Positive Directional Selection Research Articles

Evolutionary Trends of Polygenic Scores in European Populations From the Paleolithic to Modern Times.

This study examines the temporal and geographical evolution of polygenic scores (PGSs) across cognitive measures (Educational Attainment [EA], Intelligence Quotient [IQ]), Socioeconomic Status (SES), and psychiatric conditions (Autism Spectrum Disorder [ASD], schizophrenia [SCZ]) in various populations. Our findings indicate positive directional selection for EA, IQ, and SES traits over the past 12,000 years. Schizophrenia and autism, while similar, showed different temporal patterns, aligning with theories suggesting they are psychological opposites. We observed a decline in PGS for neuroticism and depression, likely due to their genetic correlations and pleiotropic effects on intelligence. Significant PGS shifts from the Upper Paleolithic to the Neolithic periods suggest lifestyle and cognitive demand changes, particularly during the Neolithic Revolution. The study supports a mild hypothesis of Gregory Clark's model, showing a noticeable rise in genetic propensities for intelligence, academic achievement and professional status across Europe from the Middle Ages to the present. While latitude strongly influenced height, its impact on schizophrenia and autism was smaller and varied. Contrary to the cold winters theory, the study found no significant correlation between latitude and intelligence.

Adult body mass is heritable, positively genetically correlated and under selection of differing shapes between the sexes in a bird with little apparent sexual dimorphism.

In most animals, body mass varies with ecological conditions and is expected to reflect how much energy can be allocated to reproduction and survival. Because the sexes often differ in their resource acquisition and allocation strategies, variations in adult body mass and their consequences on fitness can differ between the sexes. Assessing the relative contributions of environmental and genetic effects (i.e. heritability)-and whether these effects and their fitness consequences are sex-specific-is essential to gain insights into the evolution of sexual dimorphism and sexual conflicts. We used 20+ years of data to study the sources of variation in adult body mass and associated fitness consequences in a bird with biparental care, the Alpine swift (Tachymarptis melba). Swifts appear monomorphic to human observers, though subtle dimorphisms are present. We first investigated the effects of weather conditions on adult body mass using a sliding window analysis approach. We report a positive effect of temperature and a negative effect of rainfall on adult body mass, as expected for an aerial insectivorous bird. We then quantified the additive genetic variance and heritability of body mass in both sexes and assessed the importance of genetic constraints on mass evolution by estimating the cross-sex genetic correlation. Heritability was different from zero in both sexes at ~0.30. The positive cross-sex genetic correlation and comparable additive genetic variance between the sexes suggest the possibility for evolutionary constraints when it comes to body mass. Finally, we assessed the sex-specific selection on adjusted body mass using multiple fitness components. We report directional positive and negative selection trending towards stabilizing and diversifying selection on females and males respectively in relation to the weighted proportion of surviving fledglings. Overall, these results suggest that while body mass may be able to respond to environmental conditions and evolve, genetic constraints would result in similar changes in both sexes or an overall absence of response to selection. It remains unclear whether the weak (1%) dimorphism in Alpine swift body mass we report is simply a result of the similar fitness peaks between the sexes or of genetic constraints.

Intra-specific correlations between ejaculate traits and competitive fertilization success: a meta-analysis across species and fertilization modes.

Understanding of how selection can act on traits that improve competitiveness and subsequent paternity has advanced, including the idea that internal and external fertilization presents different environments that may select differentially on ejaculate traits. However, no studies have quantitatively synthesized the intra-specific relationships between these traits and paternity. Therefore, we conducted a meta-analysis across 52 papers to determine which ejaculate traits positively correlate with paternity share and how these correlations vary with fertilization mode. Overall, most ejaculate traits were positively associated with paternity, with the notable exception of sperm length. Sub-analyses on sperm number, sperm length, and sperm velocity revealed no statistical differences between fertilization modes in the relationship between traits and paternity when all effect sizes across species were combined. However, in a sub-analysis on fish species only, we found evidence that sperm velocity may be more important in external fertilizers. We also observed differences in the importance of phylogenetic relatedness and some species-specific differences. Our results suggest that while most ejaculate traits should be under positive directional selection in both internal and external fertilizers, sperm length may be subject to more nuanced selection pressures. Overall, we highlight important patterns of intra-specific relationships between ejaculate traits and competitive fertilization success.

Behavioral estimates of mating success corroborate genetic evidence for pre-copulatory selection

Abstract In promiscuous species, fitness estimates obtained from genetic parentage may often reflect both pre- and post-copulatory components of sexual selection. Directly observing copulations can help isolate the role of pre-copulatory selection, but such behavioral data are difficult to obtain in the wild and may also overlook post-copulatory factors that alter the relationship between mating success and reproductive success. To overcome these limitations, we combined genetic parentage analysis with behavioral estimates of size-specific mating in a wild population of brown anole lizards (Anolis sagrei). Males of this species are twice as large as females and multiple mating among females is common, suggesting the scope for both pre- and post-copulatory processes to shape sexual selection on male body size. Our genetic estimates of reproductive success revealed strong positive directional selection for male size, which was also strongly associated with the number of mates inferred from parentage. In contrast, a male’s size was not associated with the fecundity of his mates or his competitive fertilization success. By simultaneously tracking copulations in the wild via the transfer of colored powder to females by males from different size quartiles, we independently confirmed that large males were more likely to mate than small males. We conclude that body size is primarily under pre-copulatory sexual selection in brown anoles, and that post-copulatory processes do not substantially alter the strength of this selection. Our study also illustrates the utility of combining both behavioral and genetic methods to estimate mating success to disentangle pre- and post-copulatory processes in promiscuous species.

Major histocompatibility complex complement (MHC) Bf alleles show trans species evolution between man and chimpanzee

HLA and disease studies by using single allele statistics have been fruitless during the last 40 years for explaining association pathogenesis of the associated diseases.Other approaches are necessary to untangle this puzzle. We aim to revisit complement alleleism in humans and primates for both studying MHC and disease association to complotypes and extended MHC haplotypes in order to also explain the positive directional selection of maintaining immune response genes (complement, MHC adaptive and MHC non-specific genes) that keeps these three type of genes together in a short chromosome stretch (MHC) for million years. These genes may be linked to conjointly avoid microbes attack and autoimmunity. In the present paper, it is obtained a new Bf chimpanzee allele, provisionaly named Patr-Bf*A:01,that differs from other Bf alleles by having CTG at eleventh codon of exon 2 in order to start the newly suggested methodology and explain functional and evolutionary MHC obscure aspects. Exons 1 to 6 of Ba fragment of Bf gene were obtained from chimpanzee. This new chimpanzee Factor B allele (Patr-Bf*A:01) is to be identical to a infrequent human Bf allele (SNP rs641153); it stresses the strong evolutive pressure upon certain alleles that are trans specific. It also may apply to MHC extended haplotipes which may conjointly act to start an adequate immune response. It is the first time that a complement MHC class III allele is described to undergo trans species evolution,in contrast to class I and class II alleles which had already been reported . Allelism of complement factors are again proposed for studying MHC complement genes, complotypes, and extended MHC haplotypes which may be more informative that single MHC marker studies.

Genomic analysis of Plasmodium falciparum isolates across different altitudinal zones along the slope of Mount Cameroon

BackgroundMalaria elimination is threatened by the emergence and rapid spread of drug resistance. Understanding the demographic history of Plasmodium falciparum and the genetic basis of adaptation to antimalarial treatment and host immunity is critical to elimination efforts. This study sought to characterize the diversity of P. falciparum isolates across different altitudes along the slope of Mount Cameroon.MethodologyUsing the Illumina next-generation sequencing platform P. falciparum isolates from low, intermediate and high altitudes along the slope of Mount Cameroon were studied to determine their genetic diversity, population structures, and signatures of selection in known drug resistance alleles.ResultsA total of 77,253 single-nucleotide polymorphisms were identified from 220 quality P. falciparum clinical isolates from high (24,214), intermediate (24,426), and low (28,613) altitude. About 49%, 48.2% and 30% of the parasite isolates from high, intermediate, and low altitudes, respectively had FWS values > 0.95 indicative of dominant mixed genotype infections and low population sub-structure with high potential for out-crossing. No significant difference was observed in within-host diversity while population structure analysis did not separate the isolates in the three major altitudinal groups by PCA, FST and admixtures, suggesting bidirectional gene flow among the populations. A total of 94 antigenic genes under balancing selection were detected in the area including vaccine candidate gene ama1, eba175, msp1, trap, dblmsp, and clag2. Moreover, 17 of these genes were identified to be under both recent positive directional and positive balancing selection including the prominent host immune target genes surfin 8.2, trap, and ama1. Recent directional selection analysis using integrated standardized haplotype score (iHS) did not detect any selection signatures in the Pfdhfr, Pfdhps, Pfmdr1, and PfK13 genes. Furthermore, no PfKelch13 validated mutation associated with artemisinin resistance was identified in this study and no structural divergence was noticed among the P. falciparum parasite populations across different altitudes around the Mount Cameroon region.DiscussionFindings revealed high genetic diversity and low population structure suggesting that malaria transmission remain high in the study area and parasite populations circulating around the slope of Mount Cameroon are homogenous.

One Size Fits All-Venomics of the Iberian Adder (Vipera seoanei, Lataste 1878) Reveals Low Levels of Venom Variation across Its Distributional Range.

European vipers (genus Vipera) are medically important snakes displaying considerable venom variation, occurring at different levels in this group. The presence of intraspecific venom variation, however, remains understudied in several Vipera species. Vipera seoanei is a venomous snake endemic to the northern Iberian Peninsula and south-western France, presenting notable phenotypic variation and inhabiting several diverse habitats across its range. We analysed the venoms of 49 adult specimens of V. seoanei from 20 localities across the species' Iberian distribution. We used a pool of all individual venoms to generate a V. seoanei venom reference proteome, produced SDS-PAGE profiles of all venom samples, and visualised patterns of variation using NMDS. By applying linear regression, we then assessed presence and nature of venom variation between localities, and investigated the effect of 14 predictors (biological, eco-geographic, genetic) on its occurrence. The venom comprised at least 12 different toxin families, of which five (i.e., PLA2, svSP, DI, snaclec, svMP) accounted for about 75% of the whole proteome. The comparative analyses of the SDS-PAGE venom profiles showed them to be remarkably similar across the sampled localities, suggesting low geographic variability. The regression analyses suggested significant effects of biological and habitat predictors on the little variation we detected across the analysed V. seoanei venoms. Other factors were also significantly associated with the presence/absence of individual bands in the SDS-PAGE profiles. The low levels of venom variability we detected within V. seoanei might be the result of a recent population expansion, or of processes other than directional positive selection.

Population Genomics of Plasmodium falciparum and Malaria Control Implications in Abidjan (Cote d’ivoire)

Introduction: The onset of Plasmodium falciparum (P. falciparum) resistance to antimalarial drugs requires the careful surveillance of African parasite populations. Genomic tools are implemented to detect evolutionary changes that could impact malaria control and elimination strategies. Here, we evaluate the genome-wide pattern of selection and sequence variation in P. falciparum populations in Abidjan, Côte d’Ivoire. Methods: The study was conducted in three localities of Abidjan from 2013 to 2014. We collected 70 blood samples after receiving written informed consent from patients above two years of age. After extracting P. falciparum and human DNA from isolates, we performed whole-genome sequencing and used population genomics approaches to investigate the genetic diversity and complexity of infections and identify loci under positive directional selection. Results: We observed an excess of rare variants in the population, showing a clear mutation process in the isolates. Moderate Fst estimates (0.3) was detected for surfin, an immune invasion gene family. Seven iHS regions that had at least two SNPs with a score > 3.2 were identified. These regions code for genes that have been under strong directional selection. Two of these genes were the chloroquine resistance transporter (crt) on chromosome 7 and the dihydropteroate reductase (dhps) on chromosome 8. Our analyses showed that a recent selective sweep occurred for the erythrocyte membrane protein (Pfemp1). Conclusion: Our analyses identified genes under selective drug pressure and balancing selection on protective immune-specific genes. These findings demonstrate the effectiveness of genomics analyses to follow the evolution of malaria parasites and adopt appropriate strategies to eliminate malaria in Côte d’Ivoire.

A Pilot Study on The Population Genetic Structure of the Selected Fish Species from Meenachil River, India

Meenachil River is the only river originating from Southern Western Ghats of India having human settlement right from the headwaters to the mouth. The river is subjected to human-induced stressors to varying extents, resulting in a drastic decline in riverine health and fish diversity. The population genetic structure of two species commonly distributed in different geographical zones of Meenachil River, Dawkinsia filamentosa and Pseudetroplus maculatus were studied using the 16S mitochondrial ribosomal RNA gene sequences. Haplotype clustering and the presence of unique haplotypes were identified by phylogenetic and network analysis. Six haplotypes were identified for D. filamentosa and ten for P. maculatus. The neutrality estimations of the upstream and midstream populations of the species revealed the presence of an excess of common alleles with neutral mutations indicating a population expansion after bottleneck and stabilizing selection. The downstream population revealed the presence of an excess of rare alleles with non-neutral mutations indicating a positive directional selection and population sub-division. Population expansion demonstrated star-like phylogenies with rare haplotypes separated by mutational steps from the ancestral haplotypes. The private haplotypes indicated the existence of selection pressure in the downstream zone of the river.

Adaptive sequence divergence forged new neurodevelopmental enhancers in humans

Searches for the genetic underpinnings of uniquely human traits have focused on human-specific divergence in conserved genomic regions, which reflects adaptive modifications of existing functional elements. However, the study of conserved regions excludes functional elements that descended from previously neutral regions. Here, we demonstrate that the fastest-evolved regions of the human genome, which we term "human ancestor quickly evolved regions" (HAQERs), rapidly diverged in an episodic burst of directional positive selection prior to the human-Neanderthal split, before transitioning to constraint within hominins. HAQERs are enriched for bivalent chromatin states, particularly in gastrointestinal and neurodevelopmental tissues, and genetic variants linked to neurodevelopmental disease. We developed a multiplex, single-cell invivo enhancer assay to discover that rapid sequence divergence in HAQERs generated hominin-unique enhancers in the developing cerebral cortex. We propose that a lack of pleiotropic constraints and elevated mutation rates poised HAQERs for rapid adaptation and subsequent susceptibility to disease.

Population genetic analyses inferred a limited genetic diversity across the pvama-1 DI domain among Plasmodium vivax isolates from Khyber Pakhtunkhwa regions of Pakistan

BackgroundPlasmodium vivax apical membrane antigen-1 (pvama-1) is an important vaccine candidate against Malaria. The genetic composition assessment of pvama-1 from wide-range geography is vital to plan the antigen based vaccine designing against Malaria.MethodsThe blood samples were collected from 84 P. vivax positive malaria patients from different districts of Khyber Pakhtunkhwa (KP) province of Pakistan. The highly polymorphic and immunogenic domain-I (DI) region of pvama-1 was PCR amplified and DNA sequenced. The QC based sequences raw data filtration was done using DNASTAR package. The downstream population genetic analyses were performed using MEGA4, DnaSP, Arlequin v3.5 and Network.5 resources.ResultsThe analyses unveiled total 57 haplotypes of pvama-1 (DI) in KP samples with majorly prevalent H-14 and H-5 haplotypes. Pairwise comparative population genetics analyses identified limited to moderate genetic distinctions among the samples collected from different districts of KP, Pakistan. In context of worldwide available data, the KP samples depicted major genetic differentiation against the Korean samples with Fst = 0.40915 (P-value = 0.0001), while least distinction was observed against Indian and Iranian samples. The statistically significant negative values of Fu and Li’s D* and F* tests indicate the evidence of population expansion and directional positive selection signature. The slow LD decay across the nucleotide distance in KP isolates indicates low nucleotide diversity. In context of reference pvama-1 sequence, the KP samples were identified to have 09 novel non-synonymous single nucleotide polymorphisms (nsSNPs), including several trimorphic and tetramorphic substitutions. Few of these nsSNPs are mapped within the B-cell predicted epitopic motifs of the pvama-1, and possibly modulate the immune response mechanism.ConclusionLow genetic differentiation was observed across the pvama-1 DI among the P. vivax isolates acquired from widespread regions of KP province of Pakistan. The information may implicate in future vaccine designing strategies based on antigenic features of pvama-1.

Ecological determinants of variation in phenotypic selection on quantitative immune defence traits

Immune defence is an important determinant of organismal fitness. While theoretical models based on tradeoffs in resource allocation predict quantitative immune traits to be subject to stabilizing selection due to associated energetic costs and self‐harm, empirical studies report mainly positive directional selection. This discrepancy may arise from multiple ecological factors that vary in nature and could influence selection. We examined if selection on immune activity varies depending on immune challenge/infection risk, between immune traits and among populations in the freshwater snail Lymnaea stagnalis. We assessed selection on the phenoloxidase‐like and antibacterial activity of snail haemolymph while manipulating the level of immune challenge imposed by environmental microbes. We did this using snails from multiple populations and also quantified within‐population family‐level variation (i.e. evolutionary potential) in the snails' immune activity. We found that the strength of immune challenge and the examined immune trait determined selection on the snails' immune function. Thus, variation in infection risk can be an important factor in maintaining genetic variation in defence traits. Additionally, immune traits showed low among‐population differentiation but high within‐population genetic variation. This pattern could arise if natural snail populations are exposed to higher temporal than spatial variation in infection risk.

Maternal effects do not resolve the paradox of stasis in birth weight in a wild red deer populaton.

In natural populations, quantitative traits seldom show short-term evolution at the rate predicted by evolutionary models. Resolving this "paradox of stasis" is a key goal in evolutionary biology, as it directly challenges our capacity to predict evolutionary change. One particularly promising hypothesis to explain the lack of evolutionary responses in a key offspring trait, body weight, is that positive selection on juveniles is counterbalanced by selection against maternal investment in offspring growth, given that reproduction is costly for the mothers. Here, we used data from one of the longest individual-based studies of a wild mammal population to test this hypothesis. We first showed that despite positive directional selection on birth weight, and heritable variation for this trait, no genetic change has been observed for birth weight over the past 47 years in the study population. Contrarily to our expectation, we found no evidence of selection against maternal investment in birth weight-if anything, selection favors mothers that produce large calves. Accordingly, we show that genetic change in birth weight over the study period is actually lower than that predicted from models including selection on maternal performance; ultimately our analysis here only deepens rather than resolves the paradox ofstasis.

The roles of balancing selection and recombination in the evolution of rattlesnake venom.

The origin of snake venom involved duplication and recruitment of non-venom genes into venom systems. Several studies have predicted that directional positive selection has governed this process. Venom composition varies substantially across snake species and venom phenotypes are locally adapted to prey, leading to coevolutionary interactions between predator and prey. Venom origins and contemporary snake venom evolution may therefore be driven by fundamentally different selection regimes, yet investigations of population-level patterns of selection have been limited. Here, we use whole-genome data from 68 rattlesnakes to test hypotheses about the factors that drive genomic diversity and differentiation in major venom gene regions. We show that selection has resulted in long-term maintenance of genetic diversity within and between species in multiple venom gene families. Our findings are inconsistent with a dominant role of directional positive selection and instead support a role of long-term balancing selection in shaping venom evolution. We also detect rapid decay of linkage disequilibrium due to high recombination rates in venom regions, suggesting that venom genes have reduced selective interference with nearby loci, including other venom paralogues. Our results provide an example of long-term balancing selection that drives trans-species polymorphism and help to explain how snake venom keeps pace with prey resistance.

Rapid Evolutionary Adaptation in Response to Selection on Quantitative Traits.

Evolutionary adaptation after sudden environmental changes can occur very rapidly. The mechanisms facilitating rapid adaptation range from strong positive directional selection leading to large shifts in the allele frequencies at a few loci (selective sweeps) to polygenic selection causing small changes in allele frequencies at many loci. In addition, combinations of these two extreme mechanisms may also result in fast evolution. In recent years, following reports of new case studies of rapid adaptation, population genetic models have been proposed to explain these observations. In these models, the role of the major selective forces (positive directional and stabilizing selection) is highlighted as well as the genetic architecture of quantitative traits. Furthermore, the factors limiting the speed of adaptation are analyzed, in particular, the effects of random genetic drift and demography due to finite population size.

Molecular Evolution of Ecological Specialisation: Genomic Insights from the Diversification of Murine Rodents.

Adaptive radiations are characterized by the diversification and ecological differentiation of species, and replicated cases of this process provide natural experiments for understanding the repeatability and pace of molecular evolution. During adaptive radiation, genes related to ecological specialization may be subject to recurrent positive directional selection. However, it is not clear to what extent patterns of lineage-specific ecological specialization (including phenotypic convergence) are correlated with shared signatures of molecular evolution. To test this, we sequenced whole exomes from a phylogenetically dispersed sample of 38 murine rodent species, a group characterized by multiple, nested adaptive radiations comprising extensive ecological and phenotypic diversity. We found that genes associated with immunity, reproduction, diet, digestion, and taste have been subject to pervasive positive selection during the diversification of murine rodents. We also found a significant correlation between genome-wide positive selection and dietary specialization, with a higher proportion of positively selected codon sites in derived dietary forms (i.e., carnivores and herbivores) than in ancestral forms (i.e., omnivores). Despite striking convergent evolution of skull morphology and dentition in two distantly related worm-eating specialists, we did not detect more genes with shared signatures of positive or relaxed selection than in a nonconvergent species comparison. Although a small number of the genes we detected can be incidentally linked to craniofacial morphology or diet, protein-coding regions are unlikely to be the primary genetic basis of this complex convergent phenotype. Our results suggest a link between positive selection and derived ecological phenotypes, and highlight specific genes and general functional categories that may have played an integral role in the extensive and rapid diversification of murine rodents.

Bigger is not always better: Viability selection on body mass varies across life stages in a hibernating mammal.

Body mass is often viewed as a proxy of past access to resources and of future survival and reproductive success. Links between body mass and survival or reproduction are, however, likely to differ between age classes and sexes. Remarkably, this is rarely taken into account in selection analyses. Selection on body mass is likely to be the primary target accounting for juvenile survival until reproduction but may weaken after recruitment. Males and females also often differ in how they use resources for reproduction and survival. Using a long‐term study on body mass and annual survival in yellow‐bellied marmots (Marmota flaviventer), we show that body mass was under stabilizing viability selection in the first years of life, before recruitment, which changed to positive directional selection as age increased and animals matured. We found no evidence that viability selection across age classes on body mass differed between sexes. By investigating the link between running speed and body mass, we show that the capacity to escape predators was not consistent across age classes and followed a quadratic relationship at young ages only. Overall, our results indicate that mature age classes exhibit traditional patterns of positive viability selection on body mass, as expected in a hibernating mammal, but that mass in the first years of life is subjected to stabilizing selection which may come from additional predation pressures that negate the benefits of the largest body masses. Our study highlights the importance to disentangle selection pressures on traits across critical age (or life) classes.

Dissecting dynamics and differences of selective pressures in the evolution of human pigmentation.

ABSTRACTHuman pigmentation is a highly diverse and complex trait among populations and has drawn particular attention from both academic and non-academic investigators for thousands of years. Previous studies detected selection signals in several human pigmentation genes, but few studies have integrated contribution from multiple genes to the evolution of human pigmentation. Moreover, none has quantified selective pressures on human pigmentation over epochs and between populations. Here, we dissect dynamics and differences of selective pressures during different periods and between distinct populations with new approaches. We use genotype data of 19 genes associated with human pigmentation from 17 publicly available datasets and obtain data for 2346 individuals of six representative population groups from across the world. Our results quantify the strength of natural selection on light pigmentation not only in modern Europeans (0.0259/generation) but also in proto-Eurasians (0.00650/generation). Our results also suggest that several derived alleles associated with human dark pigmentation may be under positive directional selection in some African populations. Our study provides the first attempt to quantitatively investigate the dynamics of selective pressures during different time periods in the evolution of human pigmentation.This article has an associated First Person interview with the first author of the article.

Social environment: Trait, context and agent for selection in a meta‐population

In Focus: Formica, V., Donald, H., Marti, H., Irgebay, Z., Brodie III, E. Social network position experiences more variable selection than weaponry in wild subpopulations of forked fungus beetles. Journal of Animal Ecology, 90, 168-182, https://doi.org/10.1111/1365-2656.13322. That social network traits can exhibit consistent-individual differences among individuals and confer a fitness benefit or cost is increasingly well-established. However, how selection-natural or sexual-affects those social traits and at what scale remains an open question. In this Special Feature, Formica and colleagues employ a meta-population of forked fungus beetles to test and contrast whether sexual selection on social network traits contrasted to morphological traits occurs at the local (soft) or global (hard) scales. The authors demonstrate that morphological traits are largely under hard directional positive selection, whereas social traits are under soft and variable selection. The findings are compelling and raise interesting discussion of multi-level selection and the evolution of social traits in a meta-population.

The Potential for Genotype-by-Environment Interactions to Maintain Genetic Variation in a Model Legume–Rhizobia Mutualism

The maintenance of genetic variation in mutualism-related traits is key for understanding mutualism evolution, yet the mechanisms maintaining variation remain unclear. We asked whether genotype-by-environment (G×E) interaction is a potential mechanism maintaining variation in the model legume–rhizobia system, Medicago truncatula–Ensifer meliloti. We planted 50 legume genotypes in a greenhouse under ambient light and shade to reflect reduced carbon availability for plants. We found an expected reduction under shaded conditions for plant performance traits, such as leaf number, aboveground and belowground biomass, and a mutualism-related trait, nodule number. We also found G×E for nodule number, with ∼83% of this interaction due to shifts in genotype fitness rank order across light environments, coupled with strong positive directional selection on nodule number regardless of light environment. Our results suggest that G×E can maintain genetic variation in a mutualism-related trait that is under consistent positive directional selection across light environments.