Tanja Pyhäjärvi

Comparative population genomics of maize domestication and improvement

Domestication and plant breeding are ongoing 10,000-year-old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.

Maize HapMap2 identifies extant variation from a genome in flux

Whereas breeders have exploited diversity in maize for yield improvements, there has been limited progress in using beneficial alleles in undomesticated varieties. Characterizing standing variation in this complex genome has been challenging, with only a small fraction of it described to date. Using a population genetics scoring model, we identified 55 million SNPs in 103 lines across pre-domestication and domesticated Zea mays varieties, including a representative from the sister genus Tripsacum. We find that structural variations are pervasive in the Z. mays genome and are enriched at loci associated with important traits. By investigating the drivers of genome size variation, we find that the larger Tripsacum genome can be explained by transposable element abundance rather than an allopolyploid origin. In contrast, intraspecies genome size variation seems to be controlled by chromosomal knob content. There is tremendous overlap in key gene content in maize and Tripsacum, suggesting that adaptations from Tripsacum (for example, perennialism and frost and drought tolerance) can likely be integrated into maize.

Demographic History Has Influenced Nucleotide Diversity in European Pinus sylvestris Populations

To infer the role of natural selection in shaping standing genetic diversity, it is necessary to assess the genomewide impact of demographic history on nucleotide diversity. In this study we analyzed sequence diversity of 16 nuclear loci in eight Pinus sylvestris populations. Populations were divided into four geographical groups on the basis of their current location and the geographical history of the region: northern Europe, central Europe, Spain, and Turkey. There were no among-group differences in the level of silent nucleotide diversity, which was ∼0.005/bp in all groups. There was some evidence that linkage disequilibrium extended further in northern Europe than in central Europe: the estimates of the population recombination rate parameter, ρ, were 0.0064 and 0.0294, respectively. The summary statistics of nucleotide diversity in central and northern European populations were compatible with an ancient bottleneck rather than the standard neutral model.

The Genomic Signature of Crop-Wild Introgression in Maize

The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

Complex Patterns of Local Adaptation in Teosinte

Populations of widely distributed species encounter and must adapt to local environmental conditions. However, comprehensive characterization of the genetic basis of adaptation is demanding, requiring genome-wide genotype data, multiple sampled populations, and an understanding of population structure and potential selection pressures. Here, we used single-nucleotide polymorphism genotyping and data on numerous environmental variables to describe the genetic basis of local adaptation in 21 populations of teosinte, the wild ancestor of maize. We found complex hierarchical genetic structure created by altitude, dispersal events, and admixture among subspecies, which complicated identification of locally beneficial alleles. Patterns of linkage disequilibrium revealed four large putative inversion polymorphisms showing clinal patterns of frequency. Population differentiation and environmental correlations suggest that both inversions and intergenic polymorphisms are involved in local adaptation.

Megabase-Scale Inversion Polymorphism in the Wild Ancestor of Maize

Chromosomal inversions are thought to play a special role in local adaptation, through dramatic suppression of recombination, which favors the maintenance of locally adapted alleles. However, relatively few inversions have been characterized in population genomic data. On the basis of single-nucleotide polymorphism (SNP) genotyping across a large panel of Zea mays, we have identified an ∼50-Mb region on the short arm of chromosome 1 where patterns of polymorphism are highly consistent with a polymorphic paracentric inversion that captures >700 genes. Comparison to other taxa in Zea and Tripsacum suggests that the derived, inverted state is present only in the wild Z. mays subspecies parviglumis and mexicana and is completely absent in domesticated maize. Patterns of polymorphism suggest that the inversion is ancient and geographically widespread in parviglumis. Cytological screens find little evidence for inversion loops, suggesting that inversion heterozygotes may suffer few crossover-induced fitness consequences. The inversion polymorphism shows evidence of adaptive evolution, including a strong altitudinal cline, a statistical association with environmental variables and phenotypic traits, and a skewed haplotype frequency spectrum for inverted alleles.

Adaptive Potential of Northernmost Tree Populations to Climate Change, with Emphasis on Scots Pine (Pinus sylvestris L.)

The adaptive potential of the northernmost Pinus sylvestris L. (and other northern tree) populations is considered by examining first the current patterns of quantitative genetic adaptive traits, which show high population differentiation and clines. We then consider the postglacial history of the populations using both paleobiological and genetic data. The current patterns of diversity at nuclear genes suggest that the traces of admixture are mostly visible in mitochondrial DNA variation patterns. There is little evidence of increased diversity due to admixture between an eastern and western colonization lineage, but no signal of reduced diversity (due to sequential bottlenecks) either. Quantitative trait variation in the north is not associated with the colonizing lineages. The current clines arose rapidly and may be based on standing genetic variation. The initial phenotypic response of Scots pine in the north is predicted to be increased survival and growth. The genetic responses are examined based on quantitative genetic predictions of sustained selection response and compared with earlier simulation results that have aimed at more ecological realism. The phenotypic responses of increased growth and survival reduce the opportunity for selection and delay the evolutionary responses. The lengthening of the thermal growing period also causes selection on the critical photoperiod in the different populations. Future studies should aim at including multiple ecological and genetic factors in evaluating potential responses.

Selection on Nuclear Genes in a Pinus Phylogeny

In this study, we investigate natural selection in a pine phylogeny. DNA sequences from 18 nuclear genes were used to construct a very well-supported species tree including 10 pine species. This tree is in complete agreement with a previously reported supertree constructed from morphological and molecular data, but there are discrepancies with previous chloroplast phylogenies within the section Pinus. A significant difference in evolutionary rate between Picea and Pinus was found, which could potentially indicate a lower mutation rate in Picea, but other scenarios are also possible. Several approaches were used to study selection patterns in a set of 21 nuclear genes in pines and in some cases in Picea and Pseudotsuga. The overall pattern suggests efficient purifying selection resulting in low branch-specific d(n)/d(s) ratios with an average of 0.22, which is similar to other higher plants. Evidence for purifying selection was common and found on at least 55% of the branches. Evidence of positive selection at several sites was found in a phytocyanin homolog and significant differences in d(n)/d(s) among the branches in the gene tree in dehydrin 1. Several genes suitable for further phylogenetic analysis at various levels of divergence were identified.

Teosinte as a model system for population and ecological genomics

As the cost of next-generation sequencing diminishes and genomic resources improve, crop wild relatives are well positioned to make major contributions to the field of ecological genomics via full-genome resequencing and reference-assisted de novo assembly of genomes of plants from natural populations. The wild relatives of maize, collectively known as teosinte, are a more varied and representative study system than many other model flowering plants. In this review of the population and ecological genomics of the teosintes we highlight recent advances in the study of maize domestication, introgressive hybridization, and local adaptation, and discuss future prospects for applying the genomic resources of maize to this intriguing group of species. The maize/teosinte study system is an excellent example of how crops and their wild relatives can bridge the model/non-model gap.

Balancing selection and heterozygote advantage in major histocompatibility complex loci of the bottlenecked Finnish wolf population

Maintaining effective immune response is an essential factor in the survival of small populations. One of the most important immune gene regions is the highly polymorphic major histocompatibility complex (MHC). We investigated how a population bottleneck and recovery have influenced the diversity and selection in three MHC class II loci, DLA‐DRB1, DLA‐DQA1 and DLA‐DQB1, in the Finnish wolf population. We studied the larger Russian Karelian wolf population for comparison and used 17 microsatellite markers as reference loci. The Finnish and Karelian wolf populations did not differ substantially in their MHC diversities ( GST″ = 0.047, P = 0.377), but differed in neutral microsatellite diversities ( GST″ = 0.148, P = 0.008). MHC allele frequency distributions in the Finnish population were more even than expected under neutrality, implying balancing selection. In addition, an excess of nonsynonymous compared to synonymous polymorphisms indicated historical balancing selection. We also studied association between helminth (Trichinella spp. and Echinococcus canadensis) prevalence and MHC diversity at allele and SNP level. MHC‐heterozygous wolves were less often infected by Trichinella spp. and carriers of specific MHC alleles, SNP haplotypes and SNP alleles had less helminth infections. The associated SNP haplotypes and alleles were shared by different MHC alleles, which emphasizes the necessity of single‐nucleotide‐level association studies also in MHC. Here, we show that strong balancing selection has had similar effect on MHC diversities in the Finnish and Russian Karelian wolf populations despite significant genetic differentiation at neutral markers and small population size in the Finnish population.