Eric J. Baack

THE DYNAMIC NATURE OF APOMIXIS IN THE ANGIOSPERMS

Apomixis, the asexual production of seed, is a trait estimated to occur in fewer than 1% of flowering plant species, with an uneven distribution among lineages. In the past decade, targeted research efforts have aimed at clarifying the genetic basis of apomixis, with the goal of engineering or breeding apomictic crops. Recent work suggests a simple genetic basis for apomixis, but it also indicates that natural populations of apomicts are much more complex than is often assumed. For example, in nature, nearly all apomicts that go through a megagametophyte stage (gametophytic apomicts) are polyploid, while their sexual relatives are typically diploid. Although populations have been characterized as obligately sexual or apomictic, it is increasingly clear that many plant populations exhibit some variation in reproductive mode. Many apomicts retain residual sexual function as pollen donors and thus have the potential to spread apomixis via male gametes, thereby increasing the genetic diversity observed within apomictic populations. Here, we summarize our current understanding of the genetic basis and transmission of apomixis. We use insights from previous case studies and models for the spread of asexuality to explore the potential for establishment and spread of apomixis in nature.

The origins of reproductive isolation in plants

Reproductive isolation in plants occurs through multiple barriers that restrict gene flow between populations, but their origins remain uncertain. Work in the past decade has shown that postpollination barriers, such as the failure to form hybrid seeds or sterility of hybrid offspring, are often less strong than prepollination barriers. Evidence implicates multiple evolutionary forces in the origins of reproductive barriers, including mutation, stochastic processes and natural selection. Although adaptation to different environments is a common element of reproductive isolation, genomic conflicts also play a role, including female meiotic drive. The genetic basis of some reproductive barriers, particularly flower colour influencing pollinator behaviour, is well understood in some species, but the genetic changes underlying many other barriers, especially pollen-stylar interactions, are largely unknown. Postpollination barriers appear to accumulate at a faster rate in annuals compared with perennials, due in part to chromosomal rearrangements. Chromosomal changes can be important isolating barriers in themselves but may also reduce the recombination of genes contributing to isolation. Important questions for the next decade include identifying the evolutionary forces responsible for chromosomal rearrangements, determining how often prezygotic barriers arise due to selection against hybrids, and establishing the relative importance of genomic conflicts in speciation.

A ROLE FOR NONADAPTIVE PROCESSES IN PLANT GENOME SIZE EVOLUTION

Genome sizes vary widely among species, but comprehensive explanations for the emergence of this variation have not been validated. Lynch and Conery (2003) hypothesized that genome expansion is maladaptive, and that lineages with small effective population size (Ne) evolve larger genomes than those with large Ne as a consequence of the lowered efficacy of natural selection in small populations. In addition, mating systems likely affect genome size evolution via effects on both Ne and the spread of transposable elements (TEs). We present a comparative analysis of the effects of Ne and mating system on genome size evolution in seed plants. The dataset includes 205 species with monoploid genome size estimates (corrected for recent polyploidy) ranging from 2Cx = 0.3 to 65.9 pg. The raw data exhibited a strong positive relationship between outcrossing and genome size, a negative relationship between Ne and genome size, but no detectable Ne× outcrossing interaction. In contrast, phylogenetically independent contrast analyses found only a weak relationship between outcrossing and genome size and no relationship between Ne and genome size. Thus, seed plants do not support the Lynch and Conery mechanism of genome size evolution. Further work is needed to disentangle contrasting effects of mating systems on the efficacy of selection and TE transmission.

Selection on domestication traits and quantitative trait loci in crop–wild sunflower hybrids

The strength and extent of gene flow from crops into wild populations depends, in part, on the fitness of the crop alleles, as well as that of alleles at linked loci. Interest in crop–wild gene flow has increased with the advent of transgenic plants, but nontransgenic crop–wild hybrids can provide case studies to understand the factors influencing introgression, provided that the genetic architecture and the fitness effects of loci are known. This study used recombinant inbred lines (RILs) generated from a cross between crop and wild sunflowers to assess selection on domestication traits and quantitative trait loci (QTL) in two contrasting environments, in Indiana and Nebraska, USA. Only a small fraction of plants (9%) produced seed in Nebraska, due to adverse weather conditions, while the majority of plants (79%) in Indiana reproduced. Phenotypic selection analysis found that a mixture of crop and wild traits were favoured in Indiana (i.e. had significant selection gradients), including larger leaves, increased floral longevity, larger disk diameter, reduced ray flower size and smaller achene (seed) mass. Selection favouring early flowering was detected in Nebraska. QTLs for fitness were found at the end of linkage groups six (LG6) and nine (LG9) in both field sites, each explaining 11–12% of the total variation. Crop alleles were favoured on LG9, but wild alleles were favoured on LG6. QTLs for numerous domestication traits overlapped with the fitness QTLs, including flowering date, achene mass, head number, and disk diameter. It remains to be seen if these QTL clusters are the product of multiple linked genes, or individual genes with pleiotropic effects. These results indicate that crop trait values and alleles may sometimes be favoured in a noncrop environment and across broad geographical regions.

Reconciling extremely strong barriers with high levels of gene exchange in annual sunflowers

In several cases, estimates of gene flow between species appear to be higher than we might predict given the strength of interspecific barriers separating these species pairs. However, as far as we are aware, detailed measurements of reproductive isolation have not previously been compared with a coalescent‐based assessment of gene flow. Here, we contrast these two measures in two species of sunflower, Helianthus annuus and H. petiolaris. We quantified the total reproductive barrier strength between these species by compounding the contributions of the following prezygotic and postzygotic barriers: ecogeographic isolation, reproductive asynchrony, niche differentiation, pollen competition, hybrid seed formation, hybrid seed germination, hybrid fertility, and extrinsic postzygotic isolation. From this estimate, we calculated the probability that a reproductively successful hybrid is produced: estimates of Phyb range from 10−4 to 10−6 depending on the direction of the cross and the degree of independence among reproductive barriers. We then compared this probability with population genetic estimates of the per generation migration rate (m). We showed that the relatively high levels of gene flow estimated between these sunflower species (Nem= 0.34–0.76) are mainly due to their large effective population sizes (Ne > 106). The interspecific migration rate (m) is very small (<10−7) and an order of magnitude lower than that expected based on our reproductive barrier strength estimates. Thus, even high levels of reproductive isolation (>0.999) may produce genomic mosaics.

Drift and Genome Complexity Revisited

51Department of Ecology and Evolutionary Biology, Rice University, Houston, Texas, United States of America, 2Department of Integrative Biology, University of CaliforniaBerkeley, Berkeley, California, United States of America, 3Laboratoire de Biome´trie et Biologie Evolutive, Universite´ de Lyon, Universite´ Lyon 1, CNRS, UMR5558,Villeurbanne, France, 4Department of Biology, Luther College, Decorah, Iowa, United States of America, 5Department of Biology, University of California Riverside,Riverside, California, United States of America

The origins of weedy rice

Where do weeds come from? How do they evolve from nonweedy ancestors? In this issue of Molecular Ecology, Londo and Schaal examine the origin of weedy rice (Oryza sativa) populations in the USA. Analysing nuclear DNA sequence and microsatellite data, they show the importance of parallel evolution, hybridization, gene flow, and migration in the evolution of these weeds.

Engineered Crops: Transgenes Go Wild

Genetically modified Agrostis stolonifera has escaped from cultivation. For the first time, a herbicide-resistant perennial weed has established itself in wild populations.

Species integrity in trees

From California sequoia, to Australian eucalyptus, to the outstanding diversity of Amazonian forests, trees are fundamental to many processes in ecology and evolution. Trees define the communities that they inhabit, are host to a multiplicity of other organisms and can determine the ecological dynamics of other plants and animals. Trees are also at the heart of major patterns of biodiversity such as the latitudinal gradient of species diversity and thus are important systems for studying the origin of new plant species. Although the role of trees in community assembly and ecological succession is partially understood, the origin of tree diversity remains largely opaque. For instance, the relative importance of differing habitats and phenologies as barriers to hybridization between closely related species is still largely uncharacterized in trees. Consequently, we know very little about the origin of trees species and their integrity. Similarly, studies on the interplay between speciation and tree community assembly are in their infancy and so are studies on how processes like forest maturation modifies the context in which reproductive isolation evolves. In this issue of Molecular Ecology, Lindtke et al. (2014) and Lagache et al. (2014) overcome some traditional difficulties in studying mating systems and sexual isolation in the iconic oaks and poplars, providing novel insights about the integrity of tree species and on how ecology leads to variation in selection on reproductive isolation over time and space.

Genome-wide analysis of allele frequency change in sunflower crop-wild hybrid populations evolving under natural conditions

Crop‐wild hybridization occurs in numerous plant species and could alter the genetic structure and evolutionary dynamics of wild populations. Studying crop‐derived alleles in wild populations is also relevant to assessing/mitigating the risks associated with transgene escape. To date, crop‐wild hybridization has generally been examined via short‐term studies, typically within a single generation, focusing on few traits or genetic markers. Little is known about patterns of selection on crop‐derived alleles over multiple generations, particularly at a genome‐wide scale. Here, we documented patterns of natural selection in an experimental crop × wild sunflower population that was allowed to evolve under natural conditions for two generations at two locations. Allele frequencies at a genome‐wide collection of SNPs were tracked across generations, and a common garden experiment was conducted to compare trait means between generations. These data allowed us to identify instances of selection on crop‐derived alleles/traits and, in concert with QTL mapping results, test for congruence between our genotypic and phenotypic results. We found that natural selection overwhelmingly favours wild alleles and phenotypes. However, crop alleles in certain genomic regions can be favoured, and these changes often occurred in parallel across locations. We did not, however, consistently observe close agreement between our genotypic and phenotypic results. For example, when a trait evolved towards the wild phenotype, wild QTL alleles associated with that trait did not consistently increase in frequency. We discuss these results in the context of crop allele introgression into wild populations and implications for the management of GM crops.