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The evolution of fruit scent: phylogenetic and developmental constraints

BACKGROUND: Fruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction. However, like all traits, fruit scent is likely to evolve in response to conflicting selective pressures and various constraints. Two major c...

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Autores principales: Nevo, Omer, Valenta, Kim, Kleiner, Annemarie, Razafimandimby, Diary, Jeffrey, Juan Antonio James, Chapman, Colin A., Ayasse, Manfred
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7590443/
https://www.ncbi.nlm.nih.gov/pubmed/33109084
http://dx.doi.org/10.1186/s12862-020-01708-2
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author Nevo, Omer
Valenta, Kim
Kleiner, Annemarie
Razafimandimby, Diary
Jeffrey, Juan Antonio James
Chapman, Colin A.
Ayasse, Manfred
author_facet Nevo, Omer
Valenta, Kim
Kleiner, Annemarie
Razafimandimby, Diary
Jeffrey, Juan Antonio James
Chapman, Colin A.
Ayasse, Manfred
author_sort Nevo, Omer
collection PubMed
description BACKGROUND: Fruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction. However, like all traits, fruit scent is likely to evolve in response to conflicting selective pressures and various constraints. Two major constraints are (i) phylogenetic constraints, in which traits are inherited from ancestors rather than adapted to current conditions and (ii) developmental constraints, if phenotypes are limited by the expression of other traits within the individual. We tested whether phylogenetic constraints play a role in fruit scent evolution by calculating the phylogenetic signal in ripe fruits of 98 species from three study sites. We then estimated the importance of developmental constraints by examining whether ripe fruits tend to emit compounds that are chemically similar to, and share biosynthetic pathways with, compounds emitted by conspecific unripe fruits from which they develop. RESULTS: We show that closely related taxa are not more similar to each other than to very distinct taxa, thus indicating that fruit scent shows little phylogenetic signal. At the same time, although ripe and unripe fruits of the same species tend to emit different chemicals, they tend to employ chemicals originating from similar biosynthetic pathways, thus indicating that some developmental constraints determine ripe fruit scent. CONCLUSIONS: Our results highlight the complex landscape in which fruit scent has evolved. On one hand, fruit scent evolution is not limited by common ancestry. On the other hand, the range of chemicals that can be employed in ripe fruits is probably constrained by the needs of unripe fruits.
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spelling pubmed-75904432020-10-27 The evolution of fruit scent: phylogenetic and developmental constraints Nevo, Omer Valenta, Kim Kleiner, Annemarie Razafimandimby, Diary Jeffrey, Juan Antonio James Chapman, Colin A. Ayasse, Manfred BMC Evol Biol Research Article BACKGROUND: Fruit scent is increasingly recognized as an evolved signal whose function is to attract animal seed dispersers and facilitate plant reproduction. However, like all traits, fruit scent is likely to evolve in response to conflicting selective pressures and various constraints. Two major constraints are (i) phylogenetic constraints, in which traits are inherited from ancestors rather than adapted to current conditions and (ii) developmental constraints, if phenotypes are limited by the expression of other traits within the individual. We tested whether phylogenetic constraints play a role in fruit scent evolution by calculating the phylogenetic signal in ripe fruits of 98 species from three study sites. We then estimated the importance of developmental constraints by examining whether ripe fruits tend to emit compounds that are chemically similar to, and share biosynthetic pathways with, compounds emitted by conspecific unripe fruits from which they develop. RESULTS: We show that closely related taxa are not more similar to each other than to very distinct taxa, thus indicating that fruit scent shows little phylogenetic signal. At the same time, although ripe and unripe fruits of the same species tend to emit different chemicals, they tend to employ chemicals originating from similar biosynthetic pathways, thus indicating that some developmental constraints determine ripe fruit scent. CONCLUSIONS: Our results highlight the complex landscape in which fruit scent has evolved. On one hand, fruit scent evolution is not limited by common ancestry. On the other hand, the range of chemicals that can be employed in ripe fruits is probably constrained by the needs of unripe fruits. BioMed Central 2020-10-27 /pmc/articles/PMC7590443/ /pubmed/33109084 http://dx.doi.org/10.1186/s12862-020-01708-2 Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Nevo, Omer
Valenta, Kim
Kleiner, Annemarie
Razafimandimby, Diary
Jeffrey, Juan Antonio James
Chapman, Colin A.
Ayasse, Manfred
The evolution of fruit scent: phylogenetic and developmental constraints
title The evolution of fruit scent: phylogenetic and developmental constraints
title_full The evolution of fruit scent: phylogenetic and developmental constraints
title_fullStr The evolution of fruit scent: phylogenetic and developmental constraints
title_full_unstemmed The evolution of fruit scent: phylogenetic and developmental constraints
title_short The evolution of fruit scent: phylogenetic and developmental constraints
title_sort evolution of fruit scent: phylogenetic and developmental constraints
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7590443/
https://www.ncbi.nlm.nih.gov/pubmed/33109084
http://dx.doi.org/10.1186/s12862-020-01708-2
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