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Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions

Explanations of floral adaptation to diverse pollinator faunas have often invoked visitor‐mediated trade‐offs in which no intermediate, generalized floral phenotype is optimal for pollination success, i.e. fitness valleys are created. In such cases, plant species are expected to specialize on partic...

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Autores principales: Ohashi, Kazuharu, Jürgens, Andreas, Thomson, James D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Blackwell Publishing Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518848/
https://www.ncbi.nlm.nih.gov/pubmed/34096158
http://dx.doi.org/10.1111/brv.12754
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author Ohashi, Kazuharu
Jürgens, Andreas
Thomson, James D.
author_facet Ohashi, Kazuharu
Jürgens, Andreas
Thomson, James D.
author_sort Ohashi, Kazuharu
collection PubMed
description Explanations of floral adaptation to diverse pollinator faunas have often invoked visitor‐mediated trade‐offs in which no intermediate, generalized floral phenotype is optimal for pollination success, i.e. fitness valleys are created. In such cases, plant species are expected to specialize on particular groups of flower visitors. Contrary to this expectation, it is commonly observed that flowers interact with various groups of visitors, while at the same time maintaining distinct phenotypes among ecotypes, subspecies, or congeners. This apparent paradox may be due to a gap in our understanding of how visitor‐mediated trade‐offs could affect floral adaptation. Here we provide a conceptual framework for analysing visitor‐mediated trade‐offs with the hope of stimulating empirical and theoretical studies to fill this gap. We propose two types of visitor‐mediated trade‐offs to address negative correlations among fitness contributions of different visitors: visitor‐mediated phenotypic trade‐offs (phenotypic trade‐offs) and visitor‐mediated opportunity trade‐offs (opportunity trade‐offs). Phenotypic trade‐offs occur when different groups of visitors impose conflicting selection pressures on a floral trait. By contrast, opportunity trade‐offs emerge only when some visitors’ actions (e.g. pollen collection) remove opportunities for fitness contribution by more beneficial visitors. Previous studies have observed disruptive selection due to phenotypic trade‐offs less often than expected. In addition to existing explanations, we propose that some flowers have achieved ‘adaptive generalization’ by evolving features to avoid or eliminate the fitness valleys that phenotypic trade‐offs tend to produce. The literature suggests a variety of pathways to such ‘trade‐off mitigation’. Trade‐off mitigation may also evolve as an adaptation to opportunity trade‐offs. We argue that active exclusion, or floral specialization, can be viewed as a trade‐off mitigation, occurring only when flowers cannot otherwise avoid strong opportunity trade‐offs. These considerations suggest that an evolutionary strategy for trade‐off mitigation is achieved often by acquiring novel combinations of traits. Thus, phenotypic diversification of flowers through convergent evolution of certain trait combinations may have been enhanced not only through adaptive specialization for particular visitors, but also through adaptive generalization for particular visitor communities. Explorations of how visitor‐mediated trade‐offs explain the recurrent patterns of floral phenotypes may help reconcile the long‐lasting controversy on the validity of pollination syndromes.
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spelling pubmed-85188482021-10-21 Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions Ohashi, Kazuharu Jürgens, Andreas Thomson, James D. Biol Rev Camb Philos Soc Original Articles Explanations of floral adaptation to diverse pollinator faunas have often invoked visitor‐mediated trade‐offs in which no intermediate, generalized floral phenotype is optimal for pollination success, i.e. fitness valleys are created. In such cases, plant species are expected to specialize on particular groups of flower visitors. Contrary to this expectation, it is commonly observed that flowers interact with various groups of visitors, while at the same time maintaining distinct phenotypes among ecotypes, subspecies, or congeners. This apparent paradox may be due to a gap in our understanding of how visitor‐mediated trade‐offs could affect floral adaptation. Here we provide a conceptual framework for analysing visitor‐mediated trade‐offs with the hope of stimulating empirical and theoretical studies to fill this gap. We propose two types of visitor‐mediated trade‐offs to address negative correlations among fitness contributions of different visitors: visitor‐mediated phenotypic trade‐offs (phenotypic trade‐offs) and visitor‐mediated opportunity trade‐offs (opportunity trade‐offs). Phenotypic trade‐offs occur when different groups of visitors impose conflicting selection pressures on a floral trait. By contrast, opportunity trade‐offs emerge only when some visitors’ actions (e.g. pollen collection) remove opportunities for fitness contribution by more beneficial visitors. Previous studies have observed disruptive selection due to phenotypic trade‐offs less often than expected. In addition to existing explanations, we propose that some flowers have achieved ‘adaptive generalization’ by evolving features to avoid or eliminate the fitness valleys that phenotypic trade‐offs tend to produce. The literature suggests a variety of pathways to such ‘trade‐off mitigation’. Trade‐off mitigation may also evolve as an adaptation to opportunity trade‐offs. We argue that active exclusion, or floral specialization, can be viewed as a trade‐off mitigation, occurring only when flowers cannot otherwise avoid strong opportunity trade‐offs. These considerations suggest that an evolutionary strategy for trade‐off mitigation is achieved often by acquiring novel combinations of traits. Thus, phenotypic diversification of flowers through convergent evolution of certain trait combinations may have been enhanced not only through adaptive specialization for particular visitors, but also through adaptive generalization for particular visitor communities. Explorations of how visitor‐mediated trade‐offs explain the recurrent patterns of floral phenotypes may help reconcile the long‐lasting controversy on the validity of pollination syndromes. Blackwell Publishing Ltd 2021-06-07 2021-10 /pmc/articles/PMC8518848/ /pubmed/34096158 http://dx.doi.org/10.1111/brv.12754 Text en © 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society. https://creativecommons.org/licenses/by-nc/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Original Articles
Ohashi, Kazuharu
Jürgens, Andreas
Thomson, James D.
Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
title Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
title_full Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
title_fullStr Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
title_full_unstemmed Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
title_short Trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
title_sort trade‐off mitigation: a conceptual framework for understanding floral adaptation in multispecies interactions
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8518848/
https://www.ncbi.nlm.nih.gov/pubmed/34096158
http://dx.doi.org/10.1111/brv.12754
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