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      Phenotypic selection on flowering phenology and pollination efficiency traits between Primula populations with different pollinator assemblages

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          Abstract

          Floral traits have largely been attributed to phenotypic selection in plant–pollinator interactions. However, the strength of this link has rarely been ascertained with real pollinators. We conducted pollinator observations and estimated selection through female fitness on flowering phenology and floral traits between two Primula secundiflora populations. We quantified pollinator‐mediated selection by subtracting estimates of selection gradients of plants receiving supplemental hand pollination from those of plants receiving open pollination. There was net directional selection for an earlier flowering start date at populations where the dominant pollinators were syrphid flies, and flowering phenology was also subjected to stabilized quadratic selection. However, a later flowering start date was significantly selected at populations where the dominant pollinators were legitimate (normal pollination through the corolla tube entrance) and illegitimate bumblebees (abnormal pollination through nectar robbing hole which located at the corolla tube), and flowering phenology was subjected to disruptive quadratic selection. Wider corolla tube entrance diameter was selected at both populations. Furthermore, the strength of net directional selection on flowering start date and corolla tube entrance diameter was stronger at the population where the dominant pollinators were syrphid flies. Pollinator‐mediated selection explained most of the between‐population variations in the net directional selection on flowering phenology and corolla tube entrance diameter. Our results suggested the important influence of pollinator‐mediated selection on floral evolution. Variations in pollinator assemblages not only resulted in variation in the direction of selection but also the strength of selection on floral traits.

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          Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing?

          The use of regression analysis has been instrumental in allowing evolutionary biologists to estimate the strength and mode of natural selection. Although directional and correlational selection gradients are equal to their corresponding regression coefficients, quadratic regression coefficients must be doubled to estimate stabilizing/disruptive selection gradients. Based on a sample of 33 papers published in Evolution between 2002 and 2007, at least 78% of papers have not doubled quadratic regression coefficients, leading to an appreciable underestimate of the strength of stabilizing and disruptive selection. Proper treatment of quadratic regression coefficients is necessary for estimation of fitness surfaces and contour plots, canonical analysis of the gamma matrix, and modeling the evolution of populations on an adaptive landscape.
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            Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation.

            Although not 'a professed botanist', Charles Darwin made seminal contributions to understanding of floral and inflorescence function while seeking evidence of adaptation by natural selection. This review considers the legacy of Darwin's ideas from three perspectives. First, we examine the process of floral and inflorescence adaptation by surveying studies of phenotypic selection, heritability and selection responses. Despite widespread phenotypic and genetic capacity for natural selection, only one-third of estimates indicate phenotypic selection. Second, we evaluate experimental studies of floral and inflorescence function and find that they usually demonstrate that reproductive traits represent adaptations. Finally, we consider the role of adaptation in floral diversification. Despite different diversification modes (coevolution, divergent use of the same pollen vector, pollinator shifts), evidence of pollination ecotypes and phylogenetic patterns suggests that adaptation commonly contributes to floral diversity. Thus, this review reveals a contrast between the inconsistent occurrence of phenotypic selection and convincing experimental and comparative evidence that floral traits are adaptations. Rather than rejecting Darwin's hypotheses about floral evolution, this contrast suggests that the tempo of creative selection varies, with strong, consistent selection during episodes of diversification, but relatively weak and inconsistent selection during longer, 'normal' periods of relative phenotypic stasis.
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              Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured.

              Flowering times of plants are important life-history components and it has previously been hypothesized that flowering phenologies may be currently subject to natural selection or be selectively neutral. In this study we reviewed the evidence for phenotypic selection acting on flowering phenology using ordinary and phylogenetic meta-analysis. Phenotypic selection exists when a phenotypic trait co-varies with fitness; therefore, we looked for studies reporting an association between two components of flowering phenology (flowering time or flowering synchrony) with fitness. Data sets comprising 87 and 18 plant species were then used to assess the incidence and strength of phenotypic selection on flowering time and flowering synchrony, respectively. The influence of dependence on pollinators, the duration of the reproductive event, latitude and plant longevity as moderators of selection were also explored. Our results suggest that selection favours early flowering plants, but the strength of selection is influenced by latitude, with selection being stronger in temperate environments. However, there is no consistent pattern of selection on flowering synchrony. Our study demonstrates that phenotypic selection on flowering time is consistent and relatively strong, in contrast to previous hypotheses of selective neutrality, and has implications for the evolution of temperate floras under global climate change. © 2011 Blackwell Publishing Ltd/CNRS.
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                Author and article information

                Contributors
                qingjun.li@ynu.edu.cn
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                17 August 2017
                October 2017
                : 7
                : 19 ( doiID: 10.1002/ece3.2017.7.issue-19 )
                : 7599-7608
                Affiliations
                [ 1 ] Key Laboratory of Tropical Forest Ecology Xishuangbanna Tropical Botanical Garden Chinese Academy of Sciences Menglun, Mengla County China
                [ 2 ] University of Chinese Academy of Sciences Beijing China
                [ 3 ] Laboratory of Ecology and Evolutionary Biology State Key Laboratory for Conservation and Utilization of Bio‐Resources in Yunnan, Yunnan University Kunming China
                Author notes
                [*] [* ] Correspondence

                Qing‐Jun Li, Laboratory of Ecology and Evolutionary Biology, State Key Laboratory for Conservation and Utilization of Bio‐Resources in Yunnan, Yunnan University, Kunming, Yunnan, China.

                Email: qingjun.li@ 123456ynu.edu.cn

                Author information
                http://orcid.org/0000-0002-6092-4913
                Article
                ECE33258
                10.1002/ece3.3258
                5632619
                9e688241-0e1a-4dbb-8afa-08c99fbd9dad
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 24 February 2017
                : 13 June 2017
                : 28 June 2017
                Page count
                Figures: 4, Tables: 2, Pages: 10, Words: 6823
                Funding
                Funded by: National Natural Science Foundation of China
                Funded by: Yunnan Provincial Government
                Award ID: U1202261
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece33258
                October 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.2.1 mode:remove_FC converted:08.10.2017

                Evolutionary Biology
                different pollinator assemblages,floral evolution,phenotypic selection,primula secundiflora,spatial variation

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