabolic rate. The mechanisms underlying this proposed connection are based on the lower surface area to volume ratios in larger cells. As relative surface area decreases, the cost of maintaining ion gradients across the cell membrane through action of the Na+/K+-ATPase pump are posited to decrease, lowering overall metabolic costs. Despite strong theoretical support for this model, and its incorporation into broader models of life history evolution, empirical measurement of Na+/K+-ATPase activity in species that differ in cell size has been lacking. Here, we study nine species of salamanders of the genus Plethodon that span a large range of cell sizes approaching the animal upper limit. We compare basal cellular respiration rates, relative cost of the Na+/K+-ATPase pump, and maximal mitochondrial respiration rates in liver and heart tissue. Contrary to predictions, we find no support for a relationship between cell size and any of these mitochondrial respiratory variables. We reconcile this surprising result with broader phylogenetic studies showing a lack of correlation between cell size and metabolic rate at the organismal level.

Although it is well established that certain stages of development are molecularly more conserved than others, the reasons for this phenomenon remain largely unknown. We study molecular conservation in the development of an organ, the molar, by comparing the temporal profiles of expression in mice and hamsters. We find that the cause of conservation of expression and of coding sequences changes over molar development. Gene expression levels display a classical increase of divergence as development progresses. In terms of genes expressed, the composition of early and late stages is better conserved and enriched in pleiotropic genes, yet each stage mobilizes different sets of pleiotropic genes, cell division for bud growth and secretion for tooth mineralization. Moreover similar patterns of higher divergence of gene sets and of coding sequences at mid development, are caused by different biological phenomena, in that case heterochronies and blood colonisation respectively. In conclusion, the patterns of molecular conservation in developing molars are shaped by a combination of processes intrinsic to the teeth, and by negative and positive selection on functions which are mostly extrinsic to the teeth. This is likely translatable to explain molecular conservation patterns in many other biological systems. AUTHOR SUMMARYFor species to evolve different adaptations to different life styles, their anatomy has to evolve correspondingly. This in turn implies evolution of the embryonic development of anatomical structures. Notably, tooth shape can evolve rapidly as an adaptation to different diets. Mice and hamsters are closely related rodents who yet differ in the shape of their molars, and thus in their development. In this study, we investigated why the genes active in molar development are more or less similar between the two species from early tooth bud to fully formed embryo molar. We found that early and late molar development were slow evolving, while mid-development was evolving faster. But surprisingly, this was in part due not to tooth evolution, but to the involvement of genes which are active in other processes in the body. For example an influx of immune cells also brings fast evolving immune genes. This helps us understand better the complexity of causes of apparently simple evolutionary patterns.

The evolutionary transition to terrestrial life required overcoming several physiological hurdles; however, such challenges were amplified in desert environments. While several xeric-adapted arachnids utilize permanent burrows or "sit-and-wait" foraging strategies as possible energy conservation adaptations in harsh habitats, camel spiders exhibit a counterintuitive, high-energy lifestyle. To investigate the molecular underpinnings distinguishing Solifugae within Chelicerata, we utilized a comparative genomics framework that incorporates a newly sequenced, previously unpublished solifuge genome. We identified lineage-specific expanded orthogroups and evaluated selective pressures acting upon paralogous sequences within our ingroup solifuge species. Additionally, we also focused on fatty acid-associated proteins and heat shock proteins to elucidate how Solifugae may have evolved such anomalous behaviors compared to their arachnid relatives. Our analyses revealed significant signatures of positive selection within key gene families across the solifuge lineage. Notably, paralogs within the cytochrome P450 and biotinidase families showed consistent evidence of selection across all three taxa, suggesting specialized metabolic or detoxification requirements. Furthermore, we identified candidate loci implicated in axonal guidance and lipid metabolism, and a specialized fatty acid enzyme repertoire. While subsequent research is required to determine whether some of the genomic signatures unveiled here are shared across a broader phylogenetic distribution within Solifugae, we establish a critical baseline for future functional validation.

Eusocial Hymenoptera present the highest known recombination rates among metazoans, which evolved several times independently among bees, ants and wasps. Several hypotheses have been proposed to explain this observation, including stronger selection for recombination caused by coevolving parasites and pathogens, and strong sexual selection among haploid males due to male-biased sex ratios among reproductive individuals. In this article, we explore the effects of haplodiploidy and differential selection between sexes on the evolution of recombination, by analyzing a three-locus model in which selection for recombination stems from negative epistasis between selected loci. Our analytical predictions are compared with the results of individual-based simulations in which deleterious mutations occur along a linear chromosome. Our results show that, at mutation-selection balance for deleterious alleles, increasing the strength of selection against deleterious alleles (due to the effect of male haploidy and/or sexual selection) tends to reduce selection for recombination. However, an increase in the overall magnitude of negative epistasis (which may also be due to male haploidy and/or sexual selection) combined with the fact that recombination only occurs in females may increase selection for recombination substantially. Our model also shows that, in conditions favoring recombination, increasing recombination in meioses leading to parthenogenetic ovules (and male offspring) may yield stronger benefits than in meioses leading to fertilized ovules (and female offspring).

Mutation is the ultimate mechanism that produces genetic novelty, and thus a central ingredient of evolution. Mutation rates are therefore thought to be tuned by natural selection, for example to optimize a delicate balance between the generation of adaptive diversity and the accumulation of deleterious mutations. As this selection occurs over very long time scales, models and simulations have been powerful tools to understand how mutation rate evolves and which factors influence it. Most simulation methods are nevertheless limited by the over-simplicity of the genotype-to-phenotype map they feature, especially regarding the encoding of mutation rate. We modified Aevol, an evolutionary simulator inspired by bacterial genomics with a realistic genome structure and a complex genotype-to-phenotype layer, to allow organisms to evolve genes coding for higher replication fidelity. This setup permits several degrees of realism absent in other models: mutation-rate modifier genes themselves experience a realistic distribution of effects of mutations and diminishing- returns epistasis, similarly to fitness modifiers. Moreover, a lower mutation rate comes with the trade-off of a larger genome to encode the genes improving replication fidelity. We use this setup to test hypotheses regarding the evolution of prokaryotic mutation rate, and its link with genome size and genetic drift. We found that evolution systematically increases replication fidelity, even when this results in lower fitness. We highlight two factors which limit the mutation rate decrease: genetic drift and the supply of gain-of-fidelity mutations.

Thermal performance curves (TPCs) are widely used to investigate the effect of changes in body temperature on an organisms performance. Despite empirical evidence that temperature-dependent performance is ubiquitous across taxa, the field lacks models for how thermal performance evolves under realistic timeseries, genetic architectures, and physiological constraints. We address this gap by integrating a mathematical model with individual-based quantitative population genetic simulations. Our model can predict the evolutionary trajectory and shape of TPCs for any given thermal regime. Our model reproduces core properties of TPC evolution from previous studies such as the emergence of generalists in variable environments, but also explains why organisms may evolve TPCs that do not match their historical body temperature range. We uncover novel dynamics of adaptive tracking, the most notable being multi-generation lags between temperature and TPC parameters that can lead to unexpected correlations between the two. Our model predicts empirically observed patterns of adaptive tracking of critical thermal minimum in the invasive pest Drosophila suzukii, including individual-level variability and multi-generation lags with changing temperature. Our results also highlight the limitations of models that ignore factors that influence TPC evolution and individual variability, such as autocorrelation in temperature timeseries, effective population size, evolution of additive genetic correlation in TPC parameters, genetic architecture, and physiological constraints. Our flexible simulation model can incorporate these factors and help generate empirically testable hypotheses of how species will evolve in response to global climate change.

Transposable elements (TE) jump from one genomic locus to another. Since increase in their copy number is a metabolic burden for the host, TE are considered as genomic parasites. Although host-TE co-existence is regarded as an evolutionary arms race, the hypothesis is not extensively tested especially using evolutionary genomics. We provide a hypothesis testing framework to understand the distribution of TE in genic regions of the host genome, variation in the regulation of TE by host, and effect of these two factors on host-TE co-evolutionary dynamics. We test our hypothesis by understanding the distributions of potentially active TEs in the genome of 78 teleost fishes, representing major families and orders within the clade. Our analysis reveals coevolutionary arms race predicted by the Red Queen dynamics.

The origin of novel phenotypes can influence access to new ecological resources, which may have positive, neutral, or negative effects on subsequent phenotypic diversification. In this study, we tested the macroevolutionary consequences of a pair of putative functional innovations occurring in deep-sea fishes of the order Stomiiformes. Integrating phylogenetic comparative methods, micro-CT scans, and external body measurements, we recover a mosaic of diversification trends associated with these innovations. We found some evidence for elevated evolutionary rates in tooth morphology associated with the predatory dragonfishes, which possess a gap between their vertebral column and skull that exposes the notochord and enables neck-like flexibility. However, a second novelty building upon the first, a functional neck joint enabling extreme cranial kinesis, was linked to faster rates of skull evolution. Our results suggest that innovations that help shift ecological roles and overcome functional constraints related to those roles, like gape-limitation in prey depauperate habitats, may play an important role in promoting phenotypic diversification. This work builds on a growing body of evidence highlighting how the deep sea promotes phenotypic diversity, generating the extreme forms that are celebrated by scientists and the public alike.

Post-reproductive lifespan is an evolutionary puzzle. In most mammals female fertility tracks survival, yet humans and a few toothed whales show survival after reproduction ends. Explaining when and why post-reproductive lifespan evolves is central to understanding the evolution of ageing, social structure, and intergenerational helping across species. Kinship-dynamics theory predicts that when males are philopatric, a females local relatedness--especially to male descendants--increases with age, potentially favoring late-life helping over continued reproduction. We develop an age-sex-structured kin-selection model to test whether a rare menopause-inducing modifier allele can invade an initially non-menopausal population through its direct effects on survival and fecundity and its indirect effects on relatives. We consider two evolutionary pathways: stop early, where reproduction ceases earlier with little change in lifespan, and live long, where lifespan extends beyond reproduction under disposable-soma trade-offs. Parameterized with demographic, dispersal, and helping-effect estimates from eight mammalian taxa, the model predicts empirically plausible ages of reproductive cessation and post-reproductive representation in humans and killer whales, but no invasion across plausible cessation ages in non-menopausal taxa. Global sensitivity analyses identify male dispersal and the effect of post-reproductive help on male survival as determinants of whether menopause evolves, motivating the "mamas boy hypothesis": menopause is most strongly favoured by selection when late-life care increases the survival and lifetime fitness of philopatric sons and grandsons.