Kenneth M. Olsen

Phylogeographic studies in plants: problems and prospects

Genetic structuring of plant populations is strongly influenced by both common ancestry and current patterns of interpopulation genetic exchange. The interaction of these two forces is particularly confounding and hence interesting in plants. This complexity of plant genetic structures is due in part to a diversity of reproductive ecologies affecting genetic exchange and the fact that reproductive barriers are often weak between otherwise morphologically well‐defined species. Phylogeographic methods provide a means of examining the history of genetic exchange among populations, with the potential to distinguish biogeographic patterns of genetic variation caused by gene flow from those caused by common ancestry. With regard to plants, phylogeography will be most useful when applied broadly across the entire spectrum of potential genetic exchange. Although current phylogeographic studies of plants show promise, widespread application of this approach has been hindered by a lack of appropriate molecular variation; this problem is discussed and possible solutions considered.

Genome-wide patterns of nucleotide polymorphism in domesticated rice.

Domesticated Asian rice (Oryza sativa) is one of the oldest domesticated crop species in the world, having fed more people than any other plant in human history. We report the patterns of DNA sequence variation in rice and its wild ancestor, O. rufipogon, across 111 randomly chosen gene fragments, and use these to infer the evolutionary dynamics that led to the origins of rice. There is a genome-wide excess of high-frequency derived single nucleotide polymorphisms (SNPs) in O. sativa varieties, a pattern that has not been reported for other crop species. We developed several alternative models to explain contemporary patterns of polymorphisms in rice, including a (i) selectively neutral population bottleneck model, (ii) bottleneck plus migration model, (iii) multiple selective sweeps model, and (iv) bottleneck plus selective sweeps model. We find that a simple bottleneck model, which has been the dominant demographic model for domesticated species, cannot explain the derived nucleotide polymorphism site frequency spectrum in rice. Instead, a bottleneck model that incorporates selective sweeps, or a more complex demographic model that includes subdivision and gene flow, are more plausible explanations for patterns of variation in domesticated rice varieties. If selective sweeps are indeed the explanation for the observed nucleotide data of domesticated rice, it suggests that strong selection can leave its imprint on genome-wide polymorphism patterns, contrary to expectations that selection results only in a local signature of variation.

Crop plants as models for understanding plant adaptation and diversification.

Since the time of Darwin, biologists have understood the promise of crop plants and their wild relatives for providing insight into the mechanisms of phenotypic evolution. The intense selection imposed by our ancestors during plant domestication and subsequent crop improvement has generated remarkable transformations of plant phenotypes. Unlike evolution in natural settings, descendent and antecedent conditions for crop plants are often both extant, providing opportunities for direct comparisons through crossing and other experimental approaches. Moreover, since domestication has repeatedly generated a suite of “domestication syndrome” traits that are shared among crops, opportunities exist for gaining insight into the genetic and developmental mechanisms that underlie parallel adaptive evolution. Advances in our understanding of the genetic architecture of domestication-related traits have emerged from combining powerful molecular technologies with advanced experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies may be combined with high-throughput evaluations of the various “omics” involved in trait transformation, revealing a diversity of underlying causative mutations affecting phenotypes and their downstream propagation through biological networks. We summarize the state of our knowledge of the mutational spectrum that generates phenotypic novelty in domesticated plant species, and our current understanding of how domestication can reshape gene expression networks and emergent phenotypes. An exploration of traits that have been subject to similar selective pressures across crops (e.g., flowering time) suggests that a diversity of targeted genes and causative mutational changes can underlie parallel adaptation in the context of crop evolution.

The Extent of Linkage Disequilibrium in Rice (Oryza sativa L.)

Despite its status as one of the worlds major crops, linkage disequilibrium (LD) patterns have not been systematically characterized across the genome of Asian rice (Oryza sativa). Such information is critical to fully exploit the genome sequence for mapping complex traits using association techniques. Here we characterize LD in five 500-kb regions of the rice genome in three major cultivated rice varieties (indica, tropical japonica, and temperate japonica) and in the wild ancestor of Asian rice, Oryza rufipogon. Using unlinked SNPs to determine the amount of background linkage disequilibrium in each population, we find that the extent of LD is greatest in temperate japonica (probably >500 kb), followed by tropical japonica (∼150 kb) and indica (∼75 kb). LD extends over a shorter distance in O. rufipogon (≪40 kb) than in any of the O. sativa groups assayed here. The differences in the extent of LD among these groups are consistent with differences in outcrossing and recombination rate estimates. As well as heterogeneity between groups, our results suggest variation in LD patterns among genomic regions. We demonstrate the feasibility of genomewide association mapping in cultivated Asian rice using a modest number of SNPs.

Selection under Domestication: Evidence for a Sweep in the Rice Waxy Genomic Region

Rice (Oryza sativa) was cultivated by Asian Neolithic farmers >11,000 years ago, and different cultures have selected for divergent starch qualities in the rice grain during and after the domestication process. An intron 1 splice donor site mutation of the Waxy gene is responsible for the absence of amylose in glutinous rice varieties. This mutation appears to have also played an important role in the origin of low amylose, nonglutinous temperate japonica rice varieties, which form a primary component of Northeast Asian cuisines. Waxy DNA sequence analyses indicate that the splice donor mutation is prevalent in temperate japonica rice varieties, but rare or absent in tropical japonica, indica, aus, and aromatic varieties. Sequence analysis across a 500-kb genomic region centered on Waxy reveals patterns consistent with a selective sweep in the temperate japonicas associated with the mutation. The size of the selective sweep (>250 kb) indicates very strong selection in this region, with an inferred selection coefficient that is higher than similar estimates from maize domestication genes or wild species. These findings demonstrate that selection pressures associated with crop domestication regimes can exceed by one to two orders of magnitude those observed for genes under even strong selection in natural systems.

Current perspectives and the future of domestication studies

It is difficult to overstate the cultural and biological impacts that the domestication of plants and animals has had on our species. Fundamental questions regarding where, when, and how many times domestication took place have been of primary interest within a wide range of academic disciplines. Within the last two decades, the advent of new archaeological and genetic techniques has revolutionized our understanding of the pattern and process of domestication and agricultural origins that led to our modern way of life. In the spring of 2011, 25 scholars with a central interest in domestication representing the fields of genetics, archaeobotany, zooarchaeology, geoarchaeology, and archaeology met at the National Evolutionary Synthesis Center to discuss recent domestication research progress and identify challenges for the future. In this introduction to the resulting Special Feature, we present the state of the art in the field by discussing what is known about the spatial and temporal patterns of domestication, and controversies surrounding the speed, intentionality, and evolutionary aspects of the domestication process. We then highlight three key challenges for future research. We conclude by arguing that although recent progress has been impressive, the next decade will yield even more substantial insights not only into how domestication took place, but also when and where it did, and where and why it did not.

Genetic perspectives on crop domestication

The process of crop domestication has long been a topic of active research for biologists, anthropologists and others. Genetic data have proved a powerful resource for drawing inferences on questions regarding the geographical origins of crops, the numbers of independent domestication events for a given crop species, the specific molecular changes underlying domestication traits, and the nature of artificial selection during domestication and subsequent crop improvement. We would argue that these genetic inferences are fundamentally compatible with recent archaeological data that support a view of domestication as a geographically diffuse, gradual process. In this review, we summarize methodologies ranging from quantitative trait locus mapping to resequencing used in genetic analyses of crop evolution. We also highlight recent major insights regarding the timing and spatial patterning of crop domestication and the distinct genetic underpinnings of domestication, diversification and improvement traits.

Microsatellite variation in cassava (Manihot esculenta, Euphorbiaceae) and its wild relatives: further evidence for a southern Amazonian origin of domestication

Genetic variation at five microsatellite loci was used to investigate the evolutionary and geographical origins of cassava (Manihot esculenta subsp. esculenta) and the population structure of cassavas wild relatives. Two hundred and twelve individuals were sampled, representing 20 crop accessions, 27 populations of cassavas closest wild relative (M. esculenta subsp. flabellifolia), and six populations of a potentially hybridizing species (M. pruinosa). Seventy-three alleles were observed across all loci and populations. These data indicate the following on cassavas origin: (1) genetic variation in the crop is a subset of that found in the wild M. esculenta subspecies, suggesting that cassava is derived solely from its conspecific wild relative. (2) Phenetic analyses group cassava with wild populations from the southern border of the Amazon basin, indicating this region as the likely site of domestication. (3) Manihot pruinosa, while closely related to M. esculenta (and possibly hybridizing with it where sympatric), is probably not a progenitor of the crop. Genetic differentiation among the wild populations is moderately high (F:(ST) = 0.42, rho(ST) = 0.54). This differentiation has probably arisen primarily through random genetic drift (rather than mutation) following recent population divergence.

A Bountiful Harvest: Genomic Insights into Crop Domestication Phenotypes

Human selection during crop domestication has resulted in remarkable transformations of plant phenotypes, providing a window into the genetic basis of morphological evolution. Recent progress in our understanding of the genetic architecture of novel plant traits has emerged from combining advanced molecular technologies with improved experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies reveal a diversity of underlying causative mutations affecting phenotypes important in plant domestication and crop improvement, including coding sequence substitutions, presence/absence and copy number variation, transposon activation leading to novel gene structures and expression patterns, diversification following gene duplication, and polyploidy leading to altered combinatorial capabilities. The genomic regions unknowingly targeted by human selection include both structural and regulatory genes, often with results that propagate through the transcriptome as well as to other levels in the biosynthetic and morphogenetic networks.

Pollination effectiveness and pollinator importance in a population of Heterotheca subaxillaris (Asteraceae)

Abstract Assessing the relative contributions to seed set for each of a plant species’ floral visitors provides an indication of the relative influence of these visitors on the plant’s reproductive success. This study examined pollinator activity and seed set in a population of Heterotheca subaxillaris, a species that exhibits a floret dimorphism (heads bearing disk and ray florets), and that is visited by both generalist foragers and specialist bees. Visits by nine bee genera and one genus of skipper were recorded in the study population. During the period of study, these insects varied in their relative abundance, in their foraging activity on a head, and in their pollination effectiveness. The pattern of pollination effectiveness shown by the different pollinators was similar for both floret types, although seed set was higher overall for ray florets. Pollinator importance, calculated as the product of pollination effectiveness and relative abundance, was dictated by a pollinator’s relative abundance. The single specialist bee species observed in the study population proved to have neither higher pollination effectiveness nor higher pollinator abundance than other pollinators. This would suggest that H. subaxillaris is not under strong selective pressure to co-specialize with its specialist visitor.