January 2025
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Publications (455)
November 2024
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121 Reads
Journal of Systematics and Evolution
Despite the importance of gamete production this topic has rarely been investigated in angiosperms using comparative approaches. Here, we investigated pollen and ovule numbers per flower in 73 species and 99 populations of Primula comprising both distylous and homostylous reproductive systems. We investigated whether phylogenetic relationships influenced associations between variation in gamete production, floral traits and elevation, and whether the evolutionary breakdown of distyly to homostyly resulted in parallel changes to gamete production. We used a Bayesian approach facilitated by the MCMCglmm method to model pollen and ovule traits across species and determined whether they exhibited phylogenetic signals. We detected significant positive correlations between pollen number and elevation in both the long-styled and short-styled morphs (L-morph and S-morph, respectively), whereas ovule number was not influenced by elevation. Pollen production was significantly higher in the L-morph than in the S-morph, but there was no significant difference between morphs in ovule number. Pollen volume exhibited a positive correlation with the style length of compatible morphs. The transition from distyly to homostyly was associated with significant decreases in pollen production but not ovule number. Our findings demonstrate the importance of elevation on pollen production, perhaps because of selection to improve pollen-transfer efficiency in uncertain pollinator environments. In contrast, ovule number variation appears to be more constrained by phylogenetic relationships. Our comparative analyses of a well defined angiosperm lineage highlight the complex interactions between intrinsic and extrinsic factors influencing gamete production in plants and emphasize the importance of considering pollen and ovule data separately.
October 2024
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38 Reads
The maintenance of genetic variation by balancing selection is of considerable interest to evolutionary biologists. An important but understudied potential driver of balancing selection is antagonistic pleiotropy between diploid and haploid stages of the plant life cycle. Despite sharing a common genome, sporophytes (2n) and gametophytes (n) may undergo differential or even opposing selection. Theoretical work suggests the antagonistic pleiotropy between life stages can generate balancing selection and maintain genetic variation. Despite the potential for far-reaching consequences of gametophytic selection, empirical tests of its pleiotropic effects (neutral, synergistic, or antagonistic) on sporophytes are generally lacking. Here, we examined the population genomic signals of selection across life stages in the angiosperm Rumex hastatulus and the moss Ceratodon purpureus. We compared gene expression among life stages and between sexes, combined with neutral diversity statistics and the analysis of the distribution of fitness effects. In contrast to what would be predicted under balancing selection due to antagonistic pleiotropy, we found that unbiased genes between life stages are under stronger purifying selection, likely explained by a predominance of synergistic pleiotropy between life stages and strong purifying selection on broadly expressed genes. In addition, we found that 30% of candidate genes under balancing selection in R. hastatulus are located within inversion polymorphisms. Our findings provide novel insights into the genome-wide characteristics and consequences of plant gametophytic selection.
October 2024
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7 Reads
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1 Citation
Evolution
Mirror-image flowers (enantiostyly) involve a form of sexual asymmetry in which a flower’s style is deflected either to the left or right side, with a pollinating anther orientated in the opposite direction. This curious floral polymorphism, which was known but not studied by Charles Darwin, occurs in at least 11 unrelated angiosperm families and represents a striking example of adaptive convergence in form and function associated with cross-pollination by insects. In several lineages, dimorphic enantiostyly (one stylar orientation per plant, both forms occurring within populations) has evolved from monomorphic enantiostyly, in which all plants can produce both style orientations. We use a modelling approach to investigate the emergence of dimorphic enantiostyly from monomorphic enantiostyly under gradual evolution. We show using adaptive dynamics that depending on the balance between inbreeding depression following geitonogamy, pollination efficiency and plant density, dimorphism can evolve from an ancestral monomorphic population. In general, the newly emergent dimorphic population is stable against invasion of a monomorphic mutant. However, our model predicts that under certain ecological conditions, e.g., a decline of pollinators, dimorphic enantiostyly may revert to a monomorphic state. We demonstrate using population genetics simulations that the observed evolutionary transitions are possible assuming a plausible genetic architecture.
August 2024
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33 Reads
Inbreeding depression is likely to play an important role during biological invasion. But relatively few studies have investigated the fitness of selfed and outcrossed offspring in self-incompatible invasive plants in natural environments in their introduced range. Moreover, the majority of studies on inbreeding depression have investigated self-compatible species with mixed mating, and less is known about the intensity of inbreeding depression in outcrossing self-incompatible species. Here, we address these questions experimentally by comparing selfed and outcrossed progeny of purple loosestrife (Lythrum salicaria) over four growing seasons, including three under field conditions in a freshwater marsh in southern Ontario, Canada, a region where L. salicaria is highly invasive. The tristylous mating system of L. salicaria involves disassortative mating among floral morphs enforced by trimorphic incompatibility. However, owing to partial incompatibility, self-fertilized seed can be obtained by manual self-pollination thus facilitating comparisons of selfed and outcrossed progeny. We compared progeny with and without intraspecific competition from selfed or outcrossed neighbours and examined the influence of breeding treatment and competition on fitness correlates by measuring a range of life-history traits including: proportion of seeds germinating, days to germination, survival, proportion of plants flowering, time to flowering, vegetative mass, and inflorescence number and mass. We analysed data for each trait using functions from time series estimates of growth and two multiplicative estimates of fitness. We detected varying intensities of inbreeding depression for several traits in three of the four years of the experiment, including inflorescence mass and reproductive output. Cumulative inbreeding depression over four years averaged δ = 0.48 and 0.68, depending on the method used to estimate multiplicative fitness. The competition treatments did not significantly affect plant performance and the magnitude of inbreeding depression. Given the primarily outcrossing mating system of L. salicaria populations, the detection of inbreeding depression for several key life-history traits was as predicted by theory. Our results suggests that biparental inbreeding and low selfing in colonizing populations may have significant effects on demographic parameters such as population growth.
July 2024
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82 Reads
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1 Citation
South African Journal of Botany
Plants with specialised pollination systems may be susceptible to reduced fertility if they are incapable of autonomous self-pollination and are visited infrequently by pollinators capable of promoting effective cross-pollination. Here, we investigate this question by examining the reproductive ecology of the Cape endemic Cyanella alba subsp. flavescens (Tecophilaeaceae), which has mirror-image flowers (enantiostyly) and dimor-phic anthers (heteranthery). These traits are usually associated with buzz pollination mediated by bees that extract pollen from the poricidal anthers of flowers through vibration. We quantified insect visitation to flowers in three populations over two years in the vicinity of the Biedouw Valley, Western Cape, South Africa to determine whether plants were visited by buzz-pollinating bees. We also recorded visits by pollinators to other co-flowering species at each site and constructed a network on insect visitation. We conducted controlled hand pollinations and bagging experiments to determine whether plants were self-compatible and capable of autonomous self-pollination, and compared natural levels of fruit and seed set with those obtained from hand cross-pollination to evaluate evidence for pollen limitation of seed fertility. Despite 74 h of field observations, only two actively buzz-pollinating bees were recorded visiting flowers, although they were observed visiting other species in the community. The most frequent visitors to C. alba were opportunistic pollen-consuming beetles although we obtained no direct evidence that they were effective in promoting cross-pollination. Plants in each population exhibited chronic pollen limitation of seed set. Controlled polli-nations demonstrated that plants were moderately self-sterile and incapable of autonomous self-pollination. Although fruit set was high following self-pollination, few seeds were evident within developing fruit. Observations of pollen-tube growth following controlled hand self-and cross-pollination revealed abundant pollen tubes at the base of styles in both treatments. Thus, self-sterility in C. alba probably results from late-acting ovarian self-incompatibility, and possibly also the abortion of developing seed due to inbreeding depression. We discuss the possible causes of scarce buzz pollination in C. alba and consider its ecological and evolutionary consequences.
June 2024
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5 Reads
Molecular Ecology
June 2024
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50 Reads
Many animals and plants show left-right (LR) asymmetry. In some animal systems, handedness has a simple genetic basis, which has allowed identifying how handedness is determined at the molecular level, even if its functional relevance often remains unclear. Mirror-image flowers represent an example of LR asymmetry of clear functional significance, with the reciprocal placement of male and female organs in left- versus right-handed flowers promoting cross-pollination. Here, we use the South African geophyte Cyanella alba to study how handedness of its mirror-image flowers is determined and elaborated during development. Inflorescences of C. alba produce flowers with a largely consistent handedness. However, we find that this handedness has no simple genetic basis, and individual plants can switch their predominant handedness between years. Rather, it is the direction of the phyllotactic spiral that determines floral handedness. Cellular analysis combined with biophysical modelling demonstrates that style deflection is driven by increased cell expansion in the adaxial carpel facing the next oldest flower compared to the other adaxial carpel. The more expanding carpel shows transcriptional signatures of increased auxin signaling compared to the less expanding one, and auxin application to the latter can reverse the orientation of style deflection. We propose that a recently described inherent LR auxin asymmetry in the initiating organs of spiral phyllotaxis determines handedness in C. alba, representing a conserved non-genetic mechanism for creating a stable floral polymorphism. This mechanism links chirality across different levels of plant development and exploits a developmental constraint in a core patterning process to produce morphological variation of ecological relevance.
May 2024
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233 Reads
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3 Citations
Journal of Systematics and Evolution
The adaptive significance of phenotypic differences between females and males can provide insights into sex-specific selection and the evolution of sexual dimorphism. Dioecious plants commonly exhibit sexual dimorphism in height, although its ecological and evolutionary significance have rarely been examined experimentally. Here, we investigate the functional consequences of the temporal reversal of height dimorphism for pollen and seed dispersal in dioecious Rumex hastatulus Baldw., a species in which males are taller than females at flowering and the reverse pattern occurs at fruiting. Populations of this colonizing weed are wind-pollinated and seeds are wind-dispersed. In a glasshouse experiment we manipulated the height of pollen donors and using sex-specific genetic markers compared the paternal success of males of contrasting height and investigated whether seed families showed evidence of sexual dimorphism in early life-history traits. In a second glasshouse experiment using fruiting plants we also examined how female height influenced the distance that seeds were dispersed. We found that taller males had significantly higher siring success than males of equivalent height to flowering females. Similarly, taller females dispersed fruit to greater distances than shorter females. Female seeds were significantly heavier than male seeds and germinated more rapidly, although early seedling growth was greater in males. Our study suggests that the striking sex reversal of height in R. hastatulus likely functions to optimize the contrasting reproductive functions of the sexes by promoting increased pollen and seed dispersal distances. Improved dispersal quality could limit inbreeding and reduce local mate and resource competition within populations.
April 2024
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13 Reads
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4 Citations
Evolutionary Journal of the Linnean Society
Morphological asymmetries in plants and animals raise intriguing questions concerning their function and how they have evolved. One of the most conspicuous asymmetries in plants involve mirror-image flowers (enantiostyly) in which styles are deflected to either the left- or right-sides (L, or R, respectively) of the flower. Species with this floral polymorphism often possess two types of stamens (heteranthery); centrally located feeding anthers and a pollinating anther orientated in the opposite direction to the style (reciprocal enantiostyly). However, some species lack heteranthery and sex-organ reciprocity can be partial or absent (non-reciprocal enantiostyly). Many enanatiostylous species have nectarless flowers and are ‘buzz-pollinated’ by pollen-collecting bees. In contrast to other stylar polymorphisms such as heterostyly, enantiostyly exists as either monomorphic or dimorphic conditions; with L and R flowers on the same plant in the former, and in the latter genetically determined floral morphs with either L or R flowers. Enantiostyly has been reliably reported from 11 angiosperm families, but in only two is their convincing evidence that dimorphic enantiostyly occurs. Various hypotheses concerning developmental or selective constraints attempt to explain the rarity of this genetic polymorphism. Experimental studies on the function of enantiostyly indicate that the reciprocity of stigmas and pollinating anthers promotes pollinator-mediated cross-pollination and limits geitonogamous selfing. Insufficient or inferior pollinator service can result in the evolutionary breakdown of enantiostyly, including reduced stigma-anther separation, increased selfing and dissolution of heteranthery. In this article we review recent advances and knowledge gaps in understanding of these curious asymmetries and discuss why they have received less attention than heterostyly.
Citations (66)
... However, floral polymorphisms in which there are correlated suites of traits that function during the pollination process can also be viewed as pollination syndromes. Mirror-image (enantiostylous) flowers, for example, have evolved independently in at least 11 largely animal-pollinated angiosperm families and are characterised by styles that are deflected to the right-and left-side of flowers (Ornduff and Dulberger, 1978;Barrett et al., 2000;Barrett and Fairnie, 2024). This stylar polymorphism is commonly associated with heteranthery and nectarless flowers primarily visited by pollen-collecting bees (e.g. ...
- Citing Article
April 2024
Evolutionary Journal of the Linnean Society
... Many empirical studies report discontinuous patterns of sequence divergence in X-Y or Z-W homologous genes that are assigned to evolutionary strata in accordance with theories predicting stepwise recombination reduction [11]. Evolutionary strata have been convincingly associated with fusions between established sex chromosomes and autosomes (neo-sex chromosomes) [16][17][18]; however, there is only very little direct evidence of inversions associated with evolutionary strata [11], for example in humans [19] and sticklebacks [20]. Assessing the role of inversions for sex chromosome evolution remains a challenging endeavour, not only due to the need for a haplotype-resolved assembly but also because sex chromosomes can degenerate to an extent that makes the detection of inversions impossible. ...
Reference:
Dynamic evolution of a sex-linked region
- Citing Article
April 2024
Molecular Biology and Evolution
... Accordingly, reproductive systems are expected to play a key role in both species diversification and extinction (Cutter, 2019). Flowering plants provide outstanding opportunities to investigate the genetic and evolutionary consequences of variation in reproductive systems (Arunkumar et al., 2015;Zhang et al., 2022;Zeng et al., 2024). Numerous angiosperm lineages include many purely sexual species with contrasting mating systems, but also others that reproduce through both seed and clonal propagation, and some that rely largely on various mechanisms of asexual reproduction (Fryxell, 1957;Klimes et al., 1997;Silvertown, 2008;Vallejo-Marín et al., 2010;Barrett, 2015). ...
- Citing Article
- Full-text available
January 2024
... Several new journal developments were discussed in my 2023 'Year in Review' [6] and I summarize below progress on each of them. Our online seminar and Q&A channel in ecology and evolution (https://cassyni.com/series/NTMZiEYLfDVdh-vAz38B4aW) ...
Reference:
Proceedings B 2024: the year in review
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- Full-text available
January 2024
... Together, these results provide little evidence that degenerative processes, associated with cessation of recombination, have occurred in the Amborella SDR. This region is younger than that of Rumex (5-10 Ma 43 ) and Silene (10 Ma 44 ), which both show signatures of degeneration 38,45 . However, in Spinacia oleracea, a younger SDR (2-3 Ma) does show signs of degeneration 46,47 . ...
- Citing Preprint
- File available
December 2023
... Convergence of the system goes beyond morphology, seemingly occurring at the biochemical, transcriptional, and genomic levels (Henning et al., 2020;Potente et al., 2022). The most strongly supported example of convergence beyond morphology is the genetic basis of distyly, which cumulative research suggests is always a hemizygous supergene, present only in the S-morph's genome (Cocker et al., 2018;Shore et al., 2019;Gutiérrez-Valencia et al., 2022;Fawcett et al., 2023;Yang et al., 2023;Zhao et al., 2023). In Turnera (Passifloraceae), this supergene is composed of three S-genes, BAHD, SPH1, and YUC6, making it one of the simplest known S-loci (Shore et al., 2019). ...
- Citing Article
- Publisher preview available
September 2023
... In insect-pollinated P. alpina, pollen dispersal distances were greater from flowers on taller floral stalks. Although a positive correlation between stalk height and pollen dispersal distance is to be expected and has been found, in wind-pollinated species (Okubo and Levin 1989;Tonnabel et al. 2019;Zeng et al. 2023; but see Nakahara et al. 2018;Aljiboury and Friedman 2022), it has, to our knowledge, not been reported for species relying on animals as their pollen dispersal vector. Flowers presented on taller stalks likely attract more pollinators, and their pollen may be dispersed further. ...
- Citing Article
- Full-text available
May 2024
Journal of Systematics and Evolution
... In particular, this phenomenon is one of the reasons crucial to the success of invasive species. It has been shown that crossing adventitious plant species with representatives of the local flora (or different adventitious species with each other) can lead to the emergence of aggressive hybrid forms that exhibit heterosis and are better adapted to environmental conditions (Musiał et al., 2020;Irimia et al., 2021;Mounger et al., 2021;Gao et al., 2022;Uemura et al., 2022;Ruhsam et al., 2023). ...
- Citing Article
- Full-text available
May 2023
... Such selection may generate syndromes of floral traits that are characteristically associated with different pollen vectors and, for animal-pollinated species, mechanisms for exploiting different body parts of pollinators for pollen transfer [20,35]. Even floral 'selfing syndromes' [36] that enable plants to reproduce in the absence of pollinators may be shaped by the local availability of pollen vectors [37]. Floral 'pollination syndromes' are particularly clear examples of trait-environment correlation and testify to the importance of the pollination niche dimension for the evolution of floral traits and to the general importance of ecological speciation driven by pollinators [32]. ...
- Citing Article
- Full-text available
January 2023
Proceedings of the National Academy of Sciences
... Along the way, we demonstrate the value of our approach (Ramanauskas and Igić, 2021), whose application can rapidly establish the genetic basis of SI across angiosperms, whether or not species employ RSI. Finally, we consider the implications of these findings in the context of recent work on the genetics of heteromorphic SI (Huu et al., 2020;Matzke et al., 2021;Zhao et al., 2022b), which jointly supports dozens of independent cases of the re-evolution of heteromorphic SI across eudicots. ...
- Citing Article
- Full-text available
November 2022