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Data from: Geographically structured genetic variation in the Medicago lupulina – Ensifer mutualism
Harrison, Tia L.; Wood, Corlett Wolfe; Heath, Katy D.; Stinchcombe, John R. — 2017-04-12 Gene flow between genetically differentiated populations can maintain variation in species interactions, especially when population structure is congruent between interacting species. However, large-scale empirical comparisons of the population structure of interacting species are rare, particularly in positive interspecific interactions (mutualisms). One agriculturally and ecologically important mutualism is the partnership between legume plants and rhizobia. Through characterizing and comparing the population genomic structure of the legume Medicago lupulina and two rhizobial species (Ensifer medicae and E. meliloti), we explored the spatial scale of population differentiation between interacting partners in their introduced range in North America. We found high proportions of E. meliloti in southeastern populations and high proportions of E. medicae in northwestern populations. Medicago lupulina and the Ensifer genus showed similar patterns of spatial genetic structure (isolation by distance). However, we detected no evidence of isolation by distance or population structure within either species of bacteria. Genome-wide nucleotide diversity within each of the two Ensifer species was low, suggesting limited introduction of strains, founder events, or severe bottlenecks. Our results suggest that there is potential for geographically structured coevolution between M. lupulina and the Ensifer genus, but not between M. lupulina and either Ensifer species.
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Data from: Evaluating population genomic candidate genes underlying flowering time in Arabidopsis thaliana using T-DNA insertion lines
Chong, Veronica K.; Stinchcombe, John R. — 2019-05-03 Population genomic scans have emerged as a powerful tool to detect regions of the genome that are potential targets of selection. Despite the success of genomic scans in identifying novel lists of loci potentially underlying adaptation, few studies proceed to validate the function of these candidate genes. In this study, we used T-DNA insertion lines to evaluate the effects of 27 candidate genes on flowering time in North American accessions of Arabidopsis thaliana. We compared the flowering time of T-DNA insertion lines which knock-out the function of a candidate gene obtained from population genomic studies to a wildtype under long- and short-day conditions. We also did the same for a collection of randomly chosen genes that had not been identified as candidates. We validated the well-known effect of long-day conditions in accelerating flowering time and found that gene disruption caused by insertional mutagenesis tends to delay flowering. Surprisingly, we found that knockouts in random genes were just as likely to produce significant phenotypic effects as knockouts in candidate genes. T-DNA insertions at a handful of candidate genes that had previously been identified as outlier loci showed significant delays in flowering time under both long and short days, suggesting that they are promising candidates for future investigation.
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Data from: Quantitative genetic variance and multivariate clines in the Ivyleaf morning glory, Ipomoea hederacea
Stock, Amanda J.; Campitelli, Brandon E.; Stinchcombe, John R. — 2015-05-27 Clinal variation is commonly interpreted as evidence of adaptive differentiation, although clines can also be produced by stochastic forces. Understanding whether clines are adaptive therefore requires comparing clinal variation to background patterns of genetic differentiation at presumably neutral markers. Although this approach has frequently been applied to single traits at a time, we have comparatively fewer examples of how multiple correlated traits vary clinally. Here, we characterize multivariate clines in the Ivyleaf morning glory, examining how suites of traits vary with latitude, with the goal of testing for divergence in trait means that would indicate past evolutionary responses. We couple this with analysis of genetic variance in clinally varying traits in 20 populations to test whether past evolutionary responses have depleted genetic variance, or whether genetic variance declines approaching the range margin. We find evidence of clinal differentiation in five quantitative traits, with little evidence of isolation by distance at neutral loci that would suggest non-adaptive or stochastic mechanisms. Within and across populations, the traits that contribute most to population differentiation and clinal trends in the multivariate phenotype are genetically variable as well, suggesting that a lack of genetic variance will not cause absolute evolutionary constraints. Our data are broadly consistent theoretical predictions of polygenic clines in response to shallow environmental gradients. Ecologically, our results are consistent with past findings of natural selection on flowering phenology, presumably due to season-length variation across the range.
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Data from: Individual chambers for controlling crosses in wind pollinated plants
McGoey, Brechann V.; Janik, Rafal; Stinchcombe, John R. — 2017-12-22 Controlled plant crosses can be an important component of studies ranging from applied artificial selection research to evolutionary investigations of heritability. Controlling pollen flow is especially challenging for wind-pollinated species. We developed a system capable of housing hundreds of ragweed (Ambrosia artemisiifolia) plants simultaneously in individual chambers through the reproductive portion of their lifecycles. We confirmed that our chambers allowed us to control pollen movement and paternity of offspring using unpollinated isolated plants and microsatellite markers for parents and their putative offspring. Our system had per plant costs and efficacy superior to pollen bags used in past studies for wind pollinated plants. Our chamber system is flexible, affordable, and widely applicable to other wind pollinated plants, or applications in which the distribution of highly mobile species, individuals, spores, or gametes must be controlled.
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Data from: A note on measuring natural selection on principal component scores
Chong, Veronica K.; Fung, Hannah F.; Stinchcombe, John R. — 2018-05-29 Measuring natural selection through the use of multiple regression has transformed our understanding of selection, although the methods used remain sensitive to the effects of multicollinearity due to highly correlated traits. While measuring selection on principal component scores is an apparent solution to this challenge, this approach has been heavily criticized due to difficulties in interpretation and relating PC axes back to the original traits. We describe and illustrate how to transform selection gradients for PC scores back into selection gradients for the original traits, addressing issues of multicollinearity and biological interpretation. In addition to reducing multicollinearity, we suggest that this method may have promise for measuring selection on high-dimensional data such as volatiles or gene expression traits. We demonstrate this approach with empirical data and examples from the literature, highlighting how selection estimates for PC scores can be interpreted while reducing the consequences of multicollinearity https://creativecommons.org/publicdomain/zero/1.0/
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Data from: Genetic conflict with a parasitic nematode disrupts the legume-rhizobia mutualism
Wood, Corlett W.; Pilkington, Bonnie L.; Vaidya, Priya; Biel, Caroline; Stinchcombe, John R. — 2018-03-12 Genetic variation for partner quality in mutualisms is an evolutionary paradox. One possible resolution to this puzzle is that there is a tradeoff between partner quality and other fitness-related traits. Here, we tested whether a susceptibility to parasitism is one such tradeoff in the mutualism between legumes and nitrogen-fixing bacteria (rhizobia). We performed two greenhouse experiments with the legume Medicago truncatula. In the first, we inoculated each plant with the rhizobia Ensifer meliloti and with one of 40 genotypes of the parasitic root-knot nematode Meloidogyne hapla. In the second experiment, we inoculated all plants with rhizobia and half of the plants with a genetically variable population of nematodes. Using the number of nematode galls as a proxy for infection severity, we found that plant genotypes differed in susceptibility to nematode infection, and nematode genotypes differed in infectivity. Second, we showed that there was a genetic correlation between the number of mutualistic structures formed by rhizobia (nodules) and the number of parasitic structures formed by nematodes (galls). Finally, we found that nematodes disrupt the rhizobia mutualism: nematode-infected plants formed fewer nodules and had less nodule biomass than uninfected plants. Our results demonstrate that there is genetic conflict between attracting rhizobia and repelling nematodes in Medicago. If genetic conflict with parasitism is a general feature of mutualism, it could account for the maintenance of genetic variation in partner quality and influence the evolutionary dynamics of positive species interactions.
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Data from: Quantitative genetic variance in experimental fly populations evolving with or without environmental heterogeneity
Huang, Yuheng; Stinchcombe, John R.; Agrawal, Aneil F. — 2015-09-07 Heterogeneous environments are typically expected to maintain more genetic variation in fitness within populations than homogeneous environments. However, the accuracy of this claim depends on the form of heterogeneity as well as the genetic basis of fitness traits and how similar the assay environment is to the environment of past selection. Here we measure quantitative genetic variance for three traits important for fitness using replicated experimental populations of Drosophila melanogaster evolving under four selective regimes: constant salt-enriched medium (Salt), constant cadmium-enriched medium (Cad), and two heterogeneous regimes that vary either temporally (Temp) or spatially (Spatial). As theory predicts, we found that Spatial populations tend to harbor more genetic variation than Temp populations or those maintained in a constant environment that is the same as the assay environment. Contrary to expectation, Salt populations tend to have more genetic variation than Cad populations in both assay environments. We discuss the patterns for quantitative genetic (QG) variances across regimes in relation to previously reported data on genome-wide sequence diversity. For some traits, the QG patterns are similar to the diversity patterns of ecological selected SNPs whereas the QG patterns for some other traits resembled that of neutral SNPs.
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Data from: The effect of leaf shape on the thermoregulation and frost tolerance of an annual vine, Ipomoea hederacea (Convolvulaceae)
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Campitelli, Brandon E.; Gorton, Amanda J.; Ostevik, Katherine L.; Stinchcombe, John R. — 2016-01-07 Premise of study: Leaf shape is predicted to have important ecophysiological consequences; for example, theory predicts that lobed leaves should track air temperature more closely than their entire-margined counterparts. Hence, leaf-lobing may be advantageous during cold nights (∼0°C) when there is the risk of damage by radiation frost (a phenomenon whereby leaves fall below air temperature because of an imbalance between radiational heat loss and convective heat gain). Methods: Here, we test whether radiation frost can lead to differential damage between leaf shapes by examining a leaf-shape polymorphism in Ipomoea hederacea, where leaves are either lobed or heart-shaped depending on a single Mendelian locus. We logged leaf temperature during midautumn, and measured chlorophyll fluorescence and survival as proxies of performance. Furthermore, we tested if the leaf-shape locus confers freezing tolerance using freezing assays on leaf tissue from different leaf shapes. Key results: We found that lobed leaves consistently remain warmer than heart-shaped leaves during the night, but that no pattern emerged during the day, and that temperature differences between leaf shapes were typically small. Furthermore, we found that leaf types did not differ in frost tolerance, but that a 1°C decrease leads to a transition from moderate to complete damage. Conclusions: Our results demonstrate that Ipomoea hederacea leaf shapes do experience different nighttime temperatures, and that only minor temperature differences can lead to disparate levels of freezing damage, suggesting that the differential thermoregulation could result in different levels of frost damage.
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Data from: Estimating uncertainty in multivariate responses to selection
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Stinchcombe, John R.; Simonsen, Anna K.; Blows, Mark W.; Blows, Mark. W. — 2013-11-15 Predicting the responses to natural selection is one of the key goals of evolutionary biology. Two of the challenges in fulfilling this goal have been the realization that many estimates of natural selection might be highly biased by environmentally induced covariances between traits and fitness, and that many estimated responses to selection do not incorporate or report uncertainty in the estimates. Here we describe the application of a framework that blends the merits of the Robertson-Price Identity approach and the multivariate breeders equation to address these challenges. The approach allows genetic covariance matrices, selection differentials, selection gradients, and responses to selection to be estimated without environmentally-induced bias, direct and indirect selection and responses to selection to be distinguished, and if implemented in a Bayesian-MCMC framework, statistically robust estimates of uncertainty on all of these parameters to be made. We illustrate our approach with a worked example of previously published data. More generally, we suggest that applying both the Robertson-Price Identity and the multivariate breeder’s equation will facilitate hypothesis testing about natural selection, genetic constraints, and evolutionary responses.
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G-matrix stability of clinally diverging populations of an annual weed
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Henry, Georgia A.; Stinchcombe, John R. — 2022-10-21 <p>How phenotypic and genetic divergence among populations is influenced by the genetic architecture of those traits, and how microevolutionary changes in turn affect the within-population patterns of genetic variation, are of major interest to evolutionary biology. Work on <em>Ipomoea hederacea</em>, an annual vine, has found genetic clines in the means of a suite of ecologically important traits, including flowering time, growth rate, seed mass, and corolla width. Here we investigate the genetic (co)variances of these clinally varying traits in two northern range-edge and two central populations of <em>Ipomoea hederacea </em>to evaluate the influence of the genetic architecture on divergence across the range. We find 1) limited evidence for clear differentiation between Northern and Southern populations in the structure of <strong>G</strong>, suggesting overall stability of <strong>G</strong> across the range despite mean trait divergence and 2) that the axes of greatest variation (g<sub>max</sub>) were unaligned with the axis of greatest multivariate divergence. Together these results indicate the role of the quantitative genetic architecture in constraining evolutionary response and divergence among populations across the geographic range.</p>
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Data from: More partners, more ranges: generalist legumes spread more easily around the globe
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Harrison, Tia L.; Simonsen, Anna K.; Stinchcombe, John R.; Frederickson, Megan E. — 2018-11-02 How does mutualism affect range expansion? On one hand, mutualists might thrive in new habitats thanks to the resources, stress tolerance, or defense provided by their partners. On the other, specialized mutualists might fail to find compatible partners beyond their range margins, limiting further spread. A recent global analysis of legume ranges found that non-symbiotic legumes have been successfully introduced to more ranges than legumes that form symbioses with rhizobia, but there is still abundant unexplained variation in introduction success within symbiotic legumes. We test the hypothesis that generalist legumes have spread to more ranges than specialist legumes. We used published data and rhizobial 16S rRNA sequences from GenBank to quantify the number of rhizobia partners that associate with 159 legume species, spanning the legume phylogeny and the globe. We found that generalist legumes occur in more introduced ranges than specialist legumes, suggesting that among mutualists, specialization hinders range expansions.
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Data from: Testing potential selective agents acting on leaf shape in Ipomoea hederacea: predictions based on an adaptive leaf shape cline
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Campitelli, Brandon E.; Stinchcombe, John R. — 2016-01-07 Leaf shape is a highly variable phenotype, and is likely influenced by many sources of selection. Ipomoea hederacea exhibits an adaptive latitudinal cline in leaf shape, which is controlled by a single Mendelian locus: lobed individuals dominate the north with entire-shaped individuals mostly in the south. We test if the following candidate selective agents, suggested by the literature, are responsible for the cline: differential insect herbivory, genetic correlations with other clinal traits like flowering time and growth rate, and thermoregulatory differences. We planted 1680 F3 individuals, segregating for leaf shape, in the north of I. hederacea's range, where we expected lobed genotypes to have higher fitness. Individuals were assigned to insect removal or control treatments, and we scored herbivory, flowering time, growth rate, leaf temperature, and fitness (seed number). Herbivory, flowering, and growth rate had significant fitness effects, but none differed between leaf shapes. Lobed leaves were consistently warmer at night, but no performance advantage was detected. Finally, we detected no overall fitness differences between leaf shape genotypes, whether we controlled for other traits under selection or not. Our data suggest these candidate selective agents may not be important contributors to the cline, and alternative approaches to understanding the mechanisms maintaining the leaf shape cline in I. hederacea may be necessary.

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(auteur : Stinchcombe, John R.)

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