Cargando…

Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought

BACKGROUND: One of the major trends in angiosperm evolution was the shift from woody to herbaceous habit. However, reversals known as derived woodiness have also been reported in numerous, distantly related clades. Among theories evoked to explain the factors promoting the evolution of derived woodi...

Descripción completa

Detalles Bibliográficos
Autores principales: Frankiewicz, Kamil E., Banasiak, Łukasz, Oskolski, Alexei A., Magee, Anthony R., Alsarraf, Mohammad, Trzeciak, Paulina, Spalik, Krzysztof
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8377965/
https://www.ncbi.nlm.nih.gov/pubmed/34416875
http://dx.doi.org/10.1186/s12870-021-03151-x
_version_ 1783740746430414848
author Frankiewicz, Kamil E.
Banasiak, Łukasz
Oskolski, Alexei A.
Magee, Anthony R.
Alsarraf, Mohammad
Trzeciak, Paulina
Spalik, Krzysztof
author_facet Frankiewicz, Kamil E.
Banasiak, Łukasz
Oskolski, Alexei A.
Magee, Anthony R.
Alsarraf, Mohammad
Trzeciak, Paulina
Spalik, Krzysztof
author_sort Frankiewicz, Kamil E.
collection PubMed
description BACKGROUND: One of the major trends in angiosperm evolution was the shift from woody to herbaceous habit. However, reversals known as derived woodiness have also been reported in numerous, distantly related clades. Among theories evoked to explain the factors promoting the evolution of derived woodiness are moderate climate theory and cavitation theory. The first assumes that woody habit evolves in response to mild climate allowing for prolonged life span, which in turn leads to bigger and woodier bodies. The second sees woodiness as a result of natural selection for higher cavitation resistance in seasonally dry environments. Here, we compare climatic niches of woody and herbaceous, mostly southern African, umbellifers from the Lefebvrea clade to assess whether woody taxa in fact occur in markedly drier habitats. We also calibrate their phylogeny to estimate when derived woodiness evolved. Finally, we describe the wood anatomy of selected woody and herbaceous taxa to see if life forms are linked to any particular wood traits. RESULTS: The evolution of derived woodiness in chamaephytes and phanerophytes as well as the shifts to short-lived annual therophytes in the Lefebvrea clade took place at roughly the same time: in the Late Miocene during a trend of global climate aridification. Climatic niches of woody and herbaceous genera from the Cape Floristic Region overlap. There are only two genera with distinctly different climatic preferences: they are herbaceous and occur outside of the Cape Floristic Region. Therefore, studied herbs have an overall climatic niche wider than their woody cousins. Woody and herbaceous species do not differ in qualitative wood anatomy, which is more affected by stem architecture and, probably, reproductive strategy than by habit. CONCLUSIONS: Palaeodrought was likely a stimulus for the evolution of derived woodiness in the Lefebvrea clade, supporting the cavitation theory. The concurrent evolution of short-lived annuals withering before summer exemplifies an alternative solution to the same problem of drought-induced cavitation. Changes of the life form were most likely neither spurred nor precluded by any qualitative wood traits, which in turn are more affected by internode length and probably also reproductive strategy. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03151-x.
format Online
Article
Text
id pubmed-8377965
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-83779652021-08-23 Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought Frankiewicz, Kamil E. Banasiak, Łukasz Oskolski, Alexei A. Magee, Anthony R. Alsarraf, Mohammad Trzeciak, Paulina Spalik, Krzysztof BMC Plant Biol Research BACKGROUND: One of the major trends in angiosperm evolution was the shift from woody to herbaceous habit. However, reversals known as derived woodiness have also been reported in numerous, distantly related clades. Among theories evoked to explain the factors promoting the evolution of derived woodiness are moderate climate theory and cavitation theory. The first assumes that woody habit evolves in response to mild climate allowing for prolonged life span, which in turn leads to bigger and woodier bodies. The second sees woodiness as a result of natural selection for higher cavitation resistance in seasonally dry environments. Here, we compare climatic niches of woody and herbaceous, mostly southern African, umbellifers from the Lefebvrea clade to assess whether woody taxa in fact occur in markedly drier habitats. We also calibrate their phylogeny to estimate when derived woodiness evolved. Finally, we describe the wood anatomy of selected woody and herbaceous taxa to see if life forms are linked to any particular wood traits. RESULTS: The evolution of derived woodiness in chamaephytes and phanerophytes as well as the shifts to short-lived annual therophytes in the Lefebvrea clade took place at roughly the same time: in the Late Miocene during a trend of global climate aridification. Climatic niches of woody and herbaceous genera from the Cape Floristic Region overlap. There are only two genera with distinctly different climatic preferences: they are herbaceous and occur outside of the Cape Floristic Region. Therefore, studied herbs have an overall climatic niche wider than their woody cousins. Woody and herbaceous species do not differ in qualitative wood anatomy, which is more affected by stem architecture and, probably, reproductive strategy than by habit. CONCLUSIONS: Palaeodrought was likely a stimulus for the evolution of derived woodiness in the Lefebvrea clade, supporting the cavitation theory. The concurrent evolution of short-lived annuals withering before summer exemplifies an alternative solution to the same problem of drought-induced cavitation. Changes of the life form were most likely neither spurred nor precluded by any qualitative wood traits, which in turn are more affected by internode length and probably also reproductive strategy. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03151-x. BioMed Central 2021-08-20 /pmc/articles/PMC8377965/ /pubmed/34416875 http://dx.doi.org/10.1186/s12870-021-03151-x Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://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
Frankiewicz, Kamil E.
Banasiak, Łukasz
Oskolski, Alexei A.
Magee, Anthony R.
Alsarraf, Mohammad
Trzeciak, Paulina
Spalik, Krzysztof
Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought
title Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought
title_full Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought
title_fullStr Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought
title_full_unstemmed Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought
title_short Derived woodiness and annual habit evolved in African umbellifers as alternative solutions for coping with drought
title_sort derived woodiness and annual habit evolved in african umbellifers as alternative solutions for coping with drought
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8377965/
https://www.ncbi.nlm.nih.gov/pubmed/34416875
http://dx.doi.org/10.1186/s12870-021-03151-x
work_keys_str_mv AT frankiewiczkamile derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought
AT banasiakłukasz derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought
AT oskolskialexeia derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought
AT mageeanthonyr derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought
AT alsarrafmohammad derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought
AT trzeciakpaulina derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought
AT spalikkrzysztof derivedwoodinessandannualhabitevolvedinafricanumbellifersasalternativesolutionsforcopingwithdrought