Animal lifespans span orders of magnitude, yet how genome sequence covaries with lifespan remains poorly characterized outside vertebrates. Although promoter CpG density has been linked to vertebrate longevity due to its gene-regulatory function through DNA methylation, it is unclear whether such patterns are promoter- and CpG-specific, or if they reflect broader sequence evolution. We curated maximum lifespan estimates for 466 protostome species spanning eight phyla with available genome assemblies and quantified mono-, di-, tri-, and tetranucleotide composition across whole genomes, intergenic regions, and six gene-associated regions (two upstream regions, exons, introns, and two downstream regions) defined using Benchmarking Universal Single-Copy Orthologs. Dinucleotide observed/expected ratios showed significant associations with lifespan and genome size in different ways. Lifespan-associated motifs were most pronounced in gene-associated non-coding regions, especially in introns and downstream regions, whereas genome-size effects were strongest in whole-genome and intergenic sequence. Tri- and tetranucleotide observed/expected ratios broadly recapitulated this regional organization. In contrast, GC content was not associated with lifespan across regions, indicating that the observed signals are not explained by mononucleotide composition but instead by how those nucleotides are arranged into short sequence motifs. These results suggest that lifespan and genome size show distinct but overlapping associations with regional sequence composition across invertebrate species and that lifespan-associated motif evolution extends beyond vertebrate promoter methylation architectures.
DNA methylation is a major component of eukaryotic genomes with an important role in the defence against transposable elements, to transcriptionally silence their activity and prevent transposition. DNA methylation also plays a major role in the regulation of gene expression. This dual role can come into conflict, where DNA methylation in gene regulatory regions becomes perturbed due to transposable element transposition, leading to disruption of gene expression. Here, we describe how this conflict is reflected in DNA methylation patterns in the sand lizard genome where there is recent transposable element activity. Using long-read sequencing technology we show that CpG islands in gene transcriptional start sites are typically hypomethylated and associated with higher gene expression. Outside transcriptional start sites, a majority of CpG islands overlapped transposable elements and were associated with hypermethylation, consistent with a host-defence role in suppressing transposition activity. We identify 605 instances where transcriptional start sites were associated with transposable elements (4.3% of all genes). These instances were far rarer in conjunction with a CpG island, when methylation signatures would be in conflict. Transposable elements were found to be closer to and at higher density the more hypermethylated a transcriptional start site was, suggesting strong selection against selfish genetic elements transposing into hypomethylated transcriptional start sites.
Senescence is age-related decline that may carry over to subsequent generations. Advanced parental age can both improve or reduce offspring fitness, however. Identification of mechanisms of parental effects senescence thus proved challenging so far. We investigated the effects of old parental age on offspring performance in a laboratory short-lived fish, Nothobranchius furzeri (Cyprinodontiformes). We followed age-related changes in parents and then focused on the effect of parental age on key offspring life-history traits (embryonic survival, hatching rate and juvenile growth). We employed telomere length as a senescence marker and a potential route for transmitting senescence effects from parents to the offspring. As parents aged, their body condition, reproductive output, and telomere length declined. Offspring of older parents showed lower survival and hatching rate. In contrast, old parental age did not compromise juvenile growth and telomere length of the successfully hatched offspring. This, among other things, resulted in decoupling of parent-offspring telomere length. Our study highlights the sensitivity of the early life-stages to old parental age in contrast to offspring post-hatching performance.
Evolutionary transitions between contrasting trait values likely occur in response to selection in new or changing environments, and these trait changes may be particularly large when a lineage shifts to occupy a completely new habitat or biome. Biome shifts can have major effects on the evolution of the species involved, including anagenetic changes in morphology, physiology, or life history and accelerated cladogenesis and diversification. Biome shifts can also be viewed as movements beyond a range margin. These shifts involve overcoming the physiological barriers that previously limited establishment, but potentially also subsequent evolution in other traits under the new environmental and biotic conditions. We examined how shifts between contrasting lowland and mountain biomes corresponded with evolution of a series of vegetative and reproductive traits, particularly focusing on transitions between combined and separate sexes (hermaphroditism and dioecy or gynodioecy) and between pigmented and white flowers in New Zealand's largest native angiosperm clade, Veronica sect. Hebe. We found an association between the evolution of a dimorphic sexual system and occupying the mountain biome, but sexual system transitions and biome shifts did not coincide. White and pigmented flowers were associated with mountain and lowland biomes, respectively, with coupled biome shifts and colour transitions. These associations between biomes, sexual system and flower colour states are likely driven by differences in types and activity of pollinators between biomes. Our findings illustrate how important changes in reproductive traits can accompany biome shifts, with some changes being more closely coupled to biome shifts than others.
Life-history traits are central to the long-term persistence of phenotypes. In reptiles, the transition to viviparity-viewed as a key innovation-and habitat use-an essential component of the ecological context-have been identified as two major drivers of phenotypic evolution. Yet their relative contributions and operating scales remain unclear. We used Bayesian phylogenetic mixed models (univariate and multivariate) and phylogenetic comparative analyses to compare the effects of parity mode and habitat use on the evolution of life-history traits in Sceloporus. We assembled data for nine traits (e.g. female snout-vent length, clutch/litter size, offspring size), parity mode, and habitat use across 88 species. We found a contrast between present-day trait associations and transition dynamics: parity mode was associated with variation in transition rates among habitat-use states, whereas habitat use better explained the multivariate phenotypic architecture. Reproductive allocation in Sceloporus was structured not only by the classic offspring size-number trade-off, but also by how reproductive effort is distributed through time. At the multivariate level, habitat use best captures the size-fecundity architecture, but when additional reproductive traits are included, parity mode dominates covariation. We outline potential mechanisms and propose a general framework to understand and generate testable hypotheses about phenotypic evolution in Sceloporus and other reptile lineages.
Abstract Trophically transmitted parasites frequently alter the phenotype of their intermediate host to increase predation by the next host in the life cycle. Still, the degree to which such manipulation is specific to the correct predator varies widely across systems. Some parasites employ mechanisms that selectively increase vulnerability to the next host, whereas others increase predation indiscriminately, exposing the parasite to dead-end predators. Despite growing empirical documentation of this variation, no theoretical model has addressed the evolution of manipulation specificity itself. Here, I develop a general analytical model in which a trophically transmitted parasite evolves two traits simultaneously: manipulation intensity and manipulation leakage—the degree to which parasite-induced changes in host vulnerability extend to nonhost predators. The parasite faces three competing outcomes in its intermediate host: predation by the suitable next host (transmission), predation by nonhost predators (dead end), and natural nonpredation mortality. I derive the condition for manipulation to be favoured, obtain the joint evolutionarily stable strategy for intensity and leakage, and provide an analytical approximation for the equilibrium. The model reveals that although dead-end predation creates the selective incentive for specificity, specificity evolves only when the fecundity costs of achieving it are sufficiently low. This condition is determined by the manipulation pathway, not by the intensity of nonhost predation.
Microchimerism-the long-term persistence of genetically distinct cells exchanged between mother and fetus-is a widespread feature of mammalian reproduction whose evolutionary significance remains debated. Recent empirical work shows that newly arriving fetal microchimeric cells actively displace resident microchimeric populations, challenging the view that maternal tissues progressively accumulate cellular memories of past pregnancies. Here, we develop models to investigate how such displacement may have evolved and what it reveals about the function of microchimeric cells. We show that the maternal microchiome contains two opposing factions: cells originating from the current offspring, which favor increased maternal investment in the ongoing pregnancy, and resident cells from previous offspring or matrilineal relatives, which favor preserving resources for future reproduction. Crucially, cells from the current offspring switch allegiances after the period of maternal care, becoming part of the inhibitory resident population in subsequent pregnancies. This recurrent reset generates selection for incoming fetal cells to displace resident microchimeric cells, because displacement increases the relative influence of the resource-enhancing faction more effectively than simple addition. Conversely, resident microchimeric cells are selected to proliferate without displacement, generating a predicted tug-of-war over microchiome composition. Our results show that pregnancy-induced displacement emerges naturally under the conflict-based Trojan Horse Hypothesis, in which fetal cells manipulate maternal physiology to enhance resource transfer to the current offspring. By contrast, displacement is difficult to reconcile with the Tolerance Hypothesis, which predicts selection for maintaining a diverse and persistent microchiome. Overall, our model suggests that the loss of maternal cellular memory is not paradoxical but instead an expected outcome of evolutionary conflict among microchimeric cell lineages.
Most multicellular animals practice anisogamy (fertilization between eggs and sperm). When mothers produce sons and daughters at a 1:1 ratio, the "twofold cost of males" arises because males do not directly contribute to population growth. If thelytokous parthenogens producing only daughters invade a population, they should spread rapidly. Although thelytoky has repeatedly evolved across invertebrate and vertebrate taxa, it remains a minority. Why? The evolutionary transition from anisogamy to thelytoky requires eggs to initiate embryonic development without fertilization. However, in metazoan animals, meiotic metaphase (MM) arrest halts oogenesis midway and normally resumes only after stimulation by sperm penetration. Empirical and experimental evidence indicates that release of MM arrest without fertilization is extremely difficult, providing a strong mechanistic barrier against parthenogenesis. Even if MM arrest were released, oogenesis would proceed to produce either a haploid embryo or a diploid embryo through refusion with the second polar body (terminal fusion automixis). Outbred species typically accumulate more than one lethal equivalent of recessive deleterious alleles per genome as heterozygotes. Upon transition to haploid or automictic development, these recessive lethals normally masked in outbred diploids would be exposed simultaneously, causing embryonic death and creating the next barrier. Thus, thelytoky cannot be achieved simply by modification of the existing meiotic system; instead, other mechanisms, such as apomixis, that bypass meiosis are required. Mathematical models and simulations support this "meiotic constraint" hypothesis. Combined with recently proposed immediate benefits of anisogamy and traditional genetic benefits (e.g., Red Queen), it may largely explain the maintenance of costly anisogamy.
Phenotypic plasticity can influence population persistence, range dynamics, and evolutionary potential in heterogeneous landscapes. If adaptive, plasticity may buffer populations against environmental variability, climate change, and extreme events. Yet, few studies have examined how plasticity and its evolution vary across species' ranges. This is especially important for edge populations, which are often most vulnerable to novel conditions. The Climate Variability Hypothesis postulates that greater environmental variability selects for genotypes that exhibit greater phenotypic plasticity. However, field tests of this hypothesis across species' ranges remain rare. Using scarlet monkeyflower (Mimulus cardinalis), we combined a resurrection approach with common gardens to test whether (1) central and edge populations differ in plasticity in drought-associated traits, (2) there were evolutionary shifts in plasticity following an extreme drought, and (3) plasticity was adaptive. We measured plasticity in first flower date, specific leaf area, and leaf dry matter content across two leading-edge, two range-center, and two trailing-edge populations, comparing pre-drought ancestors and post-drought descendants grown in three gardens spanning the latitudinal range following a historic drought event. We found significant plasticity in all traits, and plasticity in the date of first flower was greatest in trailing-edge populations that have experienced greater interannual variation in precipitation. Evolutionary changes in plasticity occurred in some populations but did not consistently increase first-year fitness. The adaptive value of plasticity was trait-specific. These results show that plasticity is shaped by both spatial and temporal environmental variation and highlight the need to examine trait- and population-level responses to understand selection on plasticity at range edges.
Some selfish genetic elements enhance their transmission to the next generation by interfering with and eliminating competing variants within the same host, typically at a cost to host fitness. These higher-level fitness costs can constrain the spread of such transmission-distorting elements. We examine three specific transmission distorters (maternal-effect killers, cytoplasmic incompatibility, and spermatogenic drivers) and show how aspects of their organismal ecology-specifically, mating systems, reproductive compensation, and population structure-can weaken or altogether eliminate these constraints, shifting selection down from the level of the individual to the level of the selfish element. Despite the mechanistic differences between our three cases, a common principle emerges: when ecological conditions allow a transmission distorter's harm to be borne under soft rather than hard selection, higher-level constraints are weakened and more extreme forms of selfishness can evolve. We show how this softening of selection can arise theoretically and offer predictions about the taxonomic distribution of certain forms of selfish elements in light of it. Thus, to understand internal conflicts requires a consideration of not only the inner mechanisms by which selfish elements gain a transmission advantage but also the outer ecological context.
In species with external fertilisation, synchronizing sperm release by males with egg release by females is generally considered crucial, yet little is known about sperm release strategies when females lay eggs over extended periods. In the intertidal goby Bathygobius fuscus, smaller males intrude into the nest during pair spawning, which lasts several hours, and release sperm. Here, we investigated how the timing of sneaker intrusion affects the paternity of sneaker males, using controlled aquarium experiments combined with genetic paternity analysis. Our results showed that early nest intrusion after the onset of egg-laying (within approximately 1 hour) significantly increased sneaker male paternity. This may be partly because early released sperm remain viable for several hours and can fertilise eggs laid later. In addition to the increased fertilization rate, another possible reason why sneaker males attempt early intrusion is that females lay more eggs during the early stages of egg-laying (approximately 70% of their total eggs during the first hour of spawning), giving the males the opportunity to fertilize a greater number of eggs. These findings suggest that early sneaking increases fertilization opportunities for sneaker males, which is thought to be favorable given the traits of long egg-laying period and long sperm longevity in this species. This study proposes the importance of considering the timing and sequence of sperm release in understanding the consequences of sperm competition in externally fertilising species with a time gap between sperm release and fertilization, similar to that of species with internal fertilisation.
From the Jurassic to the Cretaceous, most medium- to large-bodied non-avian theropods evolved toward predominantly head-driven predatory strategies. Megaraptorid dinosaurs represent a striking exception, retaining well-developed forelimbs and hypertrophied manual unguals hypothesized as a key adaptation within the clade. However, the macroevolutionary processes underlying the mode and tempo of megaraptorid claw evolution remain poorly understood. Here, we investigate the macroevolutionary trends of the megaraptorid manual claw by quantifying the shape and size of 22 manual phalanx I-2 (= manual ungual I) across different lineages of medium- to large-bodied non-avian theropods, using 2D geometric morphometric and phylogenetic comparative methods. Our results indicate that manual claw shape and size were evolutionarily coupled in Megaraptoridae, supporting a major reconfiguration of allometric trajectories during the evolution of the clade. This evolutionary coupling triggered directional shape modifications toward a distinct adaptive optimum associated with enlarged manual claws. This adaptation emerged following an early phase of rapid morphological divergence near the middle Early Cretaceous boundary and was subsequently maintained, likely under stabilizing selection throughout the Late Cretaceous, resulting in a canalized claw morphology. We further show that medium- to large-bodied non-avian theropods with well-developed forelimbs exhibit strong phylogenetic integration between distal and proximal forelimb elements. Despite this integration, the phalanx-I-2 and ulna-radius complex evolved at substantially higher evolutionary rates than the humerus. These results highlight Megaraptoridae as the only large-bodied carnivorous theropod lineage retaining a specialized forelimb-based predatory strategy until the end of the Cretaceous, with no evidence of overall claw shape convergence.
Similar phenotypic traits can evolve independently in response to comparable environmental challenges. A striking example of this process is the repeated and irreversible loss of flight in birds, particularly on islands. The rail family (Rallidae) provides an exceptional model for studying this phenomenon, as nearly a quarter of the 130 extant species have independently become flightless. Here, we present the first genome-wide comparative analysis of multiple independent flightless rail lineages to identify the molecular basis of flight loss. We compared coding regions from seven rail species (four flightless and three volant) using more than 11,000 alignments and multiple phylogeny-based tests, including branch-site models of selection, relative evolutionary rate analyses, and assessments of function-altering amino acid substitutions. Across all analyses, 116 genes showed significant associations with flightlessness, of which 37 were linked to biological functions related to flight capacity-such as muscle, bone, limb, and heart development-or to traits reflecting ecological consequences of flight loss, including immune response, renal function, lipid metabolism, cognition, and sensory perception. Many genes under selection in flightless species were also involved in gene regulation and post-translational modification. These findings suggest that convergent loss of flight in rails arises not from major mutations in a few key loci but from numerous small, repeated genetic changes affecting both developmental pathways and regulatory mechanisms.
The theory of inclusive fitness explains the process and purpose of social adaptation. However, the canonical derivation of inclusive fitness assumes a simple causal relationship between genotype and phenotype. In reality, different components of the genotype may have different impact upon the phenotype and different genetic relatedness to social partners, as for example in the case of parent-of-origin effects that have been implicated in the evolution of genomic imprinting and a diversity of pathological phenotypes. Whilst such scenarios may be framed in terms of a clash of inclusive-fitness interests of different genes or different genetic factions, it remains unclear whether and how an individual's inclusive fitness may be defined in the context of such internal conflicts. Here, I investigate how the derivation of inclusive fitness is affected in the context of an individual suffering from internal conflict between her maternal-origin versus paternal-origin genes. I show that, in relation to a single conflicted trait, the individual's inclusive fitness is given as a weighted average of the interests of the underlying genetic factions, with the power wielded by each faction providing the appropriate weight. This reveals that internal conflict per se does not erode the adaptive integrity of the individual. Rather, it is variation in the underlying balance of power across different traits that leads to a breakdown of the individual's unity of purpose.
Convergence, defined as lineages evolving to be more similar to one another than their ancestors due to selective pressures is a hallmark of adaptive evolution. Yet, the extent of convergent evolution across different taxa and in different ecological contexts remains unclear. Snakes, with over 4,100 species worldwide, provide a unique model to explore how habitat use influences morphology in a group with an at first sight uniform body plan. We quantified body, head, and tail shape in over 400 species (∼10% of the global snake diversity) to assess the role of habitat use in shaping morphological variation. Our results reveal significant differences across habitats. Terrestrial species display the highest morphological diversity in contrast to other habitats which appear morphologically more specialized. For example, whereas arboreal and semi-arboreal species exhibit elongated heads and slender necks, aquatic and semi-aquatic snakes share streamlined bodies and narrow heads. Fossorial and semi-fossorial species, on the other hand, have compact bodies. Surprisingly, morphological similarity remains limited to arboreal, semi-arboreal, and terrestrial habitat use. Thus, despite strong functional constraints, evolutionary similarity in fossorial and aquatic species is weak, indicating multiple adaptive solutions rather than a single morphological trajectory, possibly due to the relatively homogenous body plan of snakes. Morphological disparity patterns show that non-specialist ecologies generally exhibit greater disparity than highly specialized ones, in accordance with the need of these species to move in different habitats. Our findings underscore the role of ecological constraints in shaping snake morphology and highlight the complexity of adaptation beyond strict convergent evolution.
Chromosomal inversions have been consistently associated with environmental gradients, suggesting a role for local adaptation. However, the underlying selective mechanisms of inversions remain unresolved in cod. Critically, few experiments have yet tested the fitness consequences of inversions in cod under controlled environmental conditions. Such work is essential to infer causality. Here, we applied acute temperature and low salinity stressors, separately and combined, on Atlantic cod (Gadus morhua) eggs. Inversions on chromosomes 2, 7, and 12 in cod are linked to temperature and salinity in the wild. Cod eggs (N = 1265) were placed into each treatment for 24 hours and the number of eggs that floated initially and finally was counted as a proxy for eggs alive. Genotypes for the inversions on chromosomes 2, 7, and 12 were determined for eggs from the 3°C-25ppt, 7°C-25ppt, 16°C-25ppt, and 16°C-35ppt treatments. We found that sinking increased with temperature and that more eggs sank in 25 ppt than in 35 ppt after 24 hours. We found the inversions on chromosomes 2 and 12 interact with each other and might assist with temperature and salinity adaptation, respectively, in cod eggs, while the inversion on chromosome 7 did not affect floating. These results contrast with previous research that correlated environmental variables with inversions in cod. Our results provide a unique demonstration of experimentally testing genotype-by-environment associations observed in the wild to understand the functions of chromosomal inversions.
Phenotypic trade-offs, predicted to occur due to resource limitation, are not commonly detected. For this, the Y-model provides a powerful heuristic by showing that greater variation in resource acquisition than variation in allocation, masks trade-offs. However, the Y-model contains several other parameters beyond variation in acquisition and allocation, whose independent and interactive influences remain unclear. We simulate the means of, variation in, and correlation between, acquisition and allocation, to systematically explore how these parameters influence the phenotypic association between two traits. We find that the mean resources acquired by a population has no direct mathematical influence on phenotypic correlations. Instead: the mean of the resource allocation of a population; the correlation between allocation and acquisition; and the ratio of variation in acquisition to variation in acquisition plus allocation, directly impact phenotypic correlations. Importantly, a three-way interaction between these parameters provides a better prediction of the phenotypic correlation than their independent effects. We validate our simulations using an empirical dataset and analytical solutions to demonstrate their robustness. Using several biological examples such as resource limitation, we show how Y-model parameters might manifest their influence on phenotypic correlations in empirical data. Despite the simplicity of our simulations and assumptions (e.g., sampling from normal distributions), our study provides a quantitative extension of the Y-model paradigm to understand the detectability of phenotypic trade-offs.
Most organisms carry mobile DNA that enhance their own transmission to subsequent generations, generating conflict with the host genome. The selfish transmission invoked by these selfish genetic elements (SGEs) has promoted a variety of countermeasures by the host genome to reduce their impact. Maternally inherited endosymbionts are common in arthropods and frequently manipulate host reproduction, and transposable elements (TEs) are an exceptionally abundant and diverse group of SGEs. Their activity and abundance vary drastically between even closely related species and can generate evolutionary consequences of both lethal and beneficial effects. Yet, despite their plentitude, many questions remain regarding the potential interactions between different SGEs. This is in part a methodological problem as TEs, for example, often reside in highly repetitive genomic regions, making them difficult to detect. Innovations in genomics have driven renewed interest, particularly with long-read sequencing resolving repetitive regions. We can now begin to define and answer important outstanding questions. For instance, it is unclear how different types of SGEs, including TEs, may interact within host genomes. For example, while different SGEs may compete for host resources (such as availability of molecular machinery), they may also cooperate or even behave parasitically toward each other, as in the case of some TEs. Here we take an "ecology of the genome" approach to examine such interactions that, together with choice examples, may help further our understanding of how interactions between different SGE shape genome evolution.
A recent review of honest signalling theory criticised constraint-based (index) explanations for traits that serve as honest signals of individual quality, contending that such explanations offer only proximate mechanisms and fail to explain evolutionary stability or the origin of reliability. A key point in this critique is the contention that ultimate explanations require the possibility of cheating. The authors advocate for the Signaling Trade-off Theory-where trade-offs make cheating evolutionarily unfavourable-as essentially a complete explanation for the evolution of signal honesty. Here, we argue that this critique rests on a false dichotomy between proximate and ultimate explanation. When signal production is mechanistically embedded within vital cellular processes, this shared pathway inherently restricts the evolution of cheating. Using avian ketocarotenoid colouration as a model, we show that condition-dependent signal production is not explained by trade-offs because pigment transformation is coupled to mitochondrial energy metabolism and core cellular performance, making high-signal expression unattainable for low-condition individuals. Deception may therefore be physiologically inaccessible rather than merely costly. Moreover, the enzymatic machinery underlying ketocarotenoid production likely evolved for visual function before being co-opted for social assessment, such that condition-dependent colour expression preceded assessment of colouration in social interactions. Uncheatable honest signals can thus arise as an exaptation of biochemical processes needed to sustain complex life rather than as outcomes of unfavourable trade-offs.
A fruitful avenue to understand differences in lifespan is to study the factors driving differences in intrinsic mortality, such as disease. The domestic dog is an emerging model in longevity research and presents an unrivalled opportunity to analyse the effects of life history and evolutionary history on variation in vulnerability to diseases causing mortality. We analysed cause-specific mortality-categorized by the organ system affected and by pathophysiological process-across 72 dog breeds using Bayesian multinomial models. We first analysed the influence of evolutionary history (common ancestry and hybridization events) on among-breed variation in specific causes of death. We then tested the association between life-history traits and specific causes of death, controlling for non-independence due to common ancestry and hybridization. We found differences in the proportion of variance explained by common ancestry and hybridization across causes of death; mortality due to musculoskeletal and neoplastic processes exhibited the strongest genetic influence, while gastrointestinal and metabolic causes showed the weakest. Increased body size was associated with higher mortality from musculoskeletal, haematopoietic, and gastrointestinal causes, and with lower mortality from endocrine and urogenital causes. Higher reproductive investment was associated with lower mortality from congenital, degenerative, and inflammatory causes. Finally, we found a negative association between trainability and mortality due to infectious causes. These findings suggest that specific causes of death in dogs are shaped by both evolutionary history and trade-offs associated with life-history traits, underscoring the importance of incorporating genetic relatedness and evolutionary theory into the study of disease vulnerability in domesticated animals.
