Over the past several decades, a rapidly expanding field of research known as biodiversity and ecosystem functioning has begun to quantify how the world's biological diversity can, as an independent variable, control ecological processes that are both essential for, and fundamental to, the functioning of ecosystems. Research in this area has often been justified on grounds that (1) loss of biological diversity ranks among the most pronounced changes to the global environment and that (2) reductions in diversity, and corresponding changes in species composition, could alter important services that ecosystems provide to humanity (e.g., food production, pest/disease control, water purification). Here we review over two decades of experiments that have examined how species richness of primary producers influences the suite of ecological processes that are controlled by plants and algae in terrestrial, marine, and freshwater ecosystems. Using formal meta-analyses, we assess the balance of evidence for eight fundamental questions and corresponding hypotheses about the functional role of producer diversity in ecosystems. These include questions about how primary producer diversity influences the efficiency of resource use and biomass production in ecosystems, how primary producer diversity influences the transfer and recycling of biomass to other trophic groups in a food web, and the number of species and spatial /temporal scales at which diversity effects are most apparent. After summarizing the balance of evidence and stating our own confidence in the conclusions, we outline several new questions that must now be addressed if this field is going to evolve into a predictive science that can help conserve and manage ecological processes in ecosystems.
Premise of the study: Fungi are major decomposers in certain ecosystems and essential associates of many organisms. They provide enzymes and drugs and serve as experimental organisms. In 1991, a landmark paper estimated that there are 1.5 million fungi on the Earth. Because only 70000 fungi had been described at that time, the estimate has been the impetus to search for previously unknown fungi. Fungal habitats include soil, water, and organisms that may harbor large numbers of understudied fungi, estimated to outnumber plants by at least 6 to 1. More recent estimates based on high-throughput sequencing methods suggest that as many as 5.1 million fungal species exist. Methods: Technological advances make it possible to apply molecular methods to develop a stable classification and to discover and identify fungal taxa. Key results: Molecular methods have dramatically increased our knowledge of Fungi in less than 20 years, revealing a monophyletic kingdom and increased diversity among early-diverging lineages. Mycologists are making significant advances in species discovery, but many fungi remain to be discovered. Conclusions: Fungi are essential to the survival of many groups of organisms with which they form associations. They also attract attention as predators of invertebrate animals, pathogens of potatoes and rice and humans and bats, killers of frogs and crayfish, producers of secondary metabolites to lower cholesterol, and subjects of prize-winning research. Molecular tools in use and under development can be used to discover the world's unknown fungi in less than 1000 years predicted at current new species acquisition rates.
Polyploidy has long been considered a major force in plant evolution. G. Ledyard Stebbins, Jr., an architect of the Modern Synthesis, elegantly addressed a broad range of topics, from genes to chromosomes to deep phylogeny, but some of his most lasting insights came in the study of polyploidy. Here, we review the immense impact of his work on polyploidy over more than 60 years, from his entrance into this fledgling field in the 1920s until the end of his career. Stebbins and his contemporaries developed a model of polyploid evolution that persisted for nearly half a century. As new perspectives emerged in the 1980s and new genetic tools for addressing key aspects of polyploidy have become available, a new paradigm of polyploidy has replaced much of the Stebbinsian framework. We review that paradigm shift and emphasize those areas in which the ideas of Stebbins continue to propel the field forward, as well as those areas in which the field was held back; we also note new directions that plant geneticists and evolutionists are now exploring in polyploidy research. Perhaps the most important conclusion from recent and ongoing studies of polyploidy is that, following Levin and others, polyploidy may propel a population into a new adaptive sphere given the myriad changes that accompany genome doubling.
Premise of the study: It has been 8 years since the last comprehensive analysis of divergence times across the angiosperms. Given recent methodological improvements in estimating divergence times, refined understanding of relationships among major angiosperm lineages, and the immense interest in using large angiosperm phylogenies to investigate questions in ecology and comparative biology, new estimates of the ages of the major clades are badly needed. Improved estimations of divergence times will concomitantly improve our understanding of both the evolutionary history of the angiosperms and the patterns and processes that have led to this highly diverse clade. Methods: We simultaneously estimated the age of the angiosperms and the divergence times of key angiosperm lineages, using 36 calibration points for 567 taxa and a "relaxed clock" methodology that does not assume any correlation between rates, thus allowing for lineage-specific rate heterogeneity. Key results: Based on the analysis for which we set fossils to fit lognormal priors, we obtained an estimated age of the angiosperms of 167–199 Ma and the following age estimates for major angiosperm clades: Mesangiospermae (139–156 Ma); Gunneridae (109–139 Ma); Rosidae (108–121 Ma); Asteridae (101–119 Ma). Conclusions: With the exception of the age of the angiosperms themselves, these age generally are generally younger than other recent molecular estimates and very close to dates inferred from the fossil record. We also provide dates for all major angiosperm clades (including 45 orders and 335 families [208 stem group age only, 127 both stem and crown group ages], sensu APG III). Our analyses provide a new comprehensive source of reference dates for major angiosperm clades that we hope will be of broad utility.
Premise of the study. Recent analyses employing up to five genes have provided numerous insights into angiosperm phylogeny, but many relationships have remained unresolved or poorly supported. In the hope of improving our understanding of angiosperm phylogeny, we expanded sampling of taxa and genes beyond previous analyses. Methods: We conducted two primary analyses based on 640 species representing 330 families. The first included 25260 aligned base pairs (bp) from 17 genes (representing all three plant genomes, i. e., nucleus, plastid, and mitochondrion). The second included 19846 aligned bp from 13 genes (representing only the nucleus and plastid). Key results: Many important questions of deep-level relationships in the nonmonocot angiosperms have now been resolved with strong support. Amborellaceae, Nymphaeales, and Austrobaileyales are successive sisters to the remaining angiosperms (Mesangiospermae), which are resolved into Chloranthales + Magnoliidae as sister to Monocotyledoneae + [Ceratophyllaceae + Eudicotyledoneae]. Eudicotyledoneae contains a basal grade subtending Gunneridae. Within Gunneridae, Gunnerales are sister to the remainder (Pentapetalae), which comprises (1) Superrosidae, consisting of Rosidae (including Vitaceae) and Saxifragales; and (2) Superasteridae, comprising Berberidopsidales, Santalales, CaryophyHales, Asteridae, and, based on this study, Dilleniaceae (although other recent analyses disagree with this placement). Within the major subclades of Pentapetalae, most deep-level relationships are resolved with strong support. Conclusions: Our analyses confirm that with large amounts of sequence data, most deep-level relationships within the angiosperms can be resolved. We anticipate that this well-resolved angiosperm tree will be of broad utility for many areas of biology, including physiology, ecology, paleobiology, and genomics.
• Premise of the study: Separating sexual function between different individuals carries risks, especially for sedentary organisms. Nevertheless, many land plants have unisexual gametophytes or sporophytes. This study brings together data and theoretical insights from research over the past 20 yr on the occurrence and frequency of plant sexual systems, focusing on the flowering plants. • Methods: A list of genera with dioecious species, along with other information, is made available (http://www.umsl.edu/∼renners/). Frequencies of other sexual systems are tabulated, and data on the genetic regulation, ecological context, and theoretical benefits of dioecy reviewed. • Key results: There are 15600 dioecious angiosperms in 987 genera and 175 families, or 5–6% of the total species (7% of genera, 43% of families), with somewhere between 871 to 5000 independent origins of dioecy. Some 43% of all dioecious angiosperms are in just 34 entirely dioecious clades, arguing against a consistent negative influence of dioecy on diversification. About 31.6% of the dioecious species are wind‐pollinated, compared with 5.5–6.4% of nondioecious angiosperms. Also, 1.4% of all angiosperm genera contain dioecious and monoecious species, while 0.4% contain dioecious and gynodioecious species. All remaining angiosperm sexual systems are rare. Chromosomal sex determination is known from 40 species; environmentally modulated sex allocation is common. Few phylogenetic studies have focused on the evolution of dioecy. • Conclusions: The current focus is on the genetic mechanisms underlying unisexual flowers and individuals. Mixed strategies of sexual and vegetative dispersal, together with plants’ sedentary life style, may often favor polygamous systems in which sexually inconstant individuals can persist. Nevertheless, there are huge entirely dioecious clades of tropical woody plants.
Premise of the study: Near-future climate changes are likely to elicit major vegetation changes. Disequilibrium dynamics, which occur when vegetation comes out of equilibrium with climate, are potentially a key facet of these. Understanding these dynamics is crucial for making accurate predictions, informing conservation planning, and understanding likely changes in ecosystem function on time scales relevant to society. However, many predictive studies have instead focused on equilibrium end-points with little consideration of the transient trajectories. Methods: We review what we should expect in terms of disequilibrium vegetation dynamics over the next 50–200 yr, covering a broad range of research fields including paleoecology, macroecology, landscape ecology, vegetation science, plant ecology, invasion biology, global change biology, and ecosystem ecology. Key results: The expected climate changes are likely to induce marked vegetation disequilibrium with climate at both leading and trailing edges, with leading-edge disequilibrium dynamics due to lags in migration at continental to landscape scales, in local population build-up and succession, in local evolutionary responses, and in ecosystem development, and trailing-edge disequilibrium dynamics involving delayed local extinctions and slow losses of ecosystem structural components. Interactions with habitat loss and invasive pests and pathogens are likely to further contribute to disequilibrium dynamics. Predictive modeling and climate-change experiments are increasingly representing disequilibrium dynamics, but with scope for improvement. Conclusions: The likely pervasiveness and complexity of vegetation disequilibrium is a major challenge for forecasting ecological dynamics and, combined with the high ecological importance of vegetation, also constitutes a major challenge for future nature conservation.
The application of next-generation sequencing (NGS) technologies for the development of simple sequence repeat (SSR) or microsatellite loci for genetic research in the botanical sciences is described. Microsatellite markers are one of the most informative and versatile DNA-based markers used in plant genetic research, but their development has traditionally been a difficult and costly process. NGS technologies allow the efficient identification of large numbers of microsatellites at a fraction of the cost and effort of traditional approaches. The major advantage of NGS methods is their ability to produce large amounts of sequence data from which to isolate and develop numerous genome-wide and gene-based microsatellite loci. The two major NGS technologies with emergent application in SSR isolation are 454 and Illumina. A review is provided of several recent studies demonstrating the efficient use of 454 and Illumina technologies for the discovery of microsatellites in plants. Additionally, important aspects during NGS isolation and development of microsatellites are discussed, including the use of computational tools and high-throughput genotyping methods. A data set of microsatellite loci in the plastome and mitochondriome of cranberry (Vaccinium macrocarpon Ait.) is provided to illustrate a successful application of 454 sequencing for SSR discovery. In the future, NGS technologies will massively increase the number of SSRs and other genetic markers available to conduct genetic research in understudied but economically important crops such as cranberry.
Polyploidy has long been recognized as a major force in angiosperm evolution. Recent genomic investigations not only indicate that polyploidy is ubiquitous among angiosperms, but also suggest several ancient genome-doubling events. These include ancient whole genome duplication (WGD) events in basal angiosperm lineages, as well as a proposed paleohexaploid event that may have occurred close to the eudicot divergence. However, there is currently no evidence for WGD in Amborella, the putative sister species to other extant angiosperms. The question is no longer "What proportion of angiosperms are polyploid?", but "How many episodes of polyploidy characterize any given lineage?" New algorithms provide promise that ancestral genomes can be reconstructed for deep divergences (e.g., it may be possible to reconstruct the ancestral eudicot or even the ancestral angiosperm genome). Comparisons of diversification rates suggest that genome doubling may have led to a dramatic increase in species richness in several angiosperm lineages, including Poaceae, Solanaceae, Fabaceae, and Brassicaceae. However, additional genomic studies are needed to pinpoint the exact phylogenetic placement of the ancient polyploidy events within these lineages and to determine when novel genes resulting from polyploidy have enabled adaptive radiations.
Bacterial root endophytes reside in a vast number of plant species as part of their root microbiome, with some being shown to positively influence plant growth. Endophyte community structure (species diversity: richness and relative abundances) within the plant is dynamic and is influenced by abiotic and biotic factors such as soil conditions, biogeography, plant species, microbe—microbe interactions and plant—microbe interactions, both at local and larger scales. Plant-growth-promoting bacterial endophytes (PGPBEs) have been identified, but the predictive success at positively influencing plant growth in field conditions has been limited. Concurrent to the development of modern molecular techniques, the goal of predicting an organism's ability to promote plant growth can perhaps be realized by more thorough examination of endophyte community dynamics. This paper reviews the drivers of endophyte community structure relating to plant growth promotion, the mechanisms of plant growth promotion, and the current and future use of molecular techniques to study these communities.
Premise of the study: Just as Sanger sequencing did more than 20 years ago, next-generation sequencing (NGS) is poised to revolutionize plant systematics. By combining multiplexing approaches with NGS throughput, systematists may no longer need to choose between more taxa or more characters. Here we describe a genome skimming (shallow sequencing) approach for plant systematics. Methods: Through simulations, we evaluated optimal sequencing depth and performance of single-end and paired-end short read sequences for assembly of nuclear ribosomal DNA (rDNA) and plastomes and addressed the effect of divergence on reference-guided plastome assembly. We also used simulations to identify potential phylogenetic markers from low-copy nuclear loci at different sequencing depths. We demonstrated the utility of genome skimming through phylogenetic analysis of the Sonoran Desert clade (SDC) of Asclepias (Apocynaceae). Key results: Paired-end reads performed better than single-end reads. Minimum sequencing depths for high quality rDNA and plastome assemblies were 40x and 30x, respectively. Divergence from the reference significantly affected plastome assembly, but relatively similar references are available for most seed plants. Deeper rDNA sequencing is necessary to characterize intragenomic polymorphism. The low-copy fraction of the nuclear genome was readily surveyed, even at low sequencing depths. Nearly 160000 bp of sequence from three organelles provided evidence of phylogenetic incongruence in the SDC. Conclusions: Adoption of NGS will facilitate progress in plant systematics, as whole plastome and rDNA cistrons, partial mitochondrial genomes, and low-copy nuclear markers can now be efficiently obtained for molecular phylogenetics studies.
Polyploidy, or whole genome multiplication, is ubiquitous among angiosperms. Many crop species are relatively recent allopolyploids, resulting from interspecific hybridization and polyploidy. Thus, an appreciation of the evolutionary consequences of (allo)polyploidy is central to our understanding of crop plant domestication, agricultural improvement, and the evolution of angiosperms in general. Indeed, many recent insights into plant biology have been gleaned from polyploid crops, including, but not limited to wheat, tobacco, sugarcane, apple, and cotton. A multitude of evolutionary processes affect polyploid genomes, including rapid and substantial genome reorganization, transgressive gene expression alterations, gene fractionation, gene conversion, genome downsizing, and sub‐ and neofunctionalization of duplicate genes. Often these genomic changes are accompanied by heterosis, robustness, and the improvement of crop yield, relative to closely related diploids. Historically, however, the genome‐wide analysis of polyploid crops has lagged behind those of diploid crops and other model organisms. This lag is partly due to the difficulties in genome assembly, resulting from the genomic complexities induced by combining two or more evolutionarily diverged genomes into a single nucleus and by the significant size of polyploid genomes. In this review, we explore the role of polyploidy in angiosperm evolution, the domestication process and crop improvement. We focus on the potential of modern technologies, particularly next‐generation sequencing, to inform us on the patterns and processes governing polyploid crop improvement and phenotypic change subsequent to domestication.
Although the chloroplast genome contains many noncoding regions, relatively few have been exploited for interspecific phylogenetic and intraspecific phylogeographic studies. In our recent evaluation of the phylogenetic utility of 21 noncoding chloroplast regions, we found the most widely used noncoding regions are among the least variable, but the more variable regions have rarely been employed. That study led us to conclude that there may be unexplored regions of the chloroplast genome that have even higher relative levels of variability. To explore the potential variability of previously unexplored regions, we compared three pairs of single-copy chloroplast genome sequences in three disparate angiosperm lineages: Atropa vs. Nicotiana (asterids); Lotus vs. Medicago (rosids); and Saccharum vs. Oryza (monocots). These three separate sequence alignments highlighted 13 mutational hotspots that may be more variable than the best regions of our former study. These 13 regions were then selected for a more detailed analysis. Here we show that nine of these newly explored regions (rpl32-trnL(UAG), trnQ(UUG)-5′rps16, 3′trnV(UAC)-ndhC, ndhF-rpl32, psbD-trnT(GGU), psbJ-petA, 3′rps16–5′trnK(UUU), atpI-atpH, and petL-psbE) offer levels of variation better than the best regions identified in our earlier study and are therefore likely to be the best choices for molecular studies at low taxonomic levels.
Premise: Bromeliaceae form a large, ecologically diverse family of angiosperms native to the New World. We use a bromeliad phylogeny based on eight plastid regions to analyze relationships within the family, test a new, eight-subfamily classification, infer the chronology of bromeliad evolution and invasion of different regions, and provide the basis for future analyses of trait evolution and rates of diversification. Methods: We employed maximum-parsimony, maximum-likelihood, and Bayesian approaches to analyze 9341 aligned bases for four outgroups and 90 bromeliad species representing 46 of 58 described genera. We calibrate the resulting phylogeny against time using penalized likelihood applied to a monocot-wide tree based on plastid ndhF sequences and use it to analyze patterns of geographic spread using parsimony, Bayesian inference, and the program S-DIVA. Results: Bromeliad subfamilies are related to each other as follows: (Brocchinioideae, (Lindmanioideae, (Tillandsioideae, (Hechtioideae, (Navioideae, (Pitcairnioideae, (Puyoideae, Bromelioideae))). Bromeliads arose in the Guayana Shield ca. 100 million years ago (Ma), spread centrifugally in the New World beginning ca. 16–13 Ma, and dispersed to West Africa ca. 9.3 Ma. Modern lineages began to diverge from each other roughtly 19 Ma. Conclusions: Nearly two-thirds of extant bromeliads belong to two large radiations: the core tillandsioids, originating in the Andes ca. 14.2 Ma, and the Brazilian Shield bromelioids, originating in the Serro do Mar and adjacent regions ca. 9.1 Ma.
In this essay, we review research from the social sciences on how the public makes sense of and participates in societal decisions about science and technology. We specifically highlight the role of the media and public communication in this process, challenging the still dominant assumption that science literacy is both the problem and the solution to societal conflicts. After reviewing the cases of evolution, climate change, food biotechnology, and nanotechnology, we offer a set of detailed recommendations for improved public engagement efforts on the part of scientists and their organizations. We emphasize the need for science communication initiatives that are guided by careful formative research; that span a diversity of media platforms and audiences; and that facilitate conversations with the public that recognize, respect, and incorporate differences in knowledge, values, perspectives, and goals.
Premise of the study: Land plants play an essential role in the evolution of terrestrial life. Their time of origin and diversification is fundamental to understanding the evolution of life on land. We investigated the timing and the rate of molecular evolution of land plants, evaluating the effects of different types of molecular data, including temporal information from fossils, and using different molecular clock methods. Methods: Ages and absolute rates were estimated independently with two substitutionally different data sets: a highly conserved 4-gene data set and matK, a fast-evolving gene. The vascular plant backbone and the crown nodes of all major lineages were calibrated with fossil-derived ages. Dates and absolute rates were estimated while including or excluding the calibrations and using two relaxed clocks that differ in their implementation of temporal autocorrelation. Key results: Land plants diverged from streptophyte alga 912 (870–962) million years ago (Mya) but diversified into living lineages 475 (471–480) Mya. Ages estimated for all major land-plant lineages agree with their fossil record, except for angiosperms. Different genes estimated very similar ages and correlated absolute rates across the tree. Excluding calibrations resulted in the greatest age differences. Different relaxed clocks provided similar ages, but different and uncorrelated absolute rates. Conclusions: Whole-genome rate accelerations or decelerations may underlie the similar ages and correlated absolute rates estimated with different genes. We suggest that pronounced substitution rate changes around the angiosperm crown node may represent a challenge for relaxed clocks to model adequately.
Investigators have long searched for a polyploidy paradigm—rules or principles that might be common following polyploidization (whole‐genome duplication, WGD). Here we attempt to integrate what is known across the more thoroughly investigated polyploid systems on topics ranging from genetics to ecology. We found that while certain rules may govern gene retention and loss, systems vary in the prevalence of gene silencing vs. homeolog loss, chromosomal change, the presence of a dominant genome (in allopolyploids), and the relative importance of hybridization vs. genome doubling per se. In some lineages, aspects of polyploidization are repeated across multiple origins, but in other species multiple origins behave more stochastically in terms of genetic and phenotypic change. Our investigation also reveals that the path to synthesis is hindered by numerous gaps in our knowledge of even the best‐known systems. Particularly concerning is the absence of linkage between genotype and phenotype. Moreover, most recent studies have focused on the genetic and genomic attributes of polyploidy, but rarely is there an ecological or physiological context. To promote a path to a polyploidy paradigm (or paradigms), we propose a major community goal over the next 10–20 yr to fill the gaps in our knowledge of well‐studied polyploids. Before a meaningful synthesis is possible, more complete data sets are needed for comparison—systems that include comparable genetic, genomic, chromosomal, proteomic, as well as morphological, physiological, and ecological data. Also needed are more natural evolutionary model systems, as most of what we know about polyploidy continues to come from a few crop and genetic models, systems that often lack the ecological context inherent in natural systems and necessary for understanding the drivers of biodiversity.
Although theory has demonstrated rather low levels of gene flow are sufficient to counteract opposing mutation, drift, and selection, widespread recognition of the evolutionary importance of gene flow has come slowly. The perceived role of gene flow as an evolutionary force has vacillated over the last century. In the last few decades, new methods and analyses have demonstrated that plant gene flow rates vary tremendously—from nil to very high—depending on the species and specific populations involved, and sometimes over time for individual populations. In many cases, the measured gene flow rates are evolutionarily significant at distances of hundreds and sometimes thousands of meters, occurring at levels sufficient to counteract drift, spread advantageous alleles, or thwart moderate levels of opposing local selection. Gene flow in plants is likely to often act as a cohesive force, uniting individual plant species into real evolutionary units. Also, gene flow can evolve under natural selection, decreasing or increasing. The fact of frequent, but variable, plant gene flow has important consequences for applied issues in which the presence or absence of gene flow might influence the outcome of a policy, regulatory, or management decision. Examples include the unintended spread of engineered genes, the evolution of invasiveness, and conservation. New data‐rich genomic techniques allow closer scrutiny of the role of gene flow in plant evolution. Most plant evolutionists now recognize the importance of gene flow, and it is receiving increased recognition from other areas of plant biology as well.
Premise of the study: Endophytic and endolichenic fungi occur in healthy tissues of plants and lichens, respectively, playing potentially important roles in the ecology and evolution of their hosts. However, previous sampling has not comprehensively evaluated the biotic, biogeographic, and abiotic factors that structure their communities. Methods: Using molecular data we examined the diversity, composition, and distributions of 4154 endophytic and endolichenic Ascomycota cultured from replicate surveys of ca. 20 plant and lichen species in each of five North American sites (Madrean coniferous forest, Arizona; montane semideciduous forest, North Carolina; scrub forest, Florida; Beringian tundra and forest, western Alaska; subalpine tundra, eastern central Alaska). Key results: Endolichenic fungi were more abundant and diverse per host species than endophytes, but communities of endophytes were more diverse overall, reflecting high diversity in mosses and lycophytes. Endophytes of vascular plants were largely distinct from fungal communities that inhabit mosses and lichens. Fungi from closely related hosts from different regions were similar in higher taxonomy, but differed at shallow taxonomic levels. These differences reflected climate factors more strongly than geographic distance alone. Conclusions: Our study provides a first evaluation of endophytic and endolichenic fungal associations with their hosts at a continental scale. Both plants and lichens harbor abundant and diverse fungal communities whose incidence, diversity, and composition reflect the interplay of climatic patterns, geographic separation, host type, and host lineage. Although culture-free methods will inform future work, our study sets the stage for empirical assessments of ecological specificity, metabolic capability, and comparative genomics.