Influences of clonality on plant sexual reproduction

Barrett, Spencer C. H.

doi:10.1073/pnas.1501712112

Cited by 215 publications

(212 citation statements)

References 74 publications

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“…Because mating in plants typically involves near neighbors, whether or not clonality interferes with mating should depend on how clonal growth affects the spatial relations of ramets from different genets (5,(10)(11)(12). The growth forms of clonal plants range from compact with closely aggregated ramets (a so-called "phalanx" growth form) to laterally spreading with loosely aggregated ramets (a "guerrilla" growth form; ref.…”

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confidence: 99%

“…These different growth forms are likely to differ in the degree to which they can compete or resist competition, and the degree to which they can sample the environment (14)(15)(16) and "forage" for resources (17,18). In addition, by affecting the extent of genet intermingling and the proximity to mating partners, clonal growth forms should also affect the degree to which clonal growth interferes with plant mating and sexual fitness (12).…”

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Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal

Drunen

Kleunen

Dorken

2015

Proc. Natl. Acad. Sci. U.S.A.

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Clonality is a pervasive feature of sessile organisms, but this form of asexual reproduction is thought to interfere with sexual fitness via the movement of gametes among the modules that comprise the clone. This within-clone movement of gametes is expected to reduce sexual fitness via mate limitation of male reproductive success and, in some cases, via the production of highly inbred (i.e., self-fertilized) offspring. However, clonality also results in the spatial expansion of the genetic individual (i.e., genet), and this should decrease distances gametes and sexually produced offspring must travel to avoid competing with other gametes and offspring from the same clone. The extent to which any negative effects of clonality on mating success might be offset by the positive effects of spatial expansion is poorly understood. Here, we develop spatially explicit models in which fitness was determined by the success of genets through their male and female sex functions. Our results indicate that clonality serves to increase sexual fitness when it is associated with the outward expansion of the genet. Our models further reveal that the main fitness benefit of clonal expansion might occur through the dispersal of offspring over a wider area compared with nonclonal phenotypes. We conclude that, instead of interfering with sexual reproduction, clonal expansion should often serve to enhance sexual fitness.asexual reproduction | geitonogamy | genet | modularity | ramet M odular growth, clonality, and hermaphroditism are widespread features of sessile organisms. Sessile organisms might benefit from modularity and the spatial expansion of the individual via enhanced resource capture, and thereby improved growth and survival (1-3). However, growth and survival are only two of the key components of an organism's life history, and the third, reproduction, is the one that is most intimately linked to fitness. Indeed, during reproduction, the growth of a modular hermaphrodite might interfere with its success as a parent. In particular, it has been argued that the production of numerous partially or fully autonomous clonal modules (i.e., ramets) should interfere with mating success because there is a nonzero chance that sperm (or pollen) will encounter the receptive tissues associated with the female function of the same genetic individual (i.e., the genet). All else being equal, the larger the clone, the greater the chance that this kind of mating interference should occur (4, 5). The negative effects of such intraclonal mating is expected to occur through reductions in the number of offspring sired on other genets (i.e., outcross siring success, corresponding with the fitness of individuals via their male function) and, in self-compatible organisms, through inbreeding depression (i.e., a reduction in offspring fitness, with negative effects on the fitness of individuals through their female function; e.g., ref. 5). However, these forms of mating interference are simply by-products of attaining a larger size and are not exclusiv...

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mentioning

confidence: 99%

Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal

Drunen

Kleunen

Dorken

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…During clonal growth, natural selection is inoperative against mutations that impair strictly sexual functions and may even favour such mutations if resources can be reallocated from gametangia and sporophytes to vegetative growth and asexual propagules. For both these reasons, mutations that degrade sexual functions will accumulate in long-lived clones [46,47]. Successful reproduction via spores, on the other hand, is only possible for subclones that retain sexual functions.…”

Section: (A) Female Advantagementioning

confidence: 99%

Living together and living apart: the sexual lives of bryophytes

Haig¹

2016

Phil. Trans. R. Soc. B

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One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Haploid gametophytes of bryophytes spread by clonal growth but mate locally, within an area defined by the range of sperm movement. Rarity of establishment from spores or vegetative competition can result in unisexual populations unable to reproduce sexually. Females typically outcompete males, probably because females expend fewer resources than males on the production of gametes. Extreme sexual dimorphism-tiny males growing as epiphytes on much larger females-has evolved many times. Haploid selfing is common in bryophytes with bisexual gametophytes, and results in completely homozygous sporophytes. Spores from these sporophytes recapitulate the genotype of their single haploid parent. This process can be considered analogous to 'asexual' reproduction with 'sexual' reproduction occurring after rare outcrossing between haploid parents. Ferns also produce bisexual haploid gametophytes but, unlike bryophytes, haploid outcrossing predominates over haploid selfing. This difference is probably related to clonal growth and vegetative competition occurring in the haploid but not the diploid phase in bryophytes, but the reverse in ferns. Ferns are thereby subject to stronger inbreeding depression than bryophytes.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Sexual lives of bryophytesAnimal life histories are characterized by multicellular diploid individuals that produce haploid gametes by meiosis. Gametes are the only haploid cells of such life cycles. The life histories of bryophytes (mosses, liverworts and hornworts) are fundamentally different. Multicellular haploid gametophytes (gameteproducing plants) produce gametes by mitosis. The fertilization of an ovum by a sperm produces a zygote that develops into a short-lived multicellular diploid sporophyte (spore-producing plant) that grows attached to the maternal gametophyte on which it depends for nutrients. Sporophytes produce haploid spores by meiosis that germinate to produce new gametophytes (figure 1). Mating is restricted to the distance over which sperm can find ova, usually in the millimetre to centimetre range [1]. Clonal expansion occurs via vegetative spread of gametophytes into neighbouring space and production of gemmae (asexual propagules) that disperse gametophytic clones to new sites [2].Gametophytes of dioecious bryophytes are unisexual, producing either eggs or sperm, but not both. Males and females compete for space but require close proximity for sexual reproduction. By contrast, gametophytes of monoecious bryophytes are bisexual, able to produce both eggs and sperm. A bisexual gametophyte that fertilizes its own eggs engenders homozygous sporophytes all of whose spores are genetically identical (excepting meiotic errors and postzygotic mutations). Roughly 70% of liverworts, 60% of mosses and 40% of hornworts are dioecious [3]. Bryophyte life cycles are not only fascinating in th...

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“…Devido a esse aumento na autopolinização, esse conflito proporciona maior geitonogamia, que é a fração de autofertilização entre flores de uma mesma planta (Hessing 1988;, em especial em plantas onde a reprodução vegetativa (clonal) é constante e elevada (Barrett 2015;Vallejo-Marín et al 2010).…”

Section: Geitonogamia E Dilema Da Plantaunclassified

Plantas, polinizadores e algumas articulações da biologia da polinização com a teoria ecológica

et al. 2016

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A consolidação em uma área do conhecimento acontece principalmente quando as informações acerca de um determinado fato ou fenômeno são sistematizadas na forma de uma teoria explicativa, capaz de gerar novas hipóteses testáveis. Na biologia da polinização, o teste de diversas hipóteses ecológicas permitiu ampliar o entendimento sobre os processos que originam, mantêm, alteram ou ainda excluem as interações entre plantas e visitantes florais, gerando os padrões observados na natureza. Visando sintetizar esse panorama teórico e oferecer condições para que novas questões relacionadas ao funcionamento de interações de polinização sejam geradas, compilamos aqui um conjunto de 25 hipóteses, ideias e teorias ecológicas que fornecem aporte conceitual para a área. Essas ideias estão relacionadas a aspectos reprodutivos, morfológicos, cognitivos, macroecológicos e de coexistência, de acordo com a especialização das interações entre as plantas e seus polinizadores. Ao apresentarmos essas ideias principais, esperamos promover a utilização de uma abordagem teórico-conceitual explícita no planejamento e desenvolvimento de estudos em biologia da polinização. Concluímos com a expectativa de que essa contribuição direcione os estudos em biologia da polinização no Brasil e contribua para o avanço e internacionalização das pesquisas desenvolvidas no país. Palavras-chave: Fundamentação teórica, interação planta-polinizador, sucesso reprodutivo, ecologia cognitiva. AbstractA particular research area can be significantly improved when information is systematized in explanatory theories able to generate testable hypotheses. In pollination biology, such systematization contributed to several ecological theories and expanded the understanding of the patterns and processes that originated, maintain, or exclude ecological interactions. Here, we compiled a set of 25 ecological ideas that have already received conceptual contribution from pollination biology. These ideas are related to reproduction, morphology, cognition, macroecology and species coexistence. We hope to promote the use of an explicit conceptual and theoretical approach when planning and developing studies in this research field by presenting these main ideas. We conclude that this contribution will boost studies in pollination biology in Brazil and contribute to the advancement and internationalization of such research developed in the country.

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Influences of clonality on plant sexual reproduction

Cited by 215 publications

References 74 publications

Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal

Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal

Living together and living apart: the sexual lives of bryophytes

Plantas, polinizadores e algumas articulações da biologia da polinização com a teoria ecológica

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