Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism.

Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.

Erratum: Author Correction: Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism.

[This corrects the article DOI: 10.1038/s42003-018-0120-9.].

Phylogenetic ANCOVA: Estimating Changes in Evolutionary Rates as Well as Relationships between Traits.

We present a new phylogenetic comparative method-phylogenetic analysis of covariance (PANCOVA)-that uses interspecific data and a phylogeny to estimate the effects of major events on both the rate of phenotypic evolution and the association between traits. It could be used, for example, to model the impact of a key innovation, colonization of a new habitat, or environmental change. The approach is optimized with maximum likelihood and is formulated under the familiar phylogenetic generalized least squares framework, which is flexible and easily extended to incorporate other factors and parameters. As an example, we explore the relationship between parental investment and relative telencephalon size in birds and contrast the results of PANCOVA with those from other phylogenetic comparative methods.

Genome-wide maps of recombination and chromosome segregation in human oocytes and embryos show selection for maternal recombination rates.

Crossover recombination reshuffles genes and prevents errors in segregation that lead to extra or missing chromosomes (aneuploidy) in human eggs, a major cause of pregnancy failure and congenital disorders. Here we generate genome-wide maps of crossovers and chromosome segregation patterns by recovering all three products of single female meioses. Genotyping >4 million informative SNPs from 23 complete meioses allowed us to map 2,032 maternal and 1,342 paternal crossovers and to infer the segregation patterns of 529 chromosome pairs. We uncover a new reverse chromosome segregation pattern in which both homologs separate their sister chromatids at meiosis I; detect selection for higher recombination rates in the female germ line by the elimination of aneuploid embryos; and report chromosomal drive against non-recombinant chromatids at meiosis II. Collectively, our findings show that recombination not only affects homolog segregation at meiosis I but also the fate of sister chromatids at meiosis II.

Population structure, demographic history, and evolutionary patterns of a green-fruited tomato, Solanum peruvianum (Solanaceae), revealed by spatial genetics analyses.

PREMISE OF THE STUDY: Wild relatives of crop species have long been viewed as an important genetic resource for crop improvement, but basic information about the population biology of these species is often lacking. This study investigated the population structure, demographic history, and evolutionary patterns of a green-fruited relative of the cultivated tomato, Solanum peruvianum. METHODS: We investigated spatial genetics of S. peruvianum and screened for loci potentially under natural selection by integrating amplified fragment length polymorphism (AFLP) genotypes, phenotypic data, geography, and geographic information system (GIS)-derived climate data of 19 natural populations. KEY RESULTS: Solanum peruvianum had a moderate degree of population differentiation, likely reflecting partial geographic isolation between species. Populations had a distribution pattern consistent with north-to-south "stepping-stone" dispersal with significant isolation by distance (IBD), similar to other tomato species. Several AFLP loci showed evidence of selection and associated with climate variables. However, phenotypic traits generally did not correlate with climate variables. CONCLUSIONS: Geographic features of the coastal Andes is likely an important factor that determines the migration pattern and population structure of S. peruvianum, but climatic factors do not appear to be critical for its phenotypic evolution, perhaps due to a high degree of phenotypic plasticity. Spatial genetics of wild relatives of crop species is a powerful approach to understand their evolutionary patterns and to accelerate the discovery of their potential for crop improvements.

Spatial genetics of wild tomato species reveals roles of the Andean geography on demographic history.

PREMISE OF THE STUDY: Understanding the demographic history of natural populations in relation to the geographic features in their habitats is an important step toward deciphering the mechanisms of evolutionary processes in nature. This study investigates how the complex geographic and ecological features of the Andes play a role in demographic history, species divergence, dispersal patterns, and hybridization in wild tomato species. METHODS: We investigated spatial genetics of two closely related wild tomato species, Solanum lycopersicum and S. pimpinellifolium, by integrating amplified fragment length polymorphism (AFLP) marker data and geographic information system (GIS)-derived geographic and climatic data. KEY RESULTS: The two species represent genetically distinct lineages largely separated by the Andes, but hybridize extensively in central to northern Ecuador, likely mediated by the transitional climatic conditions between those of the two species. Solanum lycospericum has likely experienced a severe population bottleneck during the colonization of the eastern Andes followed by a rapid population expansion. CONCLUSIONS: The study demonstrates that the evolutionary patterns of the two wild tomatoes, including demographic history, dispersal patterns, interspecific divergence, and hybridization, are intimately related to the complex geographic and ecological features of the Andes. Integrating genetic data across the genome and GIS-derived environmental data can provide insights into the patterns of complex evolutionary processes in nature.

On the number of binary characters needed to recover a phylogeny using maximum parsimony.

We give an explicit construction to solve a conjecture of Mike Steel and David Penny that any phylogeny involving N taxa can be recovered unambiguously using on the order of log N binary characters and the method of maximum parsimony. Biologically, this means that homoplasy need not be a deterrent to parsimony methods. Some patterns of homoplasy are phylogenetically informative and can exponentially reduce the amount of data needed to resolve a phylogeny.

Methods for analysis of crossover interference in Saccharomyces cerevisiae.

Interest in crossover interference in yeast has been spurred by the discovery and characterization of mutants that alter it as well as by the development and testing of models to explain it. This chapter describes methods for detecting and for measuring interference, with emphasis on those that exploit the ability to examine all four products of individual acts of meiosis.

A genomewide study of reproductive barriers between allopatric populations of a homosporous fern, Ceratopteris richardii.

Biological factors involved in reproductive barriers between two divergent races of Ceratopteris richardii were investigated. We used a combination of spore germination rates, QTL analysis of spore germination rates, and transmission ratio distortion (TRD) of 729 RFLPs, AFLPs, and isozyme markers distributed across the genome on the basis of hybrid populations of 488 doubled haploid lines (DHLs) and 168 F(2)'s. Substantial reproductive barriers were found between the parental races, predominantly in the form of spore inviability (23.7% F(1) spore viability). Intrinsic genetic factors such as Bateson-Dobzhansky-Muller (BDM) incompatibilities involving both nuclear-nuclear and nuclear-cytoplasmic factors and chromosomal rearrangements appear to contribute to intrinsic postzygotic isolation. The genomewide distribution patterns of TRD loci support the hypothesis that reproductive barriers are a byproduct of divergence in allopatry and that the strong reproductive barriers are attributable to a small number of genetic elements scattered throughout the genome.

Genetic map-based analysis of genome structure in the homosporous fern Ceratopteris richardii.

Homosporous ferns have extremely high chromosome numbers relative to flowering plants, but the species with the lowest chromosome numbers show gene expression patterns typical of diploid organisms, suggesting that they may be diploidized ancient polyploids. To investigate the role of polyploidy in fern genome evolution, and to provide permanent genetic resources for this neglected group, we constructed a high-resolution genetic linkage map of the homosporous fern model species, Ceratopteris richardii (n = 39). Linkage map construction employed 488 doubled haploid lines (DHLs) that were genotyped for 368 RFLP, 358 AFLP, and 3 isozyme markers. Forty-one linkage groups were recovered, with average spacing between markers of 3.18 cM. Most loci (approximately 76%) are duplicated and most duplicates occur on different linkage groups, indicating that as in other eukaryotic genomes, gene duplication plays a prominent role in shaping the architecture of fern genomes. Although past polyploidization is a potential mechanism for the observed abundance of gene duplicates, a wide range in the number of gene duplicates as well as the absence of large syntenic regions consisting of duplicated gene copies implies that small-scale duplications may be the primary mode of gene duplication in C. richardii. Alternatively, evidence of past polyploidization(s) may be masked by extensive chromosomal rearrangements as well as smaller-scale duplications and deletions following polyploidization(s).

InterferenceAnalyzer: tools for the analysis and simulation of multi-locus genetic data.

BACKGROUND: Good statistical models for analyzing and simulating multilocus recombination data exist but are not accessible to many biologists because their use requires reasonably sophisticated mathematical and computational implementation. While some labs have direct access to statisticians or programmers competent to carry out such analyses, many labs do not. We have created a platform independent application with an easy-to-use graphical user interface that will carry out such analyses including the simulations needed to bootstrap confidence intervals for the parameters of interest. This software should make multi-locus techniques accessible to labs that previously relied on less powerful and potentially statistically confounded single interval or double interval techniques. RESULTS: We introduce InterferenceAnalyzer, an implementation with a user-friendly graphical interface incorporating previously developed algorithms for the analysis and simulation of multilocus recombination data. We demonstrate the use and features of the program with an example of multilocus tetrad data from the mustard plant, Arabidopsis thaliana, and the yeast, Saccharomyces cerevisiae. CONCLUSION: InterferenceAnalyzer provides easy access to the powerful and appropriate statistical tools for the multi-locus analysis of genetic data.

Crossover interference on nucleolus organizing region-bearing chromosomes in Arabidopsis.

In most eukaryotes, crossovers are not independently distributed along the length of a chromosome. Instead, they appear to avoid close proximity to one another--a phenomenon known as crossover interference. Previously, for three of the five Arabidopsis chromosomes, we measured the strength of interference and suggested a model wherein some crossovers experience interference while others do not. Here we show, using the same model, that the fraction of interference-insensitive crossovers is significantly smaller on the remaining two chromosomes. Since these two chromosomes bear the Arabidopsis NOR domains, the possibility that these chromosomal regions influence interference is discussed.

Gene conversion and crossing over along the 405-kb left arm of Saccharomyces cerevisiae chromosome VII.

Gene conversions and crossing over were analyzed along 10 intervals in a 405-kb region comprising nearly all of the left arm of chromosome VII in Saccharomyces cerevisiae. Crossover interference was detected in all intervals as measured by a reduced number of nonparental ditypes. We have evaluated interference between crossovers in adjacent intervals by methods that retain the information contained in tetrads as opposed to single segregants. Interference was seen between intervals when the distance in the region adjacent to a crossover was < approximately 35 cM (90 kb). At the met13 locus, which exhibits approximately 9% gene conversions, those gene conversions accompanied by crossing over exerted interference in exchanges in an adjacent interval, whereas met13 gene conversions without an accompanying exchange did not show interference. The pattern of exchanges along this chromosome arm can be represented by a counting model in which there are three nonexchange events between adjacent exchanges; however, maximum-likelihood analysis suggests that approximately 8-12% of the crossovers on chromosome VII arise by a separate, noninterfering mechanism.

The phylogenetic mixed model.

The phylogenetic mixed model is an application of the quantitative-genetic mixed model to interspecific data. Although this statistical framework provides a potentially unifying approach to quantitative-genetic and phylogenetic analysis, the model has been applied infrequently because of technical difficulties with parameter estimation. We recommend a reparameterization of the model that eliminates some of these difficulties, and we develop a new estimation algorithm for both the original maximum likelihood and new restricted maximum likelihood estimators. The phylogenetic mixed model is particularly rich in terms of the evolutionary insight that might be drawn from model parameters, so we also illustrate and discuss the interpretation of the model parameters in a specific comparative analysis.

Measures of synteny conservation between species pairs.

Measures of conserved synteny are important for estimating the relative rates of chromosomal evolution in various lineages. We present a natural way to view the synteny conservation between two species from an Oxford grid--an r x c table summarizing the number of orthologous genes on each of the chromosomes 1 through r of the first species that are on each of the chromosomes 1 through c of the second species. This viewpoint suggests a natural statistic, which we denote by rho and call syntenic correlation, designed to measure the amount of synteny conservation between two species. This measure allows syntenic conservation to be compared across many pairs of species. We improve the previous methods for estimating the true number of conserved syntenies given the observed number of conserved syntenies by taking into account the dependency of the numbers of orthologues observed in the chromosome pairings between the two species and by determining both point and interval estimators. We also discuss the application of our methods to genomes that contain chromosomes of highly variable lengths and to estimators of the true number of conserved segments between species pairs.

Adaptive constraints and the phylogenetic comparative method: a computer simulation test.

Recently, the utility of modern phylogenetic comparative methods (PCMs) has been questioned because of the seemingly restrictive assumptions required by these methods. Although most comparative analyses involve traits thought to be undergoing natural or sexual selection, most PCMs require an assumption that the traits be evolving by less directed random processes, such as Brownian motion (BM). In this study, we use computer simulation to generate data under more realistic evolutionary scenarios and consider the statistical abilities of a variety of PCMs to estimate correlation coefficients from these data. We found that correlations estimated without taking phylogeny into account were often quite poor and never substantially better than those produced by the other tested methods. In contrast, most PCMs performed quite well even when their assumptions were violated. Felsenstein's independent contrasts (FIC) method gave the best performance in many cases, even when weak constraints had been acting throughout phenotypic evolution. When strong constraints acted in opposition to variance-generating (i.e., BM) forces, however, FIC correlation coefficients were biased in the direction of those BM forces. In most cases, all other PCMs tested (phylogenetic generalized least squares, phylogenetic mixed model, spatial autoregression, and phylogenetic eigenvector regression) yielded good statistical performance, regardless of the details of the evolutionary model used to generate the data. Actual parameter estimates given by different PCMs for each dataset, however, were occasionally very different from one another, suggesting that the choice among them should depend on the types of traits and evolutionary processes being considered.

Phylogeny shape and the phylogenetic comparative method.

We explored the impact of phylogeny shape on the results of interspecific statistical analyses incorporating phylogenetic information. In most phylogenetic comparative methods (PCMs), the phylogeny can be represented as a relationship matrix, and the hierarchical nature of interspecific phylogenies translates into a distinctive blocklike matrix that can be described by its eigenvectors (topology) and eigenvalues (branch lengths). Thus, differences in the eigenvectors and eigenvalues of different relationship matrices can be used to gauge the impact of possible phylogeny errors by comparing the actual phylogeny used in a PCM analysis with a second phylogenetic hypothesis that may be more accurate. For example, we can use the sum of inverse eigenvalues as a rough index to compare the impact of phylogenies with different branch lengths. Topological differences are better described by the eigenvectors. In general, phylogeny errors that involve deep splits in the phylogeny (e.g., moving a taxon across the base of the phylogeny) are likely to have much greater impact than will those involving small perturbations in the fine structure near the tips. Small perturbations, however, may have more of an impact if the phylogeny structure is highly dependent (with many recent splits near the tips of the tree). Unfortunately, the impact of any phylogeny difference on the results of a PCM depends on the details of the data being considered. Recommendations regarding the choice, design, and statistical power of interspecific analyses are also made.