Allopolyploidy is an important force in plant evolution, yet studying natural allopolyploid species remains challenging due to the complexity of their genetic architecture and a lack of reference genomes. A major obstacle is the accurate phasing of subgenomes, which is a prerequisite for the application of diploid-based population genetic tools. Here, we developed allosplitter , a novel bioinformatic tool that enables precise subgenome phasing for allotetraploids using only genotyping-by-sequencing (GBS) data from a derived polyploid and its diploid progenitors. We applied allosplitter to the allotetraploid Achillea wilsoniana and its progenitors ( A. acuminata and A. asiatica ). We uncovered clear asymmetric subgenome evolution: subgenome C (derived from A. acuminata ) exhibited significantly lower genetic diversity, higher population differentiation and higher Tajima's D $$ D $$ than subgenome Y (derived from A. asiatica ). This indicated a dominant evolutionary role for subgenome C, while historical introgression from A. acuminata further amplified population divergence. Phylogenetic and structure analyses enabled us to reject the biogeographic origin of A. wilsoniana in the Qinling Mountains, instead supporting its origin in the Hengduan Mountains. This study provides a reference-genome-free framework for polyploid genomics and offers new insights into the evolution of allopolyploids.
The rise of antibiotic-resistant bacteria poses a critical global health threat. Previous studies on the evolution of bacterial antibiotic resistance have often overlooked the fact that bacteria frequently exist within complex microbial communities, where they engage in mutually beneficial interactions through nutrient exchange. Here, we studied the evolution of antibiotic resistance in an obligate cross-feeding population. After 15 days of selection under kanamycin, both co-cultures and mono-cultures of auxotrophic strains evolved significantly higher resistance. The increase in resistance was significantly lower in the co-culture consortium than in each mono-culture consortium. Strains in the co-cultures showed higher levels of amino acid secretion and a reduced growth rate than those in the mono-cultures. This suggests a higher cost of amino acid exchange in the co-cultures. Exogenous amino acids supplementation reduced the cost of metabolic exchange and intensified competition between the two strains due to niche overlap. This further resulted in decreased kanamycin resistance in both the mono-evolved and the co-evolved populations under the kanamycin-free environment. The interaction among the two auxotrophic strains shifted from positive to negative in co-evolved population. This supports the stress gradient hypothesis, which posits that facilitation is more common in stressful environments, whereas competition dominates when conditions are more benign. Our findings demonstrate that environmental stress and nutrient availability can modulate bacterial antibiotic resistance by altering microbial interactions and fitness dynamics within communities.
Syntrophic interactions based on reciprocal metabolite exchange are widespread in microbial communities, yet the factors determining their stability remain unclear. Using synthetic Escherichia coli consortia composed of lysine and arginine auxotrophs, we show that lower initial metabolite production promotes, rather than limits, syntrophic stability. During serial propagation, replicate cocultures diverged sharply: a minority maintained sustained growth, whereas most became extinct. This divergence was associated with phenotypic differences in metabolite production among founding isolates. Consortia founded by low-producing strains recovered reliably after dilution and were more resistant to invasion by non-producing mutants. By contrast, high-producing founder generated diminishing returns for consortium growth, and increased extracellular metabolite availability that favored exploitation by non-producer. Although we detected no consistent coding-region variations between high- and low-producing isolates, expression differences suggest that outside coding regions may influence these production traits. These results identify constrained initial metabolite production as a key determinant of syntrophic stability.
Estimating the effective number of breeders per reproductive cycle or cohort ( N b $$ {N}_b $$ ) can contribute to understanding the viability of wild populations. However, previous N b $$ {N}_b $$ estimators based on heterozygote-excess assume that parental genotypes are in accordance with Hardy-Weinberg equilibrium (HWE), and can only be applied to diploids. When these criteria are not fulfilled, estimates of expected heterozygosity may thus be biased. We extended a previous N b $$ {N}_b $$ estimator to autopolyploids and account for parental genotypes either in HWE or heterozygote-excess equilibrium (HEE). Results include the following: the distributions of genotypes converge to HEE within nine generations (with a relative error of 10 - 3 $$ {10}^{-3} $$ ), the corrected estimators can asymptotically estimate N b $$ {N}_b $$ without bias, and estimations for autopolyploids are slightly better than those for diploids. The relationships between N ̂ b $$ {\hat{N}}_b $$ and N b $$ {N}_b $$ and the influence of variable effective breeding numbers across generations on N ̂ b $$ {\hat{N}}_b $$ were clarified. We find N ̂ b $$ {\hat{N}}_b $$ mainly reflects N b $$ {N}_b $$ in the previous generation in diploids but is a weighted harmonic mean of N b $$ {N}_b $$ in previous generations in polyploids. Our methods are implemented in a software package, polygene v1.7, which is freely available at https://github.com/huangkang1987/polygene.
Mixed-ploidy species provide key insights into polyploid plant evolution, but the role of inter-cytotype gene-flow in their establishment and maintenance remains unclear due to the complex polysomic and heterogeneous genetic background of polyploids. Here, we established a mathematical model to describe inter-cytotype gene-flow patterns and validated it with migration rate data from the mixed-ploidy species Chamerion angustifolium. We further assessed the mechanisms underlying cytotype establishment and maintenance by estimating genetic diversity, habitat suitability distribution and population structure. Both the model and genetic analyses revealed that intermediate-level cytotypes (e.g., tetraploids in C. angustifolium) received higher inter-cytotype gene-flow, maintained greater genetic diversity, and harbored more private alleles. Habitat suitability distribution modeling revealed a significantly smaller and overlapping suitable area for polyploids relative to diploids. Genetic structure analyses revealed weak differentiation among cytotypes and a geography-driven clustering pattern, indicating multiple origins of polyploids. Taken together, we hypothesize that incomplete reproductive isolation and weak genetic isolation in C. angustifolium enables inter-cytotype gene-flow. Moreover, cytotype coexistence in mixed-ploidy species is sustained by: (i) unidirectional gene-flow (from diploids to polyploids), (ii) climatic-niche differentiation of polyploid populations, and (iii) frequent origins of polyploids.
Animals have evolved behavioural and anatomical traits to resolve conflict without direct physical aggression, often by assessing contest outcomes based on visual cues such as body posture, facial signals and piloerection. In primates, the ratio of facial width-to-height (fWHR) has been linked to aggressive behaviour and personality. However, empirical support for a relationship between a large fWHR (wide face) and aggressive behaviour in primates is inconsistent, potentially reflecting species-specific differences in the costs/benefits of aggressive interactions and the socioecological contexts in which those costs/benefits occur. Here, we investigated associations among fWHR, aggressiveness and contest outcomes in a wild population of golden snub-nosed monkeys, Rhinopithecus roxellana. These monkeys live in a multilevel society comprising multiple one-male multifemale units within a larger breeding band. We measured the fWHR of 126 adults, subadults and juveniles of both sexes using facial photographs and recorded aggressive interactions via all-occurrence recording. Age-specific sexual dimorphism was observed: fWHR was significantly higher in subadult females than in subadult males, with the reverse pattern present in adults. We found that in adult males, fWHR was positively correlated with both the frequency of initiating aggressive interactions and the probability of winning contests. In addition, male age and whether a male initiated the aggressive action (first-mover advantage) also positively predicted contest outcomes. Thus, the fWHR appears to serve as a signal of male aggressiveness and fighting ability in golden snub-nosed monkeys. However, given that we do not have direct evidence that resident males more frequently initiated aggression towards adult males with a smaller fWHR, further research is required to determine the degree to which fWHR serves as an honest signal for deterring conflict between potential opponents.
Competition within primate groups often translates to a social hierarchy, with high-rank individuals gaining privileged access to resources, especially food. Golden snub-nosed monkeys Rhinopithecus roxellana live in a multi-level society, with multiple one-male units (OMUs), each containing a single adult male and several females, forming a breeding-band. High-rank males have increased access to high-value foods and spend less time feeding and more time being groomed by females, potentially enhancing social cohesion within their OMUs. The adults of each OMU mainly feed and socialize together, with food competition predominantly acting at the OMU level. We thus predicted that adult females by association attain the rank and feeding privileges of their OMU leader males, and make similar time-budget trade-offs. By food-provisioning a wild breeding-band during winter and spring, when natural foods are abundant or limited, respectively, we found that females of high-rank OMUs ate more provisioned foods at higher rates, especially during winter when provisioned foods had increased value. In winter, females of low-rank OMUs fed for longer on natural foods and females of high-rank OMUs longer on provisioned foods. Females of high-rank OMUs spent longer being groomed by other OMU members, especially during winter. Our results are consistent with females attaining the feeding privileges of their OMU leader male, enhanced during winter due to increased value of provisioned foods, high thermal demands, and reduced natural food availability. Importantly, the feeding privileges attained by females of high rank OMUs were less pronounced than those previously found for leader males, possibly due to higher tolerance between females of different OMUs. We suggest that behavioral time-budget effects of food competition in female R. roxellana enhance cohesion in high-rank OMUs, contributing to OMU integrity and, hence, the social structure of this multi-level society.
Abstract In monoecious fig-wasp mutualisms (Ficus; ~350 spp.), tiny wasps obligately pollinate fig-tree inflorescences (‘figs’). Although pollination enables seed production wasp symbionts also oviposit into flowers, replacing potential seeds with wasp offspring. Consistently across Ficus, ~40-60% of developed flowers produce seeds. Although several processes are likely involved, a general explanation for why wasps do not exploit more flowers has been elusive. However, inter-specific scaling between host-symbiont reproductive traits suggests that as figs become larger across Ficus, the increase in wasp-eggs-per pollen-receptive fig will fail to match the increase in flower numbers. The potential for wasps to exploit hosts should thus decline due to an increasing excess of flowers. We tested these predictions, which were upheld, using data from 23 fig-wasp mutualisms from four continents. As fig size increases across Ficus, wasp egg-to-flower ratios, a measure of host-symbiont conflict-of-interest, declines, but the likelihood of a wasp egg successfully becoming an adult offspring increases. Host-symbiont conflict-of-interest thus varies systematically across Ficus due to variable relationships between key mutualist reproductive traits and fig size. We suggest that mutualism stability is more dependent upon mechanisms curtailing wasp flower exploitation in systems with small figs, and on preventing high foundress numbers in those with large figs.
Most mutualisms are parasitized by third-party species that inflict costs to the mutualists. How such parasites affect mechanisms that help maintain mutualism stability is poorly understood, even in well-studied systems. Angiosperm plants tend to invest most resources in tissue that yields high net benefits. In mutualisms with plant hosts, reduction in such investment can function as a key stability-promoting mechanism, such as in fig-wasp mutualisms. Here, uncooperative symbiont wasps that fail to pollinate incur "sanctions" via reduced host investment to unpollinated figs, realized via fig abortion, killing all wasp offspring, or via elevated offspring mortality within unaborted figs. We experimentally exposed host Ficus racemosa figs to parasitic wasps Sycophaga fusca, which convert fig flowers into offspring without benefitting host trees, with or without uncooperative (pollen-free) or cooperative (pollen-laden) symbiont pollinator wasps Ceratosolen fusciceps. Pollen-free C. fusciceps were still able to convert fig flower ovaries into wasp offspring, whereas those naturally pollen laden were prevented from reproducing by experimental manipulation. Independent of the effects of pollination and reproduction by pollinators, increased exposure to S. fusca parasites resulted in reduced rates of fig abortion and gall failure in unaborted figs. Although S. fusca convert flower ovaries that could otherwise become beneficial pollinator offspring or fig seeds into parasite offspring, figs with intermediate levels of parasite exposure received high levels of investment. Our results suggest that S. fusca parasite oviposition/larval activities can result in host trees boosting investment to figs, even when this may counter the tree's interests. We suggest that oviposition/larval activity by these parasites may mimic the biochemical pathways of pollinator gall formation and seed production.
A fundamental problem in ecology is to understand how mutualisms remain stable. The density-dependent regulations within interacting species potentially impact the persistence of these interspecific relationships. Yet few studies explore such intraspecific regulations' role in stabilizing mutualisms. In addition, partner species often gain unequal benefits in mutualisms. To what extent such an interspecific asymmetry affects the stability of mutualisms is also poorly understood. We here developed a dynamic model for the asymmetric interaction between plants and their pollinators in nursery mutualisms, considering the intraspecific competition of each mutualist. We found that (i) a mutualism can be stabilized only if both mutualists are subject to the regulation of intraspecific competition; (ii) stabilizing the system also requires that the degree of asymmetry in benefits between mutualists must be limited to a range of 'tolerance', which narrows as intraspecific competition increases and even fades away with strong competition within both mutualistic species; (iii) when intraspecific competition within a species increases, the tolerant range is compressed from the side beneficial for it, with thus its partner species gaining relatively more benefit allocation; (iv) if the plant-pollinator interaction initiates from a small host plant population, these host plants must offer pollinators high levels of benefits, that can be subsequently reduced to favor plants once the mutualism has been successfully established. The agreement of empirical data to theoretical predictions suggests model reliability. These results highlight the role of intraspecific competition and the degree of benefit asymmetry between host plants and symbionts in stabilizing mutualisms.
BACKGROUND:The influence of Ficus extends beyond its numbers (800 species), and fig trees are often key-stone species in their habitats. Ficus fills many tropical forest niches. The past 15 years have witnessed an explosion of research in Ficus, and its obligate mutualists in the chalcid family Agaonidae, but also on its wider community of interactants. Long-standing ideas have been challenged and pathways to speciation have been explored. We aim to stimulate collegiate discussion: why are there not more species of fig? SCOPE:Here we critically review the literature relating to diversification in Ficus, while presenting a synthetic overview of our current understanding and knowledge gaps. We illustrate key concepts with well-studied groups of Ficus and other obligate mutualisms. Our review is unapologetically detailed and includes extensive botanical insight that is frequently over-looked in the literature. We draw on these details to develop hypotheses relating to the origin of diversity within the genus Ficus. CONCLUSIONS:We argue that the fig itself represents a new niche and explore the implications of sexual and vegetative traits in driving diversification (species richness) and diversity (in the ecological sense). An increasingly stable backbone phylogeny and the availability of genomic nuclear and chloroplast data has shed dappled light upon the deep evolutionary past. Incidences of potential diversification through introgression exist, but we must be cautious as the tools used were not always suitable for revealing ancient hybridization. An asymmetric genetic sampling of figs and wasps has further influenced our concepts of host specificity in the genus. Our comparative approach evaluates classical models of speciation in Ficus, concluding that adaptive radiations on islands have triggered diversification. We should maintain global research networks and sample widely. It is tempting to over generalise results. This leads to misconceptions and missing puzzle pieces. Further, adopting standard protocols ensures connectivity.
In social mammals, dominance status and tenure length are often important determinants of male reproductive success. Nevertheless, alternative strategies, such as extra-pair mating, and the active role of females in securing reproductive benefits can substantially modify patterns of paternity. To date, many studies have had short observation periods and small sample sizes, constraining understanding of how male social status, tenure length, and female mating strategies jointly affect male long-term reproductive success, especially in species with complex social systems. Using longitudinal demographic and genetic data from a free-ranging population of a golden snub-nosed monkey (Rhinopithecus roxellana) multilevel society in the Qinling Mountains, central China, we investigated how leader males' ranks and tenure lengths influence their reproductive success through within-unit and extra-unit paternities. We found that although high rank increases the likelihood of producing within-unit paternity offspring in the short term, tenure length is a stronger determinant of long-term reproductive success via both within-unit and extra-unit paternities. Females may gain direct benefits from producing extra-pair paternity offspring by reducing the risk of infanticide through mating with all-male band males and/or by selecting high-ranking leader males for better access to resources. Moreover, females may also accrue additional indirect benefits from producing extra-pair paternity offspring when more adult males are available in the breeding band. Our findings highlight extra-pair paternity as a reproductive strategy for both male and female golden snub-nosed monkeys to optimize reproductive success, which may also play a role in maintaining stability in this complex primate society.
Understanding how cooperation evolves in microbial populations, particularly under environmental stress such as antibiotic exposure, remains a key topic in evolutionary biology. Here, we investigate cooperative interactions between antibiotic-resistant and antibiotic-sensitive strains of Escherichia coli. Under antibiotic stress, a small number of antibiotic-sensitive strains rapidly evolve into antibiotic-resistant strains. Resistant E. coli produce indole, which induces a protective response in sensitive cells, enabling them to survive in antibiotic stress conditions. In turn, antibiotic-sensitive E. coli could help reduce toxic accumulation of indole, indirectly benefiting the resistant strain. Indole is harmful to the growth of the antibiotic-resistant strain but benefits the antibiotic-sensitive strain by helping turn-on the multi-drug exporter to neutralize the antibiotic. This mutual exchange leads to increased fitness for both strains in cocultures, demonstrating a mechanism by which mutually beneficial cooperation can evolve in bacterial communities. Our findings provide insight into how mutualism can emerge under antibiotic pressure through metabolic byproduct exchange, revealing new dynamics in the evolution of bacterial cooperation.
The order Myrtales, one of the most species-rich lineage within the Superrosidae clade, with the majority of its species distributed across five families: Myrtaceae, Melastomataceae, Lythraceae, Onagraceae, and Combretaceae. Despite the ecological and economic importance of the Myrtales, its phylogenetic relationships remain unresolved, with previous studies yielding inconsistent results based on gene fragments and plastid genomes. Genomic data, particularly single-copy/low-copy nuclear genes, provide valuable insights for resolving these phylogenetic relationships. However, phylogenetic studies still lack sufficient clade coverage, particularly for less studied families such as the Onagraceae. Epilobieae is an important tribe of the Onagraceae, characterized by substantial chromosomal number variation and whole genome duplication event (WGD). Nevertheless, the mechanisms of chromosomal evolution remain unresolved. Here, we sequenced and assembled the genomes of two representative species from the Epilobieae, Chamerion angustifolium (formerly Chamaenerion angustifolium) and Epilobium hirsutum, with genome sizes of 636.59 Mb and 400.23 Mb, respectively. Genome evolution analysis revealed two WGD events, during which the chromosome number increased from n=9 to n=18 , followed by aneuploid reduction, leading to the diverse chromosomal numbers observed within this tribe. The WGD retained genes are enriched in Environmental information processing pathways, potentially enhancing resistance to biotic and abiotic stresses. These genes also show a preference for multiple exons, which may promote alternative splicing and functional diversification. Additionally, integrating genomic data from 24 Myrtales species, a robust phylogenetic framework based on 994 single-copy/low-copy orthogroups were reconstructed. Our results supported Combretaceae as the sister group to Myrtaceae and Melastomataceae, providing new insights into the evolutionary relationships within the Myrtales.
Golden snub-nosed monkeys show inconsistent frequency of placentophagy between wild and captive populations, with almost all births in the wild but around half of the births in captivity accompanied by the female's consumption of placenta. This aligns with nutritional demands-driven placentophagy, as captive populations are generally under less nutritional constraints for breeding females than the wild population. Placentophagy is probably adaptive in the wild and under positive selection due to nutritional benefits to both mothers and infants.
Changes in diet causing ecological stress pose a significant challenge to animal survival. In response, the gut microbiota, a crucial part of the host’s digestive system, exhibits patterns of change reflective of alterations in the host’s food component. The impact of temporal dietary shifts on gut microbiota has been elucidated through multidimensional modeling of both food component and macronutrient intake. However, the broad distribution of wild generalist and the intricate complexity of their food component hinder our capacity to ascertain the degree to which their gut microbiota assist in adapting to spatial dietary variations. We examined variation in patterns of the gut microbial community according to changes in diet and in a colobine monkey with a regional variable diet, the golden snub-nosed monkey (Rhinopithecus roxellana). Specifically, we analyse the interactions between variation in food component, macronutrient intake and the gut microbial community. We compared monkeys from four populations by quantifying food component and macronutrient intake, and by sequencing 16S rRNA and the microbial macro-genomes from the faecal samples of 44 individuals. We found significant differences in the diets and gut microbial compositions, in nutrient space and macronutrient intake among some populations. Variations in gut microbiota composition across distinct populations mirror the disparities in macronutrient intake, with a notable emphasis on carbohydrate. Geographical differences in the diet among of golden snub-nosed monkey populations will result in macronutrient intake variation, with corresponding differences in macronutrient intake driving regional differences in the compositions and abundances of gut microbiota. Importantly, the gut microbiota associated with core digestive functions does not vary, with the non-core gut microbiota fluctuating in response to variation in macronutrient intake. This characteristic may enable species heavily reliant on gut microbiota for digestion to adapt to diet changes. Our results further the understanding of the roles gut microbiota play in the formation of host dietary niches.
Although understanding mutualism stability has advanced over the last few decades, two fundamental problems still remain in explaining how mutualisms maintain stable. (i) How does resolve conflict between mutualists over resources? (ii) In the presence of less cooperative and/or uncooperative symbionts, how does prevent symbiont populations from becoming dominated by uncooperative individuals? Many past explanations of mutualism stability have assumed that interactions between mutualists are symmetrical. However, in most mutualisms, interactions between hosts and symbionts show varying degrees of asymmetry at different levels. Here, we review three major types of asymmetric interactions within obligate mutualisms: (i) asymmetric payoffs, which is also defined as individual power differences, (ii) asymmetric potential rates of evolutionary change, and (iii) asymmetric information states between hosts and symbionts. We suggest that these asymmetries between mutualists help explain why cooperation and conflict are inherent in the evolution of mutualisms, and why both hosts and symbionts present diversified phenotypes while cooperation predominates.
Social insects are prone to pathogen infection because of high exposure rates from social interactions. However, it remains unclear whether queens have enhanced pathogen resistance, because reproduction is largely confined to queens. Here, we used a natural host–pathogen system, the subterranean termite Reticulitermes chinensis and the entomopathogenic fungus Metarhizium anisopliae , to investigate the differences in allogrooming, locomotion, and immune gene expression between queens and workers against pathogen infection. We found that fungal infection significantly reduced survival in both queens and workers. Infected queens received significantly more grooming time from sanitary nestmates than infected workers, but they returned much less grooming time to sanitary nestmates than infected workers. Infection resulted in a reduction in the average locomotion speed and distance of queens but had no effect on worker locomotion. Infection resulted in upregulated expression of two immune genes ( termicin and transferrin ), two antioxidant genes ( CAT and SOD ), and phosphate genes CYP450 in queens but not in workers. Our results indicated that eusocial termites evolved strategies that prioritize the reproductive castes' welfare in defending against the pathogen infection to ensure continued reproduction and colony persistence.
Explaining how cooperative individuals positively assort into a cohesive community is one of the greatest challenges for evolutionary biology. Here, we show that in antibiotic culture, many and even all of Escherichia coli bacteria cells will plastically mutate to be antibiotic resistant with the increase of antibiotic concentration and then altruistically protect antibiotic-sensitive individuals from the attack of antibiotics. A further experiment showed that antibiotic-sensitive E. coli strain could in turn help reduce the indole produced by the resistant strain;whistthis metabolic product is harmful to the growth of the antibiotic-resistant strain but benefits the antibiotic-sensitive strain by helping turn on the multi-drug exporter to discharge the antibiotic. A reciprocal cooperation can therefore evolve via a non-positive exchange between the metabolism byproduct indole of antibiotic-resistant cells and the indole-aborting service of antibiotic sensitive cells as unconscious help in nullifying indole side effect of antibiotic resistant strain.
Although tag-based donation and recognition have well explained how the cooperative individuals are positively assorted if the cooperative individuals possess some signals and are also able to detect such signals, an additional mechanism is required to explain why some individuals pay the costs of evolving such a tag that may not be rewarded subsequently, and how such tag-based cooperative individuals will meet other similar individuals with a very low mutation rate. Here, we show that many and even all Escherichia coli bacteria cells in the increased antibiotic concentration will plastically evolve to be antibiotic resistant individuals who could protect antibiotic sensitive strain from the attack of antibiotics, and the antibiotic resistant strain could reversibly evolve to be antibiotic sensitive in non-antibiotic supplement medium but in a harsher environment with low glucose. A further experiment showed that antibiotic-sensitive E. coli strain could in turn help reduce the concentration of indole produced by the resistant strain. This metabolic product is harmful to the growth of the antibiotic-resistant strain but benefits the antibiotic-sensitive strain by helping turn on the multi-drug exporter to discharge the antibiotic. The utilization of metabolism byproduct indole produced by antibiotic-resistant cells benefits antibiotic-sensitive cells, while the indole-absorbing service of antibiotic sensitive cells unconsciously help in nullifying the indole side effect on antibiotic resistant strain, and a mutual benefit cooperation could therefore evolve.