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Selected species of Exochaenium investigated in this study illustrating variation in flower morphology. (A) Exochaenium grande with large inclined distylous flowers. (B, C) Exochaenium teucszii with erect flowers and long, narrow corolla tubes associated with hawkmoth pollination. (D) Infundibuliform corolla tube of distylous E. exiguum. (E) Yellow, erect flower of homostylous E. clavatum. (F, G) Tiny, erect flowers of homostylous E. baumianum. Scale bars ¼ 1 cm.
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Backgrounds and AimsThe spatial separation of stigmas and anthers (herkogamy) in flowering plants functions to reduce self-pollination and avoid interference between pollen dispersal and receipt. Little is known about the evolutionary relationships among the three main forms of herkogamy - approach, reverse and reciprocal herkogamy (distyly) - or a...
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Context 1
... species of Exochaenium exhibit considerable floral diversity ( Fig. 1), including variation in the length and form of the corolla tube (infundibuliform or cylindrical), corolla colour (white or bright yellow to salmon) and flower presentation (inclined/pendulous or erect). This diversity provides an oppor- tunity to assess to what extent variation in floral traits may be associated with evolutionary ...
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Pollen viability and stigma receptivity are prerequisite for successful pollination and fruit and/or seed set in flowering plants. The present paper deals with dependence of tree canopy height on pollen viability and stigma receptivity of Shorea robusta in a cultivated mature Dipterocarp forest. Pollen and stigma samples were collected from differe...
Citations
... Evidence supporting higher selfing in homostylous than distylous plants has been reported both intra-and inter-specifically (Mora-Carrera et al., 2021;Schoen et al., 1997;Zhao et al., 2023;Zhong et al., 2019). Additionally, independent shifts from distyly to homostyly have been documented both within and between species (Costa et al., 2019;de Vos et al., 2014;Kissling & Barrett, 2013;Ruiz-Martín et al., 2018;Zhou et al., 2012). ...
Distyly, a floral dimorphism that promotes outcrossing, is controlled by a hemizygous genomic region known as the S ‐locus. Disruptions of genes within the S ‐locus are responsible for the loss of distyly and the emergence of homostyly, a floral monomorphism that favors selfing. Using whole‐genome resequencing data of distylous and homostylous individuals from populations of Primula vulgaris and leveraging high‐quality reference genomes of Primula we tested, for the first time, predictions about the evolutionary consequences of transitions to selfing on S ‐genes. Our results reveal a previously undetected structural rearrangement in CYPᵀ associated with the shift to homostyly and confirm previously reported, homostyle‐specific, loss‐of‐function mutations in the exons of the S ‐gene CYPᵀ . We also discovered that the promoter and intronic regions of CYPᵀ in distylous and homostylous individuals are conserved, suggesting that down‐regulation of CYPᵀ via mutations in its promoter and intronic regions is not a cause of the shift to homostyly. Furthermore, we found that hemizygosity is associated with reduced genetic diversity in S ‐genes compared with their paralogs outside the S ‐locus. Additionally, the shift to homostyly lowers genetic diversity in both the S ‐genes and their paralogs, as expected in primarily selfing plants. Finally, we tested, for the first time, long‐standing theoretical models of changes in S ‐locus genotypes during early stages of the transition to homostyly, supporting the assumption that two copies of the S ‐locus might reduce homostyle fitness.
... the african genus Exochaenium grisebach (1845: 55; gentianaceae; see Kissling 2012 for a detailed taxonomic history) currently includes 23 taxa (Kissling 2015). Exochaenium species are only found in sub-Saharan africa (Kissling et al. 2009) and most of them are distylous (Kissling & Barrett 2013 and references therein). among them, Exochaenium grande (Meyer 1837(Meyer : 183) grisebach (1845 is not only the type species of the genus, but also the species with the widest distribution. ...
Based on morphological and ecological considerations, Belmontia natalensis (syn. Exochaenium grande var. homostylum) is reinstated as Exochaenium natalense (gentianaceae). It only occurs in a section of the coastal region of the Eastern Cape (Pondoland) and southern KwaZulu-Natal provinces, South africa. Exochaenium natalense differs from E. grande, the only other South african Exochaenium taxon, by having smaller flowers (corolla diameter < 2 cm vs > 3 cm) with a different colour (white vs cream-salmon or yellow). Because the type material of E. natalense consists of two sheets, a lectotype is designated.
... A study of the variation and evolution of heterogametes in Exochaenium has led to the conclusion that interactive dioecy originated from an ancestor with stigma-probing dioecy. The results of this study also support Lloyd and Webb's model (Kissling and Barrett 2013). However, to date, no model has been able to explain perfectly how heterostyly evolves in plants. ...
Main conclusion
This paper reviews the progress of research on the morphology, physiology and molecular biology of distyly in plants. It will help to elucidate the mysteries of distyly in plants.
Abstract
Distyly is a unique representative type of heterostyly in plants, primarily characterized by the presence of long style and short style within the flowers of the same species. This interesting trait has always fascinated researchers. With the rapid development of molecular biology, the molecular mechanism for the production of dimorphic styles in plants is also gaining ground. Researchers have been studying plant dimorphic styles from various perspectives. The researchers are gradually unravelling the mechanisms by which plants produce distyly traits. This paper reviews advances in the study of plant dimorphic style characteristics, mainly in terms of the morphology, physiology and molecular biology of plants with dimorphic styles. The aim is to provide a theoretical basis for the study of the mechanism of distyly formation in plants.
... Evidence supporting higher selfing in homostylous than distylous plants has been reported in diverse taxa (Belaoussoff & Shore, 1995;Schoenet al. , 1997;Mora-Carrera et al. , 2021). Independent shifts from distyly to homostyly have been documented both within and among species (Zhou et al. , 2012;Kissling & Barrett, 2013;de Vos et al. , 2014;Ruiz-Martín et al. , 2018;Costa et al. , 2019). ...
Distyly, a floral dimorphism that promotes outcrossing, is controlled by a hemizygous genomic region known as the S-locus. Disruptions of genes within the S-locus are responsible for the loss of distyly and the emergence of homostyly, a floral monomorphism that favors selfing. Using whole genome resequencing data of distylous and homostylous individuals from populations of Primula vulgaris and leveraging high-quality reference genomes of Primula we tested, for the first time, predictions about the evolutionary consequences of transitions to selfing on S-locus genes. Our results confirm the presence of previously reported homostyle-specific, loss-of-function mutations in the exons of the S-locus gene CYPᵀ , while also revealing a previously undetected structural rearrangement in CYPᵀ associated with the shift to homostyly. Additionally, we discovered that the promoter region of CYPᵀ in distylous and homostylous individuals is identical, suggesting that down-regulation of CYPᵀ via mutations in its promoter region is not a cause of shift to homostyly. Furthermore, we found that hemizygosity leads to reduced genetic diversity and less efficient purifying selection in S-locus genes compared to genes outside the S-locus, and that the shift to homostyly further lowers genetic diversity, as expected for mating-system shifts. Finally, we tested, for the first time, long-standing theoretical models of changes in S-locus genotypes during early stages of the transition to homostyly, supporting the assumption that two (diploid) copies of the S-locus might reduce homostyle viability.
... genetic variation in the expression of floral morphology associated with distyly could be an important source of standing variation to permit rapid and flexible breeding system responses to a changeable pollination environment Kissling and Barrett 2013;Brys and Jacquemyn 2015;Jiang et al. 2017;Simón-Porcar 2018). Differences in distyly expression between populations might be driven by spatial variation in pol-lination efficiency or the presence of other plant species that might compete for shared pollinators (Kálmán et al. 2007;Keller et al. 2012;Kissling and Barrett 2013). ...
... genetic variation in the expression of floral morphology associated with distyly could be an important source of standing variation to permit rapid and flexible breeding system responses to a changeable pollination environment Kissling and Barrett 2013;Brys and Jacquemyn 2015;Jiang et al. 2017;Simón-Porcar 2018). Differences in distyly expression between populations might be driven by spatial variation in pol-lination efficiency or the presence of other plant species that might compete for shared pollinators (Kálmán et al. 2007;Keller et al. 2012;Kissling and Barrett 2013). For example, finetuning of reciprocal pistil-stamen length differences might contribute to avoidance of interspecific hybridization, as observed in a morphological survey of three Primula species (Primulaceae; Keller et al. 2014). ...
... Homostyly enables reproductive assurance through autonomous self-pollination, as demonstrated in Primula (Carlson et al., 2008;de Vos et al., 2012;Yuan et al., 2017), and increases selfing rates (Husband & Barrett, 1993;Schoen et al., 1997;Zhong et al., 2019). Repeated shifts from heterostyly to homostyly have been reported both between (Costa, Torices, & Barrett, 2019;Kissling & Barrett, 2013;Kohn et al., 1996;Ruiz-Martín et al., 2018;de Vos, Hughes, et al., 2014) and within species (Ness et al., 2010;Shao et al., 2019;Zhou et al., 2017). However, none of these studies identified the molecular basis of such transitions, probably because the necessary genomic resources have only recently become available. ...
The repeated transition from outcrossing to selfing is a key topic in evolutionary biology. However, the molecular basis of such shifts has been rarely examined due to lack of knowledge of the genes controlling these transitions. A classic example of mating system transition is the repeated shift from heterostyly to homostyly. Occurring in 28 angiosperm families, heterostyly is characterized by the reciprocal position of male and female sexual organs in two (or three) distinct, usually self‐incompatible floral morphs. Conversely, homostyly is characterized by a single, self‐compatible floral morph with reduced separation of male and female organs, facilitating selfing. Here, we investigate the origins of homostyly in Primula vulgaris and its microevolutionary consequences by integrating surveys of the frequency of homostyles in natural populations, DNA sequence analyses of the gene controlling the position of female sexual organs (CYPᵀ), and microsatellite genotyping of both progeny arrays and natural populations characterized by varying frequencies of homostyles. As expected, we found that homostyles displace short‐styled individuals, but long‐style morphs are maintained at low frequencies within populations. We also demonstrated that homostyles repeatedly evolved from short‐styled individuals in association with different types of loss‐of‐function mutations in CYPᵀ. Additionally, homostyly triggers a shift to selfing, promoting increased inbreeding within and genetic differentiation among populations. Our results elucidate the causes and consequences of repeated transitions to homostyly within species, and the putative mechanisms precluding its fixation in P. vulgaris. This study represents a benchmark for future analyses of losses of heterostyly in other angiosperms.
... The latter, by shifts to new plant-pollinator interactions or to wind pollination (Culley et al. 2002;Friedman and Barrett 2009;Lord 2015). Wind pollination is favoured on islands when there are, (i) few animal pollinators (Anderson et al. 2001;Schueller 2004;Eckert et al. 2006;Kissling and Barrett 2013), or (ii) stronger wind currents (Carta et al. 2009), or when, (iii) wind is more effective than animals (Carlquist 1974;Rech et al. 2016). ...
Background and Aims: The factors that facilitate successful colonization of islands should be especially evident where the establishment filter is strongest. Colonizers of small, remote oceanic islands should be initially rare, extremely mate-limited, and often without pollinators. Hence, plant communities on such islands should reflect an establishment history in which young "naturalized" species are most likely to display self-compatibility and autonomous selfing, whereas "indigenous" species may exhibit more diverse reproductive strategies. To test this prediction, we characterized breeding systems of 28 species on Pohnpei, in the Federated States of Micronesia, a group of remote Pacific islands that are considered a global biodiversity hotspot. Methods: Three families with both naturalized and indigenous species were selected-Fabaceae, Malvaceae, and Melastomataceae. Measurements included field observations of dichogamy/herkogamy and floral attraction traits, pollen:ovule (P:O) ratios, and experimental hand-pollinations for self-compatibility and pollen limitation. Phylogenetic generalized least squares analyses tested for trait correlations between naturalized and indigenous species. Key Results: Flowers of all 28 species were bisexual, and pollinator attraction features were common. P:O ratios ranged from 9 to 557 (median = 87), and all 11 hand-pollinated species were self-compatible. All species had > 5 ovules and < 3,500 pollen grains per flower. Indigenous species did not differ significantly from naturalized species for any trait. Conclusion: There is a dearth of data from remote islands bearing on the question of establishment history. In this study, we inferred all species to have some degree of autogamy and indigenous species were no more likely than naturalized species to display outcrossing mechanisms. On Pohnpei, high ovule numbers, and the inaccessibility of wind pollination and obligate outcrossing strategies, reflect the importance of retaining reproductive assurance mechanisms in the face of pollinator uncertainty.
... Homostyly enables reproductive assurance through autonomous self-pollination, as demonstrated in Primula (Carlson, Gisler, & Kelso, 2008;de Vos, Keller, Isham, Kelso, & Conti, 2012;Yuan et al., 2017), and increases selfing rates (Husband & Barrett, 1993;Schoen, Johnston, L'Heureux, & Marsolais, 1997;Zhong et al., 2019). Repeated shifts from heterostyly to homostyly have been reported both between (de Vos, Hughes, Schneeweiss, Moore, Kissling & Barrett, 2013;Kohn, Graham, Morton, Doyle, & Barrett, 1996;Ruiz-Martin et al., 2018) and within species (Ness et al., 2010;Shao et al., 2019;Zhou et al., 2017). However, none of these studies identified the molecular basis of such transitions, likely because the necessary genomic resources have only recently become available. ...
The repeated transition from outcrossing to selfing is a key topic in evolutionary biology. However, the molecular basis of such shifts has been rarely examined due to lack of knowledge of the genes controlling these transitions. A classic example of mating system transition is the repeated shift from heterostyly to homostyly. Occurring in 28 angiosperm families, heterostyly is characterized by the reciprocal position of male and female sexual organs in two (or three) distinct, usually self-incompatible floral morphs. Conversely, homostyly is characterized by a single, self-compatible floral morph with reduced separation of male and female organs, facilitating selfing. Here, we investigate the origins of homostyly in Primula vulgaris and its microevolutionary consequences by integrating surveys of the frequency of homostyles in natural populations, DNA sequence analyses of the gene controlling the position of female sexual organs ( CYPᵀ ), and microsatellite genotyping of both progeny arrays and natural populations characterized by varying frequencies of homostyles. As expected, we found that homostyles displace short-styled individuals, but long-style morphs are maintained at low frequencies within populations. We also demonstrated that homostyles repeatedly evolved from short-styled individuals in association with different types of loss-of-function mutations in CYPᵀ . Additionally, homostyly triggers a shift to selfing, promoting increased inbreeding within and genetic differentiation among populations. Our results elucidate the causes and consequences of repeated transitions to homostyly within species, enabling a likely explanation for the fact that homostyly has not become fixed in P. vulgaris . This study represents a benchmark for future analyses of losses of heterostyly.
... The phenotypic origins of homostyly have been investigated at the inter-and intraspecific levels. Phylogenetic analyses inferred convergent shifts to homostyly in ancestrally heterostylous lineages of Primulaceae (de Vos, Hughes, Schneeweiss, Moore, Mast et al., 2006;Zhong et al., 2019), Pontederiaceae (Kohn, Graham, Morton, Doyle, & Barrett, 1996), Rubiaceae (Ferrero, Rojas, Vale, & Navarro, 2012), Gentianaceae (Kissling & Barrett, 2013), and Plumbaginaceae (Costa, Torices, & Barrett, 2019). At the intraspecific level, population genetic analyses suggested independent origins of homostyly within the heterostylousEichhornia paniculata (Husband & Barrett, 1993;Ness, Wright, & Barrett, 2010),Primula chungensis (Zhou et al., 2017), P. oreodoxa (Yuan et al., 2017) and P. merrilliana (Shao et al., 2019). ...
The molecular basis of phenotypic convergence, a key topic in evolutionary biology and ecology, has been investigated especially between species. However, it remains unclear whether mutations in the same or different positions of the same gene, or in different genes underlie phenotypic convergence within species. A classic example of convergence is the transition from outcrossing to selfing in plants, illustrated by the repeated shift from heterostyly to homostyly. Heterostyly is characterized by the reciprocal position of male and female sexual organs in two (or three) distinct, incompatible floral morphs, while homostyly is characterized by a single, self-compatible floral morph. Primula has long served as the prime model for studies of heterostyly and homostyly. Here, we elucidate the phenotypic and molecular origins of homostyly in P. vulgaris and its microevolutionary consequences by integrating microsatellite analyses of both progeny arrays and natural populations characterized by varying frequencies of homostyles with DNA sequence analyses of the gene controlling the position of female sexual organs ( CYPᵀ ). We found that: homostyles evolved repeatedly from short-styled individuals in association with different types of loss-of-function mutations in CYPᵀ and, consequently, short-styled individuals occur at lower frequencies than long-styled individuals across populations with all three morphs; the shift to homostyly promotes a shift to selfing; and intra-population frequency of homostyles is positively correlated with selfing rate and inbreeding level, increasing genetic differentiation among populations. These results elucidate the connections between the genotypic and phenotypic levels of convergence and the effects of contrasting floral morphologies on reproductive strategies.
... Gentianaceae is a cosmopolitan family, with many species typical of high-altitude environments (Albert and Struwe 2002). Species from this family possess a wide diversity of reproductive strategies, like herkogamy (Brys et al. 2013;Wang et al. 2017), heterostyly (Crespo and Ferreira 2006;Kissling and Barrett 2013), protandry (Webb and Pearson 1993;Wang et al. 2017), and protogyny (Freitas and Sazima 2009). As most Gentianaceae species are self-compatible, promotion of outcross mating and/or reduction in sexual interference between male and female floral functions were probably the selective pressures involved in the appearance of many of these reproductive mechanisms Webb and Lloyd 1986;Barrett 2002). ...
... Examples include the singular case of diplostigmaty, observed in Sebaea Sol. ex R. Br. (Gentianaceae), where the presence of spatially and temporally distinct stigmas enables delayed autonomous selfpollination, without limiting opportunities for outcrossing (Kissling and Barrett 2013). ...
... The absence of pollen limitation is related to the high reproductive success of the pollination due to visits and to the mechanisms (movement herkogamy and extended anthesis) that increase the chances of crossing. However, we share with other investigators the idea that the ability of autonomous selfing (Goodwillie and Weber 2018), which is widespread among species of Gentianaceae (Webb and Pearson 1993;Brys and Jacquemyns 2011;Kissling and Barrett 2013;Goodwillie and Weber 2018), can provide a backup to compensate for occasional pollination failures. ...
The genus Prepusa Martius is endemic to montane regions of Brazil and comprises only six species, most of them endangered. Although studies on reproductive biology are necessary to increase knowledge of this genus and to implement conservation plans, to date, no such studies have been conducted. This study assessed the floral biology, breeding system, and pollinators of Prepusa hookeriana, an endangered species of high-altitude grasslands. We perform field observations and manual pollination experiments. Certain floral traits of this species appear to be associated with hummingbird pollination, although ornithophily is unusual in Gentianaceae. Even though cross-pollination is favoured by the presence of movement herkogamy and protandry, both prior and delayed autonomous self-pollination were observed. The only pollinator observed was the hummingbird Amazilia versicolor. Prepusa hookeriana did not show pollen limitation in the year of study. The absence of pollen limitation is related to the high reproductive success of pollination due to visits, not to autonomous self-pollination. However, we share the idea that the ability of autonomous selfing can provide a backup to cope with occasional pollination failures.
