Polyploidy in vertebrate ancestry: Ohno and beyond

Over 30 years ago, Susumu Ohno proposed that two rounds of polyploidy occurred early in vertebrate evolution. We re-examine this proposal using three recent lines of evidence. First, total gene number estimates from completely sequenced genomes suggest an increase in total gene number somewhere along the vertebrate or prevertebrate lineage, compatible with Ohno's model. Second, analyses of homeobox and other genes from amphioxus reveal very extensive gene duplication specifically on the vertebrate lineage. This refines the timing of putative polyploidy to after the divergence of amphioxus and vertebrates. Third, the existence of four-fold paralogy regions in the human genome is suggestive of two rounds of polyploidy, although other explanations are possible. We propose an experimental test, based on chromosomal localization of genes in amphioxus, that should resolve whether paralogy regions are indeed remnants of duplication in vertebrate ancestry.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 425–430.     

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.     

Polyploidy in fishes: patterns and processes

Fishes are the most speciose group of vertebrates, with more than 24 000 species. They are characterized by great diversity in ecology, morphology, life history, behaviour and physiology. Here, the phylogenetic patterns of orders in which polyploidy has been recorded are considered, with special reference to patterns of species richness and hybridization: these orders include such phylogenetically diverse taxa as the Lepidosireniformes (lungfish) and the Perciformes (perch). Examples, predominantly drawn from the Cyprinidae and Salmonidae, are used to illustrate attributes of polyploidy in fishes. It is concluded (i) that polyploidy may have been of considerable importance in the evolution of fishes, and (ii) that fishes, with their diverse life histories, represent a useful model system with which to test theories relating to the origin and consequences of polyploidy that have been derived from work on plants.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 431–442.     

The development of an Arabidopsis model system for genome-wide analysis of polyploidy effects

Arabidopsis is a model system not only for studying numerous aspects of plant biology, but also for understanding mechanisms of the rapid evolutionary process associated with genome duplication and polyploidization. Although in animals interspecific hybrids are often sterile and aneuploids are related to disease syndromes, both Arabidopsis autopolyploids and allopolyploids occur in nature and can be readily formed in the laboratory, providing an attractive system for comparing changes in gene expression and genome structure among relatively 'young' and 'established' or 'ancient' polyploids. Powerful reverse and forward genetics in Arabidopsis offer an exceptional means by which regulatory mechanisms of gene and genome duplication may be revealed. Moreover, the Arabidopsis genome is completely sequenced; both coding and non-coding sequences are available. We have developed spotted oligo-gene and chromosome microarrays using the complete Arabidopsis genome sequence. The oligo-gene microarray consists of ∼26 000 70-mer oligonucleotides that are designed from all annotated genes in Arabidopsis , and the chromosome microarray contains 1 kb genomic tiling fragments amplified from a chromosomal region or the complete sequence of chromosome 4. We have demonstrated the utility of microarrays for genome-wide analysis of changes in gene expression, genome organization and chromatin structure in Arabidopsis polyploids and related species.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 689–700.     

Exploring the genomic mysteries of polyploidy in cotton

For several years allopolyploid cottons have been the subject of evolutionary investigations into the genomic mysteries of polyploidy. An array of genomic interactions have been documented, including interlocus concerted evolution, differential rates of genomic evolution and intergenomic sequence transfer. Substantial alterations in gene expression have occurred in response to allopolyploidization, including gene silencing and expression changes that vary by organ. Some of the molecular phenomena occurring in polyploids appear to be non-Mendelian. Many of the genomic and expression alterations have occurred on an evolutionary timescale, whereas others reflect more immediate consequences of genomic merger.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 573–581.     

Genomic creativity and natural selection: a modern synthesis

In the early 1930s, the synthesis of Darwinian natural selection, mutation, and Mendelian genetics gave rise to the paradigm of 'modern Darwinism', also known as 'neo-Darwinism'. This has contributed greatly to our understanding. But increasing knowledge of other mechanisms, including endosymbiosis, genetic and genomic duplication, polyploidy, hybridization, epigenetics, horizontal gene transfer in prokaryotes, and the modern synthesis of embryonic development and evolution, has widened our horizons to a diversity of possibilities for change. All of these can be gathered under the umbrella concept of 'genomic creativity', which, in partnership with natural selection, affords a more comprehensive modern explanation of evolution.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 655–672.     

New perspectives on the mechanisms of chromosome evolution in parasitic flowering plants

In an attempt to find any association between chromosomal characters and parasitism, a cytological study of parasitic flowering plants in Israel has been carried out. While no such association was found, evidence for three levels of chromosome evolution could be discerned: intra-chromosomal modifications, polyploidy per se , and genome restructuring in polyploids. Our conclusions may serve as a paradigm of the multiple pathways of chromosomal evolution in plants in general. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 138 , 117–122.     

Is lack of cycad (Cycadales) diversity a result of a lack of polyploidy?

Many hypotheses exist for the relative diversity of seed plant taxa. We discuss one of them: how the relative dearth of cycad diversity throughout their 300 million year history may be a result of a lack of duplication of their entire nuclear genome, often termed polyploidy. We show theoretically how polyploidy causes speciation via cryptic reproductive isolation. Polyploidy can also cause radiations via epigenetically induced heterochrony and plasticity. Most cycads have only a few large chromosomes because of a lack of whole genome duplication or, except possibly in the genus Zamia, chromosomal fission. Large chromosomes and extremely small effective population sizes result in substantial linkage disequilibrium, genetic hitchhiking and genetic drift in cycads. By contrast, other seed plants have higher incidences of polyploidy and may therefore have been more prone to radiations. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 165 , 156–167.     

Plant polyploidy and the evolutionary ecology of plant/animal interactions

Until recently almost nothing was known about the effects of plant polyploidy on interactions with herbivores and pollinators. Studies of the saxifrage Heuchera grossulariifolia throughout its geographical range in the US northern Rockies have shown that autopolyploidy has probably arisen multiple times within this species since the end of the Pleistocene. Tetraploids from those different origins experience higher levels of attack by the moth Greya politella (Prodoxidae) than sympatric or parapatric diploids. In addition, within one intensively studied region, the plants are also attacked by two other lepidopteran species: G. piperella , which preferentially attack diploids, and Eupithecia misturata (Geometridae), which preferentially attacks tetraploids. Sympatric diploid and tetraploid plants also differ in the overall suites of pollinators they attract. Hence, the evolution of polyploid populations has the potential to change significantly the evolutionary ecology of interactions with herbivores and pollinators. Because a large number of plant lineages include polyploid species, the evolution of plant polyploidy may have had major effects on the interaction structure of terrestrial communities.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 511–519.     

Contribution to the karyological knowledge of Echinops (Asteraceae, Cardueae) and related genera

Twenty-six chromosome counts were made of several genera of the tribe Cardueae from various European and Asian provenances: Acantholepis (one species studied), Amphoricarpus (1), Chardinia (1), Echinops (14 species, 15 populations), Siebera (1), Staehelina (3) and Xeranthemum (4). Eleven of the reports are made for the first time, ten confirm previous counts, while the remainder report disparities with earlier records. The existence of different basic chromosome numbers and ploidy levels suggests dysploidy and polyploidy as the main mechanisms of chromosomal evolution in the taxa considered.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 145 , 337−344.     

Polyploidy and the sexual system: what can we learn from Mercurialis annua?

The evolutionary success of polyploidy most directly requires the ability of polyploid individuals to reproduce and transmit their genes to subsequent generations. As a result, the sexual system (i.e. the mating system and the sex allocation of a species) will necessarily play a key role in determining the fate of a new polyploid lineage. The effects of the sexual system on the evolution of polyploidy are complex and interactive. They include both aspects of the genetic system, the genetic load maintained in a population and the ecological context in which selection takes place. Here, we explore these complexities and review the empirical evidence for several potentially important genetic and ecological interactions between ploidy and the sexual system in plants. We place particular emphasis on work in our laboratory on the European annual plant Mercurialis annua , which offers promising scope for detailed investigations on this topic. M. annua forms a polyploid complex that varies in its sexual system from dioecy (separate sexes) through androdioecy (males and hermaphrodites) to functional hermaphroditism.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 547–560.     

Dating and functional characterization of duplicated genes in the apple (<Emphasis Type="Italic">Malus domestica</Emphasis> Borkh.) by analyzing EST data

Background  

Gene duplication is central to genome evolution. In plants, genes can be duplicated through small-scale events and large-scale duplications often involving polyploidy. The apple belongs to the subtribe Pyrinae (Rosaceae), a diverse lineage that originated via allopolyploidization. Both small-scale duplications and polyploidy may have been important mechanisms shaping the genome of this species.     

Spartina anglica C. E. Hubbard: a natural model system for analysing early evolutionary changes that affect allopolyploid genomes

Spartina anglica arose during the end of the 19th century in England by hybridization between the indigenous Spartina maritima and the introduced East American Spartina alterniflora and following genome duplication of the hybrid ( S.  ×  townsendii ). This system allows investigations of the early evolutionary changes that accompany stabilization of a new allopolyploid species in natural populations. Various molecular data indicate that S. anglica has resulted from a unique parental genotype. This young species contains two distinctly divergent homoeologous genomes that have not undergone extensive change since their reunion. No burst of retroelements has been encountered in the F₁ hybrid or in the allopolyploid, suggesting a 'structural genomic stasis' rather than 'rapid genomic changes'. However, modifications of the methylation patterns in the genomes of S.  ×  townsendii and S. anglica indicate that in this system, epigenetic changes have followed both hybridization and polyploidization.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 475–484.     

Breaking down taxonomic barriers in polyploidy research

Polyploidy is important in the evolutionary history of plants, and it has played a crucial role in shaping the genome structures of all eukaryotes. New and rapidly improving techniques in genomics, cytogenetics and molecular ecology have resulted in a dramatic increase in publications about duplicate genes, genome rearrangements and detection of ancient duplication events. Similarly, research associated with the origins of polyploidy, its persistence in natural populations and the resulting ecological consequences is receiving more attention. Although polyploidy research has been conducted using both animal and plant systems, inferences based on cross-disciplinary comparisons have been rare. Here, I review recent developments in the field in both plants and animals, emphasizing the benefits of communication between the two groups.     

Polyploid organisms

Polyploids are organisms with three or more complete chromosome sets. Polyploidization is widespread in plants and animals, and is an important mechanism of speciation. Genome sequencing and related molecular systematics and bioinformatics studies on plants and animals in recent years support the view that species have been shaped by whole genome duplication during evolution. The stability of polyploids depends on rapid genome recombination and changes in gene expression after formation. The formation of polyploids and subsequent diploidization are important aspects in long-term evolution. Polyploids can be formed in various ways. Among them, hybrid organisms formed by distant hybridization could produce unreduced gametes and thus generate offspring with doubled chromosomes, which is a fast, efficient method of polyploidization. The formation of fertile polyploids not only promoted the interflow of genetic materials among species and enriched the species diversity, but also laid the foundation for polyploidy breeding. The study of polyploids has both important theoretical significance and valuable applications. The production and application of polyploidy breeding have brought remarkable economic and social benefits.     

Whole-genome duplications in South American desert rodents (Octodontidae)

The discovery of tetraploidy in the red viscacha rat, Tympanoctomys barrerae (4 n  = 102) has emphasized the evolutionary role of genome duplication in mammals. The tetraploid status of this species is corroborated here by in situ PCR and Southern blot analysis of a single-copy gene. The species meiotic configuration strongly suggests a hybrid derivation. To investigate the origin of T. barrerae further, the recently described Pipanacoctomys aureus was studied. This 92-chromosome species also has a duplicated genome size, redundant gene copy number and diploid-like meiotic pairing, consistent with an event of allotetraploidization. Phylogenetic analysis of mitochondrial sequences indicates sister-group relationships between these two tetraploid rodents. The new karyotypic data and the phylogenetic relationships suggest the participation of the ancestral lineages of Octomys mimax in the genesis of P. aureus . The high overall DNA similarity and shared band homology revealed by genomic Southern hybridization as well as matching chromosome numbers between O. mimax and the descendant tetraploid species support the notion of introgressive hybridization between these taxa.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 443–451.     

Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles

Two new polyploid species of Senecio have originated in the British Isles in recent times following hybridization between native S. vulgaris (2 n  = 40) and introduced S. squalidus (2 n  = 20). One of these is the allohexaploid S. cambrensis (2 n  = 60), the other is the recombinant tetraploid S. eboracensis (2 n  = 40). We review what is known about when and how each species originated, and their reproductive isolation from parents due to high selfing rates. We also review evidence that suggests S. cambrensis may have undergone rapid genome evolution since its origin, and comment on the risks of extinction to each species due to chance factors operating during the early establishment phase. The discovery of both species soon after their origin provides an unparalleled opportunity to examine two different but related forms of speciation following hybridization between the same parent species. Further detailed study of the ecology and genomics of S. cambrensis and S. eboracensis will help improve our understanding of the process of polyploid speciation in plants.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 467–474.     

Genome redundancy and plasticity within ancient and recent Brassica crop species

The crop species within the genus Brassica have highly replicated genomes. Three base 'diploid' species, Brassica oleracea , B. nigra and B. rapa , are likely ancient polyploids, and three derived allopolyploid species, B. carinata , B. juncea and B. napus , are created from the interspecific hybridization of these base genomes. The base Brassica genome is thought to have hexaploid ancestry, and both recent and ancient polyploidization events have been proposed to generate a large number of genome rearrangements and novel genetic variation for important traits. Here, we revisit and refine these hypotheses. We have examined the B. oleracea linkage map using the Arabidopsis thaliana genome sequence as a template and suggest that there is strong evidence for genome replication and rearrangement within the base Brassicas, but less evidence for genome triplication. We show that novel phenotypic variation within the base Brassicas can be achieved by replication of a single gene, BrFLC , that acts additively to influence flowering time. Within the derived allopolyploids, intergenomic heterozygosity is associated with higher seed yields. Some studies have reported that de novo genomic variation occurs within derived polyploid genomes, whereas other studies have not detected these changes. We discuss reasons for these different findings. Large translocations and tetrasomic inheritance can explain some but not all genomic changes within the polyploids. Transpositions and other small-scale sequence changes probably also have contributed to genomic novelty. Our results have shown that the Brassica genomes are remarkably plastic, and that polyploidy generates novel genetic variation through gene duplication, intergenomic heterozygosity and perhaps epigenetic change.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 665–674.     

When may green plants be aposematic?

During the long, dry summers, the deserts of the Middle East are almost devoid of green plants. In the summer, most annuals, geophytes and hemicryptophytes either are dormant in the soil or have already been eaten by the grazing flocks. Many shrubs are summer deciduous or enter summer dormancy with minimal green canopy. However, there are several common plants that, contrary to the general phenology, are conspicuously green during summer, when all the surroundings are yellow. In such conditions, green is conspicuous and contrasts with the background, as do yellow, red and black in 'greener' ecosystems. The summer-green plants are also characterized by being poisonous or thorny as protection against herbivory. During winter and spring, when there are plenty of other green, more palatable annual plants, herbivory pressure is much lower and they need less protection. We propose that during summer in the dry desert, when most other plants are dry or indistinctive, a vivid green colour can be aposematic.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 413–416.     

Reversible frequency-dependent predation of a puffer, Takifugu niphobles (Pisces: Tetraodontidae), related to spatial distribution of colour-polymorphic prey

The puffer Takifugu niphobles is a top predator of hard-shelled prey such as molluscs; its predatory tactics may affect the evolution of prey coloration. Two hypotheses concerning its foraging were tested: (1) T. niphobles shows frequency dependence in foraging colour-polymorphic prey, and (2) such dependence reverses in response to changes in prey distribution. Captive fish were provided with 70 artificial prey, coloured either dark brown or pale brown, at four frequencies (1 : 4, 2 : 3, 3 : 2, 4 : 1) and in two distribution patterns (uniform and aggregated). When prey were uniformly distributed, frequency and feeding rate significantly influenced colour preference: the common morph was consumed more. When prey were aggregated, frequency significantly affected preference only when the feeding rate was low, in which case the rare morph was consumed more. Thus both hypotheses were supported. The impact of T. niphobles 's frequency-dependent predation and its reversal on the colour evolution of prey species, especially molluscs, is discussed.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 197–202.