We report the consequences of >330 generations of experimental evolution under larval undernutrition for male postcopulatory success and traits thought to mediate it in Drosophila melanogaster, comparing them to phenotypically plastic responses. Males from populations evolved on standard diet showed a >30% plastic reduction in the size of accessory glands (AG) when raised on a nutrient-poor larval diet. Experimental evolution on the poor diet led to a further reduction that was more pronounced in smaller individuals, changing the allometric slope between AG and wing size. Rather than the expected reduction in seminal fluid protein expression, we observed a plastic increase on poor diet in investment in Acp36DE and Acp62F at the expense of Acp26Aa and SP, and an evolutionary shift in the time course towards lower virgin and higher post-mating SFP expression. Surprisingly, neither the plastic nor evolved reduction in AG was associated with impaired performance in reproductive output from matings with excess females, the ability to induce female oviposition or performance in sperm competition ("sperm defense"), except when poor diet-adapted males were raised on standard diet. Thus, larval nutrient shortage favors reduced investment in AG development, but this is compensated for by other mechanisms, minimizing consequences for postcopulatory success.
Species coexistence is critical to the assembly of biodiverse communities. When closely related species come into secondary contact, competitive and reproductive interactions can both influence the potential for coexistence. We tested whether ecological and/or evolutionary factors affect coexistence dynamics in a pair of closely related honeyeaters that have come into secondary contact in the Solomon Islands. Myzomela cardinalis colonized the island of Makira and established a population in sympatry with the endemic M. tristrami. These taxa are ecologically similar and hybridize. If ecological factors are promoting coexistence, we expect species to partition where they forage for resources or defend breeding territories. In addition, evolutionary pressures may facilitate coexistence if species mate assortatively, avoiding production of potentially low-fitness hybrid offspring. Using data on foraging locations, nest locations, and mate pairing, we find support for partitioning of space use, specifically in the context of nest placement. Phenotypic pairs of the recently arrived species nested significantly closer to the coastline than did endemic species pairs. We also find strong evidence of assortative mating based on phenotype. Thus, both ecological and evolutionary factors appear to contribute to the coexistence of these closely related hybridizing species.
Testis morphology may act as a determinant of sperm size, and the evolutionary pressure to produce longer sperm may impose functional constraints on testicular architecture. Postcopulatory sexual selection, particularly sperm competition, is widely recognised as a primary driver of the remarkable interspecific variation in sperm size and number across animals. Theoretical hypotheses predict that longer sperm require wider seminiferous tubules and that intense sperm competition favours an increased proportion of sperm-producing (seminiferous) tissue relative to non-spermatogenic components, independent of overall testis size. Using a phylogenetic comparative approach across 78 anuran species, we tested these two predictions. Our analyses revealed that the cross-sectional area of the seminiferous tubules was significantly and positively correlated with sperm length, thereby supporting the proposed morphogenetic constraint. Furthermore, relative testis size, which was used as a validated proxy for sperm competition intensity, was positively associated with the proportion of seminiferous tissue. In contrast, absolute testis size did not predict this tissue proportion. Our findings suggest that sperm competition shapes anuran testicular architecture through two distinct evolutionary pathways: indirect selection for wider tubules mediated by longer sperm, and direct selection for increased investment in seminiferous tissue. This tissue optimisation extends beyond simple testicular enlargement and reveals sophisticated evolutionary adaptations to postcopulatory sexual selection.
In temperate climates, dormancy enables organisms to survive winter, with timing often tied to environmental cues, such as daylength, that differ along latitudinal gradients. Adaptation to these gradients is crucial during range expansion. Clark et al. (2026) found that in the introduced northern tamarisk beetle (Diorhabda carinulata), populations from the range core were locally adapted in dormancy timing to core environments, while newly arrived edge populations showed heterogeneous responses to daylength, consistent with adaptation to seasonal timing. Genetic variation and high heritability in dormancy traits in the core populations likely drive range expansion potential through rapid evolution of dormancy traits.
Insects produce a vast diversity of sex pheromone compounds despite strong stabilizing selection on species-specific signals. In multiple insect lineages, these pheromones chemically resemble the volatiles produced by plants. Here, I propose that adaptation of insect sensory systems to plant chemistry biases the origin and diversification of insect pheromones. Repeated independent recruitment of plant-like compounds, either through sequestration or de novo biosynthesis, suggests that pheromone evolution can be shaped by ecological interactions. Receptors with dual roles in host detection and pheromone detection may be functionally constrained, further influencing signal diversification and receptor specialization. This framework links sensory biases with macroevolutionary patterns, generating testable predictions about how sensory biases shape insect pheromone evolution.
Environmental shifts often dictate Arthropod morphological evolution, yet certain lineages maintain remarkably conserved body plans across diverse habitats. Whip spiders (Amblypygi) emerged over 300 Ma and exhibit striking morphological conservatism; nonetheless, what drives this apparent conservatism remains an open question. Here, we analyzed how body size and shape evolved in response to climate and habitat by examining the contributions of bioclimatic variables and habitat type to morphology, alternative macroevolutionary models, estimating the strength of the phylogenetic signal, and testing whether evolutionary rates differ. Habitat was the strongest predictor of body size, with cave-dwelling species approximately 22% larger than surface species, while climatic gradients accounted for almost none of the shape variation. The evolution of both body size and shape was best described by a single-peak Ornstein-Uhlenbeck model, suggesting stabilizing selection toward a shared adaptive peak. Body size exhibited a moderate phylogenetic signal consistent with a Brownian motion process, whereas body shape lacked a clear phylogenetic signal, indicating stronger stabilizing selection on shape. Together, our findings suggest that the morphological conservatism of whip spiders is maintained by a "jack-of-all-trades" strategy, in which stabilizing selection favors a versatile phenotype that facilitates the occupation of diverse ecological niches without marked morphological divergence.
Environmental heterogeneity can favor phenotypic plasticity, but whether evolutionary responses in one environment predict trait expression after environmental change remains unclear for threshold traits. Polyphenisms-plasticity characterized by discrete alternative morphs-rely on developmental thresholds, and as a consequence, are often expected to permit partial evolutionary decoupling among alternative phenotypes. Using replicated experimental evolution and artificial selection of a resource polyphenism in the nematode Pristionchus exspectatus, which develops either a predatory morph or a microbivorous morph, I tested whether evolutionary changes in morph frequency are coupled across environments. Across independent lineages, I asked whether evolutionary increase in predatory morph frequency under selection predicted phenotypic change when populations were reared back in the ancestral environment. I found a strong positive cross-environment coupling: for both sexes, lineages showing larger evolutionary responses during the first 25 generations, and across the full 50-generation experiment, also showed larger increases in predatory morph expression after environmental reversal. Artificial selection on mouth-form produced the same pattern. These results show that even a discrete threshold trait can retain strong and repeatable correlated responses across environments, consistent with morph-frequency evolution being channeled by developmental architecture shared across environments.
Modularity is a pattern whereby traits evolve as interrelated systems, resulting in lower covariation between modules than within. Modularity may facilitate diversification by permitting the phenotype to independently respond to selection. The Appalachian Mountains are a biodiversity hotspot for lungless salamanders (Plethodontidae). Despite their ecological diversity, putative catalysts of their radiation in the Appalachians are poorly understood. We test whether (i) Appalachian salamanders exhibit modularity in functional, morphological characters and (ii) if the rate of evolution-a fundamental macroevolutionary signal of ecological opportunity-varies among modules and if their rates are correlated. We find that Appalachian salamanders exhibit modularity under two different models in which their head, trunk, limbs, and tail or the head, body, and limbs act as separate modules. The three major clades, Plethodon, Eurycea, and Desmognathus, vary in the presence and extent of modularity. Across Appalachian salamanders, modules exhibit non-significant differences in rates of evolution (~1.5-fold), with the trunk and tail modules exhibiting the slowest and fastest rates, respectively. We also find that the rate of modular evolution can be highly correlated, suggesting that modules may respond similarly to ecological opportunity. These results suggest that modularity underlies the morphological diversity of Appalachian salamanders by permitting localized regions of the phenotype to respond independently to selection, but not evolve at different rates.
Anglerfishes (Lophiiformes) have evolved diverse morphological solutions for life in the deep sea (>200 m). Previous studies have shown that the bathypelagic lineage (Ceratioidei) exhibits high evolutionary rates; however, the intrinsic mechanisms underlying this accelerated evolution remained unclear. Here, we examine patterns of modularity and integration, rates of morphological evolution, and evolutionary rate matrices across the skulls of 100 anglerfish species spanning shallow and deep-sea habitats using geometric morphometrics and phylogenetic comparative methods. We find that both deep-benthic and bathypelagic anglerfishes exhibit stronger patterns of integration compared to their shallow-water relatives. The iconic bathypelagic anglerfishes (Ceratioidei) differ from other Lophiiformes by exhibiting an integrated upper-lower jaw system, likely driven by selection for feeding efficiency in resource-scarce environments. Jaw evolution in Ceratioidei, Chaunacoidei, and Ogcocephaloidei exhibits novel evolutionary trajectories that differ from the dominant pattern across Lophiiformes. Our findings suggest that extreme environments promoted morphological innovation in anglerfishes through evolution in novel phenotypic directions and strengthening of evolutionary integration.
While theory has long explained how selection can favor dispersal, we know much less about the capacity for dispersal to evolve in natural populations. One challenge is to identify how heritable genetic variation in multiple dispersal traits aligns with directions of selection on these traits. Therefore, we used an experimental pedigree in the solitary ascidian Molgula occidentalis and constructed Bayesian quantitative genetic models to estimate evolvability of dispersal traits. We compared the evolvability of dispersal traits by: 1) assessing the average evolvability of the G-matrix, 2) considering specific directions of selection hypothesized from biomechanical and life history reasoning, and 3) estimating the predicted response to selection from the observed additive genetic covariance between dispersal traits and fitness components. There was greater additive genetic variation in tail length than in trunk length, as there was for maternal effect and dominance variance. As a result, selection for longer tails (faster swimming) was associated with a higher evolvability compared to selection for shorter tails and longer trunks (energetic efficiency) or shorter tails and trunks (fecundity). The predicted response to selection at hatching and settlement, based on observed additive genetic covariances, was similar for trunk and tail length. Overall, evolutionary change in dispersal distances would occur more rapidly under selection on swimming ability than on energetic economy and fecundity. Furthermore, multiple lineages within Molgulidae have repeatedly diverged along the larval morphology axis in which we measured the highest evolvability. Our results demonstrate the utility of combining estimates of evolvability with hypothesized and observed selection gradients.
Differences in ploidy levels represent a significant barrier to interspecific gene flow, but growing evidence from natural and experimental systems suggests that this barrier may not be as strong as commonly believed. In this study, we aimed to examine patterns of interploidy hybridization between two ecologically similar and partially sympatric wetland perennials in the central Apennines: diploid Cardamine apennina and allotetraploid C. amporitana. Our detailed chromosomal, flow cytometric, and genomic (RADseq) analyses revealed a strikingly high frequency of allotriploids across multiple sites, with no evidence of backcrossing, later-generation hybrids, or higher-level allopolyploids. Contrary to expectations, clonal propagation is not the primary mechanism underlying the observed abundance of triploids. Instead, a high hybridization rate with recurrent, bidirectional, and polytopic hybrid formation, together with the presumed longevity of triploid individuals, appears to explain their persistence. Our findings also raise two key issues: the possible triggers of this apparently recent burst of hybridization, and the potential long-term consequences of frequent allotriploid formation for the survival of the parental (sub)endemic species in the Apennines. From a broader perspective, this study underscores the evolutionary significance and dynamics of species contact zones.
Vertebrates have varied body size distributions. Among these, non-avian dinosaurs have uniquely large minimum and maximum sizes, but the reasons remain unknown. Energetic fitness models provide a potential explanation, by describing how physiological scaling relationships should structure body size distributions under selection to maximize the conversion of energy into offspring. We show that the body size distributions of birds, mammals, and turtles fit the expectations of energetic fitness models, but snakes, lizards, and crocodylians do not. Moreover, no reasonable combination of physiological scaling relationships explains the up-shifted minimum body size of non-avian dinosaurs or flightless birds. We propose that energetic fitness models perform well when body size distributions are governed primarily by intrinsic energetic factors. However, extrinsic constraints imposed by ecological factors such as competition, predation, or ecological niche may also be needed to explain why species body size distributions differ from the model expectations in some groups. The abrupt macroevolutionary shift from non-avian dinosaurs with minimum adult body sizes of 400 g, to birds with modal body size of 30 g cannot be explained by changes in intrinsic physiological factors, and may instead have been caused by an abrupt release of ecological constraints, potentially related to the origin of flight.
Transgenerational immune priming increases the resistance or tolerance of offspring from pathogen-exposed parents. This phenomenon can have substantial ecological and evolutionary consequences, highlighting the importance of understanding its generality both across host taxa and within a host species. Transgenerational immune priming has been reported in multiple invertebrate species, but the robustness and generality of priming in offspring is not clear. For instance, prior studies using Daphnia spp., which are freshwater invertebrates and dominant grazers, found contrasting results for transgenerational immune priming. Some studies found transgenerational immune priming for certain genotypes and in specific contexts while others found no evidence of transgenerational immune priming. Our study addresses multiple questions about transgenerational immune priming using three clones of Daphnia dentifera and three pathogen species varying in their fitness impacts on hosts. We collected offspring from mothers either unexposed or exposed to pathogens and then exposed offspring to either the same pathogen as the maternal exposure (a homologous challenge) or a different pathogen (a heterologous challenge). We measured offspring susceptibility for all treatments and pathogen burden for the two 'obligate killer' pathogens. We did not find any evidence of transgenerational immune priming related to offspring susceptibility. Following a heterologous challenge, one clone showed a reduction in spore burden of one pathogen, which could be an indication of increased tolerance, but no significant reduction in susceptibility. Our results, paired with mixed support from previous studies, suggest that transgenerational immune priming is not a consistent or strong factor influencing disease dynamics in the D. dentifera system.
Mesozoic ecosystems differed from the present in the abundance of large-bodied herbivores that grew through several feeding envelopes, raising the question as to whether large-bodied adults were specialized for different resources than juveniles. Most investigations for ontogenetic resource partitioning in hadrosaurids show an ontogenetic trend towards tough plant material, but have been limited to 2D analyses of cranial shape, tooth wear, and occlusal shape. Here, we use 3D biomechanical modeling of an ontogenetic series of the hadrosaurid Corythosaurus casuarius to evaluate adaptations for resource partitioning. Results demonstrate adults had higher bite forces than juveniles and could process a wider range of materials, but jaw muscle size was negatively allometric, an uncommon trend that increased juvenile bite force and diet breadth relative to expectations for their size. Average stress and strain do not change ontogenetically, but there are changes in stress distribution. Crestless juvenile individuals exhibit a plesiomorphic stress distribution, whereas mature crested individuals experience low stress in the snout and higher stress in the braincase. This ontogenetic transition coincides with the expansion of the premaxillae and nasals to form the supracranial crest and is likely an evolutionary consequence of changes in cranial shape directing pressure away from this delicate structure.
Abstract Association with temporally dynamic habitats has been proposed as a strong predictor of effective population size (Ne) and speciation rates, and thus also potentially of molecular evolution rates, but empirical insights remain limited. We use a genomic dataset of over 2,000 single-copy orthologs to evaluate how habitat association shapes molecular evolution in closely related flightless beetle lineages (Coleoptera: Tenebrionidae: Eutagenia), co-distributed across Eastern Mediterranean islands. The focal taxa occupy either dynamic coastal sand dunes or stable compact-soil habitats but share uniform life-history traits and morphology. Species delimitation analyses identified a single widespread coastal dune species, whereas the stable-habitat clade has diversified into nine allopatric species across the same geographic space and timeframe. Despite its wide distribution, the dynamic-habitat lineage exhibits the lowest long-term Ne and accordingly the highest mean nonsynonymous-to-synonymous substitution rate ratio (dN/dS), yet its total substitution rate is not significantly higher. We propose that recurrent local population extinction in dynamic habitats hinders the completion of speciation and reduces the efficacy of purifying selection, thus elevating the dN/dS ratio. More broadly, these findings indicate that diversification and molecular evolution rates may become decoupled under recurrent population turnover, a hypothesis that requires further empirical and theoretical investigation.
Biologists have long sought to understand the forces driving speciation. Contrasts in dispersal ability (e.g., migration) are hypothesized to influence rates of lineage diversification. However, past inferences of migration-diversification relationships have been contradictory, suggesting the need for further investigation and more nuanced explanations. Here, we test for a relationship between diadromy (marine-freshwater migration) and diversification in salmonids, a dominant group of fishes native across the temperate Northern Hemisphere. We reconstruct a molecular phylogeny comprising 140 species and apply State-dependent Speciation Extinction models to quantify diversification. Diversification rates are higher in non-diadromous relative to diadromous salmonid lineages, echoing the findings of a recent study of homologous southern temperate freshwater fishes, but conflicting with global studies incorporating tropical lineages. Climate appears to be a key factor explaining diadromy-diversification relationships, with the negative relationship observed in temperate lineages likely reflecting increased isolation and speciation of non-diadromous lineages following recolonization of glacially perturbed habitats. In contrast, the positive diadromy-diversification relationships observed in studies spanning tropical fishes may reflect the role of diadromy in facilitating colonization of stable, low-competition habitats.
Parasitism has independently evolved hundreds of times among metazoans. Nonetheless, parasites have explored only a limited range of ecologies, and they display frequent convergence in morphological, behavioral, and life-history traits. Although gene loss in particular parasitic species has been documented, it is not known if gene loss converges along the same lines as these other traits. To test for convergent gene loss, we characterized the housekeeping, regulatory, and DNA-repair complements of 48 bilaterian species, including 20 parasites belonging to 6 different bilaterian phyla. We found that different parasitic strategies do not display characteristic tempos or modes of gene loss. Further, the accelerated rates of gene loss seen in some parasites were almost always shared with their free-living relatives, indicating that the increased rate of loss preceded the rise of parasitism. Therefore, the convergent ecological strategies and adaptations that have arisen in distantly related parasitic lineages overlay contingent gene losses, which largely reflect their phylogenetic history. These results have important implications for how ecologists and evolutionary biologists should model the acquisition of parasitism, especially regarding the long-held assumption that reversion from a parasitic to a free-living state is impossible.
Fisher's "Fundamental Theorem of Natural Selection" purports to relate the rate of change of the mean fitness of a diploid sexual population to the additive genetic variance in fitness. On one interpretation, the "theorem" concerns the total change in fitness and is false under general conditions. According to another interpretation, Fisher's claim relates to only one component of the change in fitness, which corresponds to the change attributable to selection or to changes in allele frequencies. However, this correspondence is the subject of debate. I argue, based on illustrative scenarios, that the quantity in question has neither of these meanings, nor any other meaning related to the effect of selection on fitness. First, I show that this quantity can differ dramatically from the effect of selection on fitness and from the effect of changing allele frequencies. Second, I demonstrate that this quantity is sensitive to the presence of selectively neutral genetic differences, which do not alter the effects of selection on fitness. Thus, interpreting it as a measure of such effects leads to incoherent conclusions. Such interpretations must therefore be rejected, along with the claim that the Fundamental Theorem represents an important biological truth.
