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      Hermaphroditism promotes mate diversity in flowering plants

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          Abstract

          Premise

          Genetically diverse sibships are thought to increase parental fitness through a reduction in the intensity of sib competition, and through increased opportunities for seedling establishment in spatially or temporally heterogeneous environments. Nearly all research on mate diversity in flowering plants has focused on the number of fathers siring seeds within a fruit or on a maternal plant. Yet as hermaphrodites, plants can also accrue mate diversity by siring offspring on several pollen recipients in a population. Here we explore whether mate composition overlaps between the dual sex functions, and discuss the implications for plant reproductive success.

          Methods

          We established an experimental population of 49 Mimulus ringens (monkeyflower) plants, each trimmed to a single flower. Following pollination by wild bees, we quantified mate composition for each flower through both paternal and maternal function. Parentage was successfully assigned to 240 progeny, 98% of the sampled seeds.

          Results

          Comparison of mate composition between male and female function revealed high mate diversity, with almost no outcross mates shared between the two sexual functions of the same flower.

          Conclusions

          Dual sex roles contribute to a near doubling of mate diversity in our experimental population of Mimulus ringens. This finding may help explain the maintenance of hermaphroditism under conditions that would otherwise favor the evolution of separate sexes.

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          Most cited references36

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          New insights from fine-scale spatial genetic structure analyses in plant populations.

          Many empirical studies have assessed fine-scale spatial genetic structure (SGS), i.e. the nonrandom spatial distribution of genotypes, within plant populations using genetic markers and spatial autocorrelation techniques. These studies mostly provided qualitative descriptions of SGS, rendering quantitative comparisons among studies difficult. The theory of isolation by distance can predict the pattern of SGS under limited gene dispersal, suggesting new approaches, based on the relationship between pairwise relatedness coefficients and the spatial distance between individuals, to quantify SGS and infer gene dispersal parameters. Here we review the theory underlying such methods and discuss issues about their application to plant populations, such as the choice of the relatedness statistics, the sampling scheme to adopt, the procedure to test SGS, and the interpretation of spatial autocorrelograms. We propose to quantify SGS by an 'Sp' statistic primarily dependent upon the rate of decrease of pairwise kinship coefficients between individuals with the logarithm of the distance in two dimensions. Under certain conditions, this statistic estimates the reciprocal of the neighbourhood size. Reanalysing data from, mostly, published studies, the Sp statistic was assessed for 47 plant species. It was found to be significantly related to the mating system (higher in selfing species) and to the life form (higher in herbs than trees), as well as to the population density (higher under low density). We discuss the necessity for comparing SGS with direct estimates of gene dispersal distances, and show how the approach presented can be extended to assess (i) the level of biparental inbreeding, and (ii) the kurtosis of the gene dispersal distribution.
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            The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database.

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              Animals mix it up too: the distribution of self-fertilization among hermaphroditic animals.

              Excluding insects, hermaphroditism occurs in about one-third of animal species, providing numerous opportunities for the evolution of selfing. Here we provide an overview of reproductive traits in hermaphroditic animal species, review the distribution of selfing rates in animals, and test for ecological correlates of selfing. Our dataset (1342 selfing-rate estimates for 142 species) is 97% based on estimates derived from the analysis of population structure (F(IS)-estimates) using genetic markers. The distribution of selfing is slightly U-shaped and differs significantly from the more strongly U-shaped plant distribution with 47% of animal t-estimates being intermediate (falling between 0.2 and 0.8) compared to 42% for plants. The influence of several factors on the distribution of selfing rates was explored (e.g., number of populations studied per species, habitat, coloniality, sessility, or fertilization type), none of which significantly affect the distribution. Our results suggest that genetic forces might contribute to the evolution of self-fertilization to the same extent in animals and plants, although the high proportion of intermediate outcrossing suggests a significant role of ecological factors (e.g., reproductive assurance) in animals. However, we caution that the distribution of selfing rates in animals is affected by various factors that might bias F(IS)-estimates, including phylogenetic underrepresentation of highly selfing and outcrossing species, various genotyping errors (e.g., null alleles) and inbreeding depression. This highlights the necessity of obtaining better estimates of selfing for hermaphroditic animals, such as genotyping progeny arrays, as in plants.
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                Author and article information

                Contributors
                christod@uwm.edu
                Journal
                Am J Bot
                Am. J. Bot
                10.1002/(ISSN)1537-2197
                AJB2
                American Journal of Botany
                John Wiley and Sons Inc. (Hoboken )
                0002-9122
                1537-2197
                12 August 2019
                August 2019
                : 106
                : 8 ( doiID: 10.1002/ajb2.v106.8 )
                : 1131-1136
                Affiliations
                [ 1 ] Department of Biological Sciences University of Wisconsin – Milwaukee 3209 N. Maryland Ave Milwaukee Wisconsin 53211 USA
                [ 2 ] Department of Biology University of Akron Akron Ohio 44325 USA
                [ 3 ] Department of Plant Biology University of Georgia 120 Carlton St Athens Georgia 30602 USA
                Author notes
                [*] [* ]Author for correspondence (e‐mail: christod@ 123456uwm.edu )
                Author information
                https://orcid.org/0000-0002-8734-2243
                Article
                AJB21336
                10.1002/ajb2.1336
                6852098
                31403705
                828bc666-c4ea-4476-b24a-e8259f9d7702
                © 2019 The Authors. American Journal of Botany is published by Wiley Periodicals, Inc. on behalf of the Botanical Society of America.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 April 2019
                : 04 June 2019
                Page count
                Figures: 2, Tables: 0, Pages: 6, Words: 4333
                Funding
                Funded by: National Science Foundation , open-funder-registry 10.13039/100000001;
                Award ID: 1654943
                Award ID: 1654967
                Award ID: 1654951
                Categories
                Research Article
                Research Articles
                Brief Communications
                Custom metadata
                2.0
                August 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.1 mode:remove_FC converted:13.11.2019

                hermaphrodite,male fitness,mate diversity,mating network,mating portfolio,multiple paternity,paternity,pollination,selfing,sexual system

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