Evolution

Macroevolutionary analyses typically treat species as discrete units and account for shared evolutionary history. However, speciation is a continuous process and taxa are often spatially clustered, potentially biasing inferences of diversification. Here, we investigate how species delimitation and spatial non-independence influence speciation dynamics and inferred drivers using cichlid fishes as a model system. Using a phylogeny and trait dataset of 1,712 species, we first generated a reduced dataset of 820 species by removing incipient species based on known breeding compatibilities. We then fit phylogenetic and spatiophylogenetic models using an integrated nested Laplace approximation framework to jointly account for phylogenetic and spatial covariance. We find that the treatment of incipient species and spatial non-independence both alter speciation patterns and inferred drivers. Analyses of the full phylogeny identified strong trait associations and spatial hotspots driven by young adaptive radiations in Lake Victoria and Lake Malawi, whereas removing incipient species and accounting for spatial non-independence reduced extreme speciation rates, weakened or removed trait effects, and largely eliminated spatial hotspots. These results demonstrate that macroevolutionary inference is sensitive to species delimitation and spatial structure, highlighting the need to consider the influence of incipient species and spatial covariance in comparative analyses.

Article summaryGene interactions are common, yet additive genetic models often predict short-term evolution and breeding response. This study argues that additivity can arise because populations sample only a small neighbourhood of a curved fitness landscape. In additive channels, genetic variation is small enough that local curvature contributes little to heritable fitness differences. The study defines an additivity index ([A]g) that compares variance from the local slope of log-fitness with variance from curvature, and links this ratio to expected prediction accuracy under Gaussian assumptions. A selection-inheritance framework shows when additive channels persist and when populations leave them. It yields testable predictions.

Self-fertilisation is common in hermaphrodites, but selfing rates vary among species and populations and among individuals within populations. Most evolutionary theory seeking to explain this variation assumes genetically determined selfing rates. Here we study the evolution and consequences of condition-dependent selfing, where individuals adjust selfing in response to their deleterious mutation load. We analyse a two-locus population-genetic model in which one locus determines condition and the other is a modifier locus that determines condition-dependent selfing rates, and we extend the analysis to a polygenic background in which condition is determined by many loci. Our results show that selection favours positive condition dependence: high-condition individuals self-fertilise whereas low-condition individuals outcross. The resulting reaction norm generates stable within-population variation in realised selfing rates at evolutionary equilibrium and reduces the mutation load. We further show that it persists under environmental heterogeneity, and that pollen discounting favours a gradual increase in selfing with condition, leading to a continuum of selfing phenotypes. Altogether, our results indicate that condition-dependent selfing can generate substantial within-population variation in selfing rates. It may therefore contribute to mating-system diversity, and in particular to the maintenance of mixed mating.

Parasite defense is the ability of a host to minimize fitness loss to parasites, and it is among the most variable phenotypes in natural populations. We expect this variation in defense to facilitate rapid adaptation under parasite-mediated selection. What we do not know is what traits are most likely to evolve in response to this selection. A common assumption is that the most defended hosts are the most resistant, meaning they limit the establishment and growth of infecting parasites. Under this assumption, resistance traits should evolve readily under parasite selection. Resistance is, however, just one of many strategies hosts use to defend against parasites, and it does not consistently covary with parasite defense. We accordingly ask: which host traits covary with parasite defense and are thus likely to respond to parasite selection? We use controlled exposures to characterize genetic variation in defense of the nematode Caenorhabditis elegans against its natural microsporidian parasites. We report extensive variation in parasite defense among wild strains of C. elegans: some strains lost 60% of fecundity under parasite exposure, while others were unaffected. We then tested the covariance of defense with two prominent host traits, resistance and reproductive timing. Our results did not support the hypothesis that resistance covaries with defense: strains with lower parasite burden did not have higher relative fecundity under exposure. Our results instead supported the hypothesis that life history covaries with defense: host strains that reproduced quickly had higher relative fecundity under exposure, consistent with the idea that parasites diminish future reproductive opportunities. Moreover, we detected substantial heritability of fecundity traits but low heritability of resistance traits. Together, these findings indicate significant potential for adaptation of wild C. elegans populations to defend against their natural parasites. They further predict that life history traits will evolve rapidly in response to parasite selection. AUTHOR SUMMARYSome hosts fare much better than others in the face of parasite infection. What traits differentiate defended hosts from undefended hosts? The answer to this question is critical for identifying the strategies that best protect hosts from their parasites. It also allows us to predict and interpret the evolution of host populations over the course of epidemics. To address this question, we surveyed wild strains of a tractable model host, the nematode Caenorhabditis elegans, for their response to two species of microsporidian parasites. We found that, on average, parasite exposure substantially impaired the ability of hosts to reproduce. Host strains, however, varied widely: some experienced major losses in fecundity with exposure, while others were highly defended, showing little to no change. We identified reproductive timing as the trait that differentiated defended hosts from undefended hosts. Our results indicate that reproducing quickly was protective, because hosts were able to make most of their offspring before parasites impaired reproduction. We did not find evidence that resistance was protective - hosts with lower parasite burdens did not reproduce better than those with high parasite burdens. These findings give added weight to life history as a major component of host defense against parasites.

Reproductive Character Displacement (RCD) often occurs when species with mating-related polymorphism come into secondary contact, leading to divergence in reproductive traits. Ischnura elegans and Ischnura graellsii have formed two independent hybrid zones in Spain where reinforcement has strengthened a mechanical barrier, and RCD has shaped mating-related structures, although reinforcement is asymmetric only in gynochrome females. This study examines the link between asymmetric reinforcement and asymmetric RCD. Using geometric morphometrics, we analyze prothorax shape and size in both female morphs and males, and male caudal appendages, to assess morphological divergence, determine whether gynochrome females show stronger divergence, and test for morphological covariation between male traits involved in the tandem position. Our results reveal consistent patterns of size and shape variation across species and zones: in I. elegans, androchromes are larger and resemble males in size, with clear shape differentiation between female morphs that diminishes in hybrid zones. In contrast, I. graellsii shows less consistent size differences between males and morphs, and weaker shape differentiation. Our results confirm RCD in prothorax shape in I. elegans females from both hybrid zones, but reveal that RCD in prothorax size is asymmetric, occurring only in gynochrome females from the NC hybrid zone. We also detected RCD in the prothorax shape of I. elegans males from the NC hybrid zone, extending previous evidence of RCD in male caudal appendages, while morphological covariation between male cerci and the prothorax was limited to size in I. elegans. Together, these findings illustrate how hybridization may generate morph-specific patterns of reproductive divergence.

The body size of adults and immature stages are fundamental animal traits that influence animal physiology, ecology, and range distribution. While the importance of egg size has been acknowledged as a proxy of parental investment in animals, little work has addressed the tempo and mode of evolution of egg size and shape. Here, we present a comparative study of this trait using a phylogeny based on genome-wide markers together with measurements of egg size and adult body size from 29 drosophilid species. Our analyses revisit the allometric relationship between egg size and body size and show that egg size scales negatively with respect to adult size, even after accounting for shared evolutionary history. In other words, larger species tend to produce proportionally smaller eggs. We also detect a moderate phylogenetic signal in both egg size and egg shape, indicating that closely related species resemble each other in these traits. Model comparisons show that the evolution of egg morphology in drosophilids is best described by gradual divergence through time driven by stochastic evolutionary change. This pattern contrasts with findings from other animal groups, including birds, cephalopods, and reptiles, where alternative evolutionary models better explain trait evolution. Together, these results suggest that the evolutionary dynamics shaping egg morphology in drosophilids differ from those operating in other major lineages and underscore the importance of comparative analyses of early developmental traits across taxa.

In many systems, mutations can have background-dependent fitness effects due to genetic interactions between loci within a genome (intragenomic epistasis). In some cases, such as when species are coevolving, genetic interactions between loci can span across species; this is described as intergenomic epistasis. It is known that intragenomic epistasis can make adaptation more repeatable by constraining accessible mutational paths. Here, we investigate whether intergenomic epistasis leads to the same pattern of increased repeatability and how repeatability is influenced by the interplay of intra- and intergenomic epistasis. For this, we model a two-species system in which the fitness of a species depends on the combination of genotypes that are present in both species. We implement this system using an NKC model, which allows us to construct coevolutionary fitness landscapes on which we simulate adaptation by means of mutations in both species. To quantify the repeatability of adaptation, we track the realised endpoints of adaptive walks and record the distribution of fitnesses of the focal and partner species at these evolutionary endpoints. We find that intergenomic epistasis creates highly repeatable patterns of adaptation that depend on the underlying shape of the coevolutionary landscapes. The patterns of repeatability deviate from expectations based on intragenomic epistasis due to fitness trade-offs between species, which can lead to cycling and large co-evolutionary fitness loads.

How evolutionary and developmental processes interact to determine axes of neural variation that produce behavioural diversity has been debated for many decades, with alternative hypotheses giving differential emphasis to functional coupling, which favours co-evolution, and developmental constraint, which enforces it. A critical omission is data on the genetic architecture of brain size and structure, which more closely illuminates the shared developmental dependencies between components of an integrated system. Here, we exploit ecological divergence between Astatotilapia calliptera and Aulonocara stuartgranti, two closely related cichlid species from Lake Malawi, to explore the genetic architecture of brain evolution. Using computer vision and machine learning techniques to extract volumetric data from micro-tomographic images, we first demonstrate significant divergence in brain composition between these species. Genomic and micro-tomographic imaging data from a population of hybrids generated between the two species were used to investigate genetic factors shaping this differentiation. We show that the majority of brain components are integrated phenotypically in hybrids, but genetic correlations between them are generally weaker. We further show that variation in multiple brain components is associated with variation in largely structure-specific quantitative trait loci, rather than determined by genetic factors with broad effects across the entire brain. These results suggest a genetic architecture that can facilitate modular changes in brain structure, and imply that individual components are independently evolvable.

The fitness landscape metaphor remains resonant in evolutionary theory and has facilitated the birth of newer concepts--like the fitness seascape--that consider the role of environmental context in shaping the dynamics of evolution. Since the emergence of the fitness seascape, it has appeared in several studies that examine how different and fluctuating environments shape evolutionary outcomes. Despite a growing interest in these topics, we lack comprehensive examinations of the role of environmental context in shaping features of fitness seascapes. In this study, we address this gap by deconstructing empirical fitness seascapes across scales of granularity: mutational steps, loci, locus interactions, alleles, trajectories, and entire seascapes. For each, we examine how environmental context influences qualitative and quantitative aspects of seascapes, and find that they change appreciably, with patterns that are specific to individual systems of study. In summary, we reflect on the implications of the seascape metaphor with respect to the incorporation of environmental effects into theoretical population genetics, for understanding how the environment shapes evolution in disease systems, and for contemporary bioengineering excursions.

A populations ability to adapt is determined by its levels of additive genetic variance (VA), and while it is agreed that most organisms have genetic variation for most traits, the extent to which it varies between species is poorly characterised. Here we investigate this question by compiling 3209 and 1852 estimates of heritability and evolvability (the additive genetic variance divided by the square of the mean) estimates respectively, for a variety of traits, from 220 and 172 multicellular eukaryotic species. Using phylogenetic generalised linear mixed models, we find substantial and highly significant interspecific variation in evolvability. Much of the variation is explained by phylogenetic relatedness, with plants in our data having substantially higher evolvability than animals. While heritability also varies between species, the differences are more subtle, and plants are not exceptional. We investigate whether the variation in evolvability and heritability between species is due to variation in the mutation rate, effective population size, genome size, ploidy and recombination rate, but find little evidence of any factor being important. However, the confidence intervals are large suggesting that we have little power to detect any associations between these factors and our estimates of VA.

Wing loading is a metric of flight performance that captures the relationship between body mass and wing area and reflects how much weight each unit of wing surface supports during flight. Comparative studies have documented substantial differences in wing loading among individuals and across species. However, no study has evaluated the extent of this variation when species are reared under identical, controlled conditions. Here, we address that gap by measuring wing loading in 30 species of drosophilids raised in a common lab environment. We applied comparative phylogenetic methods to assess the extent to which the evolution of body mass, wing area, and wing loading is structured by shared ancestry. We find that wing area and body mass exhibit moderate phylogenetic signal, but wing loading does not. In addition, all three traits are best explained by a model of evolution in which most trait divergence occurs during speciation events. More conservative analyses provide no support for adaptive peaks in wing loading within drosophilids. Together, our results indicate that the evolutionary dynamics of wing loading in Drosophila differ from those described in birds and bats, and raise the question of whether similar patterns characterize other insect lineages.

Recent reviews of isolating barriers in plants conclude that prezygotic barriers play an outsized role in plant speciation; yet these conclusions derive overwhelmingly from studies of sympatric, perennial herbs in temperate zones, and at later stages of speciation. Trees possess several traits that are expected to influence barrier evolution, including prolonged generation times and reproduction, predominant outcrossing, and long-distance gene flow. We examined early-evolving post-pollination barriers between ecologically diverged, vegetatively distinct varieties of the tree species, Metrosideros polymorpha, that have a common floral morphology and highly overlapping flowering times. We performed controlled crosses between each of Hawaii Islands four varieties and maternal trees of the high-elevation variety and examined pollen-tube growth, fruit set, seed germination, and seedling phenotype. We then monitored survivorship, maturation rate, and fertility of F1 hybrids over [≥]8 years alongside parental controls and a fourth F1 genotype derived from companion studies. The four F1 crosses showed four contrasting patterns and strengths of predominantly postzygotic isolation, including high F1 mortality that manifested over several years. Results from this and other tree studies suggest that ecological speciation in trees follows the classical speciation model of early postzygotic barrier formation followed by reinforcement, whenever stable environments promote recurring hybridization.

The shared genome prevents each sex from independently responding to the selection experienced by that sex. We used experimental evolution in Drosophila melanogaster with separate pools of Chromosome 3s for males (male-limited chromosomes) and females (female-limited chromosomes) for 15 generations. Viewing each sex as a separate environment, we performed a reciprocal transplant between the sexes to quantify the strength of local adaptation to each sex environment. Each chromosome type was more beneficial in the sex it had been selected for (i.e., local adaptation to sex). Because it has been postulated that sex differences in selection may depend on how well adapted a population is to the abiotic environment, we performed experimental evolution at two thermal regimes: one benign temperature to which the populations were well-adapted and one novel temperature. Female-specific adaptation was stronger at the benign temperature whereas male-specific adaptation was stronger in the novel temperature. Within chromosome pools, male and female fitness were more positively correlated in the novel compared to the benign temperature. Though males carrying male-limited chromosomes were typically more fit than males carrying female-limited chromosomes, they were also more harmful to their female mating partners.

Adaptive radiation theory posits that speciation in such lineages is largely driven by ecological opportunity in concurrent morphological expansion in response to niche availability. Here, we use a phylogenomic estimate of Australasian diplodactyloid geckos in combination with meristic and ecological data to infer patterns of ecological diversification, quantify signatures of stabilizing selection, and the factors driving speciation processes. Specifically, we focus on two relatively young but speciose and ecomorphologically diverse assemblages from the ancient islands of New Caledonia and New Zealand. Models accounting for stabilizing selection recover shifts in morphospace along many branches that also experienced shifts in ecological guild as inferred from ancestral state reconstructions. We find convergent evolution to be present between the two insular lineages as they independently transitioned to similar guilds from different ancestral ecologies. Community assembly is integral to understanding the dynamics of adaptive radiations and various studies focused on identifying if biotic or abiotic factors drive character suits and sympatry in diverse lineages. Bayesian and multiple regression analyses suggest that abiotic factors rather than interspecific competition dictates phenotypic divergence in both insular lineages. Rather, species seem to diverge phenotypically in allopatry and environmental factors, such as climate, in combination with competitive exclusion drive phenotypic overlap in sympatry. This study provides the first modern assessment of convergence for diplodactyloid geckos and provides robust evidence indicating that similar selective pressures have shaped morphological diversity in these disparate as well the factors affecting sympatry.

Population genetic models excel at identifying the conditions for polymorphisms based on balancing selection but typically disregard the ecological processes that yield particular values of selection coefficients. We model a system that combines antagonistic pleiotropy, dominance reversal and heterozygote advantage: the wood tiger moth Arctia plantaginis, where alternative haplotypes at a major-effect locus determine male hindwing coloration. Yellow offers better protection against predators, while white is often associated with better mating success. The effects of mortality and reproductive success overlap in time because protandrous males can mate as long as they are alive, but they need to avoid predation for several days before the bulk of females emerge. We show that protandry aids polymorphism maintenance whenever the second-fittest genotype (after the heterozygote) is the poorly surviving but mating advantaged homozygote, while increased protandry harms polymorphism when the second-best fitness is that of the survival advantaged morph. Ecologically plausible protandry times predict that dominance reversal does not have to be strong for polymorphism to be maintained. Our study highlights the importance of timing traits in maintaining polymorphisms in Lepidoptera and showcases the benefits of deriving fitness explicitly in place of abstract selection coefficients that lack temporal components within the life cycle.

Multiple frameworks have been developed to investigate the evolution of species interactions on fitness landscapes, each with unique strengths and weaknesses. These include adaptive dynamics, which uses linear stability analyses to predict eco-evolutionary outcomes resulting from the invasion of rare mutants into a resident population, and population genetics, which mechanistically models finite populations and stochastic processes in finite time. Though there are some known correspondences between these frameworks, it is not clear that they will always result in the same eco-evolutionary outcomes. Moreover, while adaptive dynamics is very powerful for predicting outcomes, it is not always straightforward to relate these predictions to the data generated in experimental evolution studies. Here, we use a data-driven model of microbial species interactions to compare and contrast the predictions of population genetics and adaptive dynamics. We derive expected outcomes for one-species and two-species evolutionary trajectories by using the invasion fitness landscape concept from adaptive dynamics, and then use analytical theory and forward-in-time simulations to set these predictions within the context of population genetic models. In the context of our one-species models, we show that the timescale of evolution depends on mutation supply and effect sizes, when populations are initialized both along and off a trade-off function. For two-species competition models, we show that mutation supply, effect sizes, and asymmetries between competing species result in discrepancies between adaptive dynamics and population genetics, especially in cases where adaptive dynamics predicts stable coexistence. Our study provides insight into the role of finite timescales, mutation supplies and population sizes in the evolution of species interactions, and facilitates further research that leverages the invasion fitness landscape concept within the realm of population genetics.

Phenotypic plasticity allows plants to rapidly respond to changing environments without the need for evolutionary change or migration. While selection can create variation in plasticity across natural populations, these responses are not adaptive in all environments. To predict whether plasticity will be adaptive requires evaluation of its fitness effects across a range of environments, including novel ones. Here, we test how traits and their plasticity vary for genotypes collected across a natural hybrid zone between two tree species with contrasting climatic niches. Fast-growing Populus trichocarpa inhabits maritime environments with relatively warm and stable temperatures, while P. balsamifera inhabits continental environments with cold winters and large temperature variance throughout the year. We planted 44 clonally replicated genotypes into thirteen common gardens and measured vegetative phenology, leaf morphology, stomata morphology and conductance, and photochemistry. Overall, genotypes from colder, more continental environments exhibited higher plasticity. P. balsamifera ancestry was associated with increased plasticity in timing of fall phenology, stomatal conductance, and leaf mass per unit area. We assessed the effects of trait plasticity on fitness estimated as yearly growth across common gardens and found that the plasticity-fitness relationship was often garden-specific, indicating that the planting environment did not consistently mediate plasticity-fitness relationships. When the effects of trait plasticity on growth varied by garden temperature, higher plasticity generally had neutral or negative associations with growth in warmer environments. These results suggest that elevated plasticity evolved in a P. balsamifera genomic background as part of a climate generalist strategy to seasonal temperature variability, but that there is a trade-off between plasticity and growth in warmer environments. Consequently, less-plastic but warm-adapted P. trichocarpa genotypes are likely to have a fitness advantage under warming climates. These results demonstrate that plasticity may sometimes be maladaptive and will not be universally beneficial in a warming world.

Sarita Lake, British Columbia houses a distinctive population of threespine stickleback (Gastrosteus aculeatus L.) with a phenotype characterized by unusually large individuals relative to nearby conspecifics. We tested the hypothesis that members of this population are not isometrically larger but rather exhibit variation in allometric trajectories that reflect changes in developmental timing impacting the developmental-genetic architecture of the phenotype. We used 3D geometric morphometrics to characterize the size and shape of skulls, pectoral girdles and pelvic girdles from a sample of individuals from nearby freshwater and marine populations and compare them to a sample from Sarita Lake. We showed that individuals from the Sarita Lake population are larger in each body region compared to most other populations examined. Further, these individuals have dorsally expanded skulls and relatively robust pelvic armour. We also showed that the relationship between size and shape is differently structured among body regions and is heavily influenced by non-uniform sexually-mediated variation across populations sampled. Our results reflect complex underlying developmental trajectories, and we suggest that the large phenotype observed may be driven by fecundity selection on female size in combination with a limnetic trophic niche and relatively increased predation pressure in Sarita Lake.

Additive fitness landscapes--also called Mount Fuji landscapes--are the simplest and most widely used models of sequence-function relationships. As such, they play essential roles across multiple areas of biology, including evolutionary theory, quantitative genetics, gene regulation, and protein science. One of the most basic properties of any fitness landscape is its genotypic density--the number of sequences near a given fitness value. Understanding this density is especially important near fitness peaks, as it quantifies the supply of high-fitness genotypes. Here I study the genotypic density of additive landscapes near fitness peaks. Although this density is well known to be approximately Gaussian near the middle of the fitness range, its behavior near maximal fitness has not been reported. I begin by deriving a saddle-point approximation that accurately describes the genotypic density of additive landscapes over virtually the entire fitness range. I then show that the log density follows a power law near maximal fitness, with an exponent determined by how much the best allele at each position outperforms its nearest competitor. This power-law behavior holds over a substantial fraction of fitness values, besting the Gaussian approximation on both simulated and empirical landscapes across roughly a quarter to a third of the fitness range. Under certain conditions this behavior also extends to globally epistatic landscapes (defined as nonlinear functions over one or more additive traits), though with a reduced range of validity. These findings advance our understanding of one of the most fundamental models of sequence-function relationships. In particular, they reveal that the uppermost reaches of Mount Fuji landscapes, rather than being sharply peaked, are actually quite stubby.

Acoustic signaling is key to individual and species recognition, playing a major role in sexual and social communication. Since reproductive isolation is often maintained through pre-mating mechanisms, song can be an early isolating trait leading to assortative mating, promoting reproductive divergence, and potentially contributing to speciation. However, whether song differences alone are sufficient to prevent interbreeding or if other traits also contribute, remains a matter of debate. Playback experiments provide a more direct way to test the role of song as a reproductive barrier. Here, we use playback experiments to test the hypothesis that song acts as a pre-mating barrier in two recently diverged populations of an island passerine, the Canary Islands Chaffinch (Fringilla canariensis palmae), which inhabit ecologically distinct laurel and pine forests within the island of La Palma. Assuming that male song has diverged in the two habitats, we tested if territorial males from a given habitat responded differently to songs from intruding males from their own habitat or from the other habitat type, using a closely related mainland species as a control. We found that probability of response was weaker to songs of the closely related species and to the different-habitat birds than to songs of the same-habitat birds, but differences for the latter were weak. The intensity of response followed the same pattern. Overall, song divergence between laurel and pine forest chaffinches does not appear strong enough to cause clear behavioural discrimination against individuals from the alternative habitat. Other factors such as morphological and ecological divergence associated with adaptation to local resources might better explain population differentiation. However, testing female responses will be essential to determine whether songs convey lineage-specific information that may elicit assortative mating.