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Chromosomal distribution of cytonuclear genes in a dioecious plant with sex chromosomes.
Genome Biol Evol
PUBLISHED: 09-04-2014
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The coordination between nuclear and organellar genes is essential to many aspects of eukaryotic life, including basic metabolism, energy production, and ultimately, organismal fitness. Although nuclear genes are biparentally inherited, mitochondrial and chloroplast genes are almost exclusively maternally inherited, and this asymmetry may lead to a bias in the chromosomal distribution of nuclear genes whose products act in the mitochondria or chloroplasts. In particular, because X-linked genes have a higher probability of cotransmission with organellar genes (2/3) compared with autosomal genes (1/2), selection for coadaptation has been predicted to lead to an overrepresentation of nuclear-mitochondrial and nuclear-chloroplast genes on the X chromosome relative to autosomes. In contrast, the occurrence of sexually antagonistic organellar mutations might lead to selection for movement of cytonuclear genes from the X chromosome to autosomes to reduce male mutation load. Recent broad-scale comparative studies of N-mt distributions in animals have found evidence for these hypotheses in some species, but not others. Here, we use transcriptome sequences to conduct the first study of the chromosomal distribution of cytonuclear interacting genes in a plant species with sex chromosomes (Rumex hastatulus; Polygonaceae). We found no evidence of under- or overrepresentation of either N-mt or N-cp genes on the X chromosome, and thus no support for either the coadaptation or the sexual-conflict hypothesis. We discuss how our results from a species with recently evolved sex chromosomes fit into an emerging picture of the evolutionary forces governing the chromosomal distribution of nuclear-mitochondrial and nuclear-chloroplast genes.
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Floral variation and environmental heterogeneity in a tristylous clonal aquatic of the Pantanal wetlands of Brazil.
Ann. Bot.
PUBLISHED: 09-01-2014
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The balance between stochastic forces and frequency-dependent mating largely governs style morph frequencies in heterostylous populations. In clonal species, deviations from equal morph ratios often result from founder events and unfavourable conditions for sexual reproduction. The aim of this study was to investigate whether different flooding regimes, because of their influence on sexual vs. clonal reproduction, are associated with regional variation in morph frequencies and floral trait differentiation in populations of the clonal, tristylous, aquatic Eichhornia azurea (Pontederiaceae) in the Pantanal wetlands of Brazil.
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Size-dependent gender modification in Lilium apertum (Liliaceae): does this species exhibit gender diphasy?
Ann. Bot.
PUBLISHED: 07-25-2014
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Variation in the relative female and male reproductive success of flowering plants is widespread, despite the fundamental hermaphroditic condition of the majority of species. In many hermaphroditic populations, environmental conditions and their influence on development and size can influence the gender expression of individuals through the formation of hermaphroditic and unisexual flowers. This study investigates the hypothesis that the bulbous, animal-pollinated, perennial Lilium apertum (Liliaceae) exhibits a form of size-dependent gender modification known as gender diphasy, in which the sexual expression of individuals depends on their size, with plants often changing sex between seasons.
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The demography and population genomics of evolutionary transitions to self-fertilization in plants.
Philos. Trans. R. Soc. Lond., B, Biol. Sci.
PUBLISHED: 06-25-2014
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The evolution of self-fertilization from outcrossing has occurred on numerous occasions in flowering plants. This shift in mating system profoundly influences the morphology, ecology, genetics and evolution of selfing lineages. As a result, there has been sustained interest in understanding the mechanisms driving the evolution of selfing and its environmental context. Recently, patterns of molecular variation have been used to make inferences about the selective mechanisms associated with mating system transitions. However, these inferences can be complicated by the action of linked selection following the transition. Here, using multilocus simulations and comparative molecular data from related selfers and outcrossers, we demonstrate that there is little evidence for strong bottlenecks associated with initial transitions to selfing, and our simulation results cast doubt on whether it is possible to infer the role of bottlenecks associated with reproductive assurance in the evolution of selfing. They indicate that the effects of background selection on the loss of diversity and efficacy of selection occur rapidly following the shift to high selfing. Future comparative studies that integrate explicit ecological and genomic details are necessary for quantifying the independent and joint effects of selection and demography on transitions to selfing and the loss of genetic diversity.
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Understanding the spectacular failure of DNA barcoding in willows (Salix): does this result from a trans-specific selective sweep?
Mol. Ecol.
PUBLISHED: 05-29-2014
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Willows (Salix: Salicaceae) form a major ecological component of Holarctic floras and consequently are an obvious target for a DNA-based identification system. We surveyed two to seven plastid genome regions (~3.8 kb; ~3% of the genome) from 71 Salix species across all five subgenera, to assess their performance as DNA barcode markers. Although Salix has a relatively high level of interspecific hybridization, this may not sufficiently explain the near complete failure of barcoding that we observed: only one species had a unique barcode. We recovered 39 unique haplotypes, from more than 500 specimens, that could be partitioned into six major haplotype groups. A unique variant of group I (haplotype 1*) was shared by 53 species in three of five Salix subgenera. This unusual pattern of haplotype sharing across infrageneric taxa is suggestive of either a massive nonrandom coalescence failure (incomplete lineage sorting), or of repeated plastid capture events, possibly including a historical selective sweep of haplotype 1* across taxonomic sections. The former is unlikely as molecular dating indicates that haplotype 1* originated recently and is nested in the oldest major haplotype group in the genus. Further, we detected significant non-neutrality in the frequency spectrum of mutations in group I, but not outside group I, and demonstrated a striking absence of geographical (isolation by distance) effects in the haplotype distributions of this group. The most likely explanation for the patterns we observed involves recent repeated plastid capture events, aided by widespread hybridization and long-range seed dispersal, but primarily propelled by one or more trans-species selective sweeps.
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Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus.
Proc. Natl. Acad. Sci. U.S.A.
PUBLISHED: 05-13-2014
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Heteromorphic sex chromosomes have originated independently in many species, and a common feature of their evolution is the degeneration of the Y chromosome, characterized by a loss of gene content and function. Despite being of broad significance to our understanding of sex chromosome evolution, the genetic changes that occur during the early stages of Y-chromosome degeneration are poorly understood, especially in plants. Here, we investigate sex chromosome evolution in the dioecious plant Rumex hastatulus, in which X and Y chromosomes have evolved relatively recently and occur in two distinct systems: an ancestral XX/XY system and a derived XX/XY1Y2 system. This polymorphism provides a unique opportunity to investigate the effect of sex chromosome age on patterns of divergence and gene degeneration within a species. Despite recent suppression of recombination and low X-Y divergence in both systems, we find evidence that Y-linked genes have started to undergo gene loss, causing ? 28% and ? 8% hemizygosity of the ancestral and derived X chromosomes, respectively. Furthermore, genes remaining on Y chromosomes have accumulated more amino acid replacements, contain more unpreferred changes in codon use, and exhibit significantly reduced gene expression compared with their X-linked alleles, with the magnitude of these effects being greatest for older sex-linked genes. Our results provide evidence for reduced selection efficiency and ongoing Y-chromosome degeneration in a flowering plant, and indicate that Y degeneration can occur soon after recombination suppression between sex chromosomes.
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Clonal genetic structure and diversity in populations of an aquatic plant with combined vs. separate sexes.
Mol. Ecol.
PUBLISHED: 05-02-2014
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Clonality is often implicated in models of the evolution of dioecy, but few studies have explicitly compared clonal structure between plant sexual systems, or between the sexes in dioecious populations. Here, we exploit the occurrence of monoecy and dioecy in clonal Sagittaria latifola (Alismataceae) to evaluate two main hypotheses: (i) clone sizes are smaller in monoecious than dioecious populations, because of constraints imposed on clone size by costs associated with geitonogamy; (ii) in dioecious populations, male clones are larger and flower more often than female clones because of sex-differential reproductive costs. Differences in clone size and flowering could result in discordance between ramet- and genet-based sex ratios. We used spatially explicit sampling to address these hypotheses in 10 monoecious and 11 dioecious populations of S. latifolia at the northern range limit in Eastern North America. In contrast to our predictions, monoecious clones were significantly larger than dioecious clones, probably due to their higher rates of vegetative growth and corm production, and in dioecious populations, there was no difference in clone size between females and males; ramet- and genet-based sex ratios were therefore highly correlated. Genotypic diversity declined with latitude for both sexual systems, but monoecious populations exhibited lower genotypic richness. Differences in life history between the sexual systems of S. latifolia appear to be the most important determinants of clonal structure and diversity.
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Rapid adaptation to climate facilitates range expansion of an invasive plant.
Science
PUBLISHED: 10-19-2013
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Adaptation to climate, evolving over contemporary time scales, could facilitate rapid range expansion across environmental gradients. Here, we examine local adaptation along a climatic gradient in the North American invasive plant Lythrum salicaria. We show that the evolution of earlier flowering is adaptive at the northern invasion front where it increases fitness as much as, or more than, the effects of enemy release and the evolution of increased competitive ability. However, early flowering decreases investment in vegetative growth, which reduces fitness by a factor of 3 in southern environments where the North American invasion commenced. Our results demonstrate that local adaptation can evolve quickly during range expansion, overcoming environmental constraints on propagule production.
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Variation and evolution of herkogamy in Exochaenium (Gentianaceae): implications for the evolution of distyly.
Ann. Bot.
PUBLISHED: 05-02-2013
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The spatial separation of stigmas and anthers (herkogamy) in flowering plants functions to reduce self-pollination and avoid interference between pollen dispersal and receipt. Little is known about the evolutionary relationships among the three main forms of herkogamy - approach, reverse and reciprocal herkogamy (distyly) - or about transitions to and from a non-herkogamous condition. This problem was examined in Exochaenium (Gentianaceae), a genus of African herbs that exhibits considerable variation in floral morphology, including the three forms of herkogamy.
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Ecological context and metapopulation dynamics affect sex-ratio variation among dioecious plant populations.
Ann. Bot.
PUBLISHED: 02-26-2013
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Populations of dioecious flowering plants commonly exhibit heterogeneity in sex ratios and deviations from the equilibrium expectation of equal numbers of females and males. Yet the role of ecological and demographic factors in contributing towards biased sex ratios is currently not well understood.
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The influence of demography and local mating environment on sex ratios in a wind-pollinated dioecious plant.
Ecol Evol
PUBLISHED: 02-06-2013
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Negative frequency-dependent selection should result in equal sex ratios in large populations of dioecious flowering plants, but deviations from equality are commonly reported. A variety of ecological and genetic factors can explain biased sex ratios, although the mechanisms involved are not well understood. Most dioecious species are long-lived and/or clonal complicating efforts to identify stages during the life cycle when biases develop. We investigated the demographic correlates of sex-ratio variation in two chromosome races of Rumex hastatulus, an annual, wind-pollinated colonizer of open habitats from the southern USA. We examined sex ratios in 46 populations and evaluated the hypothesis that the proximity of males in the local mating environment, through its influence on gametophytic selection, is the primary cause of female-biased sex ratios. Female-biased sex ratios characterized most populations of R. hastatulus (mean sex ratio = 0.62), with significant female bias in 89% of populations. Large, high-density populations had the highest proportion of females, whereas smaller, low-density populations had sex ratios closer to equality. Progeny sex ratios were more female biased when males were in closer proximity to females, a result consistent with the gametophytic selection hypothesis. Our results suggest that interactions between demographic and genetic factors are probably the main cause of female-biased sex ratios in R. hastatulus. The annual life cycle of this species may limit the scope for selection against males and may account for the weaker degree of bias in comparison with perennial Rumex species.
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Evolutionarily stable sex ratios and mutation load.
Evolution
PUBLISHED: 01-09-2013
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Frequency-dependent selection should drive dioecious populations toward a 1:1 sex ratio, but biased sex ratios are widespread, especially among plants with sex chromosomes. Here, we develop population genetic models to investigate the relationships between evolutionarily stable sex ratios, haploid selection, and deleterious mutation load. We confirm that when haploid selection acts only on the relative fitness of X- and Y-bearing pollen and the sex ratio is controlled by the maternal genotype, seed sex ratios evolve toward 1:1. When we also consider haploid selection acting on deleterious mutations, however, we find that biased sex ratios can be stably maintained, reflecting a balance between the advantages of purging deleterious mutations via haploid selection, and the disadvantages of haploid selection on the sex ratio. Our results provide a plausible evolutionary explanation for biased sex ratios in dioecious plants, given the extensive gene expression that occurs across plant genomes at the haploid stage.
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Diplostigmaty in plants: a novel mechanism that provides reproductive assurance.
Biol. Lett.
PUBLISHED: 01-01-2013
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Differentiation of female sexual organs in flowering plants is rare and contrasts with the wide range of male reproductive strategies. An unusual example involves diplostigmaty, the possession of spatially and temporally distinct stigmas in Sebaea (Gentianaceae). Here, the single pistil within a flower has an apical stigma, as occurs in most flowering plants, but also a secondary stigma that occurs midway down the style, which is physically discrete and receptive several days after the apical stigma. We examined the function of diplostigmaty in Sebaea aurea, an insect-pollinated species of the Western Cape of South Africa. Floral manipulations and measurements of fertility and mating patterns provided evidence that basal stigmas function to enable autonomous delayed self-pollination, without limiting opportunities for outcrossing and thus avoiding the costs of seed discounting. We suggest that delayed selfing serves as a mechanism of reproductive assurance in populations with low plant density. The possession of dimorphic stigma function provides a novel example of a flexible mixed-mating strategy in plants that is responsive to changing demographic conditions.
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The evolution of plant reproductive systems: how often are transitions irreversible?
Proc. Biol. Sci.
PUBLISHED: 01-01-2013
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Flowering plants are characterized by striking variation in reproductive systems, and the evolutionary lability of their sexual traits is often considered a major driver of lineage diversification. But, evolutionary transitions in reproductive form and function are never entirely unconstrained and many changes exhibit strong directionality. Here, I consider why this occurs by examining transitions in pollination, mating and sexual systems, some of which have been considered irreversible. Among pollination systems, shifts from bee to hummingbird pollination are rarely reversible, whereas transitions from animal to wind pollination are occasionally reversed. Specialized pollination systems can become destabilized through a loss of pollinator service resulting in a return to generalized pollination, or more commonly a reliance on self-pollination. Homomorphic and heteromorphic self-incompatibility systems have multiple origins but breakdown to self-compatibility occurs much more frequently with little evidence for subsequent gains, at least over short time-spans. Similarly, numerous examples of the shift from outcrossing to predominant self-fertilization are known, but cases of reversal are very limited supporting the view that autogamy usually represents an evolutionary dead-end. The evolution of dioecy from hermaphroditism has also been considered irreversible, although recent evidence indicates that the occurrence of sex inconstancy and hybridization can lead to the origin of derived sexual systems from dioecy. The directionality of many transitions clearly refutes the notion of unconstrained reproductive flexibility, but novel adaptive solutions generally do not retrace earlier patterns of trait evolution.
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Reversal of height dimorphism promotes pollen and seed dispersal in a wind-pollinated dioecious plant.
Biol. Lett.
PUBLISHED: 11-02-2011
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Variation in the timing of reproductive functions in dioecious organisms may result in adaptive changes in the direction of sexual dimorphism during the breeding season. For plants in which both pollen and seeds are wind-dispersed, it may be advantageous for male plants to be taller when pollen is dispersed and female plants to be taller when seeds are dispersed. We examined the dynamics of height dimorphism in Rumex hastatulus, an annual, wind-pollinated, dioecious plant from the southern USA. A field survey of seven populations indicated that females were significantly taller than males at seed maturity. However, a glasshouse experiment revealed a more complex pattern of height growth during the life cycle. No dimorphism was evident prior to reproduction for six of seven populations, but at flowering, males were significantly taller than females in all populations. This pattern was reversed at reproductive maturity, consistent with field observations. Males flowered later than females and the degree of height dimorphism was greater in populations with a later onset of male flowering. We discuss the potential adaptive significance of temporal changes in height dimorphism for pollen and seed dispersal, and how this may be optimized for the contrasting reproductive functions of the sexes.
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The natural history of pollination and mating in bird-pollinated Babiana (Iridaceae).
Ann. Bot.
PUBLISHED: 08-10-2011
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Floral variation, pollination biology and mating patterns were investigated in sunbird-pollinated Babiana (Iridaceae) species endemic to the Western Cape of South Africa. The group includes several taxa with specialized bird perches and it has been proposed that these function to promote cross-pollination.
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Reconciling gene and genome duplication events: using multiple nuclear gene families to infer the phylogeny of the aquatic plant family Pontederiaceae.
Mol. Biol. Evol.
PUBLISHED: 06-01-2011
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Most plant phylogenetic inference has used DNA sequence data from the plastid genome. This genome represents a single genealogical sample with no recombination among genes, potentially limiting the resolution of evolutionary relationships in some contexts. In contrast, nuclear DNA is inherently more difficult to employ for phylogeny reconstruction because major mutational events in the genome, including polyploidization, gene duplication, and gene extinction can result in homologous gene copies that are difficult to identify as orthologs or paralogs. Gene tree parsimony (GTP) can be used to infer the rooted species tree by fitting gene genealogies to species trees while simultaneously minimizing the estimated number of duplications needed to reconcile conflicts among them. Here, we use GTP for five nuclear gene families and a previously published plastid data set to reconstruct the phylogenetic backbone of the aquatic plant family Pontederiaceae. Plastid-based phylogenetic studies strongly supported extensive paraphyly of Eichhornia (one of the four major genera) but also depicted considerable ambiguity concerning the true root placement for the family. Our results indicate that species trees inferred from the nuclear genes (alone and in combination with the plastid data) are highly congruent with gene trees inferred from plastid data alone. Consideration of optimal and suboptimal gene tree reconciliations place the root of the family at (or near) a branch leading to the rare and locally restricted E. meyeri. We also explore methods to incorporate uncertainty in individual gene trees during reconciliation by considering their individual bootstrap profiles and relate inferred excesses of gene duplication events on individual branches to whole-genome duplication events inferred for the same branches. Our study improves understanding of the phylogenetic history of Pontederiaceae and also demonstrates the utility of GTP for phylogenetic analysis.
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Population divergence along lines of genetic variance and covariance in the invasive plant Lythrum salicaria in eastern North America.
Evolution
PUBLISHED: 05-03-2011
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Evolution during biological invasion may occur over contemporary timescales, but the rate of evolutionary change may be inhibited by a lack of standing genetic variation for ecologically relevant traits and by fitness trade-offs among them. The extent to which these genetic constraints limit the evolution of local adaptation during biological invasion has rarely been examined. To investigate genetic constraints on life-history traits, we measured standing genetic variance and covariance in 20 populations of the invasive plant purple loosestrife (Lythrum salicaria) sampled along a latitudinal climatic gradient in eastern North America and grown under uniform conditions in a glasshouse. Genetic variances within and among populations were significant for all traits; however, strong intercorrelations among measurements of seedling growth rate, time to reproductive maturity and adult size suggested that fitness trade-offs have constrained population divergence. Evidence to support this hypothesis was obtained from the genetic variance-covariance matrix (G) and the matrix of (co)variance among population means (D), which were 79.8% (95% C.I. 77.7-82.9%) similar. These results suggest that population divergence during invasive spread of L. salicaria in eastern North America has been constrained by strong genetic correlations among life-history traits, despite large amounts of standing genetic variation for individual traits.
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The evolution of ovule number and flower size in wind-pollinated plants.
Am. Nat.
PUBLISHED: 04-05-2011
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In angiosperms, ovules are "packaged" within individual flowers, and an optimal strategy should occur depending on pollination and resource conditions. In animal-pollinated species, wide variation in ovule number per flower occurs, and this contrasts with wind-pollinated plants, where most species possess uniovulate flowers. This pattern is usually explained as an adaptive response to low pollen receipt in wind-pollinated species. Here, we develop a phenotypic model for the evolution of ovule number per flower that incorporates the aerodynamics of pollen capture and a fixed resource pool for provisioning of flowers, ovules, and seeds. Our results challenge the prevailing explanation for the association between uniovulate flowers and wind pollination. We demonstrate that when flowers are small and inexpensive, as they are in wind-pollinated species, ovule number should be minimized and lower than the average number of pollen tubes per style, even under stochastic pollination and fertilization regimes. The model predicts that plants benefit from producing many small inexpensive flowers, even though some flowers capture too few pollen grains to fertilize their ovules. Wind-pollinated plants with numerous flowers distributed throughout the inflorescence, each with a single ovule or a few ovules, sample more of the airstream, and this should maximize pollen capture and seed production.
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Genetic and environmental control of temporal and size-dependent sex allocation in a wind-pollinated plant.
Evolution
PUBLISHED: 03-29-2011
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Sex allocation in hermaphrodites can be affected by spatial and temporal variation in resources, especially in plants where size-dependent gender modification is commonplace. The evolution of sex allocation will depend on the relative importance of genetic and environmental factors governing patterns of investment in female and male function. In wind-pollinated plants, theoretical models predict a positive relation between size and male investment because of the fitness advantages associated with more effective pollen dispersal. Theory also predicts that the timing and allocation to each sex function should depend on available resources. We grew maternal half-sibling families of annual, wind-pollinated, Ambrosia artemisiifolia in sun and shade treatments to investigate these predictions. There was significant genetic variation for female and male flower production in both sun and shade treatments. Size-dependent sex allocation occurred in the direction predicted by theory, with male flower production increasing more rapidly in larger plants. The timing of sex function also varied, with significant genetic variation for dichogamy within environments and plasticity of this trait between environments. Protandry was expressed more commonly in the sun and protogyny in the shade. The occurrence of dynamic sex allocation with changing size and experimental treatment indicates the potential for adaptive responses under different ecological conditions.
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Floral dimorphism in plant populations with combined versus separate sexes.
Ann. Bot.
PUBLISHED: 03-07-2011
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Dimorphism among floral traits can evolve through variation in selection intensity between female and male performance, especially when sex functions are separated between flowers on a plant (monoecy), or between individuals (dioecy). In animal-pollinated species, male floral traits are predicted to be larger because competition for pollinators should favour larger displays. Floral dimorphism may be greater in dioecious than monoecious populations because of trade-offs between female and male function and opportunities for selfing in hermaphrodites.
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Spatial patterns of plant diversity below-ground as revealed by DNA barcoding.
Mol. Ecol.
PUBLISHED: 01-22-2011
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Our understanding of the spatial organization of root diversity in plant communities and of the mechanisms of community assembly has been limited by our ability to identify plants based on root tissue, especially in diverse communities. Here, we test the effectiveness of the plastid gene rbcL, a core plant DNA barcoding marker, for investigating spatial patterns of root diversity, and relate observed patterns to above-ground community structure. We collected 3800 root fragments from four randomly positioned, 1-m-deep soil profiles (two vertical transects per plot), located in an old-field community in southern Ontario, Canada, and extracted and sequenced DNA from 1531 subsampled fragments. We identified species by comparing sequences with a DNA barcode reference library developed previously for the local flora. Nearly 85% of sampled root fragments were successfully sequenced and identified as belonging to 29 plant species or species groups. Root abundance and species richness varied in horizontal space and were negatively correlated with soil depth. The relative abundance of taxa below-ground was correlated with their frequency above-ground (r = 0.73, P = 0.0001), but several species detected in root tissue were not observed in above-ground quadrats. Multivariate analyses indicated that diversity was highly structured below-ground, and associated with depth, root morphology, soil chemistry and soil texture, whereas little structure was evident above-ground. Furthermore, analyses of species co-occurrence indicates strong species segregation overall but random co-occurrence among confamilials. Our results provide insights into the role of environmental filtering and competitive interactions in the organization of plant diversity below-ground, and also demonstrate the utility of barcoding for the identification of plant roots.
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De novo sequence assembly and characterization of the floral transcriptome in cross- and self-fertilizing plants.
BMC Genomics
PUBLISHED: 01-06-2011
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The shift from cross-fertilization to predominant self-fertilization is among the most common evolutionary transitions in the reproductive biology of flowering plants. Increased inbreeding has important consequences for floral morphology, population genetic structure and genome evolution. The transition to selfing is usually characterized by a marked reduction in flower size and the loss of traits involved in pollinator attraction and the avoidance of self-fertilization. Here, we use short-read sequencing to assemble, de novo, the floral transcriptomes of three genotypes of Eichhornia paniculata, including an outcrosser and two genotypes from independently derived selfers, and a single genotype of the sister species E. paradoxa. By sequencing mRNA from tissues sampled at various stages of flower development, our goal was to sequence and assemble the floral transcriptome and identify differential patterns of gene expression.
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Trait correlates and functional significance of heteranthery in flowering plants.
New Phytol.
PUBLISHED: 08-31-2010
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• Flowering plants display extraordinary diversity in the morphology of male sexual organs, yet the functional significance of this variation is not well understood. Here, we conducted a comparative analysis of floral correlates of heteranthery - the morphological and functional differentiation of anthers within flowers - among angiosperm families to identify traits associated with this condition. • We performed a phylogenetic analysis of correlated evolution between heteranthery and several floral traits commonly reported from heterantherous taxa. In addition, we quantified the effect of phylogenetic uncertainty in the observed patterns of correlated evolution by comparing trees in which polytomous branches were randomly resolved. • Heteranthery is reported from 12 angiosperm orders and is phylogenetically associated with the absence of floral nectaries, buzz-pollination and enantiostyly (mirror-image flowers). These associations are robust to particularities of the underlying phylogenetic hypothesis. • Heteranthery has probably evolved as a result of pollinator-mediated selection and appears to function to reduce the conflict of relying on pollen both as food to attract pollinators and as the agent of male gamete transfer. The relative scarcity of heteranthery among angiosperm families suggests that the conditions permitting its evolution are not easily met despite the abundance of pollen-collecting bees and nectarless flowers.
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The population genomics of plant adaptation.
New Phytol.
PUBLISHED: 07-30-2010
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There has been an enormous increase in the amount of data on DNA sequence polymorphism available for many organisms in the last decade. New sequencing technologies provide great potential for investigating natural selection in plants using population genomic approaches. However, plant populations frequently show significant departures from the assumptions of standard models used to detect selection and many forms of directional selection do not fit with classical population genetics theory. Here, we explore the extent to which plant populations show departures from standard model assumptions, and the implications this has for detecting selection on molecular variation. A growing number of multilocus studies of nucleotide variation suggest that changes in population size, particularly bottlenecks, and strong subdivision may be common in plants. This demographic variation presents important challenges for models used to infer selection. In addition, selection from standing genetic variation and multiple independent adaptive substitutions can further complicate efforts to understand the nature of selection. We discuss emerging patterns from plant studies and propose that, rather than treating population history as a nuisance variable when testing for selection, the interaction between demography and selection is of fundamental importance for evolutionary studies of plant populations using molecular data.
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Ecological genetics of sex ratios in plant populations.
Philos. Trans. R. Soc. Lond., B, Biol. Sci.
PUBLISHED: 07-21-2010
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In many angiosperm species, populations are reproductively subdivided into distinct sexual morphs including females, males and hermaphrodites. Sexual polymorphism is maintained by frequency-dependent selection, leading to predictable sex ratios at equilibrium. Charles Darwin devoted much of his book The Different Forms of Flowers on Plants of the Same Species (1877) to investigating plant sexual polymorphisms and laid the foundation for many problems addressed today by integrating theory with empirical studies of the demography and genetics of populations. Here, we summarize our recent work on the ecological and genetic mechanisms influencing variation in sex ratios and their implications for evolutionary transitions among sexual systems. We present the results of a survey of sex ratios from 126 species from 47 angiosperm families and then address two general problems using examples from diverse angiosperm taxa: (i) the mechanisms governing biased sex ratios in dioecious species; (ii) the origins and maintenance of populations composed of females, males and hermaphrodites. Several themes are emphasized, including the importance of non-equilibrium conditions, the role of life history and demography in affecting sex ratios, the value of theory for modelling the dynamics of sex ratio variation, and the utility of genetic markers for investigating evolutionary processes in sexually polymorphic plant populations.
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Cryptic dioecy in Mussaenda pubescens (Rubiaceae): a species with stigma-height dimorphism.
Ann. Bot.
PUBLISHED: 07-19-2010
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Evolutionary transitions from heterostyly to dioecy have been proposed in several angiosperm families, particularly in Rubiaceae. These transitions involve the spread of male and female sterility mutations resulting in modifications to the gender of ancestral hermaphrodites. Despite sustained interest in the gender strategies of plants, the structural and developmental bases for transitions in sexual systems are poorly understood.
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Genetic uniformity characterizes the invasive spread of water hyacinth (Eichhornia crassipes), a clonal aquatic plant.
Mol. Ecol.
PUBLISHED: 06-10-2010
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Aquatic plant invasions are often associated with long-distance dispersal of vegetative propagules and prolific clonal reproduction. These reproductive features combined with genetic bottlenecks have the potential to severely limit genetic diversity in invasive populations. To investigate this question we conducted a global scale population genetic survey using amplified fragment length polymorphism markers of the worlds most successful aquatic plant invader -Eichhornia crassipes (water hyacinth). We sampled 1140 ramets from 54 populations from the native (South America) and introduced range (Asia, Africa, Europe, North America, Central America and the Caribbean). Although we detected 49 clones, introduced populations exhibited very low genetic diversity and little differentiation compared with those from the native range, and approximately 80% of introduced populations were composed of a single clone. A widespread clone (W) detected in two Peruvian populations accounted for 70.9% of the individuals sampled and dominated in 74.5% of the introduced populations. However, samples from Bangladesh and Indonesia were composed of different genotypes, implicating multiple introductions to the introduced range. Nine of 47 introduced populations contained clonal diversity suggesting that sexual recruitment occurs in some invasive sites where environmental conditions favour seedling establishment. The global patterns of genetic diversity in E. crassipes likely result from severe genetic bottlenecks during colonization and prolific clonal propagation. The prevalence of the W genotype throughout the invasive range may be explained by stochastic sampling, or possibly because of pre-adaptation of the W genotype to tolerate low temperatures.
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Evolutionary constraints on adaptive evolution during range expansion in an invasive plant.
Proc. Biol. Sci.
PUBLISHED: 02-17-2010
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Biological invasions may expose populations to strong selection for local adaptation along geographical gradients in climate. However, evolution during contemporary timescales can be constrained by low standing genetic variation and genetic correlations among life-history traits. We examined limits to local adaptation associated with northern migration of the invasive wetland plant purple loosestrife (Lythrum salicaria) using a selection model incorporating a trade-off between flowering time and size at reproduction, and common garden experiments of populations sampled along a latitudinal transect of approximately 1200 km in eastern North America. A strong trade-off between flowering time and size at reproduction caused early-flowering plants to be smaller with reduced seed production in northern populations. Northward spread was associated with a decline in genetic variance within populations and an increase in genetic skew for flowering time and size, with limited genetic variation for small, early-flowering genotypes. These patterns were predicted by our selection model of local adaptation to shorter growing seasons and were not consistent with expectations from non-adaptive processes. Reduced fecundity may limit population growth and rates of spread in northern populations. Identifying genetic constraints on key life-history traits can provide novel insights into invasion dynamics and the causes of range limits in introduced species.
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Darwins legacy: the forms, function and sexual diversity of flowers.
Philos. Trans. R. Soc. Lond., B, Biol. Sci.
PUBLISHED: 01-06-2010
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Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction. These works have provided the conceptual foundation for understanding floral adaptations that promote cross-fertilization and the mechanisms responsible for evolutionary transitions in reproductive systems. Many of Darwins insights, gained from careful observations and experiments on diverse angiosperm species, remain remarkably durable today and have stimulated much current research on floral function and the evolution of mating systems. Here I review Darwins seminal contributions to reproductive biology and provide an overview of the current status of research on several of the main topics to which he devoted considerable effort, including the consequences to fitness of cross- versus self-fertilization, the evolution and function of stylar polymorphisms, the adaptive significance of heteranthery, the origins of dioecy and related gender polymorphisms, and the transition from animal pollination to wind pollination. Post-Darwinian perspectives on floral function now recognize the importance of pollen dispersal and male outcrossed siring success in shaping floral adaptation. This has helped to link work on pollination biology and mating systems, two subfields of reproductive biology that remained largely isolated during much of the twentieth century despite Darwins efforts towards integration.
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Mating-system variation, demographic history and patterns of nucleotide diversity in the Tristylous plant Eichhornia paniculata.
Genetics
PUBLISHED: 11-16-2009
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Inbreeding in highly selfing populations reduces effective size and, combined with demographic conditions associated with selfing, this can erode genetic diversity and increase population differentiation. Here we investigate the role that variation in mating patterns and demographic history play in shaping the distribution of nucleotide variation within and among populations of the annual neotropical colonizing plant Eichhornia paniculata, a species with wide variation in selfing rates. We sequenced 10 EST-derived nuclear loci in 225 individuals from 25 populations sampled from much of the geographic range and used coalescent simulations to investigate demographic history. Highly selfing populations exhibited moderate reductions in diversity but there was no significant difference in variation between outcrossing and mixed mating populations. Population size interacted strongly with mating system and explained more of the variation in diversity within populations. Bayesian structure analysis revealed strong regional clustering and selfing populations were highly differentiated on the basis of an analysis of F(st). There was no evidence for a significant loss of within-locus linkage disequilibrium within populations, but regional samples revealed greater breakdown in Brazil than in selfing populations from the Caribbean. Coalescent simulations indicate a moderate bottleneck associated with colonization of the Caribbean from Brazil approximately 125,000 years before the present. Our results suggest that the recent multiple origins of selfing in E. paniculata from diverse outcrossing populations result in higher diversity than expected under long-term equilibrium.
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Evolutionary pathways to self-fertilization in a tristylous plant species.
New Phytol.
PUBLISHED: 07-08-2009
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Evolutionary transitions from outcrossing to selfing occur commonly in heterostylous genera. The morphological polymorphisms that characterize heterostyly provide opportunities for different pathways for selfing to evolve. Here, we investigate the origins and pathways by which selfing has evolved in tristylous Eichhornia paniculata by providing new evidence based on morphology, DNA sequences and genetic analysis. The primary pathway from outcrossing to selfing involves the stochastic loss of the short-styled morph (S-morph) from trimorphic populations, followed by the spread of selfing variants of the mid-styled morph (M-morph). However, the discovery of selfing variants of the long-styled morph (L-morph) in Central America indicates a secondary pathway and distinct origin for selfing. Comparisons of multi-locus nucleotide sequences from 27 populations sampled from throughout the geographical range suggest multiple transitions to selfing. Genetic analysis of selfing variants of the L- and M-morphs demonstrates recessive control of the loss of herkogamy, although the number of factors appears to differ between the forms. Early stages in the establishment of selfing involve developmental instability in the formation of flowers capable of autonomous self-pollination. The relatively simple genetic control of herkogamy reduction and frequent colonizing episodes may often create demographic conditions favouring transitions to selfing in E. paniculata.
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Are plant species inherently harder to discriminate than animal species using DNA barcoding markers?
Mol Ecol Resour
PUBLISHED: 05-01-2009
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The ability to discriminate between species using barcoding loci has proved more difficult in plants than animals, raising the possibility that plant species boundaries are less well defined. Here, we review a selection of published barcoding data sets to compare species discrimination in plants vs. animals. Although the use of different genetic markers, analytical methods and depths of taxon sampling may complicate comparisons, our results using common metrics demonstrate that the number of species supported as monophyletic using barcoding markers is higher in animals (> 90%) than plants (~70%), even after controlling for the amount of parsimony-informative information per species. This suggests that more than a simple lack of variability limits species discrimination in plants. Both animal and plant species pairs have variable size gaps between intra- and interspecific genetic distances, but animal species tend to have larger gaps than plants, even in relatively densely sampled genera. An analysis of 12 plant genera suggests that hybridization contributes significantly to variation in genetic discontinuity in plants. Barcoding success may be improved in some plant groups by careful choice of markers and appropriate sampling; however, overall fine-scale species discrimination in plants relative to animals may be inherently more difficult because of greater levels of gene-tree paraphyly.
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Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants.
Ann. Bot.
PUBLISHED: 02-14-2009
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The rich literature that characterizes the field of pollination biology has focused largely on animal-pollinated plants. At least 10 % of angiosperms are wind pollinated, and this mode of pollination has evolved on multiple occasions among unrelated lineages, and hence this discrepancy in research interest is surprising. Here, the evolution and functional ecology of pollination and mating in wind-pollinated plants are discussed, a theoretical framework for modelling the selection of wind pollination is outlined, and pollen capture and the occurrence of pollen limitation in diverse wind-pollinated herbs are investigated experimentally.
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Modification of flower architecture during early stages in the evolution of self-fertilization.
Ann. Bot.
PUBLISHED: 02-06-2009
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The evolution of selfing from outcrossing is characterized by a series of morphological changes to flowers culminating in the selfing syndrome. However, which morphological traits initiate increased self-pollination and which are accumulated after self-fertilization establishes is poorly understood. Because the expression of floral traits may depend on the conditions experienced by an individual during flower development, investigation of changes in mating system should also account for environmental and developmental factors. Here, early stages in the evolution of self-pollination are investigated by comparing floral traits among Brazilian populations of Eichhornia paniculata (Pontederiaceae), an annual aquatic that displays variation in selfing rates associated with the breakdown of tristyly to semi-homostyly.
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Isolation and characterization of 11 microsatellite markers from Sagittaria latifolia (Alismataceae).
Mol Ecol Resour
PUBLISHED: 01-16-2009
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We developed 11 microsatellite loci for Sagittaria latifolia, an aquatic plant common to wetlands of North America. From an (AG)-enriched library, we identified 66 unique microsatellite sequences for which primers could be designed. Twenty-two loci reliably amplified a clear single band of expected size, and 11 loci were scoreable and polymorphic. For these 11 loci, we genotyped a monoecious and a dioecious population, yielding four to 14 alleles per locus. Three loci exhibited significant linkage disequilibrium leaving eight independent variable loci. Eight loci also amplified in four other Sagittaria species. These microsatellite loci will be useful to compare genetic structure among monoecious and dioecious populations of S. latifolia.
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The consequences of monoecy and protogyny for mating in wind-pollinated Carex.
New Phytol.
PUBLISHED: 01-06-2009
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Monoecy and protogyny are widespread in wind-pollinated plants and have been interpreted as outcrossing mechanisms, though few studies have investigated their function. Carex, a large genus of anemophilous herbs, is predominantly monoecious and many species are protogynous. We investigated whether monoecy and protogyny limit self-pollination in seven Carex species. We conducted field experiments comparing stigmatic pollen loads and seed set between intact and emasculated stems. We tested for self-compatibility and evaluated pollen limitation of seed set by supplemental pollination. Finally, we measured outcrossing rates in open-pollinated and emasculated stems using allozyme markers. Emasculated stems captured significantly less pollen than open-pollinated stems and set less seed. Pollen deposition during the female-only phase for intact stems was only 12% of the total captured. Outcrossing rates for three species indicated high selfing (range t = 0.03-0.39). Allozyme loci in the remaining species were monomorphic also suggesting high selfing. These results demonstrate that neither monoecy nor protogyny is particularly effective at limiting self-fertilization. Selection for the avoidance of selfing is unlikely to maintain monoecy in many Carex species although protogyny may provide limited opportunities for outcrossing. We propose that geitonogamy in self-compatible wind-pollinated species with unisexual flowers may be widespread and provides reproductive assurance.
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Comparative analyses of sex-ratio variation in dioecious flowering plants.
Evolution
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Dioecious plant species commonly exhibit deviations from the equilibrium expectation of 1:1 sex ratio, but the mechanisms governing this variation are poorly understood. Here, we use comparative analyses of 243 species, representing 123 genera and 61 families to investigate ecological and genetic correlates of variation in the operational (flowering) sex ratio. After controlling for phylogenetic nonindependence, we examined the influence of growth form, clonality, fleshy fruits, pollen and seed dispersal vector, and the possession of sex chromosomes on sex-ratio variation. Male-biased flowering sex ratios were twice as common as female-biased ratios. Male bias was associated with long-lived growth forms (e.g., trees) and biotic seed dispersal and fleshy fruits, whereas female bias was associated with clonality, especially for herbaceous species, and abiotic pollen dispersal. Female bias occurred in species with sex chromosomes and there was some evidence for a greater degree of bias in those with heteromorphic sex chromosomes. Although the role of interactions among these correlates require further study, our results indicate that sex-based differences in costs of reproduction, pollen and seed dispersal mechanisms and sex chromosomes can each play important roles in affecting flowering sex ratios in dioecious plants.
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Sexual dimorphism in flowering plants.
J. Exp. Bot.
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Among dioecious flowering plants, females and males often differ in a range of morphological, physiological, and life-history traits. This is referred to as sexual dimorphism, and understanding why it occurs is a central question in evolutionary biology. Our review documents a range of sexually dimorphic traits in angiosperm species, discusses their ecological consequences, and details the genetic and evolutionary processes that drive divergence between female and male phenotypes. We consider why sexual dimorphism in plants is generally less well developed than in many animal groups, and also the importance of sexual and natural selection in contributing to differences between the sexes. Many sexually dimorphic characters, including both vegetative and flowering traits, are associated with differences in the costs of reproduction, which are usually greater in females, particularly in longer-lived species. These differences can influence the frequency and distribution of females and males across resource gradients and within heterogeneous environments, causing niche differences and the spatial segregation of the sexes. The interplay between sex-specific adaptation and the breakdown of between-sex genetic correlations allows for the independent evolution of female and male traits, and this is influenced in some species by the presence of sex chromosomes. We conclude by providing suggestions for future work on sexual dimorphism in plants, including investigations of the ecological and genetic basis of intraspecific variation, and genetic mapping and expression studies aimed at understanding the genetic architecture of sexually dimorphic trait variation.
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Genomic consequences of transitions from cross- to self-fertilization on the efficacy of selection in three independently derived selfing plants.
BMC Genomics
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Transitions from cross- to self-fertilization are associated with increased genetic drift rendering weakly selected mutations effectively neutral. The effect of drift is predicted to reduce selective constraints on amino acid sequences of proteins and relax biased codon usage. We investigated patterns of nucleotide variation to assess the effect of inbreeding on the accumulation of deleterious mutations in three independently evolved selfing plants. Using high-throughput sequencing, we assembled the floral transcriptomes of four individuals of Eichhornia (Pontederiaceae); these included one outcrosser and two independently derived selfers of E. paniculata, and E. paradoxa, a selfing outgroup. The dataset included ~8000 loci totalling ~3.5 Mb of coding DNA.
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Loss of floral polymorphism in heterostylous Luculia pinceana (Rubiaceae): a molecular phylogeographic perspective.
Mol. Ecol.
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Both deterministic and stochastic forces determine the representation and frequency of floral morphs in heterostylous plant populations. Phylogeographic analysis of molecular variation can provide information on the role of historical factors, including founder events, in affecting population morph structure. Here, we investigate geographical patterns of floral morph variation in a distylous shrub Luculia pinceana (Rubiaceae) by examining the relations between floral polymorphism and molecular (cpDNA and microsatellite) variation in 25 populations sampled throughout the distribution of the species in southwest China and adjacent countries. In 19 of the 25 populations, the frequency of floral morphs was not significantly different from the expected 1:1 ratio. The remaining populations were either L-morph biased (2) or monomorphic (4) for this form and were morphologically differentiated from the remaining populations in several floral traits, that is, corolla tube length, sex organ position and stigma-anther separation. Phylogeographic analysis supports the hypothesis that L. pinceana was initially split into west-central and eastern lineages in the Early Pleistocene (~1.982 Mya). A centrally located lineage composed of morph-biased and monomorphic populations appears to have been subsequently derived from the west-central lineage, perhaps by a founder event after the last glacial maximum. Hypotheses to explain why these populations have not returned to equilibrium morph frequencies are considered.
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Rain pollination provides reproductive assurance in a deceptive orchid.
Ann. Bot.
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Abiotic pollination by wind or water is well established in flowering plants. In some species pollination by rain splashes, a condition known as ombrophily, has been proposed as a floral strategy. However, evidence for this type of abiotic pollination has remained controversial and many reported cases have subsequently been shown to be false. This study investigates ombrophily in the deceptive orchid Acampe rigida to determine the mechanism by which this species is able to maintain high fecundity, despite flowering during the rainy season in south-west China when pollinators are scarce.
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Disassortative mating and the maintenance of sexual polymorphism in painted maple.
Mol. Ecol.
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Since Darwins pioneering research on plant reproductive biology (e.g. Darwin 1877), understanding the mechanisms maintaining the diverse sexual strategies of plants has remained an important challenge for evolutionary biologists. In some species, populations are sexually polymorphic and contain two or more mating morphs (sex phenotypes). Differences in morphology or phenology among the morphs influence patterns of non-random mating. In these populations, negative frequency-dependent selection arising from disassortative (intermorph) mating is usually required for the evolutionary maintenance of sexual polymorphism, but few studies have demonstrated the required patterns of non-random mating. In the current issue of Molecular Ecology, Shang et al. (2012) make an important contribution to our understanding of how disassortative mating influences sex phenotype ratios in Acer pictum subsp. mono (painted maple), a heterodichogamous, deciduous tree of eastern China. They monitored sex expression in 97 adults and used paternity analysis of open-pollinated seed to examine disassortative mating among three sex phenotypes. Using a deterministic pollen transfer model, Shang et al. present convincing evidence that differences in the degree of disassortative mating in progeny arrays of the sex phenotypes can explain their uneven frequencies in the adult population. This study provides a useful example of how the deployment of genetic markers, demographic monitoring and modelling can be integrated to investigate the maintenance of sexual diversity in plants.
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The effect of mammalian herbivory on inflorescence architecture in ornithophilous Babiana (Iridaceae): implications for the evolution of a bird perch.
Am. J. Bot.
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The showiness of floral displays is usually explained as an adaptation to attract pollinators. However, selection for less attractive displays imposed by non-pollinating agents, particularly herbivores, may balance pollinator-driven selection for highly visible inflorescences. We investigated whether inflorescence architecture, particularly the unusual ground-level flowering associated with a specialized bird perch in Babiana ringens may have originated, in part, as an adaptive response to mammalian herbivory.
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