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.     

Noncorrelated evolution between herbivore- and pollinator-linked features in Aristolochia chilensis (Aristolochiaceae)

The effect of mutualists (i.e. pollinators) and antagonists (i.e. herbivores) can have non-additive effects on plant fitness. This is often interpreted as evidence for correlated evolution on a suite of traits leading to an increase and decrease of the interaction of plants with mutualists and antagonists, respectively. This situation has been found to prevail in plants that have large floral and fruit displays but are not limited by pollinators for seed set. We suggest the alternative hypothesis, where plants limited by pollinators for seed set (e.g. deceit-pollinated plants) exhibit additive effects of pollinators and herbivores on fitness (i.e. noncorrelated evolution). Using a 2 × 2 factorial design, we tested this hypothesis by solely and simultaneously evaluating the effects of pollinators and the single herbivore, Battus polydamas archidamas , on female reproductive success of Aristolochia chilensis . Plants exposed to herbivores presented 2.6-fold greater herbivory than plants that excluded them. In addition, plants exposed to pollinators showed strong limitation by pollinators for seed set compared with other plants of the genus Aristolochia. However, only pollinators had a significant effect on fruit and seed set because plants that excluded them did not set fruits or seeds. Furthermore, herbivores and pollinators exerted additive effects on fruit and seed production. Collectively, these results indicate that herbivore- and pollinator-linked traits in A. chilensis exhibit noncorrelated evolution.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 239–245.     

Endogenous pararetroviruses of allotetraploid Nicotiana tabacum and its diploid progenitors, N. sylvestris and N. tomentosiformis

Endogenous pararetroviruses (EPRVs) represent a new class of dispersed repetitive DNA in plants. The genomes of many Nicotiana species and other solanaceous plants are rich in EPRVs. Distinct EPRV families are present in N. sylvestris ( Ns ) and in N. tomentosiformis ( Nto ), the two diploid progenitors of allotetraploid N. tabacum . Nicotiana EPRVs represent an interesting type of repetitive sequence to analyse in polyploids because of their potential impact on plant fitness and the epigenetic architecture of plant genomes. The Ns EPRV family appears identical in N. sylvestris and N. tabacum , indicating little change has occurred in either species since polyploid formation. By contrast, the Nto EPRV family is larger in N. tomentosiformis than in N. tabacum , suggesting either preferential elimination from the polyploid genome or specific accumulation in the diploid genome following polyploidization. The lability of Nto EPRVs might be enhanced by a frequent association with gypsy retrotransposons. Although some EPRVs are probably benign, others are potentially pathogenic or, conversely, determinants of virus resistance. Normally quiescent EPRVs can be reactivated and cause symptoms of infection in hybrids of species that differ in their EPRV content. EPRVs that furnish immunity to the free virus exemplify the selective value of so-called 'junk' DNA. Variation in the abundance and distribution of EPRVs among related species can be useful in taxonomic and evolutionary studies.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 627–638.     

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.     

Noncorrelated effects of seed predation and pollination on the perennial herb Ruellia nudiflora remain spatially consistent

By simultaneously manipulating both seed predator and pollinator effects on the perennial herb Ruellia nudiflora at two sites in Yucatan (Mexico), the present study evaluated (1) whether a correlation (interaction) existed between seed predator and pollinator effects on R. nudiflora seed production and (2) whether such an interaction varied geographically. We used three populations per site, and a total of 20 plants per population ( N  = 120). Groups of five plants were randomly chosen at each population to simultaneously receive one of two seed predator and pollinator exclosure levels (present or excluded in each case). These two factors were fully crossed, resulting in each group being subjected to one of four possible combinations: pollinators excluded/herbivores present; herbivores excluded/pollinators present; herbivores excluded/pollinators excluded; or control (neither excluded). Response variables were the number of seeds produced per plant and the proportion of attacked fruits by seed predators per plant. Seed predators had a large impact on R. nudiflora seed production but did not show any preference for fruits from plants not excluded from pollinators. In addition, the pollination treatment was not significant, indicating no effect of pollinators on reproductive success. These findings resulted in a nonsignificant herbivory × pollination interaction, which was consistent across sites, indicating lack of correlated selection of these two guilds on R. nudiflora seed production.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 800–807.     

'Why polyploidy is rarer in animals than in plants': myths and mechanisms

Although polyploidy has been involved in speciation in both animals and plants, the general perception is often that it is too rare to have been a significant factor in animal evolution and its role in plant diversification has been questioned. These views have resulted in a bias towards explanations for what deters polyploidy, rather than the somewhat more interesting question of the mechanisms by which polyploidy arises and becomes established in both plants and animals. The evidence for and against some of the traditional views on polyploidy is reviewed, with an attempt to synthesize factors promoting evolution through genome duplication in both groups. It is predicted that polyploidy should be more common in temperate than in tropical breeders because environmental fluctuations may promote unreduced gamete formation, it should be most common in organisms with sufficient numbers of gametes that random meiotic problems can be overcome, and it should be more frequent when mechanisms to promote assortative mating are a direct byproduct of genome duplication.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 82 , 453–466.     

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.     

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.     

No effect of ploidy level in plant response to competition in a common garden experiment

One of the important aspects explaining the evolutionary success of polyploid plants is that polyploids often, although not always, occupy a wider range of environments than their diploid ancestors. The two most likely explanations for this pattern are a wider plasticity in polyploid species and the existence of a range of locally adapted types. Most studies on patterns of distribution of different ploidy levels are only observational, and do not distinguish between these alternative explanations. The present study investigated the performance and plasticity of diploid and hexaploid cytotypes of a perennial plant, Aster amellus . The hexaploid plants occur in habitats with a wider range of competition intensity. Nine different populations of the species were selected: three diploid (from low competition habitats) and six hexaploid (from both low and high competition habitats). Plants were grown from seeds from these populations with and without competition in a common garden. Competition had strong effect on plant performance. There was, however, little effect of the ploidy levels and home environment. There was also almost no interaction between competition and ploidy level/home environment. The results of this study provide no support for any of the two suggested explanations for the wider range of habitats occupied by hexaploid plants. Other explanations thus must be thought. Generally, the results indicate that, although the higher plasticity of higher ploidy levels is often suggested, this may not be true. We therefore should attempt to assemble more experimental data to support or reject this assumption.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 211–219.     

Differential attack on diploid, tetraploid, and hexaploid Solidago altissima L. by five insect gallmakers

Genetic variation among plants can influence host choice and larval performance in insect herbivores. Ploidy (cytotype) variation is a particularly dramatic form of plant genetic variation, and where diploid and polyploid cytotypes of a species occur in sympatry, they may provide herbivores with choices that are distinguished by profound and genome-wide genetic differences. We tested for non-random attack by five gallmaking insect herbivores on diploid, tetraploid, and hexaploid cytotypes of the goldenrod Solidago altissima L., working in seven midwestern US populations where the ploidies co-occur on spatial scales relevant to insect host choice. For four of the five herbivores, attack was non-random with respect to ploidy at one or more sites. Ploidy effects on attack were complex: the ploidy subjected to highest attack varied both across herbivores within sites and (for most herbivores) across sites within herbivores. Ploidy effects on attack will alter rates of encounter between insect herbivores—either increasing or decreasing the likelihood of two herbivores sharing a host plant ramet, compared with the case with no effects of ploidy. Plant ploidy variation appears likely to have a major impact on insect community organization, and perhaps on plant–herbivore coevolution, but that impact is likely to be spatially heterogeneous. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Ploidal levels in the arctic-alpine polyploid Draba lactea (Brassicaceae) and its low-ploid relatives

Ploidal level information is of particular importance in intricate polyploid complexes such as in arctic-alpine Draba . Relative DNA content is reported for the tetra- and hexaploid D. lactea and seven of its low-ploid relatives. Flow cytometry was used to study 200 plants from 93 populations, the screening based on relative fluorescence. Absolute DNA content was determined by Feulgen densitometry for 13 plants from seven species, and reference chromosome numbers were determined in 12 plants (1–3 per species) representing six species. The plants grouped into diploids (2 n  = 16), tetraploids (2 n  = 32), hexaploids (2 n  = 48), and two triploids. Each ploidal level showed a linear increase in relative DNA content, pointing to a relatively recent polyploid origin. The diploid level was confirmed in D. nivalis, D. subcapitata, D. fladnizensis , and D. lonchocarpa. Draba palanderiana , reported previously as di-, tetra- and octoploid, was diploid in all investigated accessions. Hexa- and tetraploids were observed in D. lactea , in approximately the same ratio (8 : 1) as reported previously. The ploidal levels of the Central Asian D. altaica and D. turczaninovii are reported here for the first time as diploid and tetraploid, respectively.  © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society , 2005, 147 , 333–347.     

Polyploidy in invasive plant species of Singapore

Singapore is a recognized global hotspot for invasive species and many introduced plant species have become major weeds there. Some of the common invasive taxa, such as Asystasia gangetica ssp. micrantha , Mimosa pigra , Neptunia plena , Panicum maximum , and Urochloa mutica , are spread over large areas and dominate the indigenous flora in some habitats. In a study aimed at understanding the relationship between polyploidy and invasiveness, we show that all the investigated invasive taxa are polyploids. A. gangetica ssp. micrantha , N. plena , and P. maximum vary in chromosome number and ploidy level across the world, but we recorded only one chromosome count for each of these species in Singapore. Similarly, the cytology of M. pigra and U. mutica also revealed that these species are polyploid, each with only one chromosome number across all populations. The results indicate that one polyploid line in each of these species has been selected favourably and has become invasive. We also show that all the species exhibit normal male meiosis and possess high percentages of pollen fertility. Based on the present study and an analysis of previously reported ploidy levels, we suggest that these taxa are probably of allopolyploid origin. We conclude that polyploidy and an effective reproductive system are a perfect mix for successful invasion by these species in Singapore.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 151 , 395–403.     

Variation in native pollinators in the absence of honeybees: implications for reproductive success of an Australian generalist-pollinated herb Trachymene incisa (Apiaceae)

Most plants are generalist in terms of pollination, with the potential for significant spatial and temporal variation in their pollinators. Few studies have investigated how variable pollinators are in a generalist pollination system or how this variation affects plant reproduction. We investigated the degree of variation in pollinators and resulting reproductive success among populations of a widespread generalist-pollinated herb, Trachymene incisa (Apiaceae). The European honeybee was unexpectedly absent from the pollinator assemblages, providing the unique opportunity to study the native Australian pollinators. Insect visitation rates and the taxonomic composition of the pollinator assemblage varied significantly across populations, indicating that populations of T. incisa are not equally serviced and are not equally generalist. This highlights that sampling one population would not characterize the extent of species generalization. There was no positive correlation between insect visitation rate and reproductive success, with the Agnes Banks population receiving the highest visitation rate but producing the lowest reproductive output, and the Myall Lakes population receiving the lowest visitation rate and producing the highest seedling emergence. This study shows that variation in pollinators can have measurable effects on populations of generalist-pollinated plants, therefore there is potential for large-scale change in all plant–pollinator interactions.  © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society , 2008, 156 , 479–490.     

Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study

1.  There are myriad ways in which pollinators and herbivores can interact via the evolutionary and behavioural responses of their host plants.
2.  Given that both herbivores and pollinators consume and are dependent upon plant-derived nutrients and secondary metabolites, and utilize plant signals, plant chemistry should be one of the major factors mediating these interactions.
3.  Here we build upon a conceptual framework for understanding plant-mediated interactions of pollinators and herbivores. We focus on plant chemistry, in particular plant volatiles and aim to unify hypotheses for plant defence and pollination. We make predictions for the evolutionary outcomes of these interactions by hypothesizing that conflicting selection pressures from herbivores and pollinators arise from the constraints imposed by plant chemistry.
4.  We further hypothesize that plants could avoid conflicts between pollinator attraction and herbivore defence through tissue-specific regulation of pollinator reward chemistry, as well as herbivore-induced changes in flower chemistry and morphology.
5.  Finally, we test aspects of our predictions in a case study using a wild tomato species, Solanum peruvianum , to illustrate the diversity of tissue-specific and herbivore-induced differences in plant chemistry that could influence herbivore and pollinator behaviour, and plant fitness.     

Polyploidy in arctic plants

The Arctic is an excellent model system for the study of polyploidy. It is one the Earth's most polyploid‐rich areas, in particular of high‐level and recently evolved polyploids. Here we re‐address previous hypotheses on arctic polyploidy based on a new analysis of the circumarctic flora, and review recent molecular, cytological and reproductive studies. The frequency and level of polyploidy strongly increase northwards within the Arctic. We found no clear‐cut association between polyploidy and the degree of glaciation for the arctic flora as a whole, which contains many widespread species. However, for ‘arctic specialist’ taxa with restricted distributions, the frequency of diploids is much higher in the Beringian area, which remained largely unglaciated during the last ice age, than in the heavily glaciated Atlantic area. This result supports the hypothesis that polyploids are more successful than diploids in colonizing after deglaciation. There is abundant molecular evidence for recurrent formation of arctic polyploids at different scales in time and space. Examples are given of low‐level polyploids formed after the last glaciation and of repeated and successively more high‐level polyploidizations throughout the Quaternary. Recurrent polyploid origins, followed by interbreeding within and across ploidal levels, provide a major explanation for the taxonomic complexity of the arctic flora. In the well‐studied, recently deglaciated archipelago of Svalbard, most species are mainly self‐fertilizing or clonal. All Svalbard polyploids examined so far are genetic allopolyploids with fixed heterozygosity at isozyme loci. The level of heterozygosity in 65 taxa increases dramatically from diploids to high‐level polyploids. In the circumarctic area, there is evidence for numerous recently evolved sibling species within diploid taxonomic species. Rapid evolution of crossing barriers at the diploid level promotes further diversification after expansion from different refugia, and may provide new raw materials for allopolyploid formation. We conclude that the evolutionary success of polyploids in the Arctic may be based on their fixed‐heterozygous genomes, which buffer against inbreeding and genetic drift through periods of dramatic climate change. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 82 , 521–536.     

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.     

Species interactions and plant polyploidy

Polyploidy is a common mode of speciation that can have far‐reaching consequences for plant ecology and evolution. Because polyploidy can induce an array of phenotypic changes, there can be cascading effects on interactions with other species. These interactions, in turn, can have reciprocal effects on polyploid plants, potentially impacting their establishment and persistence. Although there is a wealth of information on the genetic and phenotypic effects of polyploidy, the study of species interactions in polyploid plants remains a comparatively young field. Here we reviewed the available evidence for how polyploidy may impact many types of species interactions that range from mutualism to antagonism. Specifically, we focused on three main questions: (1) Does polyploidy directly cause the formation of novel interactions not experienced by diploids, or does it create an opportunity for natural selection to then form novel interactions? (2) Does polyploidy cause consistent, predictable changes in species interactions vs. the evolution of idiosyncratic differences? (3) Does polyploidy lead to greater evolvability in species interactions? From the scarce evidence available, we found that novel interactions are rare but that polyploidy can induce changes in pollinator, herbivore, and pathogen interactions. Although further tests are needed, it is likely that selection following whole‐genome duplication is important in all types of species interaction and that there are circumstances in which polyploidy can enhance the evolvability of interactions with other species.     

Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa

We studied an assemblage of 17 species of bird-pollinated Ecuadorian plants (from 14 angiosperm families), including taxa pollinated by short-billed (trochiline) and sickle-billed (hermit) hummingbirds. Hummingbirds are widely supposed to ignore fragrance while visiting flowers. We collected floral headspace odours in order to test the general prediction that specialist hummingbird-pollinated flowers are scentless. In nine out of 17 of these species we failed to detect any odours using gas chromatography-mass spectrometry (GC-MS), whereas the remaining eight species produced trace levels of volatile compounds. Most of these odour compounds were of terpenoid or lipoxygenase derivation and are commonly emitted by vegetative as well as floral plant tissues. Further studies will be required to determine whether these weak odours attract alternative pollinators, repel enemies or represent vestiges of a scented ancestry.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 146 , 191–199.     

Uniformity of karyotypes in Ligularia (Asteraceae: Senecioneae), a highly diversified genus of the eastern Qinghai–Tibet Plateau highlands and adjacent areas

Ligularia , a highly diversified genus in the eastern Qinghai–Tibet Plateau and adjacent areas, was chosen as a suitable subject in which to study speciation patterns in this 'hot spot' area at the chromosomal level. Chromosome numbers and karyotypes were studied in 23 populations of 14 species, most of which are endemic to this area. The basic number x  = 29 was confirmed for all species. Ligularia virgaurea was found to have diploid and triploid cytotypes, 2 n  = 58 and 87. Other species are only diploid, with 2 n  = 58. The karyotypes of all populations within any species, and all species spanning most sections and covering most of the morphological range in Ligularia , are very similar to each other, belonging to type 2A according to Stebbin's classification. This karyotype was also found in its close allies, e.g. Cremanthodium , Ligulariopsis , Parasenecio , and Sinacalia . Aneuploid reduction of chromosome number from 2 n  = 60 to 58 and karyotypic variation was found in Ligularia and its allies. Such a chromosomal pattern with few polyploids infers that variation of karyotype structure at the diploid level seems to be the predominant feature of chromosomal evolution in this group and sympatric speciation via hybridization and polyploidization has played a minor role in its species diversity.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 144 , 329–342.