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Adaptation and Constraint in the Plant Reproductive Phase
Stockholm University, Faculty of Science, Department of Botany.
2004 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Conservatism is a central theme of organismic evolution. Related species share characteristics due to their common ancestry. Some concern have been raised among evolutionary biologists, whether such conservatism is an expression of natural selection or of a constrained ability to adapt.

This thesis explores adaptations and constraints within the plant reproductive phase, particularly in relation to the evolution of fleshy fruit types (berries, drupes, etc.) and the seasonal timing of flowering and fruiting. The different studies were arranged along a hierarchy of scale, with general data sets sampled among seed plants at the global scale, through more specific analyses of character evolution within the genus Rhamnus s.l. L. (Rhamnaceae), to descriptive and experimental field studies in a local population of Frangula alnus (Rhamnaceae). Apart from the field study, this thesis is mainly based on comparative methods explicitly incorporating phylogenetic relationships. The comparative study of Rhamnus s.l. species included the reconstruction of phylogenetic hypotheses based on DNA sequences.

Among geographically overlapping sister clades, biotic pollination was not correlated with higher species richness when compared to wind pollinated plants. Among woody plants, clades characterized by fleshy fruit types were more species rich than their dry-fruited sister clades, suggesting that the fleshy fruit is a key innovation in woody habitats. Moreover, evolution of fleshy fruits was correlated with a change to more closed (darker) habitats.

An independent contrast study within Rhamnus s.l. documented allometric relations between plant and fruit size. As a phylogenetic constraint, allometric effects must be considered weak or non-existent, though, as they did not prevail among different subclades within Rhamnus s.l. Fruit size was correlated with seed size and seed number in F. alnus. This thesis suggests that frugivore selection on fleshy fruit may be important by constraining the upper limits of fruit size, when a plant lineage is colonizing (darker) habitats where larger seed size is adaptive.

Phenological correlations with fruit set, dispersal, and seed size in F. alnus, suggested that the evolution of reproductive phenology is constrained by trade-offs and partial interdependences between flowering, fruiting, dispersal, and recruitment phases. Phylogenetic constraints on the evolution of phenology were indicated by a lack of correlation between flowering time and seasonal length within Rhamnus cathartica and F. alnus, respectively. On the other hand, flowering time was correlated with seasonal length among Rhamnus s.l. species. Phenological differences between biotically and wind pollinated angiosperms also suggested adaptive change in reproductive phenology.

Abstract [sv]

Äpplet faller inte långt från trädet. Men varför? Den biologiska mångfalden präglas i stor utsträckning av fylogenetiskt bevarade karaktärsdrag; närbesläktade arter är lika. Det pågår en diskussion bland evolutionsbiologer om i vilken utsträckning denna konservatism är ett resultat av naturlig selektion eller av en begränsad anpassningsförmåga.

Denna avhandling diskuterar begreppet evolutionära begränsningar i relation till den reproduktiva fasen hos växter. I fokus ligger särskilt evolutionen av bärliknande (endozoochora) frukter respektive evolutionen av säsongsmässiga mönster (fenologi) för blomning och fruktsättning. Avhandlingen är hierarkiskt organiserad så att olika delstudier gjordes på olika skalnivåer: fenologi- och fruktevolution analyserades för fröväxter respektive gömfröiga växter; inom brakvedssläktena Rhamnus och Frangula (Rhamnaceae); samt för en lokal population av brakved (Frangula alnus). Populationsstudien baserades på såväl experimentella som deskriptiva data, medan övriga studier i huvudsak genomfördes med fylogenetisk komparativ metodik baserade på litteraturdata. Som en del av de komparativa studierna rekonstruerades fylogenetiska hypoteser för Rhamnus s.l. utifrån DNA-sekvenser (ITS, trnL-F), vilka gav stöd för att Frangula och Rhamnus är monofyletiska systersläkten.

I en biogeografiskt kontrollerad fylogenetisk kontrastanalys upptäcktes inga skillnader i artrikedom mellan djur- och vindpollinerade växter. Bärliknande frukter verkar dock vara en betydelsefull karaktär (key innovation) i skogsmiljöer. För det första var fylogenetiska klader med bärliknande frukter mer artrika än systerklader med torra frukter. Dessutom var uppkomster av bärliknande frukt korrelerad till habitat med mer sluten vegetation.

En fylogenetisk kontrastanalys av allometriska effekter visade på en positiv korrelation mellan växtindividens och fruktens storlek inom Rhamnus s.l. Upprepade analyser av dessa allometriska samband i olika monofyletiska subklader inom Rhamnus s.l. indikerar dock att allometri, såsom evolutionär begränsning, är svag. I populationsstudien av F. alnus var fruktstorlek positivt korrelerad till såväl fröantal som frövikt. En generell hypotes utifrån denna avhandling blir därför att frugivorer (de djur som äter bären och därmed sprider växtens frön) utövar ett starkt selektionstryck på växter som koloniserar ett habitat där fröstorlek är adaptivt, eftersom fruktstorlek påverkar frugivorernas (ssk. fåglars) sätt att hantera frukten.

Reproduktiv fenologi var korrelerad till fruktsättning, fröspridning och fröstorlek hos F. alnus. Detta stödjer tanken att evolutionen av blomnings- och fruktsättningstider begränsas av avvägningar (trade-offs) och partiella beroenden mellan blomning-, fruktsättnings-, spridnings och rekryteringsfaserna. Inomartsvariation i blomningstid för F. alnus respektive getapel (Rhamnus cathartica) över en nordeuropeisk latitudinell transekt var inte korrelerad till säsongslängd, vilket antyder att utvecklingen av blomningstider är evolutionärt begränsad. Å andra sidan påvisades en sådan korrelation mellan blomningstid och säsongslängd i en mellanartsstudie inom Rhamnus s.l. Den fylogenetiska kontrastanalysen mellan djur- och vindpollinerade växter visade också på adaptiva skillnader i fenologi. Blomningstiderna inom en klad med biotiskt pollinerade arter var mer åtskilda än inom den vindpollinerade systerkladen, och den välkända iakttagelsen att vindpollinerade träd blommor tidigare på säsongen fick även stöd i ett fylogenetiskt komparativt perspektiv.

Place, publisher, year, edition, pages
Stockholm: Botaniska institutionen , 2004. , 175 p.
Keyword [en]
phenology, fleshy fruits, phylogenetic comparative methods, phylogenetic constraints, Rhamnus, Frangula, Frangula alnus, key innovations, allometry, diversity, phylogeny, seed size, frugivory, germination, recruitment
National Category
Ecology
Identifiers
URN: urn:nbn:se:su:diva-99ISBN: 91-7265-856-8 (print)OAI: oai:DiVA.org:su-99DiVA: diva2:200799
Public defence
2004-05-03, föreläsningssalen, Botanicum, Lilla Frescativägen 5, Stockholm, 10:00
Opponent
Supervisors
Available from: 2004-04-08 Created: 2004-04-08Bibliographically approved
List of papers
1. Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms
Open this publication in new window or tab >>Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms
2003 In: Evolution, ISSN 0014-3820, Vol. 57, no 9, 2001-2011 p.Article in journal (Refereed) Published
Identifiers
urn:nbn:se:su:diva-25914 (URN)
Note
Part of urn:nbn:se:su:diva-99Available from: 2004-04-08 Created: 2004-04-08Bibliographically approved
2. Fleshy fruits – origins, niche shifts, and diversification.
Open this publication in new window or tab >>Fleshy fruits – origins, niche shifts, and diversification.
2005 (English)In: Oikos, ISSN 0030-1299, E-ISSN 1600-0706, Vol. 109, no 2, 255-272 p.Article in journal (Refereed) Published
Abstract [en]

We examined shifts in fruit type, fleshy vs non-fleshy, in relation to habitat-related niche shifts, species richness, and historical distribution, in 50 phylogenetically independent plant lineages. Each lineage consisted of a sister-group pair of fleshy vs non-fleshy taxa and their outgroup. Niche shifts were assessed based on plant community characteristics. Two niche dimensions assumed to reflect community dynamics were derived: spatial predictability of disturbances and canopy closure. Phylogenetically independent origins of fleshy fruit types (1) were correlated with changes to habitats characterized by more shaded and spatially more unpredictable disturbances, (2) had an opposite effect on species richness in woody and herbaceous clades, enhancing species richness in woody clades, and (3) were continuously distributed over a period covering the last 70 million years. These results support the hypothesis that fleshy fruit evolution is driven by vegetation dynamics, and suggest that the strength of frugivore mediated selection on fleshy fruits increases when recruitment sites are spatially unpredictable and/or characterized by low light conditions.

National Category
Natural Sciences
Identifiers
urn:nbn:se:su:diva-25915 (URN)10.1111/j.0030-1299.2005.12663.x (DOI)
Note
Part of urn:nbn:se:su:diva-99Available from: 2004-04-08 Created: 2004-04-08 Last updated: 2017-12-13Bibliographically approved
3. Generic limits in Rhamnus s.l. L. (Rhamnaceae) inferred from nuclear and chloroplast DNA sequence phylogenies.
Open this publication in new window or tab >>Generic limits in Rhamnus s.l. L. (Rhamnaceae) inferred from nuclear and chloroplast DNA sequence phylogenies.
2004 (English)In: Taxon, ISSN 0040-0262, E-ISSN 1996-8175, Vol. 53, no 2, 383-390 p.Article in journal (Refereed) Published
Abstract [en]

This study tested the monophyly of the previously proposed genera Alaternus, Frangula, Oreoherzogia, and Rhamnus s.str., and the phylogenetic relations suggested by Grubov (1949), within the Rhamnus s.l. clade.Based on a global sample of 22 species, we derived phylogenetic hypotheses using parsimony analysis of variation in trnL-F (chloroplast) and ITS (nuclear) DNA regions. Both Alaternus, Frangula, and Oreoherzogia gained strong support, and our results further support recognition of Frangula as a monophyletic genus. The resolution between Alaternus, Oreoherzogia, and the rest of Rhamnus s.str. was less clear, and the mainly Mediterranean Oreoherzogia was strongly grouped with the American R. crocea. Therefore, we consider it as unjustified to split the rest of Rhamnus into smaller genera. Regarding Grubov's phylogenetic hypothesis, our study could only support the dichotomy between Frangula and the rest of Rhamnus.

Place, publisher, year, edition, pages
International Association for Plant Taxonomy, 2004
Keyword
ALATERNUS; FRANGULA; ITS; NORTHERN HEMISPHERE; OREOHERZOGIA; PARSIMONY; TRNL-F
National Category
Botany
Identifiers
urn:nbn:se:su:diva-25916 (URN)
Note
Part of urn:nbn:se:su:diva-99Available from: 2004-04-08 Created: 2004-04-08 Last updated: 2017-12-13Bibliographically approved
4. Constraints, conservatism and adaptation in the evolution of fleshy fruits and flowering phenology of Rhamnus s.l. (Rhamnaceae).
Open this publication in new window or tab >>Constraints, conservatism and adaptation in the evolution of fleshy fruits and flowering phenology of Rhamnus s.l. (Rhamnaceae).
Article in journal (Refereed) Submitted
Identifiers
urn:nbn:se:su:diva-25917 (URN)
Note
Part of urn:nbn:se:su:diva-99Available from: 2004-04-08 Created: 2004-04-08Bibliographically approved
5. Phenology and ovule fate in Frangula alnus (Rhamnaceae) – interdependence or decoupling of flowering, fruiting, dispersal, and early recruitment phases?
Open this publication in new window or tab >>Phenology and ovule fate in Frangula alnus (Rhamnaceae) – interdependence or decoupling of flowering, fruiting, dispersal, and early recruitment phases?
Manuscript (Other academic)
Identifiers
urn:nbn:se:su:diva-25918 (URN)
Note
Part of urn:nbn:se:su:diva-99Available from: 2004-04-08 Created: 2004-04-08 Last updated: 2010-01-13Bibliographically approved

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