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Mean relative percentage (±SEM) of floral scent compounds of three Achimenes species collected at La Tzararacua site and grown in a greenhouse.
Source publication
Premise:
Closely related species occurring in sympatry may experience the negative consequences of interspecific pollen transfer if reproductive isolation (RI) barriers are not in place. We evaluated the importance of pre- and post-pollination RI barriers in three sympatric species of Achimenes (Gesneriaceae), including ecogeographic, phenological...
Contexts in source publication
Context 1
... scents-Organic volatiles in flowers included the terpenoids pinene, limonene, cineole, the benzenoid naphthalene, and the fatty-acid derived alkene tetradecane, but the presence and concentration of these compounds varied among species (Table 4). The floral scent profile of A. antirrhina showed two of the five volatiles, while the profile of A. flava and A. patens showed four of the five volatile compounds. ...Context 2
... floral scent profile of A. antirrhina showed two of the five volatiles, while the profile of A. flava and A. patens showed four of the five volatile compounds. The last two species differed in one volatile compound; limonene was exclusive to A. patens, and cineole was exclusive to A. flava (Table 4). ...Similar publications
Forest fragmentation may affect mating and pollen dispersal patterns through conversion of continuous forests into small, spatially isolated remnant patches and individual trees in an anthropogenic landscape. We investigated reproductive investment and success, pollen dispersal, mating system, and genetic diversity and spatial structure of Qualea g...
Pollen-flowers with heteromorphic stamens have been shown to promote an intrafloral division of labour as a solution to fitness costs arising from pollen consumption by bees, known as the pollen dilemma. Usually, the division is based on morphological differences in anther and pollen traits that correlate with stamen function: pollinating anthers a...
Citations
... for C. aconitifolius but positive for C. souzae (RI = 0.24), meaning that a greater proportion of heterospecific pollen reached the base of the styles of C. aconitifolius compared with conspecific pollen. This result (negative RI for pollen-pistil incompatibility) is not uncommon in the literature and is usually attributed to differences in style length or the degree of self-compatibility (e.g., Costa et al., 2007;Ramírez-Aguirre et al., 2019;Scopece et al., 2013). ...
Reproductive isolation is conferred by several barriers that occur at different stages of reproduction. Comprehensive reviews on the topic have identified that barriers occurring prior to zygote formation are often stronger than those that occur afterward. However, the overrepresentation of temperate perennial herbs in the current literature precludes any generalization of this pattern to plants that present other life forms and patterns of distribution. Here, we assessed reproductive isolation barriers and their absolute contribution to reproductive isolation and asymmetry in Cnidoscolus aconitifolius and C. souzae , two closely related tropical shrub species that co‐occur on the Yucatan peninsula. The reproductive barriers assessed were phenological mismatch, pollinator differentiation, pollen–pistil incompatibility (three pre‐zygotic barriers), fruit set failure, and seed unviability (post‐zygotic barriers). Reproductive isolation between the study species was found to be complete in the direction C. aconitifolius to C. souzae , but only partial in the opposite direction. One post‐zygotic barrier was the strongest example. Most barriers, particularly the pre‐zygotic examples, were asymmetrical and predicted the direction of heterospecific pollen flow and hybrid formation from C. souzae to C. aconitifolius . Both parental species, as well as the hybrids, were diploid and had a chromosome number 2n = 36. More studies with tropical woody perennials are required to fully determine whether this group of plants consistently shows stronger post‐zygotic barriers.
... Floral chemical compounds, and their particular patterns, have proven to be crucial in the attraction of specific pollinator guilds (e.g., Knudsen & Tollsten, 1993, 1995Dobson, 2006;Schäffler et al., 2015) and promote floral isolation among closely related species (e.g., species of the same genus; Schiestl & Schlüter, 2009). Although closely related species pollinated by the same pollinator guild would still have a speciesspecific pattern of chemical compounds (e.g., Stökl et al., 2005;van der Niet et al., 2010;Gong et al., 2015;Milet-Pinheiro et al., 2015), it is expected that these differences in chemical composition would be greater when they are pollinated by different pollinator guilds (e.g., Ramírez-Aguirre et al., 2019). Effectively, we show that all Neotinea species have a specific floral cuticular chemical composition, but the cuticular composition of the predominantly tachinid-pollinated N. ustulata is particularly distinct among all Neotinea species. ...
Among terrestrial orchids, and particularly among the subtribe Orchidinae, flies are underrepresented as pollinators. The European Neotinea ustulata, which developed specialized pollination by tachinid flies, is known to produce high relative concentrations of the floral cuticular alkenes (Z)-11-tricosene and (Z)-11-pentacosene (referred to as (Z)-11-C23/C25enes), which seem to be uncommon among orchid flowers. If the evolution of tachinid pollination is related to that of (Z)-11-C23/C25enes, we can expect that closely related species have a different floral chemical pattern and significantly small or no production of (Z)-11-C23/C25enes, independently of their pollinator guild identity (e.g., bees, flies, moths). We chemically compared the floral cuticular composition among Neotinea species, performed electrophysiological analyses, reconstructed the phylogenetic Orchidinae tree, and identified the evolutionary history of pollinator guild and (Z)-11-C23/C25enes production within the Orchidinae. Neotinea ustulata has evolved a markedly different floral cuticular composition compared to other Neotinea and produces both compounds ((Z)-11-C23/C25enes) in high relative quantities (i.e., above 8% in combination), which are detectable by tachinid antennae. Moreover, most Orchidinae taxa have minimal or no production of these alkenes, independently of the identity of their pollinator guild. Our ancestral reconstruction suggested that (Z)-11-C23/C25enes production was an evolutionary exaptation in Neotinea, whereas tachinid pollination was a unique evolutionary innovation for N. ustulata. Floral cuticular composition and, in particular, the combined production of (Z)-11-C23/C25enes at relatively high concentrations is intimately linked to the evolution of tachinid pollination within the Orchidinae.
... The high prevalence of hybridization in Henckelia is not surprising given the high frequency of this process in the family Gesneriaceae (Arisum, 1964;Morley, 1976;Smith et al., 1996;Puglisi et al., 2011;Qiu et al., 2011;Afkhami-Sarvestani et al., 2012;de Pillon et al., 2013;de Villiers et al., 2013;Smith et al., 2017;Roberts and Roalson, 2018;Kleinkopf et al., 2019;de Araujo et al., 2021). Extensive Downloaded from https://academic.oup.com/aob/article/131/6/953/7161305 by National Science & Technology Library user on 21 August 2023 hybridization in Henckelia can probably be explained by a lack of complete reproductive isolation in Gesneriaceae (Zhang et al., 2017;Ramírez-Aguirre et al., 2019;Feng et al., 2020b). Therefore, artificial hybrids can be easily produced using different parental species, even from different genera (Lü et al., 2017). ...
Background and Aims
Hybridization has long been recognized as an important process for plant evolution and is often accompanied by polyploidization, another prominent force in generating biodiversity. Despite its pivotal importance in evolution, the actual prevalence and distribution of hybridization across the tree of life remain unclear.
Methods
We used whole-genome shotgun (WGS) sequencing and cytological data to investigate the evolutionary history of Henckelia, a large genus in the family Gesneriaceae with a high frequency of suspected hybridization and polyploidization events. We generated WGS sequencing data at about 10× coverage for 26 Chinese Henckelia species plus one Sri Lanka species. To untangle the hybridization history, we separately extracted whole plastomes and thousands of single-copy nuclear genes from the sequencing data, and reconstructed phylogenies based on both nuclear and plastid data. We also explored sources of both genealogical and cytonuclear conflicts and identified signals of hybridization and introgression within our phylogenomic dataset using several statistical methods. Additionally, to test the polyploidization history, we evaluated chromosome counts for 45 populations of the studied 27 Henckelia species.
Key Results
We obtained well-supported phylogenetic relationships using both concatenation and coalescent-based methods. However, the nuclear phylogenies were highly inconsistent with the plastid phylogeny, and we observed intensive discordance among nuclear gene trees. Further analyses suggested that both incomplete lineage sorting (ILS) and gene flow contributed to the observed cytonuclear and genealogical discordance. Our analyses of introgression and phylogenetic networks revealed a complex history of hybridization within the genus Henckelia. In addition, based on chromosome counts for 27 Henckelia species, we found independent polyploidization events occurred within Henckelia after different hybridization events.
Conclusions
Our findings demonstrated that hybridization and polyploidization are common in Henckelia. Furthermore, our results revealed that H. oblongifolia is not a member of the redefined Henckelia and suggested several other taxonomic treatments in this genus.
... On the one hand, pre-zygotic barriers that limit interspecific gene flow between congeners could explain why multiple morphotypes can coexist. Such pre-zygotic barriers could include occurrence in specific habitats (Schnitzler et al., 2011;Anacker & Strauss, 2014;Mantel & Sweigart, 2019), divergent flowering phenology (Anderson, Alexandersson & Johnson, 2010;Newman, Anderson & Johnson, 2012;Matsumoto et al., 2019;Ramírez-Aguirre et al., 2019;Osborne et al., 2020), use of different pollinators or divergent use of the same pollinator (Peakall et al., 2010;Pedron et al., 2012;Ramírez-Aguirre et al., 2019) and divergence in mechanical features leading to character displacement (Queiroz et al., 2015;Zheng et al., 2017;Newman & Anderson, 2020). Studies of the reproductive biology of S. longicauda have shown that TELW, TFLP and TFLP are visited by nocturnal moths that differ in the length of their proboscis (Harder & Johnson, 2005;Jersáková & Johnson, 2007;Ellis & Johnson, 2010;Johnson et al., 2011Johnson et al., , 2019Duffy & Johnson, 2014). ...
... On the one hand, pre-zygotic barriers that limit interspecific gene flow between congeners could explain why multiple morphotypes can coexist. Such pre-zygotic barriers could include occurrence in specific habitats (Schnitzler et al., 2011;Anacker & Strauss, 2014;Mantel & Sweigart, 2019), divergent flowering phenology (Anderson, Alexandersson & Johnson, 2010;Newman, Anderson & Johnson, 2012;Matsumoto et al., 2019;Ramírez-Aguirre et al., 2019;Osborne et al., 2020), use of different pollinators or divergent use of the same pollinator (Peakall et al., 2010;Pedron et al., 2012;Ramírez-Aguirre et al., 2019) and divergence in mechanical features leading to character displacement (Queiroz et al., 2015;Zheng et al., 2017;Newman & Anderson, 2020). Studies of the reproductive biology of S. longicauda have shown that TELW, TFLP and TFLP are visited by nocturnal moths that differ in the length of their proboscis (Harder & Johnson, 2005;Jersáková & Johnson, 2007;Ellis & Johnson, 2010;Johnson et al., 2011Johnson et al., , 2019Duffy & Johnson, 2014). ...
Species-level taxonomy is traditionally based on herbarium collections that typically include few, or even single, representatives per site. This can lead to underestimation of diversity when there are sympatric populations of superficially similar plants belonging to different lineages. Satyrium longicauda (Orchidaceae) represents a taxonomic challenge for the delimitation of species boundaries due to the high degree of morphological variation detected within and among populations. Currently, just two varieties are accepted based mainly on length differences of the lateral sepal and nectar spur. However, there is extensive morphological variation within South African populations and evidence for several pollination ecotypes, indicating that this taxon represents an actively diverging species complex. Here, we evaluate intraspecific morphological variation through uni- and multivariate morphometrics and analyse internal transcribed spacer sequences for individuals sampled from 36 sites, including 14 sites where divergent morphotypes occur sympatrically. Morphometric analyses of 1802 individuals revealed the presence of eight morphotypes based on vegetative and floral characters. Up to six morphologically and genetically distinct morphotypes can coexist in sympatry. Morphological and genetic distances among populations were significantly correlated. Phylogenetic analyses of 120 accessions indicated that neither of the two varieties nor S. longicauda as a species is monophyletic, and provided evidence for the monophyly of some of the morphotypes including the newly described S. cernuiflorum. The presence of distinct morphological and genetic sympatric variants, which in several cases scale up to distinct evolutionary lineages, is consistent with the existence of different taxa according to morphological and biological species concepts. Our results therefore confirm that taxonomy based mainly on herbarium collections can grossly under-estimate actual diversity of disparate lineages, although further work is required to finalize taxonomic decisions. These findings have implications for efforts to estimate species diversity in groups that are in the process of diversifying and for conservation practice.
... It should be an ecologically important issue how these species have survived and preserved their populations in isolated habitats since the last glacial period, particularly when competitive species exist. Generally, spatial and temporal niche separation is effective for the coexistence of sympatricrelated species (Coyne and Orr 2004;Ramírez-Aguirre et al. 2019). Habitat use separation at the microscale and phenological isolation of resource use timing can mitigate exploitation competition for limited resources (Shigesada, Kawasaki, and Teramoto 1979;Snyder 2008) or pollinator acquisition (Waser 1978). ...
Reproductive interference between sympatric-related species often causes adverse impacts on rare species, which increases the risk of local extinction, particularly in small and isolated populations. To evaluate the congeneric interactions in alpine plants, we compared the ecological and genetic properties and assessed the reproductive interference between tetraploid Rhododendron diversipilosum (widespread species) and diploid Rhododendron subarcticum (rare species in alpine fellfields) in northern Japan. In alpine fellfields, R. diversipilosum is commonly distributed close to shrubby patches, whereas R. subarcticum tends to grow in more exposed places, although they are sometimes mixed. R. subarcticum initiated flowering one week earlier; however, the flowering periods overlapped between species, indicating incomplete phenological isolation. The pollination experiment showed that both species were self-incompatible. Furthermore, heterospecific pollination occurred only for R. subarcticum; however, hybrid seeds seldom germinated. These results indicate that reproductive interference is asymmetric between species, where only the rare R. subarcticum may suffer from heterospecific pollination. Genetic analysis showed that R. subarcticum populations had lower genetic diversity but higher divergence among populations than R. diversipilosum. Although spatiotemporal niche separations may mitigate reproductive interference, the risk of local extinction could be higher in R. subarcticum populations because of isolated distributions with low genetic diversity.
... Therefore, prezygotic reproductive isolation barriers may be favored, especially when species or lineages co-occur in parapatry or sympatry (Ramsey et al., 2003;Baack et al., 2015). As a consequence, temporal isolation through differences in phenology (Michalski and Durka, 2015), and/or pollinator isolation, i.e. distinct pollinator assemblages, may be favored (Okamoto et al., 2015;Ramıŕez-Aguirre et al., 2019). However, pollinator sharing might also represent an advantage through increasing pollinator services and facilitating pollen dispersal for both plant species or lineages (Ghazoul, 2006;Phillips et al., 2020), and through offering more resources to pollinators, also possibly over a longer period of time (Moeller, 2004). ...
... flower color and size, scent and nectar composition, resulting in different visiting pollinator assemblages and in pollinator isolation (e.g. Schemske and Bradshaw, 1999;Waelti et al., 2008;Ramıŕez-Aguirre et al., 2019). Divergence in floral traits between S. nutans ecotypes, such as flower color (white for calcicolous plants and greenish, yellowish to pink for silicicolous plants) and size of the petal scale (1.9 times longer for the calcicolous ecotype; De Bilde, 1973), indeed suggests possible pollinator isolation. ...
... Pollinator isolation can be expected between genetically distinct lineages due to mating costs associated with interlineage pollination events (pollen losses and investment in inviable hybrids), and the incompleteness of other prezygotic barriers (e.g., partial phenological isolation, and habitat isolation but no geographic isolation) (Baack et al., 2015;Moreira-Hernańdez and Muchhala, 2019;Ramıŕez-Aguirre et al., 2019). The two ecotypes of S. nutans might thus benefit from attracting different pollinator assemblages, but we found no pollinator isolation. ...
High reciprocal pollination specialization leading to pollinator isolation can prevent interspecific pollen transfer and competition for pollinators. Sharing pollinators may induce mating costs, but it may also increase pollination services and pollen dispersal and offer more resources to pollinators, which may be important in case of habitat fragmentation leading to pollination disruption. We estimated pollen dispersal and pollinator isolation or sharing between two reproductively isolated genetic lineages of Silene nutans (Caryophyllaceae), which are rare and occur in parapatry in southern Belgium, forming two edaphic ecotypes. As inter-ecotypic crosses may lead to pollen wastage and inviable progeny, pollinator isolation might have evolved between ecotypes. Silene nutans is mainly pollinated by nocturnal moths, including nursery pollinators, which pollinate and lay their eggs in flowers, and whose caterpillars feed on flowers and seeds. Pollinator assemblages of the two ecotypes are largely unknown and inter-ecotypic pollen flows have never been investigated. Fluorescent powdered dyes were used as pollen analogues to quantify intra- and inter-ecotypic pollen transfers and seeds were germinated to detect chlorotic seedlings resulting from inter-ecotypic pollination. Nocturnal pollinators were observed using infrared cameras on the field, and seed-eating caterpillars were collected and reared to identify nursery pollinator species. No pollinator isolation was found: we detected long-distance (up to 5 km) inter-ecotypic dye transfers and chlorotic seedlings, indicating inter-ecotypic fertilization events. The rare moth Hadena albimacula, a nursery pollinator specialized on S. nutans, was found on both ecotypes, as well as adults visiting flowers (cameras recordings) as seed-eating caterpillars. However, S. nutans populations harbor different abundance and diversity of seed predator communities, including other rare nursery pollinators, suggesting a need for distinct conservation strategies. Our findings demonstrate the efficiency of moths, especially of nursery pollinators, to disperse pollen over long distances in natural landscapes, so to ensure gene flow and population sustainability of the host plant. Seed-predator specificities between the two reproductively isolated genetic lineages of S. nutans, and pollinator sharing instead of pollinator isolation when plants occur in parapatry, suggest that conservation of the host plant is also essential for sustaining (rare) pollinator and seed predator communities.
... Both natural selection and neutral evolution lead to genetic differentiation between species (Abbott et al., 2013). Reproductive isolation occurs when genetic differentiation hinders fertilization and hybrid development (Ramírez Aguirre et al., 2019;Sobel et al., 2010). In general, as the genetic distance increases, the RI becomes more comprehensive and stronger. ...
Daylily (Hemerocallis) is a perennial with high ornamental value. It is difficult to obtain innovative daylily germplasm by conventional crossbreeding. To enrich the genetic variation of Hemerocallis, daylily was used as male parent to cross with lycoris (Lycoris). Artificial pollination and embryo rescue were performed to overcome reproductive isolation. Cross‐compatibility and pollen germination were analysed to investigate interfamily reproductive isolation. Leaf morphological analysis and inter‐simple sequence repeat (ISSR) were performed to identify the hybrid at seedling stage. Results showed that most pollen grains failed to adhere to stigmas, and pollen tubes germinated in a disordered direction. Ten days after pollination, 77.19% of ovaries aborted. Ovaries were harvested only in 10 hybridization combinations, the fruit setting rates were 7.69%–42.86%, and the ovule numbers were 0–6.0 per ovary. One embryo developed into plantlets eventually, whose parental combination was L. aurea × H. ‘My Complementary’. The hybrid was identified and exhibited both intermediate and novel characteristics of parents. This research is the first attempt to explore a protocol to obtain interfamily hybrid between daylily and lycoris.
... isolation values range from 1 (complete isolation) to -1 (complete disassortative mating). RI = 0 indicates random mating (Sobel & Chen, 2014;Ramírez-Aguirre et al., 2019). We considered for the analysis of reproductive isolation only plants greater than 400,000 cm 3 (41 large plants of a total of 48) because we observed that smaller plants have reduced fertility (mean of large plant fruits 5.1 ± 0.66 SE and small plants 2.9 ± 0.98 SE; Espinosa et al., 2019; see Supplementary Information Fig. S4). ...
Elevation gradients generate different environmental conditions. This environmental differentiation can influence morphological adaptation, habitat isolation, reproductive isolation, and pollinator limitation in plants. Habitat differentiation and isolation often act first on phenotypic traits and then on genotype variation, causing genetic divergences between populations. We evaluated the effect of elevation on morphological traits, reproductive isolation, and pollinator limitation in Croton aff. wagneri in dry shrublands of inter-Andean valleys in Ecuador. We measured morphological traits of Croton at three elevations and carried out experimental pollination crosses between and within each population at different elevations to assess the degree of reproductive isolation and pollinator limitation. Morphological traits such as leaf thickness, plant volume, inflorescence length and inflorescence number were dissimilar between plants in different elevations. There was evidence of incipient reproductive isolation between plants in populations at the highest and the lowest studied elevations. Pollination experiments within each elevation showed a limitation of pollinators in Croton in the highest elevation. Intrinsic barriers to pollen dispersal and ecological divergence can produce reproductive incompatibilities between individuals with different traits along the Croton elevation gradient.
... These new pollinators may be more efficient (Ashworth et al., 2015), or the only present, if e.g., the occurrence of pollinator shift is enforced by the loss of ancestral pollinators (Cox and Elmqvist, 2000). Indeed, significant changes in floral traits, such as corolla symmetry, petal colour, and type of reward, are generally associated with pollinator shifts, strongly supporting the idea that flower traits reflect new pollinators preferences (Bruneau, 1997;Ramírez-Aguirre et al., 2019;Barrionuevo et al., 2021). ...
Pollinators are often perceived as a primary selective agent influencing flower traits such as colour, size, and nectar properties. The genus Fritillaria L. (Liliaceae), comprising approximately 150 species, is described as generally insect pollinated. However, there are at least three exceptions: two hummingbird-pollinated North American species and one passerine-pollinated Asian species. Despite this variation in pollination, little is known about flower traits that may accompany this shift in fritillaries. In this study, we aimed to assess the attractiveness of the floral traits for (new) pollinators and track the evolution of flowers traits in the context of a shift in the principal pollinator. Therefore, we studied 14 flower traits related to the pollination in 60 Fritillaria species and traced the evolutionary trajectory of these traits. We used a phylogenetic tree of the genus, based on five DNA markers (matK, rpl16, and rbcL, 18S, and ITS) to reconstruct the ancestral state of studied flower traits. The results show that in bird-pollinated species several new traits evolved. For example, flower colouration, nectar sugar, and amino acid concentration and composition fulfil the criteria of ornithophilous flowers, although flower traits do not exclude insect pollinators in bird-pollinated fritillaries. Interestingly, we recorded potential reversals from bird to insect pollination. Our analysis, showing a broad study of flower traits among closely related species in the context of pollinator shift, serves as a starting point for future work exploring the genetic and physiological mechanisms controlling flower traits in the genus Fritillaria.
... Achimenes is a young lineage (c. 7-12 Mya; Roalson & Roberts, 2016) known for its floral diversity (Fig. 1), a feature thought to be associated with speciation (Ramírez Roa, 1987;Roalson, Skog & Zimmer, 2003). Four pollination syndromes are found in Achimenes, including melittophily (bees), psychophily (butterflies), euglossophily (female euglossine bees) and ornithophily (hummingbirds) (Fig. 2). ...
... Four pollination syndromes are found in Achimenes, including melittophily (bees), psychophily (butterflies), euglossophily (female euglossine bees) and ornithophily (hummingbirds) (Fig. 2). These syndromes have traditionally been defined on the basis of flower color and flower shape (Fig. 2;Ramírez Roa, 1987) and recently through pollinator observations (Martén-Rodríguez et al., 2015;Ramírez-Aguirre et al., 2019). ...
... Four pollination syndromes are found in Achimenes, including melittophily (bees), psychophily (butterflies), euglossophily (female euglossine bees) and ornithophily (hummingbirds) (Fig. 2). These syndromes have traditionally been defined on the basis of flower color and flower shape (Fig. 2;Ramírez Roa, 1987) and recently through pollinator observations (Martén-Rodríguez et al., 2015;Ramírez-Aguirre et al., 2019). ...
Background
Genetic pathways involved with flower color and shape are thought to play an important role in the development of flowers associated with different pollination syndromes, such as those associated with bee, butterfly, or hummingbird pollination. Because pollination syndromes are complex traits that are orchestrated by multiple genes and pathways, the gene regulatory networks have not been explored. Gene co-expression networks provide a systems level approach to identify important contributors to floral diversification.
Methods
RNA-sequencing was used to assay gene expression across two stages of flower development (an early bud and an intermediate stage) in 10 species of Achimenes (Gesneriaceae). Two stage-specific co-expression networks were created from 9,503 orthologs and analyzed to identify module hubs and the network periphery. Module association with bee, butterfly, and hummingbird pollination syndromes was tested using phylogenetic mixed models. The relationship between network connectivity and evolutionary rates ( dN / dS ) was tested using linear models.
Results
Networks contained 65 and 62 modules that were largely preserved between developmental stages and contained few stage-specific modules. Over a third of the modules in both networks were associated with flower color, shape, and pollination syndrome. Within these modules, several hub nodes were identified that related to the production of anthocyanin and carotenoid pigments and the development of flower shape. Evolutionary rates were decreased in highly connected genes and elevated in peripheral genes.
Discussion
This study aids in the understanding of the genetic architecture and network properties underlying the development of floral form and provides valuable candidate modules and genes for future studies.