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Transgressive phenotypes and generalist pollination in the floral evolution of Nicotiana polyploids
Abstract
Polyploidy is an important driving force in angiosperm evolution, and much research has focused on genetic, epigenetic and transcriptomic responses to allopolyploidy. Nicotiana is an excellent system in which to study allopolyploidy because half of the species are allotetraploids of different ages, allowing us to examine the trajectory of floral evolution over time. Here, we study the effects of allopolyploidy on floral morphology in Nicotiana, using corolla tube measurements and geometric morphometrics to quantify petal shape. We show that polyploid morphological divergence from the intermediate phenotype expected (based on progenitor morphology) increases with time for floral limb shape and tube length, and that most polyploids are distinct or transgressive in at least one trait. In addition, we show that polyploids tend to evolve shorter and wider corolla tubes, suggesting that allopolyploidy could provide an escape from specialist pollination via reversion to more generalist pollination strategies.
... Interestingly, all native Australian Nicotiana species belong to section Suaveolentes (Bally et al., 2021). In addition, Nicotiana species exhibit a spectacular range of floral morphology and color, genome size, and karyotypic diversity (Leitch et al., 2008;Marks et al., 2011;Renny-Byfield et al., 2013;McCarthy et al., 2015;McCarthy et al., 2016) and the polyploids of Nicotiana formed at different stages of evolutionary divergence (Leitch et al., 2008). The genus Nicotiana is, therefore, an excellent system in which to take advantage of recent advances in the research of speciation, biodiversity, and phytogeography (Aoki and Ito, 2000;McCarthy et al., 2016). ...
... In addition, Nicotiana species exhibit a spectacular range of floral morphology and color, genome size, and karyotypic diversity (Leitch et al., 2008;Marks et al., 2011;Renny-Byfield et al., 2013;McCarthy et al., 2015;McCarthy et al., 2016) and the polyploids of Nicotiana formed at different stages of evolutionary divergence (Leitch et al., 2008). The genus Nicotiana is, therefore, an excellent system in which to take advantage of recent advances in the research of speciation, biodiversity, and phytogeography (Aoki and Ito, 2000;McCarthy et al., 2016). ...
... Polyploidization has been pivotal in shaping this genus (Leitch et al., 2008;McCarthy et al., 2016). Approximately half of the Nicotiana species were considered natural tetraploid species of different ages (Goodspeed, 1956;Knapp et al., 2004;Leitch et al., 2008). ...
Introduction
Nicotiana L. (Solanaceae) is of great scientific and economic importance, and polyploidization has been pivotal in shaping this genus. Despite many previous studies on the Nicotiana phylogenetic relationship and hybridization, evidence from whole genome data is still lacking.
Methods
In this study, we obtained 995 low-copy genes and plastid transcript fragments from the transcriptome datasets of 26 Nicotiana species, including all sections. We reconstructed the phylogenetic relationship and phylogenetic network of diploid species.
Results
The incongruence among gene trees showed that the formation of N. sylvestris involved incomplete lineage sorting. The nuclear–plastid discordance and nuclear introgression absence indicated that organelle capture from section Trigonophyllae was involved in forming section Petunioides. Furthermore, we analyzed the evolutionary origin of polyploid species and dated the time of hybridization events based on the analysis of PhyloNet, sequence similarity search, and phylogeny of subgenome approaches. Our results highly evidenced the hybrid origins of five polyploid sections, including sections Nicotiana, Repandae, Rusticae, Polydicliae, and Suaveolentes. Notably, we provide novel insights into the hybridization event of section Polydicliae and Suaveolentes. The section Polydicliae formed from a single hybridization event between maternal progenitor N. attenuata and paternal progenitor N. undulata; the N. sylvestris (paternal progenitor) and the N. glauca (maternal progenitor) were involved in the formation of section Suaveolentes.
Discussion
This study represents the first exploration of Nicotiana polyploidization events and phylogenetic relationships using the high-throughput RNA-seq approach. It will provide guidance for further studies in molecular systematics, population genetics, and ecological adaption studies in Nicotiana and other related species.
... We used the TpsDig 2 software (Rohlf, 2015) to digitize landmarks manually. For AVCL, we digitized 15 landmarks to the corolla tube opening, to the apex of each petal and at the junction of adjacent petals following the flower venation pattern (Fig. 2E) (Gómez & Perfectti, 2010;McCarthy et al., 2016). For PV, we digitized 11 landmarks positioned at the corolla tube extremities. ...
... hummingbird-pollinated species) and is less variable within pollinator groups (Kaczorowski et al., 2012). Studies investigating the evolution of floral shape in allopolyploids of Nicotiana (McCarthy et al., 2016(McCarthy et al., , 2019 revealed that corolla limb shape is a more labile trait than floral tube width. Floral limb shape also can be variable in other taxa of Solanaceae (e.g. ...
... Such studies indicated coevolution between floral tube and pollinator guilds and pollinator behaviours, a significant evolutionary force in angiosperm radiations (Hu et al., 2008;Soltis, Folk & Soltis, 2019). McCarthy et al. (2016) suggested that allopolyploids in Nicotiana tend to have shorter and broader corolla tubes, indicating a more generalist pollination system. The wide and short corolla tube of rastroensis highlight ideas already presented in previous studies on the importance of other pollinators (e.g. ...
Floral shape and size play a role in plant diversification and reproductive isolation. Different floral forms can rise by selective pressures by pollinators/ecological constraints and/or genetic drift. Nicotiana (Solanaceae) has c. 82 currently recognized species grouped in 13 sections. Nicotiana forgetiana and N. alata belong to section Alatae and present different floral traits related to their primary pollinators. These species co-occur in a region of plant endemism in southern Brazil marked by a mosaic between open grasslands and Araucaria forest. Here, we conducted a population-level sampling across the range of N. forgetiana and combined geometric morphometric analyses and ecological niche modelling to shed light on the patterns underlying intraspecific floral shape variation. Corolla shape and size varied significantly across the geographical distribution of N. forgetiana and ‘rastroensis’, a putative new species. These floral shape differences were related to variations in temperature, precipitation and elevation. We also observed a range of intermediate floral traits in two populations, and our results of geometric morphometric analyses reveal morphological overlap between N. alata and N. forgetiana. Moreover, we found that habitat suitability for both species was impacted by past climatic oscillations, with severe reduction for N. forgetiana during the Last Glacial Maximum. We discuss the results to shed light on the evolution of N. forgetiana.
... We used the TpsDig 2 software (Rohlf, 2015) to digitize landmarks manually. For AVCL, we digitized 15 landmarks to the corolla tube opening, to the apex of each petal and at the junction of adjacent petals following the flower venation pattern (Fig. 2E) (Gómez & Perfectti, 2010;McCarthy et al., 2016). For PV, we digitized 11 landmarks positioned at the corolla tube extremities. ...
... hummingbird-pollinated species) and is less variable within pollinator groups (Kaczorowski et al., 2012). Studies investigating the evolution of floral shape in allopolyploids of Nicotiana (McCarthy et al., 2016(McCarthy et al., , 2019 revealed that corolla limb shape is a more labile trait than floral tube width. Floral limb shape also can be variable in other taxa of Solanaceae (e.g. ...
... Such studies indicated coevolution between floral tube and pollinator guilds and pollinator behaviours, a significant evolutionary force in angiosperm radiations (Hu et al., 2008;Soltis, Folk & Soltis, 2019). McCarthy et al. (2016) suggested that allopolyploids in Nicotiana tend to have shorter and broader corolla tubes, indicating a more generalist pollination system. The wide and short corolla tube of rastroensis highlight ideas already presented in previous studies on the importance of other pollinators (e.g. ...
Floral morphological traits are frequently used to identify species, including those that are closely related and show low genetic diversity, and floral shape and colour are known to play an important role in diversification and species isolation. Floral morphology in Petunia (Solanaceae) is considered a driver of diversification because of its association with pollinators. Here, flower morphology was characterized through morphometric analyses and floral pigments. Our main aim was to determine corolla shape in populations of Petunia axillaris and P. exserta and their natural hybrids and how floral display, size and colour are involved in pollinator attraction. In addition, we investigated floral pigments in P. exserta and different hybrid classes. The results from morphometric analyses revealed that each species has a specific floral shape, independent of the collection site. By contrast, in two contact zones, a mosaic of floral phenotypes was observed with some hybrid classes based on corolla colour being placed close to P. exserta. The results suggest that several generations of hybrids or backcrossing could have given rise to this floral diversity in contact zones.
... Polyploids of different ages, along with available synthetic lines created from the same progenitor species as natural polyploids, allow for investigation into the consequences of immediate, short-term, and long-term polyploid evolution. In addition, Nicotiana displays wide variation in corolla tube length and width [91]. Young Nicotiana polyploids (<1 million years old (myo)) tend to evolve shorter and wider corolla tubes than what would be expected based on the intermediate values of their diploid progenitors, whereas diploids and older polyploids (> 1 myo) do not show any trends in corolla tube size evolution [90]. ...
... Based on previous studies showing wider corolla tubes in allopolyploids than expected [90,91], we tested the hypothesis that increases in tube width are due to increased cell width in polyploids. Cell size, cell number, and corolla tube circumference vary across accessions (Figure 2A-C). ...
... Young allopolyploids tend to evolve shorter and wider corolla tubes than expected based on the mean of the morphology of their progenitors, which may allow for a greater variety of pollinator types to access the nectar rewards of these flowers [90,91]. Cell width, cell number, and ploidy positively influence corolla tube circumference, and polyploids have significantly wider cells than diploids, with either the same number of cells or fewer ( Figure 2). ...
Floral organ size, especially the size of the corolla, plays an important role in plant reproduction by facilitating pollination efficiency. Previous studies have outlined a hypothesized organ size pathway. However, the expression and function of many of the genes in the pathway have only been investigated in model diploid species; therefore, it is unknown how these genes interact in polyploid species. Although correlations between ploidy and cell size have been shown in many systems, it is unclear whether there is a difference in cell size between naturally occurring and synthetic polyploids. To address these questions comparing floral organ size and cell size across ploidy, we use natural and synthetic polyploids of Nicotiana tabacum (Solanaceae) as well as their known diploid progenitors. We employ a comparative transcriptomics approach to perform analyses of differential gene expression, focusing on candidate genes that may be involved in floral organ size, both across developmental stages and across accessions. We see differential expression of several known floral organ candidate genes including ARF2, BIG BROTHER, and GASA/GAST1. Results from linear models show that ploidy, cell width, and cell number positively influence corolla tube circumference; however, the effect of cell width varies by ploidy, and diploids have a significantly steeper slope than both natural and synthetic polyploids. These results demonstrate that polyploids have wider cells and that polyploidy significantly increases corolla tube circumference.
... Capsicum (CA02g15000) and eggplant (Sme2.5_02187.1_g00005.1), but two different scaffolds are returned in searching the genome of Nicotiana benthamiana, a known allopolyploid [43]. Thus, HD-AGP appears to be a single-copy gene in diploid members of the Solanaceae. ...
... Interspecific barriers in Nicotiana are complicated by the prevalence of allopolyploids, which make up about half of all the species in the genus [43]. Although N. sylvestris and N. tomentosiformis do not hybridize readily, a presumably rare hybridization event followed by polyploidization generated allotetraploid N. tabacum about 0.2 million years ago [43]. ...
... Interspecific barriers in Nicotiana are complicated by the prevalence of allopolyploids, which make up about half of all the species in the genus [43]. Although N. sylvestris and N. tomentosiformis do not hybridize readily, a presumably rare hybridization event followed by polyploidization generated allotetraploid N. tabacum about 0.2 million years ago [43]. The presence of HD-AGP homeologs from both ancestral species, NsPRP1 (=TTS1) from N. sylvestris and NtPRP1 (=TTS 2) from N. tomentosiformis, explains why N. sylvestris and N. tomentosiformis pollen readily set seed on N. tabacum pistils. ...
Transmitting tissue-specific proteins (TTS proteins) are abundant in the extracellular matrix of Nicotiana pistils, and vital for optimal pollen tube growth and seed set. We have identified orthologs from several species in the Solanaceae, including Petunia axillaris axillaris and Petunia integrifolia. We refer to TTS proteins and their orthologs as histidine domain-arabinogalactan proteins (HD-AGPs). HD-AGPs have distinctive domains, including a small histidine-rich region and a C-terminal PAC domain. Pairwise comparisons between HD-AGPs of 15 species belonging to Petunia, Nicotiana, and Solanum show that the his-domain and PAC domain are under purifying selection. In contrast, a proline-rich domain (HV2) is conserved among cross-hybridizing species, but variant in species-pairs that are reproductively isolated by post-pollination pre-fertilization reproductive barriers. In particular, variation in a tetrapeptide motif (XKPP) is systematically correlated with the presence of an interspecific reproductive barrier. Ka/Ks ratios are not informative at the infrageneric level, but the ratios reveal a clear signature of positive selection on two hypervariable domains (HV1 and HV2) when HD-AGPs from five solanaceous genera are compared. We propose that sequence divergence in the hypervariable domains of HD-AGPs reinforces sympatric speciation in incipient species that may have first diverged as a consequence of pollinator preferences or other ecological factors.
... The merger of two distinct genomes in one allopolyploid nucleus may result in 'genomic shock' [7], which yields changes in gene expression [8][9][10][11][12], chromosomal rearrangements [13,14], increase of transposable element activity [15,16], alterations of physiological processes [17,18], changes in morphology [19,20], and niche shifts [21]. These processes and their results can isolate newly formed allopolyploids from their diploid progenitors and may facilitate their establishment as a new species. ...
... Previous studies in angiosperms have investigated allopolyploid phenotypic evolution with respect to plant biomass [19,28], photosynthetic capacity [29], non-photochemical quenching [18], defense response to herbivory [17], and flower morphology and color [20,[30][31][32]. These studies have compared allopolyploid phenotypes to those of their diploid progenitors to evaluate whether allopolyploids display novel traits or combinations of traits, but these studies have not addressed whether allopolyploids follow different evolutionary trends than diploids. ...
... Nicotiana has been well studied phylogenetically [36][37][38][39][40], and putative parentage of all allopolyploid species/groups has been determined. Nicotiana displays considerable diversity in floral morphology and color [20,31,41], facilitating study of the effects of allopolyploidy on floral evolution. Nicotiana allopolyploids can display transgressive morphologies that fall outside the range of their diploid progenitors and are thought to have evolved shorter, wider corolla tubes than expected, assuming the nascent polyploid has a morphology predicted by the morphologies of the flowers of extant diploids [20]. ...
Background
Polyploidy has played a major role in angiosperm evolution. Previous studies have examined polyploid phenotypes in comparison to their extant progenitors, but not in context of predicted progenitor phenotypes at allopolyploid origin. In addition, differences in the trends of polyploid versus diploid evolution have not been investigated. We use ancestral character-state reconstructions to estimate progenitor phenotype at allopolyploid origin to determine patterns of polyploid evolution leading to morphology of the extant species. We also compare trends in diploid versus allopolyploid evolution to determine if polyploidy modifies floral evolutionary patterns.
Results
Predicting the ancestral phenotype of a nascent allopolyploid from reconstructions of diploid phenotypes at the time of polyploid formation generates different phenotype predictions than when extant diploid phenotypes are used, the outcome of which can alter conclusions about polyploid evolution; however, most analyses yield the same results. Using ancestral reconstructions of diploid floral phenotypes indicate that young polyploids evolve shorter, wider corolla tubes, but older polyploids and diploids do not show any detectable evolutionary trends. Lability of the traits examined (floral shape, corolla tube length, and corolla tube width) differs across young and older polyploids and diploids. Corolla length is more evolutionarily labile in older polyploids and diploids. Polyploids do not display unique suites of floral characters based on both morphological and color traits, but some suites of characters may be evolving together and seem to have arisen multiple times within Nicotiana, perhaps due to the influence of pollinators.
Conclusions
Young polyploids display different trends in floral evolution (shorter, wider corolla tubes, which may result in more generalist pollination) than older polyploids and diploids, suggesting that patterns of divergence are impacted by the early consequences of allopolyploidy, perhaps arising from genomic shock and/or subsequent genome stabilization associated with diploidization. Convergent evolution in floral morphology and color in Nicotiana can be consistent with pollinator preferences, suggesting that pollinators may have shaped floral evolution in Nicotiana.
Electronic supplementary material
The online version of this article (10.1186/s12870-019-1771-5) contains supplementary material, which is available to authorized users.
... The application of GMM in plant science is vast and varied, spanning across diverse disciplines such as taxonomy, systematics, ecology, plant physiology, paleobotany, and evolutionary and developmental biology [33][34][35][36]. Christodoulou and colleagues [37] revised for the first time the combination of GMM with statistical/machine learning analyses for plant classification, emphasizing the importance of evaluating performance using standardized metrics like accuracy, sensitivity, and specificity, as well as the practicality of GMM approaches for non-destructive plant sample identification due to advancements in high-resolution imaging and desktop computing power. ...
... The last set of selected reports included in this topic focused on different aspects of the morphological evolution of flowers. McCarthy et al. [33,34] investigated the effects of allopolyploidy on floral morphology in Nicotiana genus, revealing that polyploid morphological divergence from progenitor phenotypes increases over time, particularly in floral limb shape and corolla tube length. They found that most polyploids exhibit distinct or transgressive traits, evolving shorter and wider corolla tubes, potentially leading to a shift towards more generalist pollination strategies. ...
Geometric morphometrics (GMM) is an advanced morphometric method enabling quantitative analysis of shape and size variations in biological structures. Through high-resolution imaging and mathematical algorithms, GMM provides valuable insights into taxonomy, ecology, and evolution, making it increasingly relevant in plant science. This review synthesizes the existing literature and explores methodological details, research questions, and future directions, establishing a strong foundation for further study in plant biology. Following PRISMA 2020 guidelines, a rigorous literature search finally identified 83 studies for review. The review organized data on plant species, organs studied, GMM objectives, and methodological aspects, such as imaging and landmark positioning. Leaf and flower structures emerged as the most frequently analyzed organs, primarily in studies of shape variations. This review assesses the use of GMM in plant sciences, identifying knowledge gaps and inconsistencies, and suggesting areas for future research. By highlighting unaddressed topics and emerging trends, the review aims to guide researchers towards methodological challenges and innovations necessary for advancing the field.
... Polyploidization allows organisms to react and survive; by their very nature, polyploids have a much higher range of genetic diversity than diploids, which certain environmental factors, such as habitat disturbance, nutritional stress, physical stress, and climate changes, can trigger new phenotypes, like increased allelopathic effect (Hegarty and Hiscock, 2007;Ramsey, 2011;Te Beest et al., 2012;Omezzine et al., 2017). New phenotypes may arise through heterosis, gene redundancy, or the formation of transgressive traits (Comai, 2005;McCarthy et al., 2016;Wei et al., 2019). The effects of heterosis was first identified by Darwin, whose experimental crosses resulted in more vigorous hybrids, i.e., heterosis (Darwin, 1876). ...
... The overdominance model is used to describe polyploidization, as the progressive heterosis associated with polyploids is more complex due to the increasing vigor with increasing number of genomes (Birchler et al., 2010). While heterosis generally results in polyploids with better phenotypic performance than its parent species, plants with transgressive traits display extreme phenotypes outside of the range of its progenitors (McCarthy et al., 2016). Heterosis and transgressive traits have been shown to be potential improvements for epigenetic mechanisms in allopolyploids, like histone modification or cytosine methylation (Renny-Byfield and Wendel, 2014). ...
Whole genome duplication via polyploidization is a major driver of diversification within angiosperms and it appears to confer the most benefit during times of rapid environmental change. Polyploidization offers expanded access to novel phenotypes that facilitate invasion of new environments and increased resistance to stress. These new phenotypes can arise almost immediately through the novel interactions among or between transcription factors of the duplicated genomes leading to transgressive traits, and general heterosis, or they can occur more slowly through processes like neofunctionalization, and subfunctionalization. These processes are characterized by the changes within homologs of the duplicated genomes, homoeologs. It has been proposed that redundant homoeologs are released from selective constraints and serve as an additional source of adaptive genetic variation, particularly in neo and meso-polyploids. Current practices in weed management create rapid environmental change through the use of chemicals, practices that are meant to cause the extirpation of the designated weed, and represent a strong recurrent selective event—a scenario that should favor polyploidy species. Here we ask the question, “Do polyploids make better weeds?” It is our conclusion that such a question is impossible to answer at this time due to the lack of resources and understanding in weed genomics. The growing contingent of research in weed genomics, however, driven by herbicide resistance evolution is rapidly improving our understanding of weed molecular biology and will aid in improving understanding of the impacts of ploidy levels on weed evolution and adaptation in the future.
... Polyploidy seems also to affect floral traits associated with premating barries between polyploids and diploids, especially when these changes are related with phenology and morphology (Pegoraro et al. 2016 Since pollinators may respond to small variations in floral signals and rewards (Junker et al. 2013), changes in floral traits following hybridization and polyploidization may affect plant-pollinator interactions by modifying pollinator taxon, behavior, morphological match with floral parts, and thus the selection regime (Nuismer & Cunningham 2005;Thompson & Merg 2008;Cortis et al. 2009;Chase et al. 2010;Svensson et al. 2016). These ecological consequences may be strongly context-dependent, once they are subjected to the availability of pollinators in the community, as well as their requirements, i.e. pollinator preferences that affect floral choice behavior and visitation pattern (Shuttleworth & Johnson 2010;Vereecken et al. 2010;McCarthy et al. 2016). Nevertheless, the overall impact of changes in floral traits that affect plant-pollinator interactions will also correspond to the degree of plant dependence on pollinators for pollen exchange and sexual reproduction (Whitney & Glover 2007). ...
... The giga effect could also be detected among homoploid hybrids. Examples include the homoploids Narcissus sp., which presents an increase in floral tube mouth in comparison to the parental plants (Marques et al. 2016); Nicotiana glauca and Nicotiana linearis, for which the floral limb size is larger in comparison to progenitors (McCarthy et al. 2016); and also the hybrid between Epidendrum denticulatum × Epidendrum fulgens (Pinheiro et al. 2015;Fig. 3C). ...
Events of both hybridization and polyploidy are capable of completely restructuring the genome, modifying phenotypic traits and affecting ecological interactions. For plants, these changes may affect floral traits that are important for interactions with pollinators, which could lead to shifts in pollinator behavior and taxa between hybrids/polyploids and parental/diploid species. Such pollinator shifts have great ecological and evolutionary relevance since they play a key role in the diversification of angiosperms. There is a growing number of studies that explicitly address the relationship between plant hybridization/polyploidy and pollinator shifts. However, questions remain about how often hybridization and polyploidy lead to pollinator shifts and what are the mechanisms that mediate this process. We reviewed studies that compared the reproductive biology of hybrids/polyploid with that of parental/diploid species. These studies are based on modifications of floral traits involved in attracting and rewarding pollinators. We also discussed how such changes in flower traits are widespread among plant taxa and affect pollinator visitation rates, pollinator fidelity, pollen movement, and could lead to pollinator shifts. All of these consequences are underexplored, especially from the perspective of pollinators, which foster future research that integrates genetics, ecology, and evolution of plant-pollinator interactions.
... The peak flowering time was closer to that of C. amara, while the duration of flowering and the size of flowers and petals were closer to those of C. hirsuta (Figs. 1, 2). This trait-dependent divergence of the allopolyploid from the parental species is in accordance with the findings obtained by a study of Nicotiana in the laboratory (McCarthy et al. 2016), in which multiple species collected worldwide were grown in a uniform condition. Therefore, the reproductive traits of an allopolyploid and its diploid parents can diverge in both controlled and natural conditions. ...
... Whether the floral organ size of self-fertilizing allopolyploids is negatively correlated with time since allopolyploidization can be examined by a comparative field study of multiple taxa featuring different mating systems, different time since allopolyploidization, and different locations (laboratory and natural habitat). Such a study should provide a perspective on the interpretation of previous studies performed in the field or laboratory that reported that the floral organs of allopolyploids are larger than, not different from, or smaller than those of the parents (Abbott and Lowe 2004;Alexander-Webber et al. 2016;Allen 2001;Anssour et al. 2009;Benedict et al. 2012;McCarthy et al. 2016;Perný et al. 2005; Vallejo-Marín 2012; Table 2 in Vamosi et al. 2007). ...
Allopolyploids possess complete sets of genomes derived from different parental species and exhibit a range of variation in various traits. Reproductive traits may play a key role in the reproductive isolation between allopolyploids and their parental species, thus affecting the thriving of allopolyploids. However, empirical data, especially in natural habitats, comparing reproductive trait variation between allopolyploids and their parental species remain rare. Here, we documented the flowering phenology and floral morphology of the allopolyploid wild plant Cardamine flexuosa and its diploid parents C. amara and C. hirsuta in their native range in Switzerland. The flowering of C. flexuosa started at an intermediate time compared with those of the parents and the flowering period of C. flexuosa overlapped with those of the parents. Cardamine flexuosa resembled C. hirsuta in the size of flowers and petals and the length/width ratio of petals, while it resembled C. amara in the length/width ratio of flowers. These results provide empirical evidence of the trait-dependent variation of allopolyploid phenotypes in natural habitats at the local scale. They also suggest that the variation in some reproductive traits in C. flexuosa is associated with self-fertilization. Therefore, it is helpful to consider the mating system in furthering the understanding of the processes that may have shaped trait variation in polyploids in nature.
... Recognition of ancient WGD, noted as early as 1950 (Stebbins, 1950) for specific families of angiosperms and now a hallmark of nearly every sequenced plant genome (Wendel, 2015;Barker, 2016b), confirms that many WGDs may have long-lasting evolutionary impacts. Moreover, many studies have shown evidence that polyploid events may provide the genetic framework necessary for rapid evolution, as seen in Nicotiana (Solanaceae) with changes in flower morphology and pollinators (McCarthy et al., 2016), the glucosinolate defense pathway in Brassicales (Edger et al., 2015), and the success of many domesticated crop species (Renny-Byfield and Wendel, 2014;Salman-Minkov et al., 2016). Indeed, ancient WGD events were likely catalysts for key innovations that led to the success and diversification of major clades of angiosperms (Soltis and Soltis, 2016). ...
... Indeed, 70 of the 99 WGDs investigated showed a higher number of species than did their sister clades. Additionally, there is evidence that WGD events have direct consequences on pollination success (Gross and Schiestl, 2015;McCarthy et al., 2016), invasiveness (Pandit et al., 2011;te Beest et al., 2012), tolerance to a broader range of ecological and environmental conditions (Van de Peer et al., 2009;Hahn et al., 2012), tolerance to salt concentrations (Chao et al., 2013), and range expansion (Voss et al., 2012). In fact, many diverse and successful plant lineages that show a WGD event near the base of the lineage exhibit key innovations that may be a direct response to the WGD (Soltis and Soltis, 2016). ...
... Initially, the flower was trimmed at its base, and the length was measured from the base to the apex of the lobes. Subsequently, geometric morphometric analyses were performed in the region covering the corolla lobes in frontal view, employing 15 landmarks as reference points (McCarthy et al., 2016). To achieve this, we initially separated the region containing the floral lobes and arranged them on a surface with a scaled background for photographic documentation. ...
Nitrogen is a crucial element that affects plant metabolic processes and indirectly influences the structure and dynamics of ecological interactions in terrestrial ecosystems. Since the invention of the Haber–Bosch process, human activity has significantly influenced the amount of nitrogen released into the environment. However, how do these overfertilization processes affect flora and fauna in urban ecosystems?
In our experiments, we used elevated nitrogen concentrations to simulate terrestrial eutrophication processes in Nicotiana tabacum L. We evaluated reproductive traits such as floral morphology using geometric morphometrics. Additionally, nectar volume and solute concentration, along with other vegetative traits, were quantified. Subsequently, the impacts of these modifications on herbivory and pollination interactions in a peri‐urban environment were measured.
Overfertilization resulted in notable modifications to the floral shape of the lobes, as well as a significant increase in percentage of herbivory by chewing insects, without affecting floral visitation rates. We also observed that elevated herbivory on fertilised plants did not show a direct correlation with overall pollination rates per plant or seed set. In contrast, the reduction in leaf size during the second phase of the experiment, owing to overfertilization effects, affected seed production. The roles of potential pollinators and their influence on seed quantity in control plants are discussed.
Nitrogen is a crucial element not only for plants in natural terrestrial ecosystems but also plays a fundamental role in the modification and shaping of reproductive and vegetative structures. Moreover, it affects the functionality of ecological interactions of pollination and herbivory in anthropogenic environments, such as peri‐urban areas.
... The impact of allopolyploidization on different Nicotiana's floral traits has been the aim of studies focusing on flower morphology and color. Transgressive phenotypes were observed in allopolyploid species of Nicotiana(McCarthy et al. 2016(McCarthy et al. , 2017(McCarthy et al. , 2019, suggesting a shift in the pollination system. These major changes in the floral phenotypes following genomic events (color change related to VOC's blend modification) can be linked to the competition of enzymes for substrate in the pigment biosynthetic pathways(Ben Zvi et al. 2008;Berardi et al. 2021). ...
Plant-pollinator relationships drive floral diversity. Among many floral signals, floral scent attracts and ensures efficient pollination, like benzyl acetone and its derivatives are important for hawkmoth species to detect flowers. Nicotiana is a diverse genus in terms of floral phenotypes. Its evolution was driven by the close relationship with pollinators through floral specialization and hybridization, causing the emergence of new species. Nicotiana has a wide variety of floral shapes and colors. Hybridization is prevalent in the group, resulting in transgressive phenotypes impacting pollination-related visual traits. This study investigated the diversity of floral Volatile Organic Compounds (VOCs) of Nicotiana species and discussed the data according to pollinator functional groups and the known phylogenetic relationships of the species. A bibliographic review was carried out, including 30 years of floral volatile emissions studies. The results of 18 studies investigating floral volatiles in 19 species of Nicotiana were revised and organized by temporal emissions, day and night emissions. We retrieved information concerning methodology, volatile compounds, day/night emissions, and pollinator functional groups for each study and species. In total, 179 compounds were found, including mono- and sesquiterpenoids, nitrogenous compounds, and benzenoids. Most allopolyploid species lack floral emissions data, and total temporal emissions in Nicotiana are still underrepresented. The results suggest that night-pollinated species of Nicotiana have high emission blends’ similarity to each other, compound-wise and class-wise. However, phylogeny still plays an important role in scent emission for species with different pollinators functional groups, considering the known phylogenetic relationship in the genus. Species known to be closely related by current phylogeny, like N. forgetiana and N. alata, share similar blends even though their pollinator functional groups are entirely different and opposite, suggesting a phylogenetic relationship in this phenotype and/or other processes, such as hybridization.
... Yet, tolerance to biotic stressors has received much less attention, despite the likelihood that phenotypic differences also impact species interactions (Segraves and Anneberg, 2016;Forrester and Ashman, 2017;Rezende et al., 2020;Anneberg et al., 2023aAnneberg et al., , 2023b. Specifically, polyploidy-induced phenotypic and genotypic changes can lead to novel interactions with other species, such as herbivores, pollinators, and microbes (Arvanitis et al., 2010;McCarthy et al., 2016;Porturas et al., 2019;Walczyk and Hersch-Green, 2019;Forrester et al., 2020;Rezende et al., 2020;Curé et al., 2022;Anneberg et al., 2023b). ...
Premise
Polyploidy is a widespread mutational process in angiosperms that may alter population performance of not only plants but also their interacting species. Yet, knowledge of whether polyploidy affects plant–herbivore dynamics is scarce. Here, we tested whether aphid herbivores exhibit preference for diploid or neopolyploid plants, whether polyploidy impacts plant and herbivore performance, and whether these interactions depend on the plant genetic background.
Methods
Using independently synthesized neotetraploid strains paired with their diploid progenitors of greater duckweed ( Spirodela polyrhiza ), we evaluated the effect of neopolyploidy on duckweed's interaction with the water‐lily aphid ( Rhopalosiphum nymphaeae ). Using paired‐choice experiments, we evaluated feeding preference of the herbivore. We then evaluated the consequences of polyploidy on aphid and plant performance by measuring population growth over multiple generations.
Results
Aphids preferred neopolyploids when plants were provided at equal abundances but not at equal surface areas, suggesting the role of plant population surface area in driving this preference. Additionally, neopolyploidy increased aphid population performance, but this result was dependent on the plant's genetic lineage. Lastly, the impact of herbivory on neopolyploid vs. diploid duckweed varied greatly with genetic lineage, where neopolyploids appeared to be variably tolerant compared to diploids, sometimes mirroring the effect on herbivore performance.
Conclusions
By experimentally testing the impacts of polyploidy on trophic species interactions, we showed that polyploidization can impact the preference and performance of herbivores on their plant hosts. These results have significant implications for the establishment and persistence of plants and herbivores in the face of plant polyploidy.
... Traditionally, morphometric comparisons between populations were based on the analysis of differences in their linear dimensions (Toro et al. 2010), but new methods that generate quantitative descriptions of shapes are quite useful for comparing shapes within-and among-species (Jensen et al. 2002). Geometric morphometric analyses have been applied to discriminate between parental species and their hybrids in plants, mainly using leaf shape (Jensen et al. 2002;Lexer et al. 2009;Viscosi et al. 2009;Peñaloza-Ramírez et al. 2010;Liu et al. 2018) and to a lesser degree flower shape (Shipunov and Bateman 2005;McCarthy et al. 2016;Pisano et al. 2018). In this study, in addition to leaves, we included various floral structures and found that the shape of leaves and the floral tube differentiated the two species to a greater extent, however, F. microphylla has less intraspecific variation in floral tube shape while F. thymifolia has less intraspecific variation in leaf shape. ...
Hybridization is commonly reported in angiosperms, generally based on morphology, and in few cases confirmed by molecular markers. Fuchsia has a long tradition on ornamental cultivars with different hybrids produced by artificial crosses, so natural hybridization between sympatric Fuchsia species could be common.
Natural hybridization between F. microphylla and F. thymifolia was tested using six newly developed microsatellites for F. microphylla in addition to other molecular markers with codominant and maternal inheritance. Geometric morphometrics of leaves and floral structures were also used to identify putative hybrids.
Hybrids showed a different degree of genetic admixture between both parental species. Chloroplast DNA (cpDNA) sequences indicated that hybridization occurs in both directions, in fact, some of the hybrids showed new haplotypes for cpDNA and ITS (Internal Transcriber Spacer of nuclear ribosomal RNA genes) sequences. The morphology of hybrid individuals varied between the two parental species, but they could be better identified by their leaves and floral tube.
Our study is the first to confirm the hybridization in natural populations of Fuchsia species and suggests that hybridization has probably occurred repeatedly throughout the entire distribution of the species. Phylogeographic analysis of both species will be essential to understand the impact of hybridization throughout their complete distribution.
... Anthocyanin concentration is higher for N. tomentosiformis than N. tabacum 095-55, despite similar values of DFR accumulation at 60% of anthesis (Fig. 8A) and more intense magenta pigmentation in N. tabacum 095-55 flowers compared to those of N. tomentosiformis (Fig. 1A, Supporting Information, Fig. S1). The flower size of N. tabacum 095-55 is greater than that of N. tomentosiformis, with a lower proportion of floral limb to corolla tube tissue (Fig. 1A, Supporting Information, Fig. S1, McCarthy et al. 2016McCarthy et al. , 2019, which may also explain why N. tabacum 095-55 has lower anthocyanin concentration values than N. tomentosiformis. The genetic basis of flavonol content appears to be more complicated. ...
Homeologue expression bias occurs when one progenitor copy of a gene is expressed at a higher level than the other in allopolyploids. Morphological variation, including differences in flower colour, exists between natural and synthetic allopolyploids of Nicotiana tabacum and their progenitors. In this study, we use a comparative transcriptomic approach to investigate gene expression differences as well as homeologue bias in the flavonoid biosynthetic pathway (FBP) in these accessions. We do not observe reciprocal homeologue bias between dark and light pink allopolyploids, but the production of light pink flowers is correlated with high FLAVONOL SYNTHASE:DIHYDROFLAVONOL-4-REDUCTASE (FLS:DFR) ratio at 60% of anthesis length due to delayed activation of DFR in these accessions. We do find that natural allopolyploids have stronger homeologue bias than synthetic allopolyploids in both FBP genes and across the transcriptome. While there is no overall subgenome dominance, there is a bias towards expression of N. tomentosiformis homeologues in FBP genes; however, the magnitude of this bias is reduced in allopolyploids compared to the progenitors, suggesting that N. sylvestris homeologues play an active role in the development of flower colour in N. tabacum allopolyploids. In addition, synthetic allopolyploids tend to exhibit trans regulation of homeologues whereas natural allopolyploids often have evolved cis-regulatory differences between homeologues since their origin.
... The floral traits in Nicotiana, such as corolla shape and size, corolla colour, and nectar composition, may be associated with different kinds of pollinators, such nocturnal hawkmoths, and diurnal hummingbirds in the Alatae section (Ippolito et al. 2004, Kaczorowski et al. 2012, Silva et al. 2020). On the other hand, wider and shorter corollas were suggested to have more generalist pollination strategies in allopolyploid species (McCarthy et al. 2016). ...
Floral traits are used as signals to attract pollinators and play an important role in species identification and isolation. Nicotiana is a genus with a diverse range of flower morphologies, colours, and pollination systems related to a natural history of hybridization, a driver of speciation in this genus. Nicotiana alata and Nicotiana forgetiana are pollinated by hawkmoths and hummingbirds, respectively, and a putative hybrid population was recently found. This population presents flowers with intermediate phenotypes providing an opportunity to investigate the impact of hybridization on floral trait variation. Here we investigated the floral shape, floral pigments, and nectar traits in a putative hybrid population, hereafter termed atypical populations (AP) compared to phenotypes of allopatric populations of both species. We found a high variation in floral pigmentation in AP plants and observed phenotype segregation in some genotypes. Nicotiana forgetiana and AP plants showed the same flavanol peaks as Nicotiana alata, suggesting the same UV-absorbent phenotype attractive to hawkmoths. The geometric morphometric results showed that the intermediate-coloured flowers had similar floral shape and size to N. alata. Our results suggest that the putative hybrid population would be able to attract the same parental pollinator—hawkmoths and hummingbirds—making backcrossing events possible and attracting other pollinators, such as bees.
... The polyploid origin of many plant species has long been recognized [1,2], but while polyploidy is commonly observed in angiosperms, its evolutionary importance has been controversial. Some studies support the hypothesis that polyploidy can drive rapid adaptive evolution [3,4], while others have argued that polyploidy has played a minimal role in evolution and contributed little to adaptation [5]. However, there is growing evidence that ancestral WGD events caused key changes in major angiosperm clades, supporting their successful diversification [6]. ...
Background:
The adaptive significance of polyploidy has been extensively debated, and chromosome-level genome assemblies of polyploids can provide insight into this. The Australian grass Bothriochloa decipiens belongs to the BCD clade, a group with a complex history of hybridization and polyploid. This is the first genome assembly and annotation of a species that belongs to this fascinating yet complex group.
Findings:
Using Illumina short reads, 10X Genomics linked reads, and Hi-C sequencing data, we assembled a highly contiguous genome of B. decipiens, with a total length of 1,218.22 Mb and scaffold N50 of 42.637 Mb. Comparative analysis revealed that the species experienced a relatively recent whole-genome duplication. We clustered the 20 major scaffolds, representing the 20 chromosomes, into the 2 subgenomes of the parental species using unique repeat signatures. We found evidence of biased fractionation and differences in the activity of transposable elements between the subgenomes prior to hybridization. Duplicates were enriched for genes involved in transcription and response to external stimuli, supporting a biased retention of duplicated genes following whole-genome duplication.
Conclusions:
Our results support the hypotheses of a biased retention of duplicated genes following polyploidy and point to differences in repeat activity associated with subgenome dominance. B. decipiens is a widespread species with the ability to establish across many soil types, making it a prime candidate for climate change- resilient ecological restoration of Australian grasslands. This reference genome is a valuable resource for future population genomic research on Australian grasses.
... Not only can polyploidization events lead to increased rates of speciation, but they can also generate both genetic and phenotypic novelty (Soltis et al., 2014). Importantly, changes in polyploid lineages to floral size, floral morphology, floral scent, and floral color in several plant taxa are often sufficient to attract a separate class of pollinators (Segraves and Thompson, 1999;McCarthy et al., 2016;Palmqvist et al., 2021). The changes induced by polyploidy, through several different genetic mechanisms, can have profound effects on floral signals. ...
Combinations of correlated floral traits have arisen repeatedly across angiosperms through convergent evolution in response to pollinator selection to optimize reproduction. While some plant groups exhibit very distinct combinations of traits adapted to specific pollinators (so-called pollination syndromes), others do not. Determining how floral traits diverge across clades and whether floral traits show predictable correlations in diverse groups of flowering plants is key to determining the extent to which pollinator-mediated selection drives diversification. The North American Silene section Physolychnis is an ideal group to investigate patterns of floral evolution because it is characterized by the evolution of novel red floral color, extensive floral morphological variation, polyploidy, and exposure to a novel group of pollinators (hummingbirds). We test for correlated patterns of trait evolution that would be consistent with convergent responses to selection in the key floral traits of color and morphology. We also consider both the role of phylogenic distance and geographic overlap in explaining patterns of floral trait variation. Inconsistent with phenotypically divergent pollination syndromes, we find very little clustering of North American Silene into distinct floral morphospace. We also find little evidence that phylogenetic history or geographic overlap explains patterns of floral diversity in this group. White- and pink-flowering species show extensive phenotypic diversity but are entirely overlapping in morphological variation. However, red-flowering species have much less phenotypic disparity and cluster tightly in floral morphospace. We find that red-flowering species have evolved floral traits that align with a traditional hummingbird syndrome, but that these trait values overlap with several white and pink species as well. Our findings support the hypothesis that convergent evolution does not always proceed through comparative phenotypic divergence, but possibly through sorting of standing ancestral variation.
... Therefore, the considerable morphological convergence across Microlepidieae could be best explained by gene-level diploidization that proceeded in parallel despite different pace of their genome-level (structural) diploidization. Although WGDs of different ages per se (without apparent diploidization) could alter phenotypic traits in polyploids (McCarthy et al., 2016), our study provides empirical evidence of the impact of PPD on morphological disparity in a mesopolyploie plant clade. As WGDdiploidization cycles occurred frequently during the angiosperm evolution, we propose that more polyploid models and rigorous tests (Clark and Donoghue, 2018) should be developed to investigate the impact of these genomic processes on evolution of morphological traits. ...
Angiosperm genome evolution was marked by many clade-specific whole-genome duplication (WGD) events. The Microlepidieae is one of the monophyletic clades in the mustard family (Brassicaceae) formed after an ancient allotetraploidization. Post-polyploid cladogenesis has resulted in the extant c. 17 genera and 60 species endemic to Australia and New Zealand (10 species). As post-polyploid genome diploidization is a trial-and-error process under natural selection, it may proceed with different intensity and be associated with speciation events. In Microlepidieae, different extents of homoeologous recombination between the two parental subgenomes generated clades marked by slow (“cold”) vs. fast (“hot”) genome diploidization. To gain a deeper understanding of post-polyploid genome evolution in Microlepidieae, we analyzed phylogenetic relationships in this tribe using complete chloroplast sequences, entire 35S rDNA units, and abundant repetitive sequences. The four recovered intra-tribal clades mirror the varied diploidization of Microlepidieae genomes, suggesting that the intrinsic genomic features underlying the extent of diploidization are shared among genera and species within one clade. Nevertheless, even congeneric species may exert considerable morphological disparity (e.g., in fruit shape), whereas some species within different clades experience extensive morphological convergence despite the different pace of their genome diploidization. We showed that faster genome diploidization is positively associated with mean morphological disparity and evolution of chloroplast genes (plastid-nuclear genome coevolution). Higher speciation rates in perennials than in annual species were observed. Altogether, our results confirm the potential of Microlepidieae as a promising subject for the analysis of post-polyploid genome diploidization in Brassicaceae.
... Recent genome-and transcriptome-based analyses revealed that angiosperm contains at least one paleopolyploid event and lineage-specific polyploidy events are widespread [14][15][16]. Changes in gene expression and epigenetics after polyploidization can affect the morphology and physiology of polyploidies which in turn has the potential to affect the bio-environment and interspecies interactions [17][18][19][20]. Several ancient genome-doubling events have been proved to be closely related to evolution radiation and diversification in many angiosperm lineages such as Poaceae, Solanaceae, Fabaceae, and Brassicaceae [14,21]. ...
Backgrounds
Populus and Salix belong to Salicaceae and are used as models to investigate woody plant physiology. The variation of karyotype and nuclear DNA content can partly reflect the evolutionary history of the whole genome, and can provide critical information for understanding, predicting, and potentially ameliorating the woody plant traits. Therefore, it is essential to study the chromosome number (CN) and genome size in detail to provide information for revealing the evolutionary process of Salicaceae.
Results
In this study, we report the somatic CNs of seventeen species from eight genera in Salicaceae. Of these, CNs for twelve species and for five genera are reported for the first time. Among the three subfamilies of Salicaceae, the available data indicate CN in Samydoideae is n = 21, 22, 42. The only two genera, Dianyuea and Scyphostegia, in Scyphostegioideae respectively have n = 9 and 18. In Salicoideae, Populus, Salix and five genera closely related to them (Bennettiodendron, Idesia, Carrierea, Poliothyrsis, Itoa) are based on relatively high CNs from n = 19, 20, 21, 22 to n = 95 in Salix. However, the other genera of Salicoideae are mainly based on relatively low CNs of n = 9, 10, 11. The genome sizes of 35 taxa belonging to 14 genera of Salicaceae were estimated. Of these, the genome sizes of 12 genera and all taxa except Populus euphratica are first reported. Except for Dianyuea, Idesia and Bennettiodendron, all examined species have relatively small genome sizes of less than 1 pg, although polyploidization exists.
Conclusions
The variation of CN and genome size across Salicaceae indicates frequent ploidy changes and a widespread sharing of the salicoid whole genome duplication (WGD) by the relatives of Populus and Salix. The shrinkage of genome size after WGD indicates massive loss of genomic components. The phylogenetic asymmetry in clade of Populus, Salix, and their close relatives suggests that there is a lag-time for the subsequent radiations after the salicoid WGD event. Our results provide useful data for studying the evolutionary events of Salicaceae.
... isolation between populations differing in ploidy (e.g., Coyne and Orr, 2004;Madlung, 2013;Ramsey and Ramsey, 2014;Gross and Schiestl, 2015;Sutherland and Galloway, 2017), and rapid selection against the minority cytotype resulting from a greater proportion of low fitness intercytotype matings (i.e., minority cytotype exclusion; Levin, 1975). Studies over the last several decades, however, have repeatedly documented phenotypic and ecological differences between plants differing in ploidy (e.g., Lumaret, 1988;Segraves and Thompson, 1999;Husband and Schemske, 2000;Levin, 2004;Maherali et al., 2009;Ramsey, 2011;Madlung, 2013;Gross and Schiestl, 2015;McCarthy et al., 2016;McIntyre and Strauss, 2017). Even if only slight, differences in traits such as cell size, secondary compound production, water use, flowering time, and flower color can facilitate the exploitation of novel ecological niches, ease competition between ploidies, and result in the long-term maintenance of multiple intraspecific cytotypes. ...
Premise:
Whole-genome duplication (polyploidy) is an important force shaping flowering-plant evolution. Ploidy-specific plant-pollinator interactions represent important community-level biotic interactions that can lead to nonrandom mating and the persistence of mixed-ploidy populations.
Methods:
At a naturally occurring diploid-tetraploid contact zone of the autopolyploid desert shrub Larrea tridentata, we combined flower phenology analyses, collections of bees on plants of known cytotype, and flow cytometry analyses of bee-collected pollen loads to investigate whether (1) diploid and tetraploid plants have unique bee pollinator assemblages, (2) bee taxa exhibit ploidy-specific visitation and pollen collection biases, and (3) specialist and generalist bee taxa have ploidy-specific visitation and pollen collection biases.
Results:
Although bee assemblages overlapped, we found significant differences in bee visitation to co-occurring diploids and tetraploids, with the introduced honeybee (Apis mellifera) and one native species (Andrena species 12) more frequently visiting tetraploids. Consistent with bee assemblage differences, we found that diploid pollen was overrepresented among pollen loads on native bees, while pollen loads on A. mellifera did not deviate from the random expectation. However, mismatches between the ploidy of pollen loads and plants were common, consistent with ongoing intercytotype gene flow.
Conclusions:
Our data are consistent with cytotype-specific bee visitation and suggest that pollinator behavior contributes to reduced diploid-tetraploid mating. Differences in bee visitation and pollen movement potentially contribute to an easing of minority cytotype exclusion and the facilitation of cytotype co-occurrence.
... This has made the genus an excellent model for studying the genomic, morphological and ecological effects of polyploidy in angiosperms (e.g. Renny-Byfield et al., 2011, McCarthy et al., 2015, 2016Dodsworth et al., 2017). Despite its size, N. section Suaveolentes (hereafter referred to as Suaveolentes) is comparatively much less studied than the other polyploid sections (e.g. the commercial species, homoploid hybrid involving sections Petunioides G.Don and Noctiflorae Goodsp., which is consistent with current genetic evidence Dodsworth, 2015a;Schiavinato et al., 2019). ...
Nicotiana section Suaveolentes is the largest section of Nicotiana and is a monophyletic group of allotetraploid species. Most of the species are endemic to Australia, but three species occur on islands in the South Pacific as far east as French Polynesia and one species is native to Namibia. Here, we present phylogenetic results based on genome skimming, with near-complete taxon sampling and multiple accessions sampled for several species. These represent the first phylogenetic results for the section that include most recognized taxa, using wild-sourced material wherever possible. Despite known chromosome number and genome size changes in the section, there is little divergence in the ribosomal DNA operon (26S, 18.S and 5.8S plus associated spacers) and plastid genomes, with little to no taxonomic signal in plastome phylogenetic results and clear plastid-nuclear discordance. These results contrast with strong morphological differentiation (both floral and vegetative) between most of the core Australian taxa and obvious differences in ecological preferences. Together, these initial results portray Nicotiana section Suaveolentes as experiencing recent and ongoing radiation in the arid zone of Australia.
... Lepisorus inaequibasis is more similar to its paternal than to its maternal progenitor in both morphology and the abiotic niche. -Morphologically, polyploids may show phenotypes similar to those of as one or the other progenitor, intermediate phenotypes, or novel phenotypes (Chen, 2007;McCarthy & al., 2016;Sigel, 2016). Lepisorus inaequibasis clearly shows an intermediate morphology to that of its diploid progenitors L. waltonii and L. jakonensis in terms of leaf shape (Ching & Wu, 1980). ...
Lepisorus inaequibasis is thought to be of hybrid origin due to its leaf shape and sporangia being intermediate between those of its putative progenitors. Subsequent molecular studies have supported its hybrid origin, but its progenitors have not been determined. Here, we performed molecular phylogenetic analysis, flow cytometry (FCM), morphological character observation, and ecological niche modelling (ENM) to elucidate the origin of L. inaequibasis. The phylogenetic trees inferred from single‐copy nuclear genes (pgiC and gapCp “short”) confirm the hybrid origin of L. inaequibasis from Lepisorus waltonii and Lepisorus jakonensis. Chloroplast DNA (cpDNA) phylogeny indicates that L. jakonensis is the maternal progenitor. All populations of L. inaequibasis share a single cpDNA haplotype identical to the lineage of L. jakonensis in the central Himalayas; thus, we hypothesize that L. inaequibasis originated in the central Himalaya region and dispersed to east Himalaya and Hengduan Mountain regions. Based on FCM, L. inaequibasis is tetraploid, while its progenitors are diploid. Principal component analysis of rhizome scales and observations of sporangial annuli indicated a high degree of morphological similarity between L. inaequibasis and its paternal progenitor species, L. waltonii. The ENM results showed that L. inaequibasis has a relatively high niche identity value with L. waltonii. Therefore, we conclude that L. inaequibasis is an allotetraploid that originated through hybridization between the diploid species L. waltonii and L. jakonensis. This allotetraploid species shows clear paternal bias in both its morphological characters and its ecological niche.
... In addition to its utility as a resource for breeding commercial tobacco, the genus Nicotiana has become a very powerful resource for investigating basic aspects of plant science. Historically, the genus as a whole has been a model for understanding the process of intraspecific hybridization (Smith 1968) and the evolution of polyploid species (McCarthy et al. 2016). N. tabacum and N. benthamiana Domin (an Australian species), which are known for their ease of genetic modification, are used to study an array of topics so diverse that it could fill an entire book. ...
This chapter explores plants that are used for medicinal and social uses. It first gives a brief overview of taxa that are found throughout North America, how and where they are conserved and how they are distributed. It then looks at four economically important taxa, Theobroma cacao L. (cacao), Nicotiana tabacum L. (tobacco), Actaea racemosa L. (black cohosh), Humulus lupulus L. (Hops), as case studies of how medicinal and social plants have been used over the centuries and how their wild relatives have been conserved and how we can expect these plant to be used in the future.
... However, these alternative classifications were not exactly the same: from 24 individuals which were not taxonomically assignable to either M. laxa or M. pentlandiana, the finite Gaussian mixture analysis assigned 17 to two "morphologically intermediate" groups, one to M. pentlandiana and the remaining six clustered together with M. laxa individuals (Fig. 2). Geometric morphometric analysis has been applied to discriminate among parental species and their hybrids in plants (Shipunov & Bateman 2005;Lexer et al. 2009;Peñaloza-Ramírez et al. 2010;McCarthy et al. 2016). To our knowledge, modern pattern-recognition approaches like finite Gaussian mixture analysis have not yet been applied in preliminary investigations of ill-defined plant species. ...
Phenotypic intermediacy is an indicator of putative hybrid origin, and has provided the main clues to discovering hybrid plants in nature. Mandevilla pentlandiana and M. laxa (Apocynaceae) are sister species with clear differences in floral phenotype and associated pollinator guilds: diurnal Hymenoptera and nocturnal hawkmoths, respectively. The presence of individuals with intermediate phenotypes in a wild population raises questions about the roles of visual and olfactory signals (i.e. corolla morphology and floral fragrances) as barriers to interbreeding, and how the breakdown of floral isolation occurs.
We examined phenotypic variation in a mixed Mandevilla population analysing the chemical composition of floral fragrances, characterizing floral shape through geometric morphometrics and assessing individual grouping through taxonomically relevant traits and an unsupervised learning algorithm. We quantified the visitation frequencies of floral visitors and tracked their foraging movements using pollen analogues.
The presence of morphologically intermediate individuals and pollen analogue movement suggested extensive hybridization between M. laxa and M. pentlandiana, along with asymmetrical rates of backcrossing between these putative hybrids and M. laxa. Floral volatiles from putative hybrid individuals showed a transgressive phenotype, with additional compounds not emitted by either parental species.
Our results suggest the presence of a hybrid swarm between sympatric M. pentlandiana and M. laxa and indicate that initial hybridization events between these parental species are rare, but once they occur, visits between putative hybrids and M. laxa are common and facilitate continued introgression.
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... Today, polyploidy stands accused of being responsible for evolutionary transitions that range from phylogenetically profound rare or unique events, such as the much-debated origin of the angiosperms, to frequent but smaller-scale events, such as the development of morphologically cryptic species complexes (Pillon et al., 2007;Trávníček et al., 2012). Inevitably, studies seeking processbased interpretations of ploidy change in plants have focused on model organisms such as Arabidopsis (Melaragno et al., 1993;Traas et al., 1998;Kato and Lam, 2003;Cookson et al., 2006;Berr and Schubert, 2007;Roeder et al., 2010;Adachi et al., 2011;Massonet et al., 2011;Schubert et al., 2012;Del Pozo and Ramirez-Parra, 2015;Sliwinska et al., 2015), Gossypium (Guan et al., 2014;Snodgrass et al., 2017) and Nicotiana (Renny-Byfield et al., 2011;McCarthy et al., 2016). ...
Background and aims:
Recent tissue-level observations made indirectly via flow cytometry suggest that endoreplication (duplication of the nuclear genome within the nuclear envelope in the absence of subsequent cell division) is widespread within the plant kingdom. Here, we also directly observe ploidy variation among cells within individual petals, relating size of nucleus to cell micromorphology and (more speculatively) to function.
Methods:
We compared the labella (specialized pollinator-attracting petals) of two European orchid genera: Dactylorhiza has a known predisposition to organismal polyploidy, whereas Ophrys exhibits exceptionally complex epidermal patterning that aids pseudocopulatory pollination. Confocal microscopy using multiple staining techniques allowed us to observe directly both the sizes and the internal structures of individual nuclei across each labellum, while flow cytometry was used to test for progressively partial endoreplication.
Key results:
In Dactylorhiza, endoreplication was comparatively infrequent, reached only low levels, and appeared randomly located across the labellum, whereas in Ophrys endoreplication was commonplace, being most frequent in large peripheral trichomes. Endoreplicated nuclei reflected both endomitosis and endocycling, the latter reaching the third round of genome doubling (16C) to generate polytene nuclei. All Ophrys individuals studied exhibited progressively partial endoreplication.
Conclusions:
Comparison of the two genera failed to demonstrate the hypothesized pattern of frequent polyploid speciation in genera showing extensive endoreplication. Endoreplication in Ophrys appears more strongly positively correlated with cell size/complexity than with cell location or secretory role. Epigenetic control of gene overexpression by localized induction of endoreplication within individual plant organs may represent a significant component of a plant's developmental programme, contributing substantially to organ plasticity.
... Potentially, these shifts could also reflect a switch from specialist pollination systems to generalist strategies. Such shifts in pollination systems can occur several times even within genera, and are often associated with rapid processes of genomic and phenotypic change such as hybridization and polyploidization (e.g., McCarthy et al. 2016). Smith and Kriebel (2018) also highlight reversibility and lability of floral shape and pollination system. ...
Change in floral shape is thought to be driven by pollinator-mediated selection, but drivers of floral shape evolution have been little studied at a macro-evolutionary scale. Smith and Kriebel (2018) examine floral shape across species within Iochrominae (Solanaceae) using geometric morphometrics and statistical regression analyses, and show significant correlation between corolla shape variation and shifts in pollination system. Their study highlights the importance of asking when and under what conditions the pollination-shift model may be acting. This article is protected by copyright. All rights reserved
... Duplication, loss or merging of floral structures, homeotic changes of flower organs, and changes in flower symmetry are among the mechanisms that enabled floral structure to evolve (Becker, Alix, & Damerval, 2011;Endress, 2011;Glover, Airoldi, Brockington, Fernández-Mazuecos, & Martínez-Pérez, 2015). Even among taxa that share the same floral bauplan, evolutionary changes in the sizes, shapes, and arrangement of floral structures produced extensive variation in floral morphology ( Gardner et al., 2016;Gómez, Torices, Lorite, Klingenberg, & Perfectti, 2016;McCarthy et al., 2016). These changes were accompanied by alterations of floral development, which were reflected in the respective patterns of ontogenetic allometry, the association between size and shape during development. ...
The astounding variety of angiosperm flower morphologies has evolved in response to many selective forces. Flower development is highly coordinated and involves developmental associations between size and shape, ontogenetic allometry, which in turn affect the morphology of mature flowers. Although ontogenetic allometries can act as a developmental constraint and may influence adaptive evolution, allometries can evolve themselves and may change rapidly in response to selection. We explored the evolution of ontogenetic allometry in the flowers of 11 species of Loasoideae. Seven species belong to Caiophora, which radiated recently in the central Andes, and contains species that are pollinated by bees, hummingbirds, and small rodents. According to a previous study, the diversification of Caiophora involved departures from simple allometric scaling, but the changes to allometry that enabled flower diversification have not been explored yet. We characterized the ontogenetic allometry of each species with the methods of geometric morphometrics. We studied the evolution of allometries by constructing allometric spaces, in which the allometry of each species is represented by a point and the arrangement of points indicates the relations among allometric trajectories. To examine the history of changes of ontogenetic allometries, we projected the phylogeny into the allometric spaces. Inspection of allometric spaces suggests that ontogenetic variation is limited to a few dominant features. The allometries of the two main functional flower parts under study differ in their evolutionary labilities, and patterns of variation reflect pollination systems, differences in structural organization, and abiotic environmental factors.
... Some allopolyploids are recent and have no close polyploid relatives, whereas others appear to be much older and numerous, the result of speciation at the polyploid level. Polyploidy and diploidisation have been the subject of study in the genus for around two decades: chromosome arm translocations (Lim et al. 2004), homoploid hybridisation , intergenic recombination , concerted evolution ), long-term diploidisation of genomic repeats (Clarkson et al. 2005;Dodsworth et al. 2016a), progenitor determination (Kelly et al. 2013), maternal genome donors , elimination of genomic repeats (Renny-Byfield et al. 2011), the phylogenetic signal in repeats (Dodsworth et al. 2015(Dodsworth et al. , 2016b, floral evolution (McCarthy et al. 2015), morphological character evolution (Marks et al. 2011a;McCarthy et al. 2016), biogeography (Ladiges et al. 2011) and genome size changes (Leitch et al. 2008). An earlier paper (Clarkson et al. 2005) focused on the timing of polyploid events for a subset of polyploids in Nicotiana, using nonparametric rate smoothing (NPRS), but recent advances in molecular clock analysis make another study of this subject in the genus as a whole timely. ...
We investigate the timing of diversification in allopolyploids of Nicotiana (Solanaceae) utilising sequence data of maternal and paternal origin to look for evidence of a lag phase during which diploidisation took place. Bayesian relaxed clock phylogenetic methods show recent allopolyploids are a result of several unique polyploidisation events, and older allopolyploid sections have undergone subsequent speciation at the polyploid level (i.e. a number of these polyploid species share a singular origin). The independently formed recent polyploid species in the genus all have mean age estimates below 1 million years ago (Ma). Nicotiana section Polydicliae (two species) evolved 1.5 Ma, N. section Repandae (four species) formed 4 Ma, and N. section Suaveolentes (~35 species) is about 6 million years old. A general trend of higher speciation rates in older polyploids is evident, but diversification dramatically increases at approximately 6 Ma (in section Suaveolentes). Nicotiana sect. Suaveolentes has spectacularly radiated to form 35 species in Australia and some Pacific islands following a lag phase of almost 6 million years. Species have filled new ecological niches and undergone extensive diploidisation (e.g. chromosome fusions bringing the ancestral allotetraploid number, n = 24, down to n = 15 and ribosomal loci numbers back to diploid condition). Considering the progenitors of Suaveolentes inhabit South America, this represents the colonisation of Australia by polyploids that have subsequently undergone a recent radiation into new environments. To our knowledge, this study is the first report of a substantial lag phase being investigated below the family level.
... However, most explanations of the short-term success of polyploids are centred on the effects of genomic changes and increased genetic variation, which are mediated by changes in gene expression and epigenetic remodelling [30][31][32][33][34][35][36][37] . Increased genetic variation can potentially affect the morphology, physiology and ecology of newly formed polyploids, and these changes could, in turn, affect interspecies interactions 26,33,38 . For instance, divergence in traits that are attractive to pollinators can lead to differentiation in pollinator communities 38 , causing the reproductive isolation of diploids and polyploids even within mixed populations, thereby facilitating polyploid establishment 39 . ...
Polyploidy, or the duplication of entire genomes, has been observed in prokaryotic and eukaryotic organisms, and in somatic and germ cells. The consequences of polyploidization are complex and variable, and they differ greatly between systems (clonal or non-clonal) and species, but the process has often been considered to be an evolutionary 'dead end'. Here, we review the accumulating evidence that correlates polyploidization with environmental change or stress, and that has led to an increased recognition of its short-term adaptive potential. In addition, we discuss how, once polyploidy has been established, the unique retention profile of duplicated genes following whole-genome duplication might explain key longer-term evolutionary transitions and a general increase in biological complexity.
... Some allopolyploids are recent and have no close polyploid relatives, whereas others appear to be much older and numerous, the result of speciation at the polyploid level. Polyploidy and diploidisation have been the subject of study in the genus for around two decades: chromosome arm translocations (Lim et al. 2004), homoploid hybridisation , intergenic recombination , concerted evolution ), long-term diploidisation of genomic repeats (Clarkson et al. 2005;Dodsworth et al. 2016a), progenitor determination (Kelly et al. 2013), maternal genome donors , elimination of genomic repeats (Renny-Byfield et al. 2011), the phylogenetic signal in repeats (Dodsworth et al. 2015(Dodsworth et al. , 2016b, floral evolution (McCarthy et al. 2015), morphological character evolution (Marks et al. 2011a;McCarthy et al. 2016), biogeography (Ladiges et al. 2011) and genome size changes (Leitch et al. 2008). An earlier paper (Clarkson et al. 2005) focused on the timing of polyploid events for a subset of polyploids in Nicotiana, using nonparametric rate smoothing (NPRS), but recent advances in molecular clock analysis make another study of this subject in the genus as a whole timely. ...
We investigate the timing of diversification in
allopolyploids of Nicotiana (Solanaceae) utilising sequence
data of maternal and paternal origin to look for evidence of a
lag phase during which diploidisation took place. Bayesian
relaxed clock phylogenetic methods show recent allopolyploids
are a result of several unique polyploidisation events,
and older allopolyploid sections have undergone subsequent
speciation at the polyploid level (i.e. a number of these
polyploid species share a singular origin). The independently
formed recent polyploid species in the genus all have
mean age estimates below 1 million years ago (Ma). Nicotiana
section Polydicliae (two species) evolved 1.5 Ma,
N. section Repandae (four species) formed 4 Ma, and
N. section Suaveolentes (*35 species) is about 6 million
years old. A general trend of higher speciation rates in older
polyploids is evident, but diversification dramatically
increases at approximately 6 Ma (in section Suaveolentes).
Nicotiana sect. Suaveolentes has spectacularly radiated to
form 35 species in Australia and some Pacific islands following
a lag phase of almost 6 million years. Species have
filled new ecological niches and undergone extensive
diploidisation (e.g. chromosome fusions bringing the ancestral allotetraploid number, n = 24, down to n = 15
and ribosomal loci numbers back to diploid condition).
Considering the progenitors of Suaveolentes inhabit South
America, this represents the colonisation of Australia by
polyploids that have subsequently undergone a recent radiation
into new environments. To our knowledge, this study
is the first report of a substantial lag phase being investigated
below the family level.
Allopolyploidy, a phenomenon prevalent in angiosperms involving hybridization and whole-genome duplication, results in species with multiple subgenomes, altering genome structure and gene expression, leading to novel phenotypes. Allopolyploids often experience unbalanced homeolog expression bias, the preferential expression of homeologs from one of the two progenitor genomes. To explore the consequences of allopolyploidy and unbalanced homeolog expression bias, we investigate global gene expression and the fate of homeologs in Nicotiana (Solanaceae). We focus on Nicotiana section Repandae, including three allotetraploid species, Nicotiana nudicaulis, N. repanda, and N. stocktonii, derived from diploid progenitors N. sylvestris and N. obtusifolia ∼4.3 Ma. We identify genes with differential expression and investigate expression of candidate genes for flower size variation. Our results show expression differences with the allopolyploids intermediate between the two progenitor species, with a slight bias toward N. obtusifolia. Moreover, we demonstrate unbalanced homeolog expression bias toward the N. obtusifolia subgenome across developmental stages in the allopolyploids, with a stronger bias in N. nudicaulis. In contrast, unbalanced homeolog expression bias shifts toward N. sylvestris for flower size genes in N. nudicaulis, showing that genes involved in particular phenotypes can display different patterns of unbalanced homeolog expression than the overall transcriptome. We also see differential expression of several known flower size genes across corolla developmental stages. Our results highlight the role of unbalanced homeolog expression bias in shaping the evolutionary trajectory of Nicotiana species and provide a foundation for future research into the ecological and evolutionary implications of allopolyploidy in flowering plants.
Gene duplication, as a prevalent phenomenon in the tree of life, provides a potential substrate for evolution. However, its role in the Aurantioideae remains unclear. In this study, we systematically identified, for the first time, a comprehensive landscape of five types of gene duplication in the genomes of 26 species within Aurantioideae, focusing on dissecting the duplication patterns, their potential evolutionary significance, and their impact on gene function and expression. Our results showed that the tandem duplication (TD) was a predominant duplication type and confirmed a shared ancient whole-genome duplication (γWGD) event within Aurantioideae. Ka/Ks indicated that all duplication types are under purifying selection pressure, with TD and proximal duplication (PD) undergoing rapid functional divergence. Gene Ontology (GO) enrichment analysis revealed functional specialization among different duplication types, collectively contributing to genome evolution. In addition, comparing the gene expression differentiation of the five gene duplication types between the outer and inner pericarps of Citrus maxima ‘Huazhouyou’, it was found that the proportion of gene expression differentiation in the exocarp was generally higher, suggesting tissue-specific functional roles for duplicated genes in the peel. Furthermore, gene conversion events revealed that Citrus sinensis and Citrus maxima ‘Huazhouyou’ experienced more gene conversion events, supporting that C. sinensis originated through hybridization with C. maxima as the maternal parent. Finally, the comparative analysis of gene families among 26 species in Aurantioideae revealed that small gene families (1–3 members) accounted for a substantial proportion in all species, indicating a lack of recent large-scale genome duplication events in this subfamily. These findings fill a gap in the understanding of gene duplication in Aurantioideae and provide a theoretical foundation for exploring the evolutionary mechanisms and breeding improvements within this group. Additionally, our study offers new insights into the contribution of gene duplication to functional diversification and ecological adaptation in other plants.
Polyploidization plays a pivotal role in vertebrate evolution and diversification. However, the effects of polyploidization on animals across various biological levels, and how these differences drive ecological shifts, remain unclear. Through karyotype analysis and whole-genome sequencing, we identified an autotetraploid Microhyla fissipes from Hainan Island, which shows reproductive isolation and geographic differentiation from its diploid counterpart. Tetraploids exhibited larger cell size, improved tadpole growth rates, and greater whole-body size, along with reduced cell cycle activity. Rather than being simple scaled-up diploids, tetraploids showed shifts in physiological performance, organ allometry, gene expression profiles, and metabolic patterns. Tetraploid adults demonstrated superior jumping ability and increased reproductive investment (e.g., larger gonads and steeper slopes in the relationship between gonadal weight and body weight), suggesting a potential competitive advantage over diploids. However, tetraploids exhibited higher energy expenditure at elevated temperatures, reduced hepatic energy storage, and altered pulmonary regulatory metabolites at 25 oC. Males had smaller relative heart sizes, and females showed flatter slopes in the relationship between heart and lung weight and body weight, indicating reduced investment in cardiopulmonary system. These variations suggest an increased risk of metabolic constraints under heat stress, putting tetraploids at a disadvantage in warmer regions. Importantly, the physiological trade-offs associated with polyploidization help explain the geographical differentiation between diploids and tetraploids, which reflects a climatic boundary, with tetraploids occupying cooler northeastern areas. Our findings identify an autotetraploid frog, report the first autotetraploid genome in amphibians, and demonstrate how vertebrate polyploids physiologically and ecologically diverge from their diploid counterparts.
Background and Aims
Arbuscular mycorrhizae (AM) are crucial in terrestrial ecosystems, exchanging nutrients for carbon with plants and potentially modulating events on the soil surface by making nutrients available to herbivores and pollinators. The quadruple interactions between mycorrhizae, plants, herbivores, and pollinators are a complex phenomenon as a whole; a detailed understanding of their synergistic or antagonistic effects remains a pending research challenge.
Methods
To comprehend these multiple interactions, AM were inoculated into Nicotiana tabacum and the magnitude of the symbiotic effect on floral (nectar, floral morphology, floral count) and vegetative (plant size) characteristics was evaluated, as well as the effect on pollinator visitation rate and herbivory intensity.
Results
We support the hypothesis of a symbiotic effect with a tendency toward antagonism, resulting in negative consequences for the plant. Symbiosis decreased the synthesis of floral nectar, and consequently reduced the energy content of floral nectar, without producing any effect on the pollinator visitation rate. An increase in herbivory rate was observed in mycorrhizal plants, indicating that belowground symbiotic relationships enhanced surface-level antagonistic interactions.
Conclusion
Mycorrhiza negatively influenced the plant's metabolic activity, leading to repercussions for energy investment in both pollinator manipulation resources (nectar) and defense and protection against herbivores.
Nitrogen is a crucial element that affects plant metabolic processes and indirectly influences the structure and dynamics of ecological interactions in terrestrial ecosystems. Since the invention of the Haber-Bosch process, human activity has significantly influenced the amount of nitrogen released into the environment. But, how might these processes of overfertilization impact flora and fauna within urban ecosystems? In our experiment, we employed elevated nitrogen concentrations to simulate terrestrial eutrophication in Nicotiana tabacum. We assessed the floral morphology through geometric morphometrics and quantified the nectar volume and the concentration of solutes. Subsequently, we investigated the impact of these modifications on herbivory and pollination interactions in a peri-urban setting. Overfertilization resulted in notable modifications to the floral shape of the lobes, along with a significant increase in herbivory rates due to chewing insects and daily pollination rates. However, we observed that herbivory intensity in fertilized plants and reduction in leaf size at the end of the experiments were not directly correlated with the overall pollination rate per plant. Furthermore, our findings indicate that the daily pollination rates were influenced by overfertilization. However, this increase was not attributed to the energetic content of nectar (including volume, concentration, and energy), but probably to other factors, such as the presence of nitrogen compounds in the nectar.
Nitrogen is a crucial element not only for plants in natural terrestrial ecosystems but also plays a fundamental role in the modification and shaping of reproductive and vegetative structures. Moreover, it affects the functionality of ecological interactions of pollination and herbivory in anthropogenic environments such as peri-urban areas under potential terrestrial eutrophication scenarios.
Specialized metabolite (SM) diversification is a core process to plants' adaptation to diverse ecological niches. Here, we implemented a computational mass spectrometry-based metabolomics approach to exploring SM diversification in tissues of 20 species covering Nicotiana phylogenetics sections. To markedly increase metabolite annotation, we created a large in silico fragmentation database, comprising >1 million structures, and scripts for connecting class prediction to consensus substructures. Together, the approach provides an unprecedented cartography of SM diversity and section-specific innovations in this genus. As a case study and in combination with nuclear magnetic resonance and mass spectrometry imaging, we explored the distribution of N-acylnornicotines, alkaloids predicted to be specific to Repandae allopolyploids, and revealed their prevalence in the genus, albeit at much lower magnitude, as well as a greater structural diversity than previously thought. Together, the data integration approaches provided here should act as a resource for future research in plant SM evolution.
Nicotiana section Suaveolentes is the largest section of Nicotiana and is a monophyletic group of allotetraploid species. Most of the species are endemic to Australia, but three species occur on islands in the South Pacific as far east as French Polynesia and one species is native to Namibia. Here, we present phylogenetic results based on genome skimming, with near-complete taxon sampling and multiple accessions sampled for several species. These represent the first phylogenetic results for the section that include most recognized taxa, using wild-sourced material wherever possible. Despite known chromosome number and genome size changes in the section, there is little divergence in the ribosomal DNA operon (26S, 18.S and 5.8S plus associated spacers) and plastid genomes, with little to no taxonomic signal in plastome phylogenetic results and clear plastid-nuclear discordance. These results contrast with strong morphological differentiation (both floral and vegetative) between most of the core Australian taxa and obvious differences in ecological preferences. Together, these initial results portray Nicotiana section Suaveolentes as experiencing recent and ongoing radiation in the arid zone of Australia.
This brief synopsis outlines current knowledge of the biodiversity of the genus Nicotiana L., the fifth largest genus in the family Solanaceae. Of the 82 species of Nicotiana currently recognized, most are from the New World (North, Central, and South America), but a significant radiation has occurred in arid-zone Australia (ca. 35 species). The genus is divided into 13 sections, the largest of which is section Suaveolentes, which comprises species from Africa, Australia, and the Pacific. The last complete monograph of the genus Nicotiana was published in the 1950s, but considerable work in the field has identified new species, particularly in Australia. The biology and phenotype of species of Nicotiana are reviewed, as are phylogeny and biogeography. Advances in knowledge of species-level diversity in Nicotiana are summarized and some personal priorities for future research in Nicotiana biodiversity are suggested. A table of all 82 Nicotiana species with distribution, chromosome number, and reference to a botanical description is provided, along with photographs of representative habits and flowers.
Premise:
Although polyploidy commonly occurs in angiosperms, not all polyploidization events lead to successful lineages, and environmental conditions could influence cytotype dynamics and polyploid success. Low soil nitrogen and/or phosphorus concentrations often limit ecosystem primary productivity, and changes in these nutrients might differentially favor some cytotypes over others, thereby influencing polyploid establishment.
Methods:
We grew diploid, established tetraploid, and neotetraploid Chamerion angustifolium (fireweed) in a greenhouse under low and high soil nitrogen and phosphorus conditions and different competition treatments and measured plant performance (height, biomass, flower production, and root bud production) and insect damage responses. By comparing neotetraploids to established tetraploids, we were able to examine traits and responses that might directly arise from polyploidization before they are modified by natural selection and/or genetic drift.
Results:
We found that (1) neopolyploids were the least likely to survive and flower and experienced the most herbivore damage, regardless of nutrient conditions; (2) both neo- and established tetraploids had greater biomass and root bud production under nutrient-enriched conditions, whereas diploid biomass and root bud production was not significantly affected by nutrients; and (3) intra-cytotype competition more negatively affected diploids and established tetraploids than it did neotetraploids.
Conclusions:
Following polyploidization, biomass and clonal growth might be more immediately affected by environmental nutrient availabilities than plant survival, flowering, and/or responses to herbivory, which could influence competitive dynamics. Specifically, polyploids might have competitive and colonizing advantages over diploids under nutrient-enriched conditions favoring their establishment, although establishment may also depend upon the density and occurrences of other related cytotypes in a population.
Background:
The BBAA subgenomes of hexaploid common wheat are structurally intact, which makes it possible to extract the BBAA subgenomes to constitute a novel plant type, namely, extracted tetraploid wheat (ETW). ETW displays multiple abnormal phenotypes such as massively reduced biomass and abnormal spike development, compared to extant tetraploid wheat with a BBAA genome. The genetic, biochemical and physiological basis underlying the phenotypic abnormality of ETW remains unknown.
Results:
To explore the biochemical basis of these phenotypic abnormalities, we analysed the metabolomic and proteomic profiles and quantified 46 physiological traits of ETW in comparison with its common wheat donor (genome BBAADD), and a durum tetraploid wheat cultivar (genome BBAA). Among these three types of wheat, ETW showed a saliently different pattern of nutrient accumulation and seed quality, markedly lower concentrations of many metabolites involved in carbohydrate metabolism, and higher concentrations of many metabolites related to amino acids. Among the metabolites, changes in shikimate and sucrose were the most conspicuous. Higher levels of shikimate and lower levels of sucrose influence many metabolic processes including carbohydrate and amino acid metabolism, which may contribute to the phenotypic abnormalities. Gene expression assay showed downregulation of a shikimate degradation enzyme (5-enolpyruvylshikimate-3-phosphate synthase) coding gene and upregulation of several genes coding for the sucrose hydrolysis enzyme, which could explain the higher levels of shikimate and lower levels of sucrose, respectively.
Conclusions:
Our results suggest that significant and irreversible biochemical changes have occurred in the BBAA subgenomes of common wheat during the course of its co-evolution with the DD subgenome at the hexaploid level.
I. II. III. IV. V. VI. VII. References SUMMARY: Whole-genome duplication (WGD), or polyploidy, has important effects on the genotype and phenotype of plants, potentially altering ecological interactions with other organisms. Even though the connections between polyploidy and species interactions have been recognized for some time, we are only just beginning to test whether WGD affects community context. Here I review the sparse information on polyploidy and community context and then present a set of hypotheses for future work. Thus far, community-level studies of polyploids suggest an array of outcomes, from no changes in community context to shifts in the abundance and composition of interacting species. I propose a number of mechanisms for how WGD could alter community context and how the emergence of polyploids in populations could also alter the community context of parental diploids and other plant species. Resolving how and when these changes are expected to occur will require a deeper understanding of the connections among WGD, phenotypic changes, and the direct and indirect effects of species interactions.
Premise of the study:
Both polyploidy and shifts in floral color have marked angiosperm evolution. Here, we investigate the biochemical basis of the novel and diverse floral phenotypes seen in allopolyploids in Nicotiana (Solanaceae) and examine the extent to which the merging of distinct genomes alters flavonoid pigment production.
Methods:
We analyzed flavonol and anthocyanin pigments from Nicotiana allopolyploids of different ages (N. tabacum, 0.2 million years old; several species from Nicotiana section Repandae, 4.5 million years old; and five lines of first-generation synthetic N. tabacum) as well as their diploid progenitors.
Key results:
Allopolyploid floral pigment profiles tend not to overlap with their progenitors or related allopolyploids, and allopolyploids produce transgressive pigments that are not present in either progenitor. Differences in floral color among N. tabacum accessions seems mainly to be due to variation in cyanidin concentration, but changes in flavonol concentrations among accessions are also present.
Conclusions:
Competition for substrates within the flavonoid biosynthetic pathway to make either flavonols or anthocyanins may drive the differences seen among related allopolyploids. Some of the pigment differences observed in allopolyploids may be associated with making flowers more visible to nocturnal pollinators.
A Preliminary list of the Insects and Terrestrial Arthropoda of Socorro Island, Islas Revillagigedo is presented
Following an isolation gradient in West-Mexico the avifauna of three study areas is investigated, on mainland reserve and two island groups. The avifaunas are described and analysed regarding species richness, environmental attributes, ende-mism, broader ecological niches, and brood status. The taxonomical composition is determined on different hierarchy levels. Most species records come from mainland Chamela (262), followed by the coastal Marias (191) and the oceanic Revilla-gigedos (148). Thereof 139 bird species breed in Chamela, 61 on Marias and only 29 on the Revillagigedos. In total, in the three study areas 364 species were recorded, which belong to 22 orders. On island groups generally less taxa per hierarchy level are present than on the mainland, especially on the remote Revillagigedos. Here, on average 1.7 species are found per genus, 2.2 genera per family, and 2.5 families per order. In the analysis of the taxonomical hierarchy relations to each other an isolation gradient is identified: from mainland Chamela via the coastal Marias to the oceanic Revillagigedos the degree of relatedness decreases on average. The results support the theoretical hypothesis that on islands closely related taxa tend to exclude each other and that one generalist tends to replace several specialists. Small ecological niches are often not occupied by specialist species on islands, but are used by generalists.
In this Special feature, we assemble studies that illustrate phylogenetic approaches to studying salient questions regarding the effect of specialization on lineage diversification. The studies use an array of techniques involving a wide-ranging collection of biological systems (plants, butterflies, fish and amphibians are all represented). Their results reveal that macroevolutionary examination of specialization provides insight into the patterns of trade-offs in specialized systems; in particular, the genetic mechanisms of trade-offs appear to extend to very different aspects of life history in different groups. In turn, because a species may be a specialist from one perspective and a generalist in others, these trade-offs influence whether we perceive specialization to have effects on the evolutionary success of a lineage when we examine specialization only along a single axis. Finally, how geographical range influences speciation and extinction of specialist lineages remains a question offering much potential for further insight.
Polyploidy, or whole genome multiplication, is ubiquitous among angiosperms. Many crop species are relatively recent allopolyploids, resulting from interspecific hybridization and polyploidy. Thus, an appreciation of the evolutionary consequences of (allo)polyploidy is central to our understanding of crop plant domestication, agricultural improvement, and the evolution of angiosperms in general. Indeed, many recent insights into plant biology have been gleaned from polyploid crops, including, but not limited to wheat, tobacco, sugarcane, apple, and cotton. A multitude of evolutionary processes affect polyploid genomes, including rapid and substantial genome reorganization, transgressive gene expression alterations, gene fractionation, gene conversion, genome downsizing, and sub- and neofunctionalization of duplicate genes. Often these genomic changes are accompanied by heterosis, robustness, and the improvement of crop yield, relative to closely related diploids. Historically, however, the genome-wide analysis of polyploid crops has lagged behind those of diploid crops and other model organisms. This lag is partly due to the difficulties in genome assembly, resulting from the genomic complexities induced by combining two or more evolutionarily diverged genomes into a single nucleus and by the significant size of polyploid genomes. In this review, we explore the role of polyploidy in angiosperm evolution, the domestication process and crop improvement. We focus on the potential of modern technologies, particularly next-generation sequencing, to inform us on the patterns and processes governing polyploid crop improvement and phenotypic change subsequent to domestication.
Genome sequencing has demonstrated that besides frequent small-scale duplications, large-scale duplication events such as whole genome duplications (WGDs) are found on many branches of the evolutionary tree of life. Especially in the plant lineage, there is evidence for recurrent WGDs, and the ancestor of all angiosperms was in fact most likely a polyploid species. The number of WGDs found in sequenced plant genomes allows us to investigate questions about the roles of WGDs that were hitherto impossible to address. An intriguing observation is that many plant WGDs seem associated with periods of increased environmental stress and/or fluctuations, a trend that is evident for both present-day polyploids and palaeopolyploids formed around the Cretaceous-Palaeogene (K-Pg) extinction at 66 Ma. Here, we revisit the WGDs in plants that mark the K-Pg boundary, and discuss some specific examples of biological innovations and/or diversifications that may be linked to these WGDs. We review evidence for the processes that could have contributed to increased polyploid establishment at the K-Pg boundary, and discuss the implications on subsequent plant evolution in the Cenozoic.
Spatial variation in plant-pollinator interactions may cause variation in pollinator-mediated selection on floral traits, but to establish this link conclusively experimental studies are needed. We quantified pollinator-mediated selection on flowering phenology and morphology in four populations of the fragrant orchid Gymnadenia conopsea, and compared selection mediated by diurnal and nocturnal pollinators in two of the populations. Variation in pollinator-mediated selection explained most of the among-population variation in the strength of directional and correlational selection. Pollinators mediated correlational selection on pairs of display traits, and on one display trait and spur length, a trait affecting pollination efficiency. Only nocturnal pollinators selected for longer spurs, and mediated stronger selection on the number of flowers compared with diurnal pollinators in one population. The two types of pollinators caused correlational selection on different pairs of traits and selected for different combinations of spur length and number of flowers. The results demonstrate that spatial variation in interactions with pollinators may result in differences in directional and correlational selection on floral traits in a plant with a semi-generalized pollination system, and suggest that differences in the relative importance of diurnal and nocturnal pollinators can cause variation in selection.
© 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.
Clines across hybrid zones can be produced by several forms of natural selection. We illustrate an approach to studying pollinator-mediated selection in plant hybrid zones, using two species of Ipomopsis (Polemoniaceae) as a model system. We measured visitation to flowers in natural and experimental populations by two major types of pollinators, hummingbirds and hawkmoths, at up to three different spatial scales. Using measures of pollinator visitation, we calculated phenotypic selection gradients and characterized the form of selection in the hybrid zone. Hummingbirds overvisited Ipomopsis aggregata compared with Ipomopsis tenuituba and morphological hybrids at all spatial scales, especially the largest scale of kilometers. These responses may depend in part on the presence of other hummingbird-visited plants in the community. Hummingbird behavior produced directional selection favoring wide corolla tubes and intense red coloration. Hawkmoths, in contrast, overvisited plants with narrow corolla tubes. When both types of pollinators were present, corolla width experienced disruptive selection, consistent with a model of hybrid disadvantage, in the natural hybrid zone, however, hawkmoths are rare participants. In most years plants experience visitation from hummingbirds alone. Thus, selection by pollinators usually fits an advancing wave model in which traits characteristic of I. aggregata are favored everywhere. Modeling the evolution of clines in response to such pollinator-mediated selection will require further theoretical development that allows for selection intensity to vary with spatial scale and with the abundance of unrelated plants visited by the same pollinators.
There is a voluminous literature on pollination and dispersal, very
little of which deals with the consequences of reproductive failure and
its most extreme consequence: extinction. The risk of plant extinctions
can be assessed by considering the probability of dispersal or
pollinator failure, reproductive dependence on the mutualism and
demographic dependence on seeds. Traits for ranking species rapidly
according to these three criteria are indicated. Analysis of case
studies suggests that plants often compensate for high risk in one of
the three categories by low risk in another. For example,
self-incompatible plants with rare specialist pollinators often
propagate vegetatively. Some systems, including elements of the Cape
flora and lowland tropical rain forest, lack compensatory traits and the
risk of plant extinction from failed mutualism is high. 'What escapes
the eye, however, is a much more insidious kind of extincnction: the
extinction of ecological interactions' Janzen (1974).
Symmetrical visual patterns have a salient status in human perception, as evinced by their prevalent occurrence in art, and also in animal perception, where they may be an indicator of phenotypic and genotypic quality. Symmetry perception has been demonstrated in humans, birds, dolphins and apes. Here we show that bees trained to discriminate bilaterally symmetrical from non-symmetrical patterns learn the task and transfer it appropriately to novel stimuli, thus demonstrating a capacity to detect and generalize symmetry or asymmetry. We conclude that bees, and possibly flower-visiting insects in general, can acquire a generalized preference towards symmetrical or, alternatively, asymmetrical patterns depending on experience, and that symmetry detection is preformed or can be learned as perceptual category by insects, because it can be extracted as an independent visual pattern feature. Bees show a predisposition for learning and generalized symmetry because, if trained to it, they choose it more frequently, come closer to and hover longer in front of the novel symmetrical stimuli than the bees trained for asymmetry do for the novel asymmetrical stimuli. Thus, even organisms with comparatively small nervous systems can generalize about symmetry, and favour symmetrical over asymmetrical patterns.
We studied six populations of the hummingbird-pollinated Nicotiana glauca to determine if the marked differences in the degree of floral-pollinator mismatch between populations promote divergences in the pattern of pollinator-mediated phenotypic selection on single traits and on the evolution of complexes of many interacting floral traits.We found evidence that flower phenotype is being shaped by pollinator-mediated phenotypic selection, since corolla length was consistently under contemporary directional or stabilizing selection. Weak directional selection for longer corollas was found in two populations with low flower–pollinator mismatch; much stronger directional selection was detected for shorter corollas in two populations with high flower–pollinator mismatch; finally, the remaining two populations with intermediate flower–pollinator mismatch showed stabilizing selection for corolla length. N. glauca populations differed in every flower character measured but variations in pollinator-mediated selection among populations were only observed for corolla length. Multiple covariation among traits was favoured, as suggested by the predominately functional patterns of integration and selection of complexes of many interacting floral traits. This was consistent with the patterns of correlational selection exhibited by four of the six populations, where corolla length was under significant selection in combination with corolla width, style length or stamen length. Overall floral integration was relatively high in all populations but phenotypic integration patterns were not clearly accounted by the degree of flower–pollinator mismatch or type of phenotypic selection, suggesting that trait covariation at the entire flower level is not explained by the current scenario of pollinator-mediated selection.
The number of interactions with flower visitor species differs considerably among insect pollinated plants. Knowing the causes for this variation is central to the conservation of single species as well as whole plant–flower visitor communities. Species specific constraints on flower visitor numbers are seldom investigated at the community level. In this study we tested whether flower size parameters set constraints on the morphology of the potential nectar feeding visitors and thus determine the number of visitor species. We studied three possible constraints: the depth and width of tubular structures hiding the nectar (nectar holder depth and width) and the size of flower parts that visitors can land on (size of the alighting place). In addition we assess the role of flower abundance on this relationship. We hypothesized that the stronger size constraints and the smaller flower abundance, the smaller the number of visitor species will be. Our study of a Mediterranean plant–flower visitor community revealed that nectar holder depth, nectar holder width and number of flowers explained 71% of the variation in the number of visitor species. The size of the alighting place did not restrict the body length of the visitors and was not related to visitor species number. In a second step of the analyses we calculated for each plant species the potential number of visitors by determining for each insect species of the local visitor pool whether it passed the morphological limits set by the plant. These potential numbers were highly correlated with the observed numbers (r2=0.5, p<0.001). For each plant species we tested whether the observed visitors were a random selection out of these potential visitors by comparing the mean of the observed and expected proboscis length distributions. For most plant species the observed mean was not significantly different from the random means. Our findings shed light on the way plant–flower visitor networks are structured. Knowing the constraints on interaction patterns will be an important prerequisite to formulate realistic null models and understand patterns of resource partitioning as well as coevolutionary processes.
Oligolectic bees are specialists that collect pollen from one or a few closely related species of plants, while polylectic
bees are generalists that collect pollen from both related and unrelated species of plants. Because of their more restricted
range of floral hosts, it is expected that specialists persist in more isolated populations than do generalists. We present
data on the population structure of two closely related bee species sampled from a super abundant floral host in the southern
Atacama Desert. Pairwise comparisons of population subdivision over identical distances revealed that the specialist bee had
significantly more differentiated populations in comparison to the generalist. Further, populations of the specialist had
significantly less genetic variation, measured as observed and expected heterozgyosity, than those of the generalist. Our
data support the hypothesis of decreased gene flow among populations of the specialist bee even at equivalent geographic distances.
The resulting reductions in effective population size for specialists make them particularly prone to extinction due to both
demographic and genetic reasons. Our findings have important implications for the conservation of bees and other specialist
insects.
Although it is agreed that a major polyploidy event, gamma, occurred within the eudicots, the phylogenetic placement of the event remains unclear.
To determine when this polyploidization occurred relative to speciation events in angiosperm history, we employed a phylogenomic approach to investigate the timing of gene set duplications located on syntenic gamma blocks. We populated 769 putative gene families with large sets of homologs obtained from public transcriptomes of basal angiosperms, magnoliids, asterids, and more than 91.8 gigabases of new next-generation transcriptome sequences of non-grass monocots and basal eudicots. The overwhelming majority (95%) of well-resolved gamma duplications was placed before the separation of rosids and asterids and after the split of monocots and eudicots, providing strong evidence that the gamma polyploidy event occurred early in eudicot evolution. Further, the majority of gene duplications was placed after the divergence of the Ranunculales and core eudicots, indicating that the gamma appears to be restricted to core eudicots. Molecular dating estimates indicate that the duplication events were intensely concentrated around 117 million years ago.
The rapid radiation of core eudicot lineages that gave rise to nearly 75% of angiosperm species appears to have occurred coincidentally or shortly following the gamma triplication event. Reconciliation of gene trees with a species phylogeny can elucidate the timing of major events in genome evolution, even when genome sequences are only available for a subset of species represented in the gene trees. Comprehensive transcriptome datasets are valuable complements to genome sequences for high-resolution phylogenomic analysis.
The recent development of microsatellite markers for tobacco, Nicotiana tabacum L., may be valuable for genetic studies within the genus Nicotiana. The first objective was to evaluate transferability of 100 N. tabacum microsatellite primer combinations to 5 diploid species closely related to tobacco. The number of primer combinations that amplified scorable bands in these species ranged from 42 to 56. Additional objectives were to assess levels of genetic diversity amongst available accessions of diploid relatives closely related to tobacco (species of sections Sylvestres and Tomentosae), and to evaluate the efficacy of microsatellite markers for establishing species relationships in comparison with existing phylogenetic reconstructions. A subset of 46 primer combinations was therefore used to genotype 3 synthetic tobaccos and an expanded collection of 51 Nicotiana accessions representing 15 species. The average genetic similarity for 7 diverse accessions of tobacco was greater than the average similarity for N. otophora accessions, but lower than the average genetic similarities for N. sylvestris, N. tomentosa, N. kawakamii, and N. tomentosiformis accessions. A microsatellite-based phylogenetic tree was largely congruent with taxonomic representations based on morphological, cytological, and molecular observations. Results will be useful for selection of parents for creation of diploid mapping populations and for germplasm introgression activities.
Whole-genome duplication (WGD), or polyploidy, followed by gene loss and diploidization has long been recognized as an important evolutionary force in animals, fungi and other organisms, especially plants. The success of angiosperms has been attributed, in part, to innovations associated with gene or whole-genome duplications, but evidence for proposed ancient genome duplications pre-dating the divergence of monocots and eudicots remains equivocal in analyses of conserved gene order. Here we use comprehensive phylogenomic analyses of sequenced plant genomes and more than 12.6 million new expressed-sequence-tag sequences from phylogenetically pivotal lineages to elucidate two groups of ancient gene duplications-one in the common ancestor of extant seed plants and the other in the common ancestor of extant angiosperms. Gene duplication events were intensely concentrated around 319 and 192 million years ago, implicating two WGDs in ancestral lineages shortly before the diversification of extant seed plants and extant angiosperms, respectively. Significantly, these ancestral WGDs resulted in the diversification of regulatory genes important to seed and flower development, suggesting that they were involved in major innovations that ultimately contributed to the rise and eventual dominance of seed plants and angiosperms.
A major innovation in angiosperms is the recruitment of animal pollinators as a means to enhance the efficiency and specificity of pollen transfer. The implementation of this reproductive strategy involved the rapid and presumably coordinated evolution of multiple floral traits. A major question concerns the molecular identity of the genetic polymorphisms that specify the phenotypic differences between distinct pollination syndromes. Here, we report on our work with Petunia, an attractive model system for quantitative plant genetics and genomics. From interspecific crosses, we obtained F2 plants that differed in the length of the floral tube or the size of the limb. We used these plants to study the behaviour of the hawkmoth pollinator, Manduca sexta. Plants with larger limbs were preferentially visited, consistent with the notion that flower size affects visibility under low light conditions. The moths also displayed an innate preference for shorter tubes. However, in those cases that flowers with long tubes were chosen, the animals fed for equal time. Thus, the perception of tube length may help the moths, early on, to avoid those plants that are more difficult to handle.
Reticulate evolution may function both at the species level, through homoploid and polyploid hybridization, and below the species level, through inter and intragenic recombination. These processes represent challenges for the reconstruction of evolutionary relationships between species, because they cannot be represented adequately with bifurcating trees. We use data from low-copy nuclear genes to evaluate long-standing hypotheses of homoploid (interspecific) hybrid speciation in Nicotiana (Solanaceae) and reconstruct a complex series of reticulation events that have been important in the evolutionary history of this genus. Hybrid origins for three diploid species (Nicotiana glauca, N. linearis, and N. spegazzinii) are inferred on the basis of gene tree incongruence, evidence for interallelic recombination between likely parental alleles, and support for incompatible splits in Lento plots. Phylogenetic analysis of recombinant gene sequences illustrates that recombinants may be resolved with one of their progenitor lineages with a high posterior probability under Bayesian inference, and thus there is no indication of the conflict between phylogenetic signals that results from reticulation. Our results illustrate the importance of hybridization in shaping evolution in Nicotiana and also show that intragenic recombination may be relatively common. This finding demonstrates that it is important to investigate the possibility of recombination when aiming to detect hybrids from DNA-sequence data and reconstruct patterns of reticulate evolution between species.
The acquisition of floral nectar spurs is correlated with increased species diversity across multiple clades. We tested whether variation in nectar spurs influences reproductive isolation and, thus, can potentially promote species diversity using two species of Aquilegia, Aquilegia formosa and Aquilegia pubescens, which form narrow hybrid zones. Floral visitors strongly discriminated between the two species both in natural populations and at mixed-species arrays of individual flowers. Bees and hummingbirds visited flowers of A. formosa at a much greater rate than flowers of A. pubescens. Hawkmoths, however, nearly exclusively visited flowers of A. pubescens. We found that altering the orientation of A. pubescens flowers from upright to pendent, like the flowers of A. formosa, reduced hawkmoth visitation by an order of magnitude. In contrast, shortening the length of the nectar spurs of A. pubescens flowers to a length similar to A. formosa flowers did not affect hawkmoth visitation. However, pollen removal was significantly reduced in flowers with shortened nectar spurs. These data indicate that floral traits promote floral isolation between these species and that specific floral traits affect floral isolation via ethological isolation while others affect floral isolation via mechanical isolation.
Polyploidy results in genetic turmoil, much of which is associated with new phenotypes that result in speciation. Five independent lines of synthetic allotetraploid N. x obtusiata (N x o) were created from crosses between the diploid N. attenuata (Na) (male) and N. obtusifolia (No) (female) and the autotetraploids of Na (NaT) and No (NoT) were synthesized. Their genetic, genomic and phenotypic changes were then compared with those of the parental diploid species (Na and No) as well as to the natural allotetraploids, N. quadrivalvis (Nq) and N. clevelandii (Nc), which formed 1 million years ago from crosses between ancient Na and No.
DNA fingerprinting profiles (by UP-PCR) revealed that the five N x o lines shared similar but not identical profiles. Both synthetic and natural polyploidy showed a dosage effect on genome size (as measured in seeds); however, only Nq was associated with a genome upsizing. Phenotypic analysis revealed that at the cellular level, N x o lines had phenotypes intermediate of the parental phenotypes. Both allo- and autotetraploidization had a dosage effect on seed and dry biomass (except for NaT), but not on stalk height at first flower. Nc showed paternal (Na) cellular phenotypes but inherited maternal (No) biomass and seed mass, whereas Nq showed maternal (No) cellular phenotypes but inherited paternal (Na) biomass and seed mass patterns. Principal component analysis grouped Nq with N x o lines, due to similar seed mass, stalk height and genome size. These traits separated Nc, No and Na from Nq and N x o lines, whereas biomass distinguished Na from N x o and Nq lines, and NaT clustered closer to Nq and N x o lines than to Na.
Both allo- and autotetraploidy induce considerable morphological, genetic and genomic changes, many of which are retained by at least one of the natural polyploids. It is proposed that both natural and synthetic polyploids are well suited for studying the evolution of adaptive responses.
The diurnal hawkmoth Macroglossum stellatarum is known to feed from a variety of flower species of almost all colours, forms and sizes. A newly eclosed imago, however, has to find its first flower by means of an innate flower template. This study investigates which visual flower features are represented in this template and their relative importance. Newly eclosed imagines were tested for their innate preferences, using artificial flowers made out of coloured paper or projected onto a screen through interference filters. The moths were found to have a strong preference for 440 nm and a weaker preference for 540 nm. The attractiveness of a colour increases with light intensity. The background colour, as well as the spectral composition of the ambient illumination, influences the choice behaviour. Blue paper disks against a yellowish background are chosen much more often than the same disks against a bluish background. Similarly, under ultraviolet-rich illumination, the preference for 540 nm is much more pronounced than under yellowish illumination. Disks of approximately 32 mm in diameter are preferred to smaller and larger ones, and a sectored pattern is more attractive than a ring pattern. Pattern preferences are less pronounced with coloured than with black-and-white patterns. Tests using combinations of two parameters reveal that size is more important than colour and that colour is more important than pattern.
Phylogenetic relationships in the genus Nicotiana were investigated using parsimony analyses of the internal transcribed spacer (ITS) regions of nuclear ribosomal DNA (nrDNA). In addition, origins of some amphidiploid taxa in Nicotiana were investigated using the techniques of genomic in situ hybridization (GISH), and the results of both sets of analyses were used to evaluate previous hypotheses about the origins of these taxa. Phylogenetic analyses of the ITS nrDNA data were performed on the entire genus (66 of 77 naturally occurring species, plus three artificial hybrids), comprising both diploid and polyploid taxa, and on the diploid taxa only (35 species) to examine the effects of amphidiploids on estimates of relationships. All taxa, regardless of ploidy, produced clean, single copies of the ITS region, even though some taxa are hybrids. Results are compared with a published plastid (matK) phylogeny using fewer, but many of the same, taxa. The patterns of relationships in Nicotiana, as seen in both analyses, are largely congruent with each other and previous evolutionary ideas based on morphology and cytology, but some important differences are apparent. None of the currently recognized subgenera of Nicotiana is monophyletic and, although most of the currently recognized sections are coherent, others are clearly polyphyletic. Relying solely upon ITS nrDNA analysis to reveal phylogenetic patterns in a complex genus such as Nicotiana is insufficient, and it is clear that conventional analysis of single data sets, such as ITS, is likely to be misleading in at least some respects about evolutionary history. ITS sequences of natural and well-documented amphidiploids are similar or identical to one of their two parents-usually, but not always, the maternal parent-and are not in any sense themselves 'hybrid'. Knowing how ITS evolves in artificial amphidiploids gives insight into what ITS analysis might reveal about naturally occurring amphidiploids of unknown origin, and it is in this perspective that analysis of ITS sequences is highly informative.
For Nicotiana, with 75 naturally occurring species (40 diploids and 35 allopolyploids), we produced 4656bp of plastid DNA sequence for 87 accessions and various outgroups. The loci sequenced were trnL intron and trnL-F spacer, trnS-G spacer and two genes, ndhF and matK. Parsimony and Bayesian analyses yielded identical relationships for the diploids, and these are consistent with other data, producing the best-supported phylogenetic assessment currently available for the genus. For the allopolyploids, the line of maternal inheritance is traced via the plastid tree. Nicotiana and the Australian endemic tribe Anthocercideae form a sister pair. Symonanthus is sister to the rest of Anthocercideae. Nicotiana sect. Tomentosae is sister to the rest of the genus. The maternal parent of the allopolyploid species of N. sect. Polydicliae were ancestors of the same species, but the allopolyploids were produced at different times, thus making such sections paraphyletic to their extant diploid relatives. Nicotiana is likely to have evolved in southern South America east of the Andes and later dispersed to Africa, Australia, and southwestern North America.
Flower color is often viewed as a trait that signals rewards to pollinators, such that the relationship between flower color and plant fitness might result from its association with another trait. We used experimental manipulations of flower color and nectar reward to dissociate the natural character correlations present in a hybrid zone between Ipomopsis aggregata and Ipomopsis tenuituba. Isozyme markers were used to follow the male and female reproductive success of these engineered phenotypes. One field experiment compared fitnesses of I. aggregata plants that varied only in flower color. Plants with flowers painted red received more hummingbird visits and sired more seeds than did plants with flowers painted pink or white to match those of hybrids and I. tenuituba. Our second field experiment compared fitnesses of I. aggregata, I. tenuituba, and hybrid plants in an unmanipulated array and in a second array where all flowers were painted red. In the unmanipulated array, I. aggregata received more hummingbird visits, set more seeds per flower, and sired more seeds per flower. These fitness differences largely disappeared when the color differences were eliminated. The higher male fitness of I. aggregata was due to its very high success at siring seeds on conspecific recipients. On both I. tenuituba and hybrid recipients, hybrid plants sired the most seeds, despite showing lower pollen fertility than I. aggregata in mixed donor pollinations in the greenhouse. Ipomopsis tenuituba had a fitness of only 13% relative to I. aggregata when traits varied naturally, compared to a fitness of 36% for white relative to red flowers when other traits were held constant.
Specialization has often been claimed to be an evolutionary dead end, with specialist lineages having a reduced capacity to persist or diversify. In a phylogenetic comparative framework, an evolutionary dead end may be detectable from the phylogenetic distribution of specialists, if specialists rarely give rise to large, diverse clades. Previous phylogenetic studies of the influence of specialization on macroevolutionary processes have demonstrated a range of patterns, including examples where specialists have both higher and lower diversification rates than generalists, as well as examples where the rates of evolutionary transitions from generalists to specialists are higher, lower or equal to transitions from specialists to generalists. Here, we wish to ask whether these varied answers are due to the differences in macroevolutionary processes in different clades, or partly due to differences in methodology. We analysed ten phylogenies containing multiple independent origins of specialization and quantified the phylogenetic distribution of specialists by applying a common set of metrics to all datasets. We compared the tip branch lengths of specialists to generalists, the size of specialist clades arising from each evolutionary origin of a specialized trait and whether specialists tend to be clustered or scattered on phylogenies. For each of these measures, we compared the observed values to expectations under null models of trait evolution and expected outcomes under alternative macroevolutionary scenarios. We found that specialization is sometimes an evolutionary dead end: in two of the ten case studies (pollinator-specific plants and host-specific flies), specialization is associated with a reduced rate of diversification or trait persistence. However, in the majority of studies, we could not distinguish the observed phylogenetic distribution of specialists from null models in which specialization has no effect on diversification or trait persistence.
In this investigation of orchids, first published in 1862, Darwin expands on a point made in On the Origin of Species that he felt required further explanation, namely that he believes it to be 'a universal law of nature that organic beings require an occasional cross with another individual'. Darwin explains the method by which orchids are fertilised by insects, and argues that the intricate structure of their flowers evolved to favour cross pollination because of its advantages to the species. The book is written in Darwin's usual precise and elegant style, accessible despite its intricate detail. It includes a brief explanation of botanical terms and is illustrated with 34 woodcuts.
Polyploidy has long been considered a major force in plant evolution. G. Ledyard Stebbins, Jr., an architect of the Modern Synthesis, elegantly addressed a broad range of topics, from genes to chromosomes to deep phylogeny, but some of his most lasting insights came in the study of polyploidy. Here, we review the immense impact of his work on polyploidy over more than 60 years, from his entrance into this fledgling field in the 1920s until the end of his career. Stebbins and his contemporaries developed a model of polyploid evolution that persisted for nearly half a century. As new perspectives emerged in the 1980s and new genetic tools for addressing key aspects of polyploidy have become available, a new paradigm of polyploidy has replaced much of the Stebbinsian framework. We review that paradigm shift and emphasize those areas in which the ideas of Stebbins continue to propel the field forward, as well as those areas in which the field was held back; we also note new directions that plant geneticists and evolutionists are now exploring in polyploidy research. Perhaps the most important conclusion from recent and ongoing studies of polyploidy is that, following Levin and others, polyploidy may propel a population into a new adaptive sphere given the myriad changes that accompany genome doubling.
... Fig. 9). Heuchera grossulariifolia plants on the Salmon River were frequently visited by approximately 15 species or guilds of insects. ... time Page 8. PLANT POLYPLOIDY AND POLLINATION 1121 8- * Rapid R. _
In many polyploid species, polyploids often have different suites of floral traits and different flowering times than their diploid progenitor species. We hypothesized that such differences in floral traits in polyploids may subsequently affect their interactions with pollinating and other insect visitors. We measured floral morphology and flowering phenology in 14 populations of diploid and autotetraploid Heuchera grossulariifolia Rydb. (Saxifragaceae), determined if repeated evolution of independent polyploid lineages resulted in differentiation in floral morphology among those lineages, and ascertained if there was a consistent pattern of differentiation among genetically similar diploid and autotetraploid populations. In addition, we evaluated the differences in suites of floral visitors within a natural community where diploids and autotetraploids occur sympatrically. Overall, flowers of autotetraploid plants were larger and shaped differently than those of diploids, had a different flowering phenology than that of diploids, and attracted different suites of floral visitors. In comparison with flowers of diploids, tetraploid floral morphology varied widely from pronounced differences between cytotypes in some populations to similar flower shapes and sizes between ploidal levels in other populations. Observations of floral visitors to diploids and autotetraploids in a natural sympatric population demonstrated that the cytotypes had different suites of floral visitors and six of the 15 common visitors preferentially visited one ploidy more frequently. Moreover, we also found that floral morphology differed among independent autotetraploid origins, but there was no consistent pattern of differentiation between genetically similar diploid and autotetraploid populations. Hence, the results suggest that the process of polyploidization creates the potential for attraction of different suites of floral visitors. Multiple origins of polyploidy also presents the opportunity for new or different plant-insect interactions among independent polyploid lineages. These differences in turn may affect patterns of gene flow between diploids and polyploids and also among plants of independent polyploid origin. Polyploidy, therefore, may result in a geographic mosaic of interspecific interactions across a species' range, contributing to diversification in both plant and insect groups.
Flower color is often viewed as a trait that signals rewards to pollinators, such that the relationship between flower color and plant fitness might result from its association with another trait. We used experimental manipulations of flower color and nectar reward to dissociate the natural character correlations present in a hybrid zone between Ipomopsis aggregata and Ipomopsis tenuituba. Isozyme markers were used to follow the male and female reproductive success of these engineered phenotypes. One field experiment compared fitnesses of I. aggregata plants that varied only in flower color. Plants with flowers painted red received more hummingbird visits and sired more seeds than did plants with flowers painted pink or white to match those of hybrids and I. tenuituba. Our second held experiment compared fitnesses of I. aggregata, I. tenuituba, and hybrid plants in an unmanipulated array and in a second array where all flowers were painted red. In the unmanipulated array, I. aggregata received more hummingbird visits, set more seeds per flower, and sired more seeds per flower. These fitness differences largely disappeared when the color differences were eliminated. The higher male fitness of I. aggregata was due to its very high success at siring seeds on conspecific recipients. On both I. tenuituba and hybrid recipients, hybrid plants sired the most seeds, despite showing lower pollen fertility than I. aggregata in mixed donor pollinations in the greenhouse. Ipomopsis tenuituba had a fitness of only 13% relative to I. aggregata when traits varied naturally, compared to a fitness of 36% for white relative to red flowers when other traits were held constant.
Some plants have evolved flowers of extraordinary depth, a phenomenon which puzzled Darwin1. Darwin suggested that the evolution of deep flowers could be a response to a kind of 'race' with pollinating insects: the length of the tongues of pollinating insects could increase as a result of a general size increase, or because it increased their nectar foraging efficiency. As this occurred, plants with relatively shallow flowers could be disadvantaged since pollen transfer, which is effected by physical contact between the pollinator and the anthers or stigma of the plant, could be reduced when the insect tongue is long relative to flower depth. This could lead to the evolution of increasing flower depth which in turn could drive the evolution of a further increase in insect tongue length. Various predictions of Darwin's proposal were tested here for orchid species with deep flowers that are pollinated by moths. It was found that insects do indeed insert their probosces no further than necessary to obtain nectar; that an experimental reduction in flower depth reduces both the male and female components of fitness; and that in natural populations there is a correlation between flower depth and female fitness measured by fruit set. These results all support Darwin's hypothesis to explain the evolution of flower depth.
Flowers are phenotypically integrated units that may require a precise configuration of floral organs for proper function. Plants, however, are metameric organisms that often exhibit architectural and temporal variation in floral size and shape. Clearly, architectural and temporal effects could interrupt phenotypic integration within flowers, yet such effects have not been explicitly examined. We compared correlations among floral characters for the closely related but morphologically divergent species Nicotiana alata and Nicotiana forgetiana and their artificial F3 hybrids. Principal components analysis of 16 floral traits identified two suites of correlated characters that are maintained in both taxa and in the hybrids, regardless of architectural and temporal variation in floral characters. We interpret the maintenance of these suites as evidence of common developmental regulation of correlated characters. One suite includes measures of corolla tube, gynoecium, and androecium length, while the other includes corolla limb and corolla tube aperture characters. The correlated suites of characters are tightly integrated, independent from characters of the other factor, and they participate in a common function. As such, these character suites represent phenotypic modules that have been maintained despite evolutionary changes in morphology during the divergence of the two species.
1. Corolla shape is one of many floral traits used by pollinators when making foraging decisions. Corolla shape has been implicated as a factor in floral isolation and evolutionary shifts between pollinator affinities, yet few studies have investigated how quantifiable differences in corolla shape affect pollinator behaviour.
2. This study measured variation in corolla shape (primarily corolla limb dissectedness) across eight species of Nicotiana (section Alatae) and its influence on flower choice by nocturnal hawkmoths (Manduca sexta). Behavioural assays performed under simulated moonlight tested for hawkmoth preference and performance differences between the average floral shape of sphingophilous species (CHawkmoth), the average of all Nicotiana species in this study (CAll), and/or the average of hummingbird-pollinated species (CHummingbird).
3. In mixed arrays, hawkmoths preferred CHawkmoth over CAll flowers, but only when shapes were not standardized for surface area. In homogeneous arrays, hawkmoths emptied more flowers with CHawkmoth shapes, but performance did not differ when shapes were standardized by surface area. However, hawkmoths visited fewer CHummingbird flowers than other shapes when surface area was standardized.
4. Our study shows that hawkmoth behaviour can be affected by differences in corolla shape, but that floral size may be more important than true shape differences in floral discrimination by hawkmoths.
Nicotiana (Solanaceae) provides an ideal system for understanding polyploidization, a pervasive and powerful evolutionary force in plants, as this genus contains several groups of allotetraploids that formed at different times from different diploid progenitors. However, the parental lineages of the largest group of allotetraploids, Nicotiana section Suaveolentes, have been problematic to identify. Using data from four regions of three low-copy nuclear genes, nuclear ribosomal DNA, and regions of the plastid genome, we have reconstructed the evolutionary origin of sect. Suaveolentes and identified the most likely diploid progenitors by using a combination of gene trees and network approaches to uncover the most strongly supported evidence of species relationships. Our analyses best support a scenario where a member of the sect. Sylvestres lineage acted as the paternal progenitor and a member of either sect. Petunioides or sect. Noctiflorae that also contained introgressed DNA from the other, or a hypothetical hybrid species between these two sections, was the maternal progenitor. Nicotiana exemplifies many of the factors that can complicate the reconstruction of polyploid evolutionary history and highlights how reticulate evolution at the diploid level can add even greater complexity to allopolyploid genomes.
Observations of hummingbirds feeding at flowers longer or shorter than their bills seem to contradict the view that bill lengths of hummingbirds evolved in concert with the lengths of their flowers. Recent experiments, however, indicate that a hummingbird's ability to feed at artificial flowers of different lengths depends on the widths of the flowers. We examined if the broad range of flower lengths visited by many hummingbird species can be explained by the widths of the flowers. We predicted that both short- and long-billed hummingbirds would include long, wide flower species in their diets, but that short-billed hummingbirds would not include long, narrow flower species because nectar in these species might be beyond the reach of their bills. If so, the slope of the regression for flower width versus flower length should be smaller for flower species visited by longer-billed hummingbirds relative to those visited by shorter-billed hummingbirds. Analyses of data sets for some North American and Monteverde hummingbirds and their food plants were consistent with this prediction, and bill lengths were significantly correlated with the slopes of the regressions of flower width versus length for seven hummingbird species. Comparisons of observed flower use by some Monteverde hummingbird species to flower assemblages generated at random suggest that these significant regressions were not simply a result of allometric relationships between flower lengths and widths, but in some cases reflected active choice by the birds. The two hummingbird–flower data sets also differed significandy in the scaling of corolla width relative to corolla length. In particular, the Monteverde data set contained a large number of long, narrow flower species, which we suggest is a consequence of a different floral evolutionary history and association with long-billed hummingbird species. The evolutionary effects of hummingbirds and their flowers upon one another are more complex than has generally been realized, and a consideration of corolla length jointly with other floral characters may improve our understanding of hummingbird-flower relationships.
Floral shape is a visual cue used by pollinators to discriminate between competing flower species. We investigated whether discrimination is possible between closed shapes presenting the same colour and lacking a centrally presented fixation point. Free-flying honeybees, Apis mellifera L., had to discriminate between a solid square and a solid triangle of the same colour presented on the back walls of a Y-maze. Different colours were used to vary chromatic contrast and receptor-specific contrasts. Discrimination was possible whenever shapes presented contrast to the long wavelength receptor but was independent of chromatic contrast, overall intensity contrast or short and middle wavelength receptor contrast. We suggest that the bees used the edges of the closed shapes to solve the task. Bees failed when shapes were rotated, showing that a single shape edge was not sufficient for recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal-pollinated flowers are complex structures that may require a precise configuration of floral organs for proper function. As such, they represent an excellent system with which we can examine the role of phenotypic integration and modularity in morphological evolution. We use complementary quantitative genetic and comparative phenotypic approaches to examine correlations among floral characters in Nicotiana alata, N. forgetiana and their artificial fourth-generation hybrids. Flowers of both species share basic patterns of genetic and phenotypic correlations characterized by at least two integrated character suites that are relatively independent of each other and are not disrupted by four generations of recombination in hybrids. We conclude that these integrated character suites represent phenotypic modules that are the product of a modular genetic architecture. Intrafloral modularity may have been critical for rapid specialization of these species to different pollinators.
Zoophilous flowers often appear to be precisely formed for pollen transfer and exhibit relatively little variability in structure within species. Functional optimization by the seemingly exacting requirements of pollen transfer may account for these observations. I used the results of a literature survey to examine the levels of intraspecific variation in flowers across a wide range of taxa. The least variable attributes were those potentially affecting the mechanical fit between flower and pollinator, which are potentially constrained by selection for pollination performance. I discuss six mechanisms by which plant-pollinator interactions could generate stabilizing selection on flowers. In addition, I consider the stabilizing roles of limiting resources and also two functionally-neutral mechanisms. Further work is required to identify the actual mechanisms by which selection stabilizes the evolution of flowers. Copyright 1998 Annals of Botany Company
Interspecies relationships in Nicotiana (Solanaceae) are complex because 40 species are diploid (two sets of chromosomes) and 35 species are allotetraploid (four sets of chromosomes, two from each progenitor diploid species). We sequenced a fragment (containing four introns) of the nuclear gene 'chloroplast-expressed glutamine synthetase' (ncpGS) in 65 species of Nicotiana. Here we present the first phylogenetic analysis based on a low-copy nuclear gene for this well studied and important genus. Diploid species have a single-copy of ncpGS, and allotetraploids as expected have two homeologous copies, each derived from their progenitor diploid. Results were particularly useful for determining the paternal lineage of previously enigmatic taxa (for which our previous analyses had revealed only the maternal progenitors). In particular, we were able to shed light on the origins of the two oldest and largest allotetraploid sections, N. sects. Suaveolentes and Repandae. All homeologues have an intact reading frame and apparently similar rates of divergence, suggesting both remain functional. Difficulties in fitting certain diploid species into the sectional classification of Nicotiana on morphological grounds, coupled with discordance between the ncpGS data and previous trees (i.e. plastid, nuclear ribosomal DNA), indicate a number of homoploid (diploid) hybrids in the genus. We have evidence for Nicotiana glutinosa and Nicotiana linearis being of hybrid origin and patterns of intra-allelic recombination also indicate the possibility of reticulate origins for other diploid species.
The idea of coevolution originated with Darwin's proposal that long-proboscid pollinators and long-tubed flowers might be engaged in reciprocal selection, but this has not been demonstrated. Here we test key aspects of Darwin's hypothesis of reciprocal selection in an experiment with naturally interacting populations of extremely long-proboscid flies (Moegistorhynchus longirostris: Nemestinidae) and long-tubed irises (Lapeirousia anceps: Iridaceae). We show that the benefit derived by both the fly (volume of nectar consumed) and the plant (number pollen grains received) depends on the relative length of their interacting organs. Each trait is shown to act both as agent and target in directional reciprocal selection, potentially leading to a race. This understanding of how fitness in both species varies in relation to the balance of their armament allows us to make tentative predictions about the nature of selection across multiple communities. We find that in each community a core group of long-tubed plant species might together be involved in diffuse coevolution with the fly. In poorly matched populations, the imbalance in armament is too great to allow reciprocal selection to act, and these species might instead experience one-sided selection that leads to convergence with the core species. Reciprocal selection drives the evolution of the community, then, additional species become attached to the network of interacting mutualists by convergence.
The long-standing notion that most angiosperm flowers are specialized for pollination by particular animal types, such as birds or bees, has been challenged recently on the basis of apparent widespread generalization in pollination systems. At the same time, biologists working mainly in the tropics and the species-rich temperate floras of the Southern hemisphere are documenting pollination systems that are remarkably specialized, often involving a single pollinator species. Current studies are aimed at understanding: (1) the ecological forces that have favoured either generalization or specialization in particular lineages and regions; (2) the implications for selection on floral traits and divergence of populations; and (3) the risk of collapse in plant-pollinator mutualisms of varying specificity.
We address how a conflict between pollinator attraction and avoidance of flower predation influences the evolution of flower shape in Polemonium viscosum. Flower shape in P. viscosum is the product of an isometric relationship between genetically correlated (rA = 0.70) corolla flare and length. Bumblebee pollinators preferentially visit flowers that are more flared and have longer tubes, selecting for a funnel-shaped corolla. However, flower shape also influences nectar-foraging ants that sever the style at its point of attachment to the ovary. Surveys of ant damage show that plants having flowers with flared, short corollas are most vulnerable to ant predation. Consistent with this result, the ratio of corolla length to flare is significantly greater in a krummholz (high predation risk) population than in a tundra (low predation risk) population. To explicitly test whether the evolution of a better defended flower would exact a cost in pollination, we created tubular flowers by constricting the corolla during development. Performance of tubular flowers and natural controls was compared for defensive and attractive functions. In choice trials, ants entered control flowers significantly more often than tubular ones, confirming that the evolution of tubular flowers would reduce the risk of predation. However, in a bumblebee-pollinated population, tubular flowers received significantly less pollen and set fewer seeds than controls. A fitness model incorporating these data predicts that in the absence of the genetic correlation between corolla length and flare, intermittent selection for defense could allow tubular flowers to spread in the krummholz population. However, in the tundra, where bumblebees account for nearly all pollination, the model predicts that tubular flowers should always confer a fitness disadvantage.
Floral phenotypes may be as much the result of selection for avoidance of some animal visitors as selection for improving the interaction with better pollinators. When specializing on hummingbird-pollination, Penstemon flowers may have evolved to improve the morphological fit between bird and flower, or to exclude less-efficient bees, or both. We hypothesized how such selection might work on four floral characters that affect the mechanics of pollen transfer: anther/stigma exsertion, presence of a lower corolla lip, width of the corolla tube, and angle of flower inclination. We surgically modified bee-pollinated P. strictus flowers changing one trait at a time to make them resemble hummingbird-pollinated P. barbatus flowers, and measured pollen transfer by bumblebees and hummingbirds. Results suggest that, apart from 'pro-bird' adaptations, specific 'anti-bee' adaptations have been important in shaping hummingbird-flowers. Moreover, some trait changes may have been selected for only if changing in concert with other traits.
For about 70 years, bees were assumed not to possess the capacity to discriminate among convex shapes, such as a disc, a square or a triangle, based on results of early studies conducted by presenting shapes on horizontal planes. Using shapes presented on a vertical plane, we recently demonstrated that bees do discriminate among a variety of convex shapes. Several findings, summarized here, provide indirect evidence that discrimination is based on a cue located at the shapes' boundaries. In the present study, we test this hypothesis directly in two different ways. (1) Three groups of bees are each trained with a different pair of convex shapes, one positive (rewarding), the other not (negative), producing colour contrast, luminance contrast or motion contrast against the background. The trained bees are then offered a choice between pairs of stimuli whose shapes are identical to those of the training shapes, but whose contrast against the background is varied by changing the pattern, the colour or the luminance of the areas. The results show that bees discriminate between the pairs of novel shapes, i.e. they generalize the shapes among the different types of contrast, revealing that they use a particular cue extracted from the positive shape. The bees' choices between a stimulus that produces the correct contrast but has the wrong shape and one that possesses the correct shape but the wrong contrast show, in addition, that the relevant cue is not located within the area of the shape. (2) Bees trained with pairs of convex shapes are tested with the same pairs of shapes, but which lack the inner area, i.e. only the contours or fragments of the contours are presented in the tests. Bees are found to prefer the stimulus whose contours (or fragments of contours) agree with those of the positive training shape. Taken together, the results suggest that convex shapes are not represented by the form of their areas but rather by some cue located at their boundaries.
Here, we analyze long-term evolution in Nicotiana allopolyploid section Repandae (the closest living diploids are N. sylvestris, the maternal parent, and N. obtusifolia, the paternal parent). We compare data with other more recently formed Nicotiana allopolyploids. We investigated 35S and 5S nuclear ribosomal DNA (rDNA) chromosomal location and unit divergence. A molecular clock was applied to the Nicotiana phylogenetic tree to determine allopolyploid ages. N. tabacum and species of Repandae were c. 0.2 and 4.5 Myr old, respectively. In all Repandae species, the numbers of both 35S and 5S rDNA loci were less than the sum of those of the diploid progenitors. Trees based on 5S rDNA spacer sequences indicated units of only the paternal parent. In recent Nicotiana allopolyploids, the numbers of rDNA loci equal the sum of those of their progenitors. In the Repandae genomes, diploidization is associated with locus loss. Sequence analysis indicates that 35S and 5S units most closely resemble maternal and paternal progenitors, respectively. In Nicotiana, 4.5 Myr of allopolyploid evolution renders genomic in situ hybridization (GISH) unsuitable for the complete resolution of parental genomes.