Signatures of local adaptation in lowland and highland teosintes from whole‐genome sequencing of pooled samples

Spatially varying selection triggers differential adaptation of local populations. Here, we mined the determinants of local adaptation at the genomewide scale in the two closest maize wild relatives, the teosintes Zea mays ssp parviglumis and ssp. mexicana. We sequenced 120 individuals from six populations: two lowland, two intermediate and two highland populations sampled along two altitudinal gradients. We detected 8 479 581 single nucleotide polymorphisms (SNPs) covered in the six populations with an average sequencing depth per site per population ranging from 17.0× to 32.2×. Population diversity varied from 0.10 to 0.15, and linkage disequilibrium decayed very rapidly. We combined two differentiation‐based methods, and correlation of allele frequencies with environmental variables to detect outlier SNPs. Outlier SNPs displayed significant clustering. From clusters, we identified 47 candidate regions. We further modified a haplotype‐based method to incorporate genotype uncertainties in haplotype calling, and applied it to candidate regions. We retrieved evidence for selection at the haplotype level in 53% of our candidate regions, and in 70% of the cases the same haplotype was selected in the two lowland or the two highland populations. We recovered a candidate region located within a previously characterized inversion on chromosome 1. We found evidence of a soft sweep at a locus involved in leaf macrohair variation. Finally, our results revealed frequent colocalization between our candidate regions and loci involved in the variation of traits associated with plant–soil interactions such as root morphology, aluminium and low phosphorus tolerance. Soil therefore appears to be a major driver of local adaptation in teosintes.     

Divergence with gene flow is driven by local adaptation to temperature and soil phosphorus concentration in teosinte subspecies (Zea mays parviglumis and Zea mays mexicana)

Patterns of genomic divergence between hybridizing taxa can be heterogeneous along the genome. Both differential introgression and local adaptation may contribute to this pattern. Here, we analysed two teosinte subspecies, Zea mays ssp. parviglumis and ssp. mexicana, to test whether their divergence has occurred in the face of gene flow and to infer which environmental variables have been important drivers of their ecological differentiation. We generated 9,780 DArTseqTM SNPs for 47 populations, and used an additional data set containing 33,454 MaizeSNP50 SNPs for 49 populations. With these data, we inferred features of demographic history and performed genome wide scans to determine the number of outlier SNPs associated with climate and soil variables. The two data sets indicate that divergence has occurred or been maintained despite continuous gene flow and/or secondary contact. Most of the significant SNP associations were to temperature and to phosphorus concentration in the soil. A large proportion of these candidate SNPs were located in regions of high differentiation that had been identified previously as putative inversions. We therefore propose that genomic differentiation in teosintes has occurred by a process of adaptive divergence, with putative inversions contributing to reduced gene flow between locally adapted populations.     

Clock gene polymorphism,migratory behaviour and geographic distribution: a comparative study of trans‐Saharan migratory birds

Migratory behaviour is controlled by endogenous circannual rhythms that are synchronized by external cues, such as photoperiod. Investigations on the genetic basis of circannual rhythmicity in vertebrates have highlighted that variation at candidate ‘circadian clock’ genes may play a major role in regulating photoperiodic responses and timing of life cycle events, such as reproduction and migration. In this comparative study of 23 trans‐Saharan migratory bird species, we investigated the relationships between species‐level genetic variation at two candidate genes, Clock and Adcyap1, and species’ traits related to migration and geographic distribution, including timing of spring migration across the Mediterranean Sea, migration distance and breeding latitude. Consistently with previous evidence showing latitudinal clines in ‘circadian clock’ genotype frequencies, Clock allele size increased with breeding latitude across species. However, early‐ and late‐migrating species had similar Clock allele size. Species migrating over longer distances, showing delayed spring migration and smaller phenotypic variance in spring migration timing, had significantly reduced Clock (but not Adcyap1) gene diversity. Phylogenetic confirmatory path analysis suggested that migration date and distance were the most important variables directly affecting Clock gene diversity. Hence, our study supports the hypothesis that Clock allele size increases poleward as a consequence of adaptation to the photoperiodic regime of the breeding areas. Moreover, we show that long‐distance migration is associated with lower Clock diversity, coherently with strong stabilizing selection acting on timing of life cycle events in long‐distance migratory species, likely resulting from the time constraints imposed by late spring migration.     

Environmental gradients shape the genetic structure of two medicinal Salvia species in Jordan

• Environmental gradients, and particularly climatic variables, exert a strong influence on plant distribution and, potentially, population genetic diversity and differentiation. Differences in water availability can cause among‐population variation in ecological processes and can thus interrupt populations’ connectivity and isolate them environmentally. The present study examines the effect of environmental heterogeneity on plant populations due to environmental isolation unrelated to geographic distance.
• Using AFLP markers, we analyzed genetic diversity and differentiation among 12 Salvia spinosa populations and 13 Salvia syriaca populations from three phytogeographical regions (Mediterranean, Irano‐Turanian and Saharo‐Arabian) representing the extent of the species’ geographic range in Jordan. Differences in geographic location and climate were considered in the analyses.
• For both species, flowering phenology varied among populations and regions. Irano‐Turanian and Saharo‐Arabian populations had higher genetic diversity than Mediterranean populations, and genetic diversity increased significantly with increasing temperature. Genetic diversity in Salvia syriaca was affected by population size, while genetic diversity responded to drought in S. spinosa. For both species, high levels of genetic differentiation were found as well as two well‐supported phytogeographical groups of populations, with Mediterranean populations clustering in one group and the Irano‐Turanian and Saharo‐Arabian populations in another. Genetic distance was significantly correlated to environmental distance, but not to geographic distance.
• Our data indicate that populations from moist vs. arid environments are environmentally isolated, where environmental gradients affect their flowering phenology, limit gene flow and shape their genetic structure. We conclude that environmental heterogeneity may act as driver for the observed variation in genetic diversity.

     

Higher expression of induced defenses in teosintes (Zea spp.) is correlated with greater resistance to fall armyworm,Spodoptera frugiperda

Selection for plant traits important for agriculture can come at a high cost to plant defenses. While selecting for increased growth rate and yield, domestication and subsequent breeding may lead to weakened defenses and greater susceptibility of plants to herbivores. We tested whether expression of defense genes differed among maize, Zea mays ssp. mays L. (Poaceae), and its wild relatives Zea mays ssp. parviglumis Iltis & Doebley and Zea diploperennis Iltis et al. We used two populations of Z. mays ssp. parviglumis: one expected to express high levels of an herbivore resistance gene, wound‐inducible protein (wip1), and another expected to have low expression of wip1. To test whether maize and wild Zea differed in induction of defenses against Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), we quantified expression of several genes involved in plant defense: wip1, maize protease inhibitor (mpi), pathogenesis‐related protein (PR‐1), and chitinase. Moreover, we compared growth, development, and survival of caterpillars on maize and wild Zea plants. We found that maize expressed low levels of all but one of the genes when attacked by caterpillars, whereas the wild relatives of maize expressed induced defense genes at high levels. Expression of wip1, in particular, was much greater in the Z. mays ssp. parviglumis population that we expected to naturally express high levels of wip1, with expression levels 29‐fold higher than in herbivore‐free plants. Elevated expression of defenses in wild plants was correlated with higher resistance to caterpillars. Larvae were 15–20% smaller on wild Zea compared with maize, developed 20% slower, and only 22% of them survived to pupation on Z. mays ssp. parviglumis with high levels of wip1. Our results suggest that domestication has inadvertently reduced the resistance of maize, and it is likely that expression of wip1 and other genes associated with defenses play an important role in this reduction in resistance.     

Population genetic structure of a specialist leafhopper on Zea: likely anthropogenic and ecological determinants of gene flow

Corn leafhopper, Dalbulus maidis DeLong & Wolcott (Hemiptera: Cicadellidae), is a specialist herbivore on the genus Zea (Poaceae). The genera Dalbulus and Zea evolved in central Mexico. We sought to determine whether population genetic structuring is prevalent in corn leafhoppers inhabiting three of its host plants: (1) the highland species perennial teosinte (Zea diploperennis Iltis, Doebley & Guzman), (2) the mid‐ to lowland‐species Balsas teosinte (Zea mays ssp. parviglumis Iltis & Doebley), and (3) the ubiquitous domesticated maize (Zea mays ssp. mays L.). We used amplified fragment length polymorphisms to detect population structuring and genetic differentiation among corn leafhoppers on the three host plants in western‐central and ‐northern Mexico. Our results showed that corn leafhopper in Mexico is composed of at least two genetically discrete populations: an ‘Itinerant’ population associated with the annual hosts maize and Balsas teosinte, which appears to be widely distributed in Mexico, and a ‘Las Joyas’ population restricted to perennial teosinte and confined to a small mountain range (Sierra de Manantlán) in western‐central Mexico. Our results further suggested that population structuring is not due to isolation by distance or landscape features: Las Joyas and Itinerant corn leafhopper populations are genetically distinct despite their geographic proximity (ca. 4 km), whereas Itinerant corn leafhoppers separated by hundreds of kilometers (>800 km), mountain ranges, and a maritime corridor (Sea of Cortez) are not genetically distinct. Based on our results and on published ethnohistorical and archaeological data, we propose pre‐Columbian and modern scenarios, including likely ecological and anthropogenic influences, in which the observed genetic population structuring of corn leafhopper could have originated and could be maintained. Also, we hypothesize that after evolving on the lowland Balsas teosinte, corn leafhopper expanded its host range to include maize and then the highland perennial teosinte, following the domestication and spread of maize within the last 9 000 years.     

TAXONOMY OF ZEA (GRAMINEAE). II. SUBSPECIFIC CATEGORIES IN THE ZEA MAYS COMPLEX AND A GENERIC SYNOPSIS

A compromise classification of the genus Zea, reflecting both phylogeny and practical needs, recognizes six taxa, as follows: Section Luxuriantes : Zea perennis. Zea diploperennis, Zea luxurians. Section Zea : Zea mays ssp. mexicana (Neo-volcanic Plateau), Zea mays ssp. parviglumis Iltis & Doebley ssp. n. var. parviglumis (Rio Balsas drainage, Pacific slope from Guerrero to Jalisco), Zea mexicana ssp. parviglumis var. huehuetenangensis Iltis & Doebley var. n. (Pacific slope, western Guatemala, Prov. Huehuetenango), Zea mays ssp. mays. The new subspecies is distinguished by smaller spikelets and rachis joints, the varieties by different habitats, blooming dates and their genetic behavior in relation to cultivated Zea mays. Zea mays ssp. mexicana is the ancestor of corn.     

Fine scale genetic structure in the wild ancestor of maize (Zea mays ssp. parviglumis)

Analysis of fine scale genetic structure in continuous populations of outcrossing plant species has traditionally been limited by the availability of sufficient markers. We used a set of 468 SNPs to characterize fine‐scale genetic structure within and between two dense stands of the wild ancestor of maize, teosinte (Zea mays ssp. parviglumis). Our analyses confirmed that teosinte is highly outcrossing and showed little population structure over short distances. We found that the two populations were clearly genetically differentiated, although the actual level of differentiation was low. Spatial autocorrelation of relatedness was observed within both sites but was somewhat stronger in one of the populations. Using principal component analysis, we found evidence for significant local differentiation in the population with stronger spatial autocorrelation. This differentiation was associated with pronounced shifts in the first two principal components along the field. These shifts corresponded to changes in allele frequencies, potentially due to local topographical features. There was little evidence for selection at individual loci as a contributing factor to differentiation. Our results demonstrate that significant local differentiation may, but need not, co‐occur with spatial autocorrelation of relatedness. The present study represents one of the most detailed analyses of local genetic structure to date and provides a benchmark for future studies dealing with fine scale patterns of genetic diversity in natural plant populations.     

Genetic Analysis of Central Carbon Metabolism Unveils an Amino Acid Substitution That Alters Maize NAD-Dependent Isocitrate Dehydrogenase Activity

Background

Central carbon metabolism (CCM) is a fundamental component of life. The participating genes and enzymes are thought to be structurally and functionally conserved across and within species. Association mapping utilizes a rich history of mutation and recombination to achieve high resolution mapping. Therefore, applying association mapping in maize (Zea mays ssp. mays), the most diverse model crop species, to study the genetics of CCM is a particularly attractive system.

Methodology/Principal Findings

We used a maize diversity panel to test the CCM functional conservation. We found heritable variation in enzyme activity for every enzyme tested. One of these enzymes was the NAD-dependent isocitrate dehydrogenase (IDH, E.C. 1.1.1.41), in which we identified a novel amino-acid substitution in a phylogenetically conserved site. Using candidate gene association mapping, we identified that this non-synonymous polymorphism was associated with IDH activity variation. The proposed mechanism for the IDH activity variation includes additional components regulating protein level. With the comparison of sequences from maize and teosinte (Zea mays ssp. Parviglumis), the maize wild ancestor, we found that some CCM genes had also been targeted for selection during maize domestication.

Conclusions/Significance

Our results demonstrate the efficacy of association mapping for dissecting natural variation in primary metabolic pathways. The considerable genetic diversity observed in maize CCM genes underlies heritable phenotypic variation in enzyme activities and can be useful to identify putative functional sites.     

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines

Accurately detecting signatures of local adaptation using genetic‐environment associations (GEAs) requires controlling for neutral patterns of population structure to reduce the risk of false positives. However, a high degree of collinearity between climatic gradients and neutral population structure can greatly reduce power, and the performance of GEA methods in such case is rarely evaluated in empirical studies. In this study, we attempted to disentangle the effects of local adaptation and isolation by environment (IBE) from those of isolation by distance (IBD) and isolation by colonization from glacial refugia (IBC) using range‐wide samples in two white pine species. For this, SNPs from 168 genes, including 52 candidate genes for growth and phenology, were genotyped in 133 and 61 populations of Pinus strobus and P. monticola, respectively. For P. strobus and using all 153 SNPs, climate (IBE) did not significantly explained among‐population variation when controlling for IBD and IBC in redundancy analyses (RDAs). However, 26 SNPs were significantly associated with climate in single‐locus GEA analyses (Bayenv2 and LFMM), suggesting that local adaptation took place in the presence of high gene flow. For P. monticola, we found no evidence of IBE using RDAs and weaker signatures of local adaptation using GEA and F_ST outlier tests, consistent with adaptation via phenotypic plasticity. In both species, the majority of the explained among‐population variation (69 to 96%) could not be partitioned between the effects of IBE, IBD, and IBC. GEA methods can account differently for this confounded variation, and this could explain the small overlap of SNPs detected between Bayenv2 and LFMM. Our study illustrates the inherent difficulty of taking into account neutral structure in natural populations and the importance of sampling designs that maximize climatic variation, while minimizing collinearity between climatic gradients and neutral structure.     

Genomewide scan for adaptive differentiation along altitudinal gradient in the Andrew's toad Bufo andrewsi

Recent studies of humans, dogs and rodents have started to discover the genetic underpinnings of high altitude adaptations, yet amphibians have received little attention in this respect. To identify possible signatures of adaptation to altitude, we performed a genome scan of 15 557 single nucleotide polymorphisms (SNPs) obtained with restriction site‐associated DNA sequencing of pooled samples from 11 populations of Andrew's toad (Bufo andrewsi) from the edge of the Tibetan Plateau, spanning an altitudinal gradient from 1690 to 2768 m.a.s.l. We discovered significant geographic differentiation among all sites, with an average F_ST = 0.023 across all SNPs. Apart from clear patterns of isolation by distance, we discovered numerous outlier SNPs showing strong associations with variation in altitude (1394 SNPs), average annual temperature (1859 SNPs) or both (1051 SNPs). Levels and patterns of genetic differentiation in these SNPs were consistent with the hypothesis that they have been subject to directional selection and reflect adaptation to altitudinal variation among the study sites. Genes with footprints of selection were significantly enriched in binding and metabolic processes. Several genes potentially related to high altitude adaptation were identified, although the identity and functional significance of most genomic targets of selection remain unknown. In general, the results provide genomic support for results of earlier common garden and low coverage genetic studies that have uncovered substantial adaptive differentiation along altitudinal and latitudinal gradients in amphibians.     

A Scanning Electron Microscopy Survey of Some Maydeae Pollen

Scanning electron microscopy was used to examine the wall sculpturing of pollen from Zea mays L. ssp. mays (maize), Zea mays ssp. mexicana (Schrad.) Iltis (teosinte), Zea perennis (Hitchc.) Reeves and Mangelsdorf (perennial teosinte), and two species of Tripsacum L. The Zea taxa are shown to possess similar pollen types, with spinules scattered regularly over the exine surface. Tripsacum exhibits a distinctly reticuloid pattern, with spinules clumped into isolated lacunae. Hybrids between Zea and Tripsacum are either intermediate in exine pattern or similar to Tripsacum, depending on the genome combination.     

Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations

Landscape genomics studies focus on identifying candidate genes under selection via spatial variation in abiotic environmental variables, but rarely by biotic factors (i.e., disease). The Tasmanian devil (Sarcophilus harrisii) is found only on the environmentally heterogeneous island of Tasmania and is threatened with extinction by a transmissible cancer, devil facial tumor disease (DFTD). Devils persist in regions of long-term infection despite epidemiological model predictions of species’ extinction, suggesting possible adaptation to DFTD. Here, we test the extent to which spatial variation and genetic diversity are associated with the abiotic environment (i.e., climatic variables, elevation, vegetation cover) and/or DFTD. We employ genetic-environment association analyses using 6886 SNPs from 3287 individuals sampled pre- and post-disease arrival across the devil's geographic range. Pre-disease, we find significant correlations of allele frequencies with environmental variables, including 365 unique loci linked to 71 genes, suggesting local adaptation to abiotic environment. The majority of candidate loci detected pre-DFTD are not detected post-DFTD arrival. Several post-DFTD candidate loci are associated with disease prevalence and were in linkage disequilibrium with genes involved in tumor suppression and immune response. Loss of apparent signal of abiotic local adaptation post-disease suggests swamping by strong selection resulting from the rapid onset of DFTD.     

Selection and localised genetic structure in the threatened Manauense Harlequin Frog (Bufonidae: Atelopus manauensis)

Knowledge of genome-wide variation and the processes influencing gene flow are critical to managing threatened species. Here, we characterise genetic diversity and the environmental features associated with connectivity for a narrowly distributed and threatened Amazonian frog, Atelopus manauensis. We sampled 94 individuals throughout the upper, middle and lower courses from each of the five major rivers covering the species’ known geographic range and genotyped each individual at 3859 single nucleotide polymorphisms (SNPs). Genetic variation was significantly subdivided into six groups, each mostly containing individuals sampled within the same major river system. The genetic distances among these groups increased with geographic distance, and open forests and the extremities of the altitude gradient were associated with less genetic connectivity. Using F_ST outlier approaches and environmental association analyses, we identified SNPs indicative of localised adaptation, with 28 SNPs significantly associated with forest biomass and altitude. Evidence of divergent selection among the six genetic clusters suggests the presence of six Evolutionary Significant Units (ESUs). Overall, the ESUs were characterized by low contemporary effective population sizes (N_E?<?100) suggesting that genetic variation will be lost by random genetic drift. We demonstrate surprisingly high levels of divergence across the limited distribution of A. manauensis and suggest that each of the six adaptively divergent lineages be considered in conservation planning.

     

Genetic Variation in Hippophae rhamnoides ssp. sinensis (Elaeagnaceae) Revealed by RAPD Markers

Hippophae rhamnoides ssp. sinensis is endemic to China, and it is a dioecious, outcrossing plant. Although many studies have been undertaken mainly on its agricultural, nutritional, medical, and ornamental value, little is known about its population genetics. This study uses random amplified polymorphic DNA to investigate the genetic diversity and population genetic structure of 13 natural populations of the subspecies sinensis. Fifteen primers amplified 107 reproducible bands, with 95 (88.79%) being polymorphic. The gene diversity within population was 0.168, considerably lower than that of tree species and most perennial, outcrossing species, but higher than that of annual or short-lived, selfing species. The Gst value showed that 18.3% of the total genetic variation resided among populations, a little lower than that of outcrossing species. The present results are quite similar to those previously reported in another subspecies, H ssp. . rhamnoides rhamnoides. The low genetic differentiation among populations in ssp. sinensis may be attributed to the long-distance dispersal of seeds facilitated by birds, in addition to its characteristics of outcrossing, wind pollination, and widespread distribution. No association between genetic distance and geographical distribution was found. The population relationships revealed by the UPGMA dendrogram parallel this result, in that genetic distance did not increase with geographic separation. This pattern of population differentiation may imply the adaptation of ssp. s populations to the local environment, given that its habitats vary greatly across its distribution.     

Exploring genomic variation associated with drought stress in Picea mariana populations

Predicted increases in drought and heat stress will likely induce shifts in species bioclimatic envelopes. Genetic variants adapted to water limitation may prove pivotal for species response under scenarios of increasing drought. In this study, we aimed to explore this hypothesis by investigating genetic variation in 16 populations of black spruce (Picea mariana) in relation to climate variables in Alaska. A total of 520 single nucleotide polymorphisms (SNPs) were genotyped for 158 trees sampled from areas of contrasting climate regimes. We used multivariate and univariate genotype‐by‐environment approaches along with available gene annotations to investigate the relationship between climate and genetic variation among sampled populations. Nine SNPs were identified as having a significant association with climate, of which five were related to drought stress response. Outlier SNPs with respect to the overall environment were significantly overrepresented for several biological functions relevant for coping with variable hydric regimes, including osmotic stress response. This genomic imprint is consistent with local adaptation of black spruce to drought stress. These results suggest that natural selection acting on standing variation prompts local adaptation in forest stands facing water limitation. Improved understanding of possible adaptive responses could inform our projections about future forest dynamics and help prioritize populations that harbor valuable genetic diversity for conservation.     

Lack of genetic isolation by distance,similar genetic structuring but different demographic histories in a fig‐pollinating wasp mutualism

Historical abiotic factors such as climatic oscillations and extreme climatic events as well as biotic factors have shaped the structuring of species' genetic diversity. In obligate species‐specific mutualisms, the biogeographic histories of the interacting species are tightly linked. This could be particularly true for nuclear genes in the Ficus‐pollinating wasp mutualistic association as the insects disperse pollen from their natal tree. In this study, we compare spatial genetic structure of plant and pollinator for the Ficus hirta–Valisia javana association throughout southeast China including Hainan Island, for both nuclear and cytoplasmic markers. We show that dispersal of the insect leads to plant and insect presenting similar signatures of lack of genetic isolation by distance for nuclear genes on the continent over a distance of 1000 km. But we also show that the demographic histories of plant and insect are strikingly different. This is in agreement with extreme climatic events leading to transient regional extinctions of the insects, associated with local survival of the plants. We also observe evidence of genetic differentiation for both wasps and fig‐tree between the continent and Hainan Island, although the Qiongzhou Strait is only on average 30 km wide, suggesting that geographic isolation by itself has not been sufficient to generate this differentiation. Hence, our results suggest that in highly dispersive mutualistic systems, isolation‐by‐dispersal limitation across a geographic barrier could be supplemented by isolation by adaptation, and maybe by coevolution, allowing further genetic divergence. In such systems, species may frequently be composed of a single population.     

A 34K SNP genotyping array for Populus trichocarpa: Design,application to the study of natural populations and transferability to other Populus species

Genetic mapping of quantitative traits requires genotypic data for large numbers of markers in many individuals. For such studies, the use of large single nucleotide polymorphism (SNP) genotyping arrays still offers the most cost‐effective solution. Herein we report on the design and performance of a SNP genotyping array for Populus trichocarpa (black cottonwood). This genotyping array was designed with SNPs pre‐ascertained in 34 wild accessions covering most of the species latitudinal range. We adopted a candidate gene approach to the array design that resulted in the selection of 34 131 SNPs, the majority of which are located in, or within 2 kb of, 3543 candidate genes. A subset of the SNPs on the array (539) was selected based on patterns of variation among the SNP discovery accessions. We show that more than 95% of the loci produce high quality genotypes and that the genotyping error rate for these is likely below 2%. We demonstrate that even among small numbers of samples (n = 10) from local populations over 84% of loci are polymorphic. We also tested the applicability of the array to other species in the genus and found that the number of polymorphic loci decreases rapidly with genetic distance, with the largest numbers detected in other species in section Tacamahaca. Finally, we provide evidence for the utility of the array to address evolutionary questions such as intraspecific studies of genetic differentiation, species assignment and the detection of natural hybrids.     

Adaptive phenotypic divergence in an annual grass differs across biotic contexts*

Climate is a powerful force shaping adaptation within species, yet adaptation to climate occurs against a biotic background: species interactions can filter fitness consequences of genetic variation by altering phenotypic expression of genotypes. We investigated this process using populations of teosinte, a wild annual grass related to maize (Zea mays ssp. mexicana), sampling plants from 10 sites along an elevational gradient as well as rhizosphere biota from three of those sites. We grew half‐sibling teosinte families in each biota to test whether trait divergence among teosinte populations reflects adaptation or drift, and whether rhizosphere biota affect expression of diverged traits. We further assayed the influence of rhizosphere biota on contemporary additive genetic variation. We found that adaptation across environment shaped divergence of some traits, particularly flowering time and root biomass. We also observed that different rhizosphere biota shifted expressed values of these traits within teosinte populations and families and altered within‐population genetic variance and covariance. In sum, our results imply that changes in trait expression and covariance elicited by rhizosphere communities could have played a historical role in teosinte adaptation to environments and that they are likely to play a role in the response to future selection.