Stigmatic fluid aids self-pollination in Roscoea debilis (Zingiberaceae): a new delayed selfing mechanism

Fan, Yong-Li; Liu, Qingjun

doi:10.1093/aob/mcs169

Cited by 29 publications

(44 citation statements)

References 39 publications

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“…Roscoea species are largely endemic to the Himalayas and the Hengduan Mountains, and exhibit extremely diverse floral traits that may link to local adaptations and/or distinct pollination syndromes (Zhang & Li, 2008;Zhang et al, 2011;Fan & Li, 2012;Paudel et al, 2015Paudel et al, , 2016. Compared to previous phylogenetic results (Ngamriabsakul et al, 2000), this study produced a more informative phylogenetic backbone using nrDNA and cpDNA from which testable hypotheses can be drawn for future in-depth speciation studies for this group.…”

Section: Discussionmentioning

confidence: 96%

A preliminary species‐level phylogeny of the alpine ginger Roscoea: Implications for speciation

Zhao

Zhong

Fan

et al. 2017

J of Sytematics Evolution

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Speciation, the evolutionary process forming new species, is a key mode generating biodiversity on the Earth. In this study, we produced a species‐level phylogeny of Roscoea using one nuclear ribosomal and two chloroplast DNA fragments based on Bayesian inference and maximum likelihood. We then explored the possible speciation processes using the species‐level phylogeny and the heterozygous sites in the nuclear DNA. The incongruence between nuclear and chloroplast phylogenies, and several heterozygous sites in the nuclear DNA, suggested that R. auriculata might have a hybrid origin with R. purpurea and R. alpina being two possible parental progenitors; however, one alternative possibility through incomplete lineage sorting cannot be ruled out. In addition, R. kunmingensis likely originated from R. tibetica Batalin through the process of “budding speciation”. These results provided a valuable framework to draw testable hypotheses for future in‐depth comparative studies to further our understanding of the underpinning speciation and adaptation mechanisms that contribute to ultrahigh biodiversity in the Himalayas and the Hengduan Mountains.

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Section: Discussionmentioning

confidence: 96%

A preliminary species‐level phylogeny of the alpine ginger Roscoea: Implications for speciation

Zhao

Zhong

Fan

et al. 2017

J of Sytematics Evolution

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“…Twenty flowering individuals at each population were randomly selected, and number of inflorescence per plant and number of flower or bud per inflorescence were counted. Floral longevity, time of anthesis, time of anther dehiscence, length of corolla tube, length of ovary, and length of anther were measured from freshly opened flowers ( n = 20), following the method of Fan and Li (). As the hollow cavity of corolla tube was too small to accommodate micro‐capillaries, we were unable to measure the nectar volume.…”

Section: Methodsmentioning

confidence: 99%

“…However, recent studies on the reproductive biology of North Indochinese clades of Roscoea did not find any effective pollinators as predicted by the floral syndrome and these species either reproduce by autonomous selfing or are pollinated occasionally by generalist pollinators (Zhang and Li ; Zhang et al. ; Fan and Li ). Zhang et al.…”

Section: Introductionmentioning

confidence: 98%

Out of Africa: evidence of the obligate mutualism between long corolla tubed plant and long‐tongued fly in the Himalayas

Paudel

Shrestha

Dyer

et al. 2015

Ecology and Evolution

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Summary Mutualism between long corolla tubed plants and their potential pollinators, long‐tongued flies, is a classic example of coevolution, but to date, has only been reported from the regions of southern Africa. Many plant species from the Himalayas also show botanical characteristics that could be consistent with pollination by long‐tongued flies. Here, we seek the evidence of the “long‐tongued‐long tubed fly/flower” mutualism out of Africa, in a different continent and climatic region, the Himalayas.Floral traits of Himalayan region endemic alpine genus, Roscoea, indicate possible mutualism with long‐tongued flies for pollination success; however, effective pollinators of this genus are yet unknown. This study investigates whether long‐tongued flies and Roscoea purpurea in Nepal Himalayas show exclusive mutualism for their survival/reproduction.We made extensive observations of floral visitors of R. purpurea and food source of Philoliche longirostris across their wide ranges of populations in Nepal Himalayas for three consecutive years (2012–2014). To confirm the obligate reliance of R. purpurea upon P. longirostris for pollination success, manipulated pollination experiments were conducted at two populations for 2 years. Similarly foraging behavior, visitation frequency, and pollination efficiency of P. longirostris were assessed at two populations for 2 years, and its contribution for the reproductive success of R. purpurea was evaluated. Our results indicate that R. purpurea is self‐compatible but lacks autonomous selfing and obligatorily relies on P. longirostris for reproductive success. Across all populations, P. longirostris was observed as an exclusive and highly efficient pollinator of R. purpurea, while P. longirostris exclusively depends up on R. purpurea for food source.Out of Africa, this study provides the first evidence of long‐tongued fly pollination system and indicates the possibility of additional instances of such a rare phenomenon in the Himalayas. Finding of specialized pollinator of Roscoea only at its evolutionary center indicates that Roscoea species are originally pollinated by long‐tongued flies. Spatial mismatch with specialized pollinators may have induced the evolution of autonomous selfing in North Indochinese clades of Roscoea. This finding thus substantiates how geographic disjunction causes the shifting of pollination mechanism in closely related plant species.

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“…In two species in the Zingiberaceae, Roscoea debilis (Fan and Li, 2012) and Caulokaempferia coenobialis (Wang et al, 2005) oily fluid (originating at the stigma or anther sac) spreads during anthesis and allows pollen to travel to the stigmatic surface. Delayed selfing is promoted by diplostigmaty in Sebaea aurea (Gentianaceae), in which two stigmatic forms are present.…”

Section: Mechanisms Of Delayed Selfingmentioning

confidence: 99%

“…For example, stigma removal in late anthesis was used to quantify delayed selfing in Collinsia parviflora (Plantaginaceae; Elle et al, 2010). Another experimental approach quantifies seed set in flowers that have been emasculated at different intervals during anthesis-the emasculation time point after which increases in seed set are observed provides a measure of the timing of autonomous selfing (Vaughton and Ramsey, 2010;Fan and Li, 2012). The effect of transient SI on delayed selfing was estimated using mixed self-and outcross-pollen loads and genetic markers; the proportion of selfed offspring produced by mixed pollen loads was shown to increase with the floral age at which pollen was applied, demonstrating the potential for delayed selfing (Vogler and Stephenson, 2001;Goodwillie et al, 2004).…”

Section: Experimental Support For Delayed Selfingmentioning

confidence: 99%

The best of both worlds? A review of delayed selfing in flowering plants

Goodwillie

Weber

2018

American J of Botany

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In a series of seminal papers, David G. Lloyd (1979;Lloyd and Schoen, 1992) provided new insight into plant mating-system evolution by recognizing that the selective consequences of selfand cross-pollination and fertilization depend on the specifics of how and when they occur. In phenotypic models, Lloyd showed that the conditions that select for self-fertilization (selfing) facilitated by pollinators differ from those for selfing that occurs autonomously. Further, the selective consequences of autonomous selfing were shown to depend on its timing in anthesis in relation to cross-fertilization (outcrossing). The theory predicts that selfing that occurs after opportunities for outcrossing have passed (delayed selfing) should be selected under the broadest range of conditions.In general, selection of selfing is expected to be opposed by inbreeding depression, the reduced fitness of selfed progeny that results primarily from the expression of deleterious recessive alleles Charlesworth, 1987, Charlesworth andWillis, 2009). Counteracting the cost of inbreeding depression is the 50% genetic transmission advantage of selfing, which occurs because INVITED SPECIAL ARTICLE The best of both worlds? A review of delayed selfing in flowering plantsCarol Goodwillie 1,3 and Jennifer J. Weber PREMISE OF STUDY:In a seminal body of theory, Lloyd showed that the fitness consequences of selfing will depend on its timing in anthesis. Selfing that occurs after opportunities for outcrossing or pollen dispersal can provide reproductive assurance when pollinators are limited and is expected to incur little cost, even when inbreeding depression is high. As a result, delayed selfing is often interpreted as a "best-of-both-worlds" mating system that combines the advantages of selfing and outcrossing. METHODS:We surveyed 65 empirical studies of delayed selfing, recording floral mechanisms and examining information on inbreeding depression, autofertility, and other parameters to test the support for delayed selfing as a best-of-both-worlds strategy.KEY RESULTS: Phylogenetic distribution of the diverse floral mechanisms suggests that some basic floral structures may predispose plant taxa to evolve delayed selfing. Delayed selfing appears to serve as a best-of-both-worlds strategy in some but not all species. While the capacity for autonomous selfing is often high, it is lower, in some cases, than in related species with earlier modes of selfing. In other delayed-selfers, low inbreeding depression and reduced investment in corollas and pollen suggest limited benefits from outcrossing.CONCLUSIONS: Despite a growing literature on the subject, experimental evidence for delayed selfing is limited and major gaps in knowledge remain, particularly with respect to the stability of delayed selfing and the conditions that may favor transitions between delayed and earlier selfing. Finally, we suggest a potential role of delayed selfing in facilitating transitions from self-incompatibility to selfing.

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Stigmatic fluid aids self-pollination in Roscoea debilis (Zingiberaceae): a new delayed selfing mechanism

Abstract: This study describes a new form of delayed autonomous self-pollination. As the predominant mechanism of sexual reproduction in R. debilis, delayed self-pollination ensures reproduction when pollinators are scarce.

Cited by 29 publications

References 39 publications

A preliminary species‐level phylogeny of the alpine ginger Roscoea: Implications for speciation

A preliminary species‐level phylogeny of the alpine ginger Roscoea: Implications for speciation

Out of Africa: evidence of the obligate mutualism between long corolla tubed plant and long‐tongued fly in the Himalayas

The best of both worlds? A review of delayed selfing in flowering plants

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