Evolution Letters最新文献

Multicellular organisms that form by aggregation of cells arguably do not achieve high levels of complexity. Conflict among the cells is a widely accepted explanation for this, but an alternative hypothesis is that mixing cells of different genotypes leads to failures of coordination, which we call the "coordination hypothesis." We empirically tested the coordination hypothesis in the social amoeba Dictyostelium discoideum. We mixed D. discoideum clones that had evolved in isolation for generations and acquired mutations that have not been tested against each other by selection. To quantify the effect of incompatibilities, we measured performance in terms of the developmental traits of slug migration and spore production. Importantly, we mixed lines evolved from the same ancestor under conditions that would not select for the evolution of de novo kin recognition. Our results show no evidence of incompatibilities in four traits related to the coordinated movement of slugs toward light in the social amoeba. Spore production was higher than expected in mixtures, in apparent contradiction to the coordination hypothesis. However, we found support for coordination incompatibilities in an interaction between migration and spore production: in mixtures, fewer cells succeeded at both migrating and becoming spores.

Shared developmental, physiological, and molecular mechanisms can generate strong genetic covariances across suites of traits, constraining genetic variability, and evolvability to certain axes in multivariate trait space ("variational modules" or "syndromes"). Such trait suites will not only respond jointly to selection; they will also covary across populations that diverged from one another by genetic drift. We report evidence for such a genetically correlated trait suite that links traits related to energy metabolism along a "power-endurance" axis in Drosophila melanogaster. The "power" pole of the axis is characterized by high potential for energy generation and expenditure-high expression of glycolysis and TCA cycle genes, high abundance of mitochondria, and high spontaneous locomotor activity. The opposite "endurance" pole is characterized by high triglyceride (fat) reserves, locomotor endurance, and starvation resistance (and low values of traits associated with the "power" pole). This trait suite also aligns with the first principal component of metabolome; the "power" direction is characterized by low levels of trehalose (blood sugar) and high levels of some amino acids and their derivatives, including creatine, a compound known to facilitate energy production in muscles. Our evidence comes from six replicate "Selected" populations adapted to a nutrient-poor larval diet regime during 250 generations of experimental evolution and six "Control" populations evolved in parallel on a standard diet regime. We found that, within each of these experimental evolutionary regimes, the above traits strongly covaried along this "power-endurance" axis across replicate populations which diversified by drift, indicating a shared genetic architecture. The two evolutionary regimes also drove divergence along this axis, with Selected populations on average displaced towards the "power" direction compared to Controls. Aspects of this "power-endurance" axis resemble the "pace of life" syndrome and the "thrifty phenotype"; it may have evolved as part of a coordinated organismal response to nutritional conditions.

Natural selection is believed to shape amino acid usage of the proteome by minimizing the energy cost of protein biosynthesis. Although this hypothesis explains well the amino acid frequency (AA_frequency) difference among the 20 common amino acids within a given genome (species), whether it is applicable to cross-species difference remains to be inspected. Here, we proposed and tested a "metabolic rate hypothesis," which suggests that metabolic rate impacts genome-wide AA_frequency, considering that the energy allocated to protein biosynthesis is under selection pressure due to metabolic rate constraint. We performed integrated phylogenetic comparative analyses on proteomic sequence and metabolic rate data of 166 species covering 130 eumetazoan orders. We showed that resting metabolic rate (RMR) was significantly linked to AA_frequency variation across animal lineages, with a contribution comparable to or greater than genomic traits such as GC content and codon usage bias. Consistent with the metabolic rate hypothesis, low-energy-cost amino acids are observed to be more likely at higher frequency in animal species with high (residual) metabolic rate. Correlated evolution of RMR and AA_frequency was further inferred being driven by adaptation. The relationship between RMR and AA_frequency varied greatly among amino acids, most likely reflecting a trade-off among various interacting factors. Overall, there exists no "one-size-fits-all" predictor for AA_frequency, and integrated investigation of multilevel traits is indispensable for a fuller understanding of AA_frequency variation and evolution in animal.

The origin and maintenance of sex differences in reproductive behavior (often labeled sex roles) have remained controversial topics, and recent meta-analyses and theoretical models have helped to elucidate the processes that generate diverse sex roles. We are glad to see that our study (Mokos et al., 2021) generated a healthy debate, and in agreement with recent commentaries (Janicke, 2024; Lehtonen & Parker, 2024) we call for a more comprehensive approach to understanding sex role evolution.

Sexual conflict can drive the divergence of male and female phenotypes and cross-species comparative analyses have documented patterns of correlated evolution of sex-specific traits that promote the evolutionary interests of the sexes. However, male-female coevolution can be highly dynamic, particularly if the male and female traits share an underlying genetic program. Here, we use water striders, a well-studied model system for sexually antagonistic coevolution, and ask whether sex-specific phenotypic adaptations covary across populations and whether they share a common developmental genetic basis. Using comparative analyses both at the population and species levels, we document an association between a derived male mate-grasping trait and a putative female antigrasping counteradaptation in the toothed water strider Gerris odontogaster. Interestingly, in several populations where males have partly lost their derived grasping trait, females have also reduced their antigrasping adaptation. We used RNAi to show that these male and female traits are both linked to a common developmental genetic program involving Hox- and sex-determination genes, despite the fact that they are different structures on different abdominal segments. Our work illustrates the dynamic nature of sexually antagonistic coevolution and suggests that the pleiotropic nature of developmental genetic programs can blur the distinction between inter- and intralocus genetic conflict.

The evolution and maintenance of symbiotic systems remains a fascinating puzzle. While the coevolutionary dynamics of bipartite (host-symbiont) systems are well-studied, the dynamics of more complex systems have only recently garnered attention with increasing technological advances. We model a tripartite system inspired by the marine symbiotic relationship between the alga Bryopsis sp., its intracellular defensive bacterial symbiont "Candidatus Endobryopsis kahalalidifaciens," which produces a toxin that protects the alga against fish herbivores, and the sea-slug Elysia rufescens (Zan et al., 2019), which is not deterred by the toxin. We disentangle the role of selection on different actors within this system by investigating evolutionary scenarios where defense evolves as (i) a host-controlled trait that reduces algal reproductive ability; (ii) a symbiont-controlled trait that impacts symbiont transmission; and (iii) a trait jointly controlled by both host and symbiont. Optimal investment in defensive toxins varies based on the characteristics of the host, symbiont, and sea slug; and evolutionary trajectories are modulated by trade-off shape, i.e., a strongly decelerating trade-off between defense and symbiont transmission can drive symbiont diversification via evolutionary branching. Increasing slug herbivory reduces host investment in defense to favor reproduction, while symbiont investment in defense first declines and then increases as host density declines to the degree that horizontal symbiont transmission is no longer beneficial. Increasing vertical transmission selects for reduced defense by the host when it evolves as a jointly controlled trait, as a result of investment by the symbiont. Our theoretical exploration of the evolution of defensive symbiosis in scenarios involving interactions with multiple herbivores provides a first window into the origin and maintenance of the Bryopsis sp. system, and adds another piece to the puzzle of the evolution of symbiotic systems.

The evolutionary history of canids has been shown to be complex, with hybridization and domestication confounding our understanding of speciation among various canid lineages. The dingo is a recent canid lineage that was completely isolated from other canids for over 5000 years on the Australian mainland, but the introduction of domestic dogs in 1788 has placed doubt on its independence, with recent studies highlighting hybridization between dingoes and domestic dogs. Using genomic single nucleotide polymorphism data from 434 Australian canid samples, we explicitly test for introgression between closely related canid groups and dingoes. We found no evidence of introgression between dingoes and domestic dogs and show that previous work has likely mischaracterized shared ancestral genetic variation as evidence for hybridization. Further, New Guinea Singing Dogs are the only canid group that significantly shared genetic variation with dingoes, which fits with our understanding of previous phylogenetic analyses. Despite more recent sympatric distributions with dogs, dingoes have likely maintained their independence since their arrival in Australia, even in areas with high lethal control, indicating that their evolutionary trajectory is currently being conserved. The future conservation of the dingo lineage will require policies that promote coexistence pathways between humans and dingoes that protect rangeland systems and the dingoes' evolutionary future.

The genetic basis of phenotypic or adaptive parallelism can reveal much about constraints on evolution. This study investigated the genetic basis of a canonically parallel trait: pelvic spine reduction in sticklebacks. Pelvic reduction has a highly parallel genetic basis in threespine stickleback in populations around the world, always involving a deletion of the pel1 enhancer of Pitx1. We conducted a genome-wide association study to investigate the genetic basis of pelvic spine reduction in 3 populations of brook stickleback in Alberta, Canada. Pelvic reduction did not involve Pitx1 in any of the 3 populations. Instead, pelvic reduction in 1 population involved a mutation in an exon of Tbx4, and it involved a mutation in an intron of Lmbr1 in the other two populations. Hence, the parallel phenotypic evolution of pelvic spine reduction across stickleback genera, and among brook stickleback populations, has a nonparallel genetic basis. This suggests that there may be redundancy in the genetic basis of this adaptive polymorphism, but it is not clear whether a lack of parallelism indicates a lack of constraint on the evolution of this adaptive trait. Whether different pleiotropic effects of different mutations have different fitness consequences or whether certain pelvic reduction mutations confer specific benefits in certain environments remains to be determined.

Quantifying the tempo and mode via modern phylogenetic comparative methods can provide key insights into how selection and constraints shape trait evolution on a macroevolutionary time scale. Here, we elucidate the evolution of hibernation (winter) diapause, a complex and defining life-history trait that allows temporal escape from harsh winters in temperate regions for many insects, including our model system, butterflies. Butterflies can diapause in all major life stages, and the availability of global-scale phylogenies makes them an ideal model system for studying diapause evolution. First, using a thorough literature survey, we scored the developmental stage of hibernation diapause (egg, larva, pupa, adult) vs. absence of diapause. We find that larval diapause is most common, while pupal, egg, and adult diapause are relatively rare. Next, we determined that the loss of diapause occurred at a much higher rate and that gains primarily occurred from the non-diapause state. While ancestral state estimation at deeper nodes remained uncertain, we found consistent patterns for some families and strong evidence for extensive convergence in diapause evolution. Contrary to expectations, we find no support for increased gain of diapause during the Eocene-Oligocene glaciation (~35 million years ago). Overall, the evolution of diapause in butterflies has a complex history, has evolved convergently, and has likely predated the major glaciation event consistent with the deep history of diapause evolution in insects. This study advances our understanding of the evolution of a complex and important life-history trait and establishes a macroevolutionary foundation for future studies on the ultimate and proximate basis of diapause evolution.

The evolutionary potential of traits is governed by the amount of heritable variation available to selection. While this is typically quantified based on genetic variation in a focal individual for its own traits (direct genetic effects, DGEs), when social interactions occur, genetic variation in interacting partners can influence a focal individual's traits (indirect genetic effects, IGEs). Theory and studies on domesticated species have suggested IGEs can greatly impact evolutionary trajectories, but whether this is true more broadly remains unclear. Here, we perform a systematic review and meta-analysis to quantify the amount of trait variance explained by IGEs and the contribution of IGEs to predictions of adaptive potential. We identified 180 effect sizes from 47 studies across 21 species and found that, on average, IGEs of a single social partner account for a small but statistically significant amount of phenotypic variation (0.03). As IGEs affect the trait values of each interacting group member and due to a typically positive-although statistically nonsignificant-correlation with DGEs (r _DGE-IGE = 0.26), IGEs ultimately increase trait heritability substantially from 0.27 (narrow-sense heritability) to 0.45 (total heritable variance). This 66% average increase in heritability suggests IGEs can increase the amount of genetic variation available to selection. Furthermore, whilst showing considerable variation across studies, IGEs were most prominent for behaviors and, to a lesser extent, for reproduction and survival, in contrast to morphological, metabolic, physiological, and development traits. Our meta-analysis, therefore, shows that IGEs tend to enhance the evolutionary potential of traits, especially for those tightly related to interactions with other individuals, such as behavior and reproduction.