The advantages and disadvantages of being polyploid

Polyploids - organisms that have multiple sets of chromosomes - are common in certain plant and animal taxa, and can be surprisingly stable. The evidence that has emerged from genome analyses also indicates that many other eukaryotic genomes have a polyploid ancestry, suggesting that both humans and most other eukaryotes have either benefited from or endured polyploidy. Studies of polyploids soon after their formation have revealed genetic and epigenetic interactions between redundant genes. These interactions can be related to the phenotypes and evolutionary fates of polyploids. Here, I consider the advantages and challenges of polyploidy, and its evolutionary potential.     

Rapid genomic changes in polyploid wheat and related species:implications for genome evolution and genetic improvement

A polyploid organism by possessing more than two sets of chromosomes from one species （autopolyploidy） or two or more species （allopolyploidy） is known to have evolutionary advantages. However, by what means a polyploid accommodates increased genetic dosage or divergent genomes （allopolyploidy） in one cell nucleus and cytoplasm constitutes an enormous challenge. Recent years have witnessed efforts and progress in exploring the possible mechanisms by which these seemingly intangible hurdles of polyploidy may be ameliorated or eventually overcome. In particular, the documentation of rapid and extensive non-Mendelian genetic and epigenetic changes that often accompany nascent polyploidy is revealing： the resulting non-additive and novel gene expression at global, regional and local levels, and timely restoration of meiotic chromosomal behavior towards bivalent pairing and disomic inheritance may ensure rapid establishment and stabilization as well as its long-term evolutionary success. Further elucidation on these novel mechanisms underpinning polyploidy will promote our understanding on fundamental issues in evolutionary biology and in our manipulation capacities in future genetic improvement of important crops that are currently polyploids in genomic constitution. This review is intended to provide an updated discussion on these interesting and important issues within the scope of a specific yet one of the most important plant groups--polyploid wheat and its related species.     

Genome evolution in polyploids

Polyploidy is a prominent process in plants and has been significant in the evolutionary history of vertebrates and other eukaryotes. In plants, interdisciplinary approaches combining phylogenetic and molecular genetic perspectives have enhanced our awareness of the myriad genetic interactions made possible by polyploidy. Here, processes and mechanisms of gene and genome evolution in polyploids are reviewed. Genes duplicated by polyploidy may retain their original or similar function, undergo diversification in protein function or regulation, or one copy may become silenced through mutational or epigenetic means. Duplicated genes also may interact through inter-locus recombination, gene conversion, or concerted evolution. Recent experiments have illuminated important processes in polyploids that operate above the organizational level of duplicated genes. These include inter-genomic chromosomal exchanges, saltational, non-Mendelian genomic evolution in nascent polyploids, inter-genomic invasion, and cytonuclear stabilization. Notwithstanding many recent insights, much remains to be learned about many aspects of polyploid evolution, including: the role of transposable elements in structural and regulatory gene evolution; processes and significance of epigenetic silencing; underlying controls of chromosome pairing; mechanisms and functional significance of rapid genome changes; cytonuclear accommodation; and coordination of regulatory factors contributed by two, sometimes divergent progenitor genomes. Continued application of molecular genetic approaches to questions of polyploid genome evolution holds promise for producing lasting insight into processes by which novel genotypes are generated and ultimately into how polyploidy facilitates evolution and adaptation.     

Perspectives on polyploidy in plants – ancient and neo

It is timely to re-examine the phenomenon of polyploidy in plants. Indeed, the power of modern molecular technology to provide new insights, and the impetus of genomics, make polyploidy a fit, fashionable and futuristic topic for review. Some historical perspective is essential to understand the meaning of the terms, to recognize what is already known and what is dogma, and to frame incisive questions for future research. Polyploidy is important because life on earth is predominantly a polyploid phenomenon. Moreover, civilization is mainly powered by polyploid food – notably cereal endosperm. Ongoing uncertainty about the origin of triploid endosperm epitomizes our ignorance about somatic polyploidy. New molecular information makes it timely to reconsider how to identity polyploids and what is a polyploid state. A functional definition in terms of a minimal genome may be helpful. Genes are known that can raise or lower ploidy level. Molecular studies can test if, contrary to dogma, the relationship between diploids and polyploids is a dynamic two-way system. We still need to understand the mechanisms and roles of key genes controlling ploidy level and disomic inheritance. New evidence for genome duplications should be compared with old ideas about cryptopolyploidy, and new views of meiosis should not ignore premeiotic genome separation. In practice, new knowledge about polyploidy will be most useful only when it reliably predicts which crops can be usefully improved as stable autopolyploids and which genomes combined to create successful new allopolyloids.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 411–423.     

Eco-evolutionary feedbacks,adaptive dynamics and evolutionary rescue theory

Adaptive dynamics theory has been devised to account for feedbacks between ecological and evolutionary processes. Doing so opens new dimensions to and raises new challenges about evolutionary rescue. Adaptive dynamics theory predicts that successive trait substitutions driven by eco-evolutionary feedbacks can gradually erode population size or growth rate, thus potentially raising the extinction risk. Even a single trait substitution can suffice to degrade population viability drastically at once and cause ‘evolutionary suicide’. In a changing environment, a population may track a viable evolutionary attractor that leads to evolutionary suicide, a phenomenon called ‘evolutionary trapping’. Evolutionary trapping and suicide are commonly observed in adaptive dynamics models in which the smooth variation of traits causes catastrophic changes in ecological state. In the face of trapping and suicide, evolutionary rescue requires that the population overcome evolutionary threats generated by the adaptive process itself. Evolutionary repellors play an important role in determining how variation in environmental conditions correlates with the occurrence of evolutionary trapping and suicide, and what evolutionary pathways rescue may follow. In contrast with standard predictions of evolutionary rescue theory, low genetic variation may attenuate the threat of evolutionary suicide and small population sizes may facilitate escape from evolutionary traps.     

Rarely successful polyploids and their legacy in plant genomes

Polyploidy, or whole genome duplication, is recognized as an important feature of eukaryotic genome evolution. Among eukaryotes, polyploidy has probably had the largest evolutionary impact on vascular plants where many contemporary species are of recent polyploid origin. Genomic analyses have uncovered evidence of at least one round of polyploidy in the ancestry of most plants, fueling speculation that genome duplications lead to increases in net diversity. In spite of the frequency of ancient polyploidy, recent analyses have found that recently formed polyploid species have higher extinction rates than their diploid relatives. These results suggest that despite leaving a substantial legacy in plant genomes, only rare polyploids survive over the long term and most are evolutionary dead-ends.     

The more the better? The role of polyploidy in facilitating plant invasions

Background

Biological invasions are a major ecological and socio-economic problem in many parts of the world. Despite an explosion of research in recent decades, much remains to be understood about why some species become invasive whereas others do not. Recently, polyploidy (whole genome duplication) has been proposed as an important determinant of invasiveness in plants. Genome duplication has played a major role in plant evolution and can drastically alter a plant''s genetic make-up, morphology, physiology and ecology within only one or a few generations. This may allow some polyploids to succeed in strongly fluctuating environments and/or effectively colonize new habitats and, thus, increase their potential to be invasive.

Scope

We synthesize current knowledge on the importance of polyploidy for the invasion (i.e. spread) of introduced plants. We first aim to elucidate general mechanisms that are involved in the success of polyploid plants and translate this to that of plant invaders. Secondly, we provide an overview of ploidal levels in selected invasive alien plants and explain how ploidy might have contributed to their success.

Conclusions

Polyploidy can be an important factor in species invasion success through a combination of (1) ‘pre-adaptation’, whereby polyploid lineages are predisposed to conditions in the new range and, therefore, have higher survival rates and fitness in the earliest establishment phase; and (2) the possibility for subsequent adaptation due to a larger genetic diversity that may assist the ‘evolution of invasiveness’. Alternatively, polyploidization may play an important role by (3) restoring sexual reproduction following hybridization or, conversely, (4) asexual reproduction in the absence of suitable mates. We, therefore, encourage invasion biologists to incorporate assessments of ploidy in their studies of invasive alien species.     

Parallel polyploid speciation: distinct sympatric gene‐pools of recurrently derived allo‐octoploid Asplenium ferns

Although polyploidy is widespread, its significance to the generation of biodiversity remains unclear. Many polyploids have been derived recurrently. For a particular polyploid, gene‐flow between the products of independent origin is typical where they come into contact. Here, we use AFLP DNA‐fingerprinting and chloroplast DNA sequences to demonstrate parallel polyploid speciation within both of the ferns Asplenium cimmeriorum and A. gracillimum. Both of these taxa comprise at least two allopolyploids, recurrently derived from the same progenitor pair. Each of these allopolyploids remain genetically distinguishable even with extensive sympatry, and could therefore be considered distinct species. To our knowledge, parallel speciation on this scale amongst recurrent polyploids has not been previously reported. With their parallel origins, these ‘evolutionary replicates’ provide an unrivalled opportunity to investigate how the reproductive barriers and ecological differentiation necessary for speciation arise following polyploidy.     

Polyploidy: Pitfalls and paths to a paradigm

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.     

Yesterday's polyploids and the mystery of diploidization

Thirty years after Susumu Ohno proposed that vertebrate genomes are degenerate polyploids, the extent to which genome duplication contributed to the evolution of the vertebrate genome, if at all, is still uncertain. Sequence-level studies on model organisms whose genomes show clearer evidence of ancient polyploidy are invaluable because they indicate what the evolutionary products of genome duplication can look like. The greatest mystery is the molecular basis of diploidization, the evolutionary process by which a polyploid genome turns into a diploid one.     

Watching the grin fade: Tracing the effects of polyploidy on different evolutionary time scales

Polyploidy, or whole-genome duplication (WGD), is a recurrent mutation both in cell lineages and over evolutionary time. By globally changing the relationship between gene copy number and other cellular entities, it can induce dramatic changes at the cellular and phenotypic level. Perhaps surprisingly, then, the insights that these events can bring to understanding other cellular features are not as well appreciated as they could be. In this review, we draw on examples of polyploidy from animals, plants and yeast to explore how investigations of polyploid cells have improved our understanding of the cell cycle, biological network complexity, metabolic phenotypes and tumor biology. We argue that the study of polyploidy across organisms, cell types, and time scales serves not only as a window into basic cell biology, but also as a basis for a predictive biology with applications ranging from crop improvement to treating cancer.     

Evidence for shared broad‐scale climatic niches of diploid and polyploid plants

Whole‐genome duplication (polyploidy) occurs frequently and repeatedly within species, often forming new lineages that contribute to biodiversity, particularly in plants. Establishment and persistence of new polyploids may be thwarted by competition with surrounding diploids; however, climatic niche shifts, where polyploids occupy different niches than diploid progenitors, may help polyploids overcome this challenge. We tested for climatic niche shifts between cytotypes using a new ordination approach and an unprecedentedly large data set containing young, conspecific diploids and polyploids. Despite expectations of frequent niche shifts, we show evidence for alternative patterns, such as niche conservatism and contraction, rather than a prevalent pattern of niche shifts. In addition, we explore how interpreting climatic niches plotted on environmental niche (principal component) axes can generate hypotheses about processes underlying niche dynamics. Dispersal capabilities or other life‐history traits, rather than shifts to new climatic niches, could better explain polyploid persistence in the long term.     

Plant polyploidy and non-uniform effects on insect herbivores

Genomic duplication through polyploidy has played a central role in generating the biodiversity of flowering plants. Nonetheless, how polyploidy shapes species interactions or the ecological dynamics of communities remains largely unknown. Here we provide evidence from a 4 year study demonstrating that the evolution of polyploidy has reshaped the interactions between a widespread plant and three species of phytophagous moths. Our results show that polyploidy has produced non-uniform effects, with polyploids less attacked by one insect species, but significantly more attacked by two other species. These results suggest that the evolution of plant polyploidy may not generally confer uniform resistance to multiple species of insect herbivores. In the absence of such a uniform release, the extreme evolutionary success of polyploid plants is probably due to factors other than escape from herbivory. Together, these results suggest that a primary consequence of plant polyploidy may be to shape the ecological structure of plant-insect interactions, thereby providing opportunities for diversification in both plant and insect taxa.     

Life‐history traits of the Whiting polyploid line of the parasitoid Nasonia vitripennis

In hymenopterans, males are normally haploid (1n) and females diploid (2n), but individuals with divergent ploidy levels are frequently found. In species with ‘complementary sex determination’ (CSD), increasing numbers of diploid males that are often infertile or unviable arise from inbreeding, presenting a major impediment to biocontrol breeding. Non‐CSD species, which are common in some parasitoid wasp taxa, do not produce polyploids through inbreeding. Nevertheless, polyploidy also occurs in non‐CSD Hymenoptera. As a first survey on the impacts of inbreeding and polyploidy of non‐CSD species, we investigate life‐history traits of a long‐term laboratory line of the parasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) (‘Whiting polyploid line’) in which polyploids of both sexes (diploid males, triploid females) are viable and fertile. Diploid males produce diploid sperm and virgin triploid females produce haploid and diploid eggs. We found that diploid males did not differ from haploid males with respect to body size, progeny size, mate competition, or lifespan. When diploid males were mated to many females (without accounting for mating order), the females produced a relatively high proportion of male offspring, possibly indicating that these males produce less sperm and/or have reduced sperm functionality. In triploid females, parasitization rate and fecundity were reduced and body size was slightly increased, but there was no effect on lifespan. After one generation of outbreeding, lifespan as well as parasitization rate were increased, and a body size difference was no longer apparent. This suggests that outbreeding has an effect on traits observed in an inbred polyploidy background. Overall, these results indicate some phenotypic detriments of non‐CSD polyploids that must be taken into account in breeding.     

Between Scylla and Charybdis: renegotiating resolution of the ‘obstetric dilemma’ in response to ecological change

Hominin evolution saw the emergence of two traits—bipedality and encephalization—that are fundamentally linked because the fetal head must pass through the maternal pelvis at birth, a scenario termed the ‘obstetric dilemma’. While adaptive explanations for bipedality and large brains address adult phenotype, it is brain and pelvic growth that are subject to the obstetric dilemma. Many contemporary populations experience substantial maternal and perinatal morbidity/mortality from obstructed labour, yet there is increasing recognition that the obstetric dilemma is not fixed and is affected by ecological change. Ecological trends may affect growth of the pelvis and offspring brain to different extents, while the two traits also differ by a generation in the timing of their exposure. Two key questions arise: how can the fit between the maternal pelvis and the offspring brain be ‘renegotiated’ as the environment changes, and what nutritional signals regulate this process? I argue that the potential for maternal size to change across generations precludes birthweight being under strong genetic influence. Instead, fetal growth tracks maternal phenotype, which buffers short-term ecological perturbations. Nevertheless, rapid changes in nutritional supply between generations can generate antagonistic influences on maternal and offspring traits, increasing the risk of obstructed labour.     

植物多倍体研究的回顾与展望

多倍化是促进植物进化的重要力量。多倍体主要是通过未减数配子融合,体细胞染色体加倍以及多精受精三种方式起源的。其中,不减数配子是多倍体形成的主要机制。三倍体可能在四倍体的进化中起了重要作用。过去认为多倍体只能是进化的死胡同,现在发现很多多倍体类群都是多元起源的而不是单元起源的。当多倍体形成后,基因组中的重复基因大部分保持原有的功能,也有相当比例的基因发生基因沉默。多倍体通常表现出不存在于二倍体祖先的表型,并且超出了其祖先的分布范围,因为在多倍体中发生了很多基因表达的变化。主要从多倍体的起源、影响多倍体发生的因素及多倍体基因组的进化等方面回顾并展望多倍体的研究。     

Biogeographic patterns of polyploid species for the angiosperm flora in China

Exploring the frequency and distribution pattern of polyploid species in geographic parameters is of significance in understanding the mechanisms of polyploid speciation and evolutionary drivers of biodiversity. We here explored polyploid and paleopolyploid incidence frequency in a scale of 100 × 100 km grids in China. We found 33% of angiosperm species are polyploidy in China, and 23% of polyploid speciation. Western China and eastern China showed a significantly different polyploid and paleopolyploid frequency, with an evolutionary cradle of polyploid angiosperms in the Qinghai–Tibetan plateau. Herbaceous species exhibited higher polyploid frequency but lower paleopolyploid frequency than woody species, indicating the former experienced more rapid differentiation and speciation than the latter. Our results indicate that western China is an evolutionary cradle for polyploid angiosperms where harsh environment facilitates the establishment and survival of polyploids, while polyploid lineages tend to rediploidize to be diploids with sufficient time in suitable environment.     

Multiple origins of polyploidy and the geographic structure of Heuchera grossulariifolia

Multiple origins of polyploidy from an ancestral diploid plant species were investigated using restriction site polymorphism and sequence variation in the chloroplast DNA (cpDNA) of Heuchera grossulariifolia (Saxifragaceae). Phylogenetic analysis indicated that autopolyploidy has arisen at least twice in the evolutionary history of this species and potentially up to as many as seven times. These results suggest a greater range of independent polyploid origins as compared to a previous study of H. grossulariifolia using cpDNA restriction sites that indicated a minimum of three independent origins. Moreover, most polyploid populations did not contain cpDNA haplotypes from a single origin, but rather combined haplotypes from at least two polyploid origins. Past migration among polyploid populations of independent origin or localized polyploid formation may explain the distribution of polyploid haplotypes within and among populations. The analysis also revealed a discrepancy between relatedness and geographical location. In nearly all sympatric populations of diploids and polyploids, polyploids had the same cpDNA haplotypes as diploids from a geographically remote population. This geographical discordance has several possible explanations, including small sample sizes, extinction of parental diploid haplotypes, chloroplast introgression, and homoplasy in the cpDNA sequence data. We conclude that the recurrent formation of polyploids is an important evolutionary mechanism in the diversification of H. grossulariifolia .     

Evaluating the role of reproductive constraints in ant social evolution

The reproductive division of labour is a key feature of eusociality in ants, where queen and worker castes show dramatic differences in the development of their reproductive organs. To understand the developmental and genetic basis underlying this division of labour, we performed a molecular analysis of ovary function and germ cell development in queens and workers. We show that the processes of ovarian development in queens have been highly conserved relative to the fruitfly Drosophila melanogaster. We also identify specific steps during oogenesis and embryogenesis in which ovarian and germ cell development have been evolutionarily modified in the workers. These modifications, which we call ‘reproductive constraints’, are often assumed to represent neutral degenerations that are a consequence of social evolutionary forces. Based on our developmental and functional analysis of these constraints, however, we propose and discuss the alternative hypothesis that reproductive constraints represent adaptive proximate mechanisms or traits for maintaining social harmony in ants. We apply a multi-level selection framework to help understand the role of these constraints in ant social evolution. A complete understanding of how cooperation, conflict and developmental systems evolve in social groups requires a ‘socio-evo-devo’ approach that integrates social evolutionary and developmental biology.