Download Adaptation and Constraint in the Plant Reproductive Phase Department of Botany

Adaptation and Constraint in the Plant Reproductive Phase
Kjell Bolmgren
Department of Botany
Stockholm University
Stockholm
2004
Adaptation and constraint in the plant reproductive phase
ISBN: 91-7265-856-8, pp. 1-46
© Kjell Bolmgren 2004
Cover design by Torsten Hild (www.2hild.com)
Cover photo © LSH foto Samuel Uhrdin (’Vertumnus’ by Guiseppe Arcimboldo, 1527-1593)
Jannes Snabbtryck Kuvertproffset HB
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Kjell Bolmgren
Doctoral dissertation 2004
Kjell Bolmgren
Department of Botany
Stockholm University
SE-106 91 Stockholm
Sweden
Adaptation and Constraint in the Plant Reproductive Phase
Abstract — 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.
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Adaptation and constraint in the plant reproductive phase
Den halvfärdiga himlen av Tomas Tranströmer 1962
Modlösheten avbryter sitt lopp.
Ångesten avbryter sitt lopp.
Gamen avbryter sin flykt.
Det ivriga ljuset rinner fram,
även spökena tar sig en klunk.
Och våra målningar kommer idagen,
våra istidsateljéers röda djur.
Allting börjar se sig omkring.
Vi går i hundratals.
Var människa en halvöppen dörr
som leder till ett rum för alla.
Den oändliga marken under oss.
Vattnet lyser mellan träden.
Insjön är ett fönster mot jorden.
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Kjell Bolmgren
Acknowledgments
Jag har en svaghet. Jag misstror mina närmastes uppmuntrande ord. Som om de bara
vill vara vänliga. Därför, med eftertryck:
Lott, tack för att du förväntade dig något märkvärdigt av mig.
Ove, tack för ditt obegripliga lugn. Det har vid upprepade tillfällen varit en förutsättning för att jag inte skulle lämna skutan, liksom din ständiga beredskap med och kvalitén i den röda pennan. Tack för att du lät mig gå min väg.
Tack Bengt för att du, trots mitt eviga kvacksalvande och vänsterhandsfipplande, alltid
fick konkreta saker att hända.
Mikael Mildén, Heléne Fröborg, Regina Lindborg, Sara Cousins (frustrationsklubben)
— ni har varit den ventil jag så ofta behövt . Tack.
Åsa Eriksson, Petra Korall och Didrik Vanhoenacker — ni var räddande änglar i för
mig mycket kritiska lägen. Tack.
Jens Klackenberg och Thomas Karlsson vid Naturhistoriska riksmuséet öppnade en ny
värld för mig. Stort tack.
A special thanks to Arndt Hampe, my brother-in-Frangula, and to Peter Linder for an
encouraging cooperation.
Många arbetskompisar på avdelningen har varit oersättliga diskussionskamrater om
allt från krig och fred till samplingsmetodik, och alla på avdelningen har varit viktiga
för den hjälpsamma atmosfär som varit en förutsättning för att jag skulle kunna tänka
det jag tänkt. Tack alla.
Ett särskilt tack till Thord Fransson för att du tog hand om mig trots att jag var mer
intresserad av fågelskiten än av fåglarna, till Patrik Lindenfors, Patrik Dinnetz och
Kari Lehtilä för att ni varit generösa med att diskutera mina metodologiska bryderier,
till Johan Ehrlén för att man kan lita på att du är skeptisk, till Katariina KiviniemiBirgersson för att man kan lita på att du tycker det är kul, till Lenn Jerling och Peo
Karis för att era dörrar alltid stått öppna och till Niklas Wikström, Hans-Erik Wanntorp och Torsten Eriksson för alla lunchdiskussioner.
Jenny Smedmark, Moa Holmlund, Anna Koffman, Nahid Heidari, Reija Dufva, Johan
Lind, Cilla Kullberg och Martin Starvander har UV-bestrålat pollenslangar, samlat
litteraturdata, översatt ryska texter, sekvenserat DNA, fångat fåglar och gjort mycket
annat som jag inte haft kompetens för. Stort tack.
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Adaptation and constraint in the plant reproductive phase
Contents
Summary
3
Acknowledgments
List of papers
5
Preface
9
Introduction
Adaptation and Constraint
The Plant Reproductive Phase
Objectives and Approach
Methods
Phylogenies and Comparative Biology
Data collection
Results
Discussion
Literature cited
Svensk sammanfattning
Appendix I—V
6
7
10
11
15
18
19
19
23
25
32
38
45
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Kjell Bolmgren
List of papers
This thesis is based on five separate studies listed below. They will be referred to by
their Roman numbers. The published papers are reprinted with the kind permission of
the publishers.
I
Bolmgren, K., O. Eriksson, and H. P. Linder. 2003. Contrasting flowering phenology and species richness in abiotically and biotically pollinated angiosperms. Evolution 57:2001-2011.
II
Bolmgren, K. and O. Eriksson. Fleshy fruits – origins, niche shifts,
and diversification.
III
Bolmgren, K. and B. Oxelman. in press. Generic limits in Rhamnus s.l.
L. (Rhamnaceae) inferred from nuclear and chloroplast DNA sequence
phylogenies. Taxon (in press).
IV
Bolmgren, K. Constraints, conservatism and adaptation in the evolution
of fleshy fruits and flowering phenology of Rhamnus s.l. (Rhamnaceae).
V
Bolmgren, K. and O. Eriksson. Phenology and ovule fate in Frangula
alnus (Rhamnaceae) – interdependence or decoupling of flowering,
fruiting, dispersal, and early recruitment phases?
In all papers, I performed the studies and wrote the manuscripts. In paper I and V, I
also developed the ideas, while the study in paper II was developed together with OE.
In paper III, I developed the study, while BO guided the PAUP analyses.
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Adaptation and constraint in the plant reproductive phase
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Kjell Bolmgren
Preface
At the core of evolutionary biology is the discussion about adaptations and adaptability. In a way this discussion is an analogue to the philosophical discussion about freedom and the free will, including the Nature vs. Nurture debate. To what extent are you
free? What forces restrain the manifestation of the free will? How strong are these
forces? One could even argue that evolutionary studies on the ability of organisms to
respond and adapt to local conditions are fundamental to our understanding of freedom
as a concept.
Are organisms free to adapt to the conditions they meet? To what extent does
the evolutionary history constrain adaptability? How much of an organism or the characteristics of an organism manifest adaptations to the local conditions under which
they live their lives, and how much are due to phylogenetic constraints? Are manifestations of phylogenetic constraints and local adaptation mutually exclusive?
The present thesis emanated from the hypothesis that autumn migrating seed
dispersing birds exert a selection pressure for fruiting time on fleshy fruited plants. A
preliminary literature survey found that the evolution of phenology and fleshy fruits
were considered phylogenetically constrained and that frugivores were considered too
weak a selective agent to drive fleshy fruit evolution. These ideas served as stimulus to
develop a couple of studies which revolved around constraints, conservatism, and
adaptations.
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Adaptation and constraint in the plant reproductive phase
Introduction
Diversity and conservatism characterize the evolution of organisms. Variation in behaviour and form is perhaps the strongest impression of life, but conservatism is an
equally important part of evolution; roses are roses, tulips are tulips, and anemones are
anemones. No matter how different they are, we have generally no problem in recognizing related taxa. These two sides of life, diversity and conservatism, corresponds
with the “two great laws — Unity of Type and the Conditions of Existence” (Darwin
1859, p. 233) that shape organisms. Unity of Type is a pre-Darwinian concept referred
to Cuvier, which Darwin (1859, p. 233) transformed into his own concept unity of
descent.
It is of course tempting, considering the astonishing biological diversity, to
suggest that organisms attain any form (necessary) through the work of natural selection; freezing bats, animal-eating plants, flying mammals, glass-eating lichens, nonswimming fishes, deep-sea-living mammals, individual fungi covering hundreds of
kilometres, and plants living for hundreds of years — “I’m simply saying that … life
finds a way”, as Jeff Goldblum alias Dr. Malcolm stated in Jurassic Park. JeanBaptiste de Monet de Lamarck, who was the first to develop a coherent theory on
adaptive evolution, even believed that the adaptive ability of organisms was so developed that extinction was not an issue; each species develops into a new species
(Bergström 1993; Brooks and McLennan 2002). Today we consider the character
complex of an organism as anachronistic and, at least from a reductionist view, not at
all optimally adapted to local conditions.
A previous underestimation of constraints on adaptation, particularly effects of
unity of descent, and an interpretative precedence given to adaptive explanations, got
the pendulum swinging during the seventies. Starting with the sociobiology debate,
evolutionary biologists got involved in a development shifting the focus from local
adaptations to effects related to the organisms’ phylogenetic history (Gould and Lewontin 1979). The research field ’comparative biology’, explicitly incorporating phylogenetic information, expanded rapidly, which lead to a critical examination of which
questions that could (should?) be asked (Wanntorp 1983), important insights on statistical issues (Felsenstein 1985), and, in relation to this thesis, an interest in non-
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Kjell Bolmgren
adaptive interpretations of organismic features and which characteristics that constrain
the adaptability of these features.
Adaptation and Constraint
Adaptations are features that have evolved by natural selection. That is, an adaptation
is a heritable characteristic that have replaced other variants of the character in the
population, as it yielded a superior increase of (inclusive) fitness. Phylogenetic definitions of adaptations include the somewhat controversial part that the feature should be
a phylogenetic novelty. This highlights a difference between adaptation as a process
and adaptation as a feature. Adaptation may be an ongoing process where a trait is
conserved owing to stabilizing selection, but, according to the phylogenetic definition
of adaptations, no novel features and thus no adaptations arise during such processes.
Whether one should call traits that are phylogenetically conserved through stabilizing
selection an adaptation or not, could just have been a matter of semantics, but the development of an intimate relationship between parsimony criteria and non-adaptive
interpretations have stirred up a debate on these issues (Westoby et al. 1995).
Conserved characters have played an essential role in this debate. The explicit
use of phylogenetic information in comparative biology has, as expected, confirmed
that a majority of characteristics of an organism are conserved in a phylogenetic context. It is generally acknowledged among evolutionary biologists, that present character states express a compromise between local adaptation and phylogenetic history, but
when it comes to conserved traits this balanced view has shifted in favour of phylogenetic ‘explanations’, stating ‘no change – no process’. The rationale for such views is
parsimony. Phylogenetic patterns of conserved characters do not reveal, though,
whether the conserved traits are actively maintained by selection or if they have been
conserved because they are fixed parts of the organism. In the special case of discrete
characters, it is understandable how such a line of ‘no change–no process’ reasoning
has come about. However, considering quantitative characters, for which equally
strong phylogenetic conservatism is expected, the suggestion of constrained evolution
becomes unreasonable (Westoby et al. 1995). For example, despite a large withingroup variation, Kochmer and Handel (1986) and Hodgson and Mackey (1986), respectively, interpreted significant phylogenetic effects (sensu unity of descent, see
Derrickson and Ricklefs 1988) as if character evolution was constrained. Such reason-
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Adaptation and constraint in the plant reproductive phase
ing implicitly defines phylogenetic and adaptive explanations as mutually exclusive
alternatives, and equalizes phylogenetic constraints with phylogenetic effects.
That phylogenetic history restrains the adaptability of an organism is generally
acknowledged; the lineage-specific heritage is part of the unique conditions of existence shaping each organism. Therefore, the evolutionary pathways available for each
organism are also unique and limited. Conserved characters have been understood as a
typical example of such phylogenetic ballasts, owing to the fact that in a world that is
generally perceived to be continuously changing, conserved characters are not what is
expected if adaptation is a dominant process. Taken a step further, phylogenetically
conserved characters have been classified as phylogenetically constrained. In fact,
constraint (historical, phylogenetic, or evolutionary) seem to have been the common
term when characterizing evolution of conserved characters in the aftermath of Gould
and Lewontin (1979). Once again, this could have been merely a question of semantics, but as phylogenetic explanations were often used as mutually exclusive, nonadaptive alternatives to adaptive explanations, the conception of conserved characters
being constrained has been substantially criticized. Adaptive processes may equally
well maintain conserved characters (Westoby et al. 1995), and one of these adaptive
processes, phylogenetic niche conservatism (Harvey and Pagel 1991; Lord et al.
1995), will be of particular interest in this thesis.
Phylogenetic niche conservatism (PNC) is based on the idea that the selective
milieu is not as dynamic as one might believe. All taxa in a local species pool will not
have equal opportunities in exploiting an adjacent novel niche space. Those taxa
adapted to a preceding niche space most similar to the novel conditions is expected to
be the ones that successfully exploit the novel niche space. As the novel niche space is
similar to preceding conditions for these taxa, the character complex of the exploiting
taxa will appear generally conserved, according to the PNC hypothesis. Major directional, adaptive changes will then only take place when there are major changes in the
selective milieu (extinctions, island colonization, climatic change; cf punctuated equilibrium). Thus, PNC diverges from phylogenetic constraints by not invoking intrinsic,
lineage-specific obstacles for adaptation, suggesting that conserved characters persist
due to prevailing adaptive values (Ackerly and Donoghue 1995; Westoby et al. 1995).
The potential importance of phylogenetic niche conservatism does not mean, of
course, that phylogenetic constraints are unimportant, it just illustrates that phylogeny
is not a constraint. To be able to separate between phylogenetic niche conservatism
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Kjell Bolmgren
and phylogenetic constraints, claims of phylogenetic constraints must be based on
more mechanistic evidence (Antonovics and van Tienderen 1991).
The common meaning of the word constrain is synonymous to limit and restrain, and a feature is constrained when it is forced, uneasy, or unnatural (!) according
to an Oxford dictionary. So, can life be unnatural? In fact, along with adaptive change
and genetic drift, constraint is one of the characteristics of organismic evolution, in the
sense that “yesterday’s adaptation may become tomorrow’s constraint”1. Such all
encompassing use of the concept of constraint is of little value to operational studies of
evolutionary constraints (Stearns 1986; Gould 1989). Further, a casual use of phylogenetic constraints (PC) as a non-adaptive fall-back explanation has accumulated much
critique of the concept (Stearns 1986; Gould 1989; Antonovics and van Tienderen
1991; Westoby et al. 1995), and during the last decade some necessary development of
the concept has taken place (Antonovics and van Tienderen 1991; Edwards and
Naeem 1993; McKitrick 1993; Miles and Dunham 1993; Schwenk 1995; Burt 2001;
Blomberg and Garland 2002).
McKitrick suggested that a PC is “any result or component of the phylogenetic
history of a lineage that prevents an anticipated course of evolution in that lineage”
(McKitrick 1993). An important aspect of this definition is the explicit requirement of
a specified anticipated course of evolution, meaning that claims of PC does not have
an interpretative precedence over, for example, phylogenetic niche conservatism if
both the character and the selective milieu are conserved (Figure 1). Miles and
Dunham (1993) further emphasized that PC does not necessarily concern a conservation of character states (Figure 1). If the variation of two or more traits are linked, an
adaptive change in one character, may lead to a forced, non-adaptive change in another, linked character even if the selective milieu is conserved in relation to this character (Figure 1). This is an important point, as several authors have only considered
PC in relation to conserved characters (e.g. Burt 2001). Schwenk (1995) divided conserved characters into two classes based on whether (stabilizing) selection or nonselection processes are responsible for the conservatism, and suggested that “a useful
conception of evolutionary constraint (PC) must exclude natural selection as a causation agent” (Schwenk 1995, p. 254). Schwenk’s definition thereby implies that characters that are conserved due to opposing selection pressures do not represent examples
1
This expression is used in several texts without reference to an original source. McKitrick (1993) cites a
manuscript in press, which has never been published as far as I know.
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Adaptation and constraint in the plant reproductive phase
SELECTIVE MILIEU
conserved
changed
PHYLOGENETIC
CONSTRAINTS
conserved
PHYLOGENETIC NICHE
CONSERVATISM
TRAIT
changed
PHYLOGENETIC
CONSTRAINTS
PHYLOGENETIC
CONSTRAINTS
ADAPTATION
Figure 1. An illustration of how phylogenetic niche conservatism, phylogenetic constraints, and adaptation are defined and relate to each other. A classification like this may add to the polarized view of
phylogenetic versus adaptationist explanations of character evolution that is common in the literature.
Therefore, I would like to stress that many characters are likely to express both phylogenetic constraints
and recent adaptation (Westoby et al. 1995; Orzack and Sober 2001). (Paper IV)
of phylogenetically constrained evolution. So, which are the non-selective mechanisms
that can generate phylogenetic constraints?
Allometry, trade-offs (developmental processes), and pleiotropy (a genetic
process) are mechanisms generally proposed to lead to phylogenetically constrained
character evolution. Lack of genetic variation is not considered a PC. It is the mechanism, preventing or reducing genetic or phenotypic variation, that is a PC. In conclusion, to claim that phylogenetic constraints are responsible for the evolutionary (or
lack of) response in a character, one must show that a sufficient directional selection
does not develop into an anticipated response due to a defined constraining mechanism
(Antonovics and van Tienderen 1991). An additional criteria is that the anticipated
adaptive response must appear in the phylogenetic sister clade lacking the suggested
constraining feature (Stearns 1992). None of these definitions and criteria suggest that
PC:s are unbreakable, and all of them emphasize that PC:s concern the evolution of
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Kjell Bolmgren
characters, not organisms. This focus on characters cut off the research field on key
innovations from the field of phylogenetic constraints.
Key innovations — In correspondence with the more liberal definitions of phylogenetic constraints, key innovations have been suggested as an explanation for comparatively high diversification rates in certain clades. Key innovations are phylogenetic
novelties leading its descendents into a new niche space and thus deliberating the organisms from ancestral, constraining characteristics. For example, the extraordinary
species richness of angiosperms, beetles, and passerines, have risen the question
whether the evolution of specific features can explain why these clades expanded more
than their related clades. Regarding angiosperm radiation, biotic pollination, biotic
dispersal, herbaceousness, and a short juvenile phase, are some of the features that
have been suggested as such key innovations (Stebbins 1981; Crepet 1984; Tiffney
1984; Eriksson and Bremer 1992; Dodd et al. 1999; Verdu 2002). Originally, the concept of key innovations was used in relation to singular evolutionary radiations, as the
examples above, and this approach has rendered the concept severe critique from both
statistical and phylogenetic points of view (Raikow 1986). Considering this critique,
the operational applications of the key innovation concept has been related more to
convergent evolution (Mitter et al. 1988; Eriksson and Bremer 1992; McKitrick 1993;
Miles and Dunham 1993; Dodd et al. 1999; Verdu 2002), that is, to analyse if phylogenetically independent origins of functionally analogous features have led to comparatively higher species richness. I use this approach here, when examining the effect
of pollination syndromes and fruit types on species richness (paper I and II).
The Plant Reproductive Phase
The plant reproductive phase encompasses the development of flowers (incl. ovules
and pollen) and fruits (incl. seeds). Along with the evolution of herbaceousness and a
short juvenile phase, biotic pollination and biotic seed dispersal have been suggested
to be responsible for much of angiosperm diversification (Grant 1949; Stebbins 1981;
Crepet 1984; Eriksson and Bremer 1992; Ricklefs and Renner 1994; Dodd et al. 1999;
Verdu 2002). Thus, many characteristics of the plant reproductive phase have been
subjected to evolutionary studies. This thesis deals with adaptations and constraints in
the evolution of two plant reproductive features: phenology and fleshy fruits.
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Adaptation and constraint in the plant reproductive phase
Phenology — The temporal distribution of flowers and fruits have been considered a
potential part of the reproductive isolating mechanisms leading to speciation in angiosperms (Snow 1965; Carpenter 1976; Stiles 1977; Waser 1983). Thus, phenological
niche structure, but also other aspects of phenology, have gained considerable attention (Robertson 1895; Robertson 1924; Clausen et al. 1948; Slade et al. 1975; Thompson and Willson 1979; Primack 1980; Thomson 1980; Augspurger 1981; Rabinowitz
et al. 1981; Kochmer and Handel 1986; Eriksson and Ehrlén 1991; Fuentes 1992; Pico
and Retana 2000; Oberrath and Bohning-Gaese 2002; Lacey et al. 2003; Rathcke
2003; for reviews, see Primack 1985; Rathcke and Lacey 1985; Primack 1987; Ollerton and Lack 1992; Gotelli and Graves 1996; Fenner 1998). Phenology has also been,
and probably originated as, a major subject in agri- and silviculture. The economic
importance of predicting phenological events (e.g. time of harvesting) and foreseeing
the local match between local conditions and the phenology of commercial genotypes,
have initiated a huge number of studies correlating phenology to climatic conditions.
These issues have gained renewed interest, also within ecology, due to Global Change.
The phenological strategy of a plant shall potentially attract pollinators and
seed dispersers, satiate predators and herbivores, effect cross-pollination, deal with
varying abiotic (e.g. climatic) conditions within and between seasons, and withstand
competition from co-appearing plant species. In north temperate conditions, plants
must also deal with a short reproductive season.
The basic issue in evolutionary plant reproductive phenology deals with the
seasonal position of a phenological event, that is, the timing of the event. For example,
Linnaeus’ altruistic, pre-Darwinian suggestion was that the seasonal sequence of flowering has come about so that “these hundreds of plants shall be spared from causing
each other harm” (Linnaeus 1760, p. 135). Today we consider all aspects of the temporal distribution of flowering and/or fruiting resources as parts of a plant’s phenological
strategy. That is, not only the position of the phenological curve, but also its shape is
considered evolvable traits (Thomson 1980; Eriksson 1995). Such aspects of evolutionary phenology is further strengthened by the insight that a phenological curve is
probably a compromise both between different selection pressures within the phenophase, as well as between selection pressures acting in different phenophases that are
more or less interdependent. It seems quite obvious that the evolution of flowering and
fruiting curves evolve more or less in concert (Primack 1987). These interdependences
may create counteracting selection pressures on reproductive phenology traits. More-
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Kjell Bolmgren
over, several authors have suggested that flowering and fruiting phenology may be
phylogenetically constrained (Bell and Stephens 1984; Kochmer and Handel 1986;
Johnson 1993; Jordano 2000), though without defining any constraining mechanism.
Fleshy fruits and frugivory — The germination, seedling, and early juvenile phase is
considered the most critical phase in the plant life cycle (Grubb 1977), suggesting that
improved seed dispersal may have a major impact on plant fitness. The evolution of
fleshy fruits have basically been attributed to three different, though not mutually
exclusive, ideas. First, frugivory may facilitate dispersal away from the mother plant,
reducing density-dependent offspring mortality. Second, the exploitation of animal
movements suggests that seeds are dispersed in a non-random pattern, potentially to
favourable recruitment sites as, for example, forest clearings and forest margins. Third,
gut passage may improve germination.
Irrespective of which hypothesis that is correct, fleshy fruits must attain the
right size, form, and content (nutrient, water and seeds), and appear at the right time to
attract effective dispersers. Based on such hypotheses, two decades of plant-frugivore
research have failed to find general support for a close match between frugivore and
plant characteristics (Jordano 2000; Herrera 2002b; but see Mazer and Wheelwright
1993; Noma and Yumoto 1997; Rey et al. 1997; Wenny and Levey 1998), and therefore fleshy fruit evolution has been considered phylogenetically constrained (Jordano
1995a). As an exception, fleshy fruit size has been considered the only fruit character
that may have been adapted to local seed dispersing frugivore assemblages and thus
not phylogenetically constrained (Wheelwright 1985; Mack 1993; Sallabanks 1993;
Jordano 1995a; Jordano 1995b; Herrera 2002b; Lord et al. 2002).
Considering the coarse but general observation that there are correlations between seed size, endozoochorous seed dispersal, and high statured vegetation (Willson
et al. 1990; Hughes et al. 1994), two additional hypotheses on fleshy fruit evolution
have developed. Herrera (2002a) suggested that allometric constraints may be important in governing fleshy fruit size evolution. That fleshy fruit size variation should be a
result of selection on other size traits, does not explain the evolution of fleshiness per
se, but, assuming that larger seeds disperse shorter distances, dispersal attributes, as
fleshiness, may evolve to compensate for the dispersal loss. Such a scenario does not
require a close match between frugivore and fruit characteristics. The second additional hypothesis, suggests a similar line of evolution, though it is not based on developmental constraints. In areas or times where dense vegetation predominates, for ex-
17
Adaptation and constraint in the plant reproductive phase
ample due to warmer climate, selection may act for both higher stature and larger
seeds to cope with intensified competition for light. Under these conditions, both dispersal away from density-dependent mortality and to light gaps may be a rationale for
evolving fleshiness. This potentially climate driven evolution of fleshy fruits has
sometimes been combined with an observation of conserved fruit traits (Jordano
1995a) to suggest that fleshy fruits in most taxa evolved during a limited period of
global warming in the Early Tertiary (Tiffney 1984; Jordano 1987; Herrera 1992;
Jordano 1995a; Eriksson et al. 2000).
Objectives and Approach
In this thesis I have studied adaptations and constraints in the evolution of reproductive phenology and fleshy fruits. A basic objective has been to challenge previous
claims that the evolution of both phenology (Kochmer and Handel 1986; Fenner 1998)
and fleshy fruits (Jordano 1995a; Jordano 2000; Herrera 2002b; Herrera 2002a) are
phylogenetically constrained. My approach has been to examine reproductive phenology and fleshy fruits at a hierarchy of levels, from experimental and descriptive examinations of local populations, through comparative studies using reconstructed phylogenetic hypotheses of a genus, up to comparative studies based on data sets sampled
among all seed plants at the global scale. More explicitly stated, I have examined:
anticipated courses of phenology evolution in relation to pollination systems (paper I)
and climatological gradients (paper IV); anticipated courses of fleshy fruit evolution in
relation to habitat characteristics and growth form (paper II); allometry as a phylogenetic constraint on fleshy fruit size evolution (paper III and IV); simultaneously acting
selection pressures on reproductive phenology (paper V); the strength of phylogenetic
constraints (paper III and IV); and whether biotic pollination and fleshy fruit types
may be considered key innovations (paper I and II).
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Kjell Bolmgren
Methods
The hierarchical approach structuring this thesis is based on some obvious points;
specific questions must be addressed at the right level; experimental studies are not
possible at a general level; general claims must be supported by general samples; etc.
In paper I and II, I challenged previous claims concerning flowering times of biotically
pollinated plants (Kochmer and Handel 1986) and fleshy fruit evolution (Tiffney 1984;
Jordano 1995a; Eriksson et al. 2000), and thus sampled among angiosperms and seed
plants, respectively. High level studies like these have the potential to provide more
interesting results in the sense that they suggest character complexes that are adaptive
and persistent in evolutionary time. On the other hand, conclusions about processes
governing the observed patterns can only be speculative at this level. In paper III and
IV, I explored the phylogeny and character evolution within the monophyletic clade
Rhamnus s.l. L. Such intermediate level studies allow more highly resolved phylogenies and a closer knowledge of the studied species, making more detailed interpretations
(or speculations) of the evolutionary patterns possible. Finally, low level (local) studies gave the opportunity for experiments and detailed descriptive work on different
selection pressures working within and between phenological phases. At this level it
was also possible to examine the interphase between phenology and fruit and seed
characteristics in one fleshy fruited plant species. The drawback of these fine-grained
studies are that they are sensitive to fluctuating conditions, may suggest irrelevant
(evolutionary) patterns (Ehrlén 2003), or only be able to document inconsistent patterns (Herrera 1998).
Phylogenies and Comparative Biology
Interspecific comparisons is an essential tool in evolutionary biology. Incorporating
explicit geneaological information into such studies have highlighted the issue of statistical independence. Closely related species have a common history sharing ancestral
traits, which implies that information on, for example, present character correlations in
a number of species may not be founded on statistically independent observations. If
phylogenetic hypotheses are considered in the sampling procedure, comparative stud-
19
Adaptation and constraint in the plant reproductive phase
ies may be based on independent observations. Further, the explicit application of
phylogenetic information allowed for an examination of whether patterns of phylogenetic constraints (i.e. allometry) prevailed at different levels in a clade.
During the last decades the production of phylogenetic hypotheses has increased tremendously. Irrespective of whether comparative biologists need to construct a composite phylogeny or make use of existing phylogenies, they have a vast
open source of working material at their disposal. This does not mean that there are
phylogenies available for every question, particularly not when a highly resolved phylogeny is needed. In this thesis, I have used phylogenetic information at different levels of resolution. In paper I and II, where I analysed phylogenetically matched pairs
(PIMPs), the samples were partly delimited by the availability of published phylogenetic hypotheses, and in paper IV, the analyses were based on the reconstructed phylogenies from paper III. The hands-on experience of reconstructing the phylogenetic
hypotheses of the Rhamnus s.l. clade (paper III) was important to me in revealing the
crucial issue of considering uncertainties in the topology of phylogenetic trees, when
performing comparative studies (Donoghue and Ackerly 1996). Accordingly, the phylogenetically independent contrasts (PICs) analyses of fruit and plant size relations in
paper IV were based on a sample of phylogenetic hypotheses which we reconstructed
ourselves (paper III).
Another important use of phylogenies is the possibility to polarize character
evolution, that is to derive the direction of change in character evolution, by outgroup
analyses. This is part of the independent contrast method used in paper IV, but was
also employed in paper II so that we could divide and examine the sample based on
whether fleshy fruits had evolved or been lost in the contrasted sister clades.
Reconstructing phylogenetic hypotheses — The last four decades of phylogeny reconstruction rests on Hennig’s idea (1966) of using synapomorphies, that is, shared derived traits. Developing methods which transform this idea into quantitative analyses
is a research field of its own. Methods based on the parsimony criterion were employed when reconstructing the phylogenetic hypotheses on Rhamnus s.l. (paper III).
Parsimony based methods evaluate the number of character state changes in a phylogenetic hypotheses, and chooses the phylogenetic tree that is based on the smallest
number of changes as the preferable phylogenetic hypothesis. When reconstructing
phylogenies, one often ends up with several equally parsimonious, that is, equally
preferable, phylogenetic hypotheses, meaning that other criteria have to be used to
20
Kjell Bolmgren
advocate any one of them as the most preferable hypotheses. The existence of several
equally parsimonious phylogenetic hypotheses is an important issue to comparative
biology (Donoghue and Ackerly 1996), which was considered in paper IV. In paper I
and II, I generally used single phylogenetic (consensus) trees to generate the data
points. This may be of particular concern for the data set on the temporal distribution
of origin and losses of fleshy fruits in paper II.
TIPS, PIMPs, and PICs — A major critique of traditional comparative studies have
been the common use of species as statistically independent units. This methodology is
nowadays often called TIPS, referring to the terminals or ’tips’ of a phylogeny. The
major advantage of TIPS is that it does not require an explicit phylogenetic hypothesis,
and thus allows for the inclusion of many more species. In this thesis (paper IV), I
analysed size relations within the Rhamnus s.l. phylogeny using TIPS, sampling all
species of the genera Frangula and Rhamnus s.str. The motive for this design was that
the there exists no information on phylogenetic relationships with enough resolution.
That is, as it is accepted to calculate phylogenetically uncorrected means when phylogenetic information is lacking (Møller and Birkhead 1992; Wickman 1992), I analyse phylogenetically uncorrected correlations when phylogenetic information is missing.
The localization of phylogenetically independent events reduces the risk of
confounding variables and allows for a conservative (safe) way of sampling statistically independent units. When phylogenetic information was available, I applied three
different comparative methods. First, the TIPS analyses in paper IV were developed
by performing additional TIPS on monophyletic clades subsampled from the reconstructed phylogenies of Rhamnus s.l. Second, the analyses in paper I and II were based
on phylogenetically independent matched pairs (PIMPs)2. A phylogenetically independent matched pair comprises two monophyletic sister clades separated by a phylogenetic change in the classifying variable. PIMPs thereby only requires localization
of the phylogenetic node where the trait change occurred, and knowledge about which
taxa that belong to the contrasted sister clades. Quantitative values compared between
the sister clades are derived without considering phylogenetic relationships within
2
I would like to dedicate this thesis to the anonymous student, who originally invented the phylogenetically
independent matched pairs method; ”The suggestion that pairs of closely related organisms could be used in
a way that avoided the need to know the full phylogeny was made by a student during discussion following
my seminar at the Department of Genetics, University College, London. Unfortunately, I have been unable
to discover her name.” (Felsenstein 1985, p. 15)
21
Adaptation and constraint in the plant reproductive phase
each sister clade (Felsenstein 1985; Møller and Birkhead 1992; Wickman 1992). In
paper I, PIMPs were sampled when we could locate change to wind pollination in
recently published cladograms, and in paper II, gaining or loosing fleshy fruit type was
the sampling criteria. Using PIMPs one can analyse associations between characteristics. By adding an outgroup to the PIMPs in paper II, we analysed correlated change in
fruit and habitat type. This design is related to the method of phylogenetically independent contrasts (PICs), which is the established method for analysing correlated
change within phylogenies (Mazer 1998).
I employed PICs when analysing allometric effects on fruit size evolution in
Rhamnus s.l. (paper IV). PICs analyses consider the difference in character states, that
is, the contrast, between two related taxa as independent of previous evolution, and
thus as independent in the statistical sense. Analysing PICs require detailed information on the phylogenetic relatedness for all taxa included and results therefore rests on
the assumed phylogenetic hypotheses. In paper IV, I used a software package which
allowed for the simultaneous analyses of several phylogenetic hypotheses (Schwilk
2001; Schwilk and Ackerly 2001). PICs further assume that character change evolve
as Brownian motions. From these assumptions, PICs analyses also derive and make
use of internal (‘ancestral’) contrasts.
Key innovations — We examined if biotic pollination (paper I) and fleshy fruits (paper
II) are correlated with enhanced species richness, using the PIMPs sampled in each
study (McKitrick 1993; Miles and Dunham 1993). This means that the analyses of key
innovations are based on replicates; the phylogenetically independent origins of functionally analogous characters (anemophily and fleshy fruits, respectively).
Key innovations are generally considered at a global scale, that is, not considering confounding variables. As the occurrence of wind pollination, as well as species
richness, correlates with latitude (Regal 1982; Brown and Lomolino 1998), we controlled for biogeography when sampling our data set (paper I). The sampling criteria
used, when controlling for biogeographic autocorrelations, was that each PIMP must
consist of geographically overlapping sister clades. In paper II, we controlled for
growth form when analysing the effect of fleshy fruits on species richness, as we were
interested in the correlated evolution of fruit type and growth habitat.
Moreover, by adding outgroups to each PIMP in the data set of paper II, it was
possible to separate between effects of the evolved trait and the effect of change per
se. When two sister clades are contrasted, one may suggest that the clade with con-
22
Kjell Bolmgren
served ancestral states is being detained in an existing more occupied niche space,
while the other clade, evolving a novel trait, is entering a new less occupied niche
space. Therefore, their potential radiation may not necessarily be comparable, as
change per se could be expected to enhance radiation. In paper II, this problem was
approached by separate analyses of subsamples of the PIMPs according to the direction of evolutionary fruit type change.
Data collection
All phylogenetic comparative analyses (paper I, II and IV) were based on literature
and herbarium data, while paper V was based on a field study.
In paper I, species-specific flowering onset and duration data were compiled
from floras (see paper I for references). Phenological spread, which was adopted as the
measure of phenological niche displacement, was derived as the standard deviation of
flowering onset for each sister clade. To examine whether floristic information on
flowering time was biased by pollination syndrome, phenology data taken from a regional flora (Weimarck 1963) was compared with data taken from herbarium sheets
collected in the same region. A paired t-test revealed no biases in phenology information from floras owing to pollination syndrome.
In paper IV, flowering times for species of Rhamnus s.l. were derived from
herbarium collections. This method has recently been evaluated by K. Lönnberg and
K. Bolmgren (unpublished data), who found equally strong correlations between field
and herbarium data sets, as between different field data sets (e.g. P-M correlations;
N=26; Rfield vs. herbarium = 0.96; Rfield 1 vs. field 2 = 0.94). The species sampled in paper IV
originated from different areas in North America and Europe. Comparing phenology
between distantly located species, means that flowering date is not advisable as a
measure, as it is thought to be correlated with local conditions (May in Sweden is not
phenologically equal to May in Spain.). Therefore, in addition to comparing dates,
flowering dates were transformed to temperature sums (Tuhkanen 1980; Diekmann
1996). Temperature sum is a reliable predictor of flowering events in plants (Reader
1983; White 1995; Diekmann 1996). In paper I, where we used flowering date as a
measure, these issues were considered by contrasting species taken from the same
flora and thereby reducing geographical effects.
23
Adaptation and constraint in the plant reproductive phase
In paper II, which examined relationships between fruit type and habitat characteristics, all information on growth habitats were taken from floras (see paper II for
references). Based on these habitat descriptions, we made a subjective classification of
each habitat according to how the light conditions was perceived in the habitat (open,
intermediate, or closed). Based on these classifications, a semi-quantitative value was
derived for each species, and means for each sister clade, which were then contrasted
between fruit types.
We also compiled a historical distribution of changes in fruit type (paper II),
based on a time-calibrated angiosperm phylogeny (Wikström et al. 2001). The data
taken from Wikström et al. differs from data revealed from the fossil record (Collinson
et al. 1993).
In paper IV, size measures on plant height, leaf length, and fruit diameter were
taken from floras and monographs. TIPS and PICs of allometric size correlations were
analysed using phylogenetic hypotheses derived in paper III.
In paper V, we analysed relations between phenology and components of reproductive success (i.e., fruit set, seed size, fruit size, dispersal, germination, juvenile
size, and juvenile survival). Weekly censuses were performed of phenological changes
in a Frangula alnus population, from flowering, through fruit initiation, development,
ripening, and dispersal for two years. In both years, a phenological experiment was
carried out, where the flowering curve was manipulated to represent early, late, peak,
and asynchronous flowering. During the fruit ripening phase, every second ripe fruit
was measured and collected on both untreated and treated shoots. Seeds were counted
and weighed and then used in greenhouse, common garden, and field experiments on
germination, juvenile development, and juvenile survival. Thus, we were able to follow the fate of individual ovules from flowering to second year juveniles.
As some of the processes potentially involved in the evolution of phenological
strategies may be density-dependent, we analysed both 1st-order linear and 2nd-order
curvilinear relations between phenology and components of reproductive success in
paper V.
24
Kjell Bolmgren
Results
Phenology — PIMPs were used to examine hypothesized adaptive associations between phenology and pollination syndromes (paper I). Wind pollinated trees were
found to flower earlier than their biotically pollinated sister clades, but no difference in
flowering onset time was found when all life forms were analysed together. Flowering
onset differed up to three months between sister clades. Biotic pollination, as compared to wind pollination, was associated with a larger phenological spread (Figure 2).
Phenological spread, which was applied as an analogue to phenological character
displacement, was measured as the standard deviation of flowering onset among species within each sister clade.
120
WIND POLLINATION
Phenological spread (# days)
100
80
60
40
20
0
0
20
40
60
80
100
120
Phenological spread (# days)
BIOTIC POLLINATION
Figure 2. Phylogenetically independent contrasts of phenological spread for biotically versus wind
pollinated sister clades. Phenological spread was measured as the standard deviation of flowering onset.
(Paper I)
Flowering time, expressed as temperature sums at flowering mode date, was
correlated with seasonal length in an interspecific data set of Rhamnus s.l. species
(Figure 3). No similar correlations were found in intraspecific analyses of Rhamnus
cathartica and Frangula alnus populations (paper IV). The interspecific correlation
between flowering time and seasonal length translated into relatively conserved flowering dates. Despite a four month difference in seasonal length between localities,
flowering dates were assembled within three weeks (Figure 4).
25
Adaptation and constraint in the plant reproductive phase
Temperature sum (TS2)
for flowering mode date
1000
800
600
no winter
dormancy period
400
200
800
1600
2400
3200
4000
Total annual temperature sum
(ADDT +5)
Figure 3. Interspecific (closed symbols) and intraspecific (open symbols) regressions of flowering mode
date, expressed as temperature sum, on seasonal length, expressed as total annual temperature sum
(ADDT +5). TS 2 is the temperature sum for all days above +5° C up to the date of flowering mode. The
solid line illustrates the significant correlation (lin. regr.; N=5, R2=0.85, p=0.03) found in the interspecific analyses of species from localities with a winter dormancy period. … = R. cathartica, „ = R. cathartica MEAN, ­ = R. crocea, { = F. alnus, z = F. alnus MEAN, Ú = F. purshiana, c = F. californica,
and ¡ = F. caroliniana. (Paper IV)
30
F. car
25
F. cal N
F. pur
degree Celsius
20
15
R. cat
10
F. aln
Antwerpen
5
Namur
Copenhagen
0
Ystad
baseline
temperature
-5
Karlshamn
Stockholm
-10
-15
-50
Örnsköldsvik
St Louis
0
50
100
150
200
250
300
350
400
Sawyer
Julian day
Figure 4. Flowering mode date for the sampled species marked (arrows) on the daily mean temperature curves for the locality of collection, illustrating the narrow range of flowering dates compared to the
much larger variation in seasonal length. F. car = Frangula caroliniana, F. cal N = F. californica N, F.
pur = F. purshiana, F. aln = F. alnus, and R. cat = Rhamnus cathartica. (Paper IV)
26
Kjell Bolmgren
Paper V considered descriptive and experimental relations between phenology and
components of reproductive success within and between phenophases (i.e. flowering,
fruiting, dispersal, germination, and early juvenile phases) in a local population of
Frangula alnus. Flowering and fruiting times were highly correlated, but there was
also a strong correlation between fruit development time and fruiting time. On the
other hand, germination time was completely decoupled from flowering and fruiting
times.
Seeds of Frangula alnus were mainly dispersed by frugivorous, migratory birds
(paper V), implying that frugivore abundances declines with time in the fruiting phase.
Both experimental and descriptive results suggested a positive effect of early flowering and fruiting on fruit set and dispersal, respectively. The relation between peak time
No. of
flowers
a
1600
b
Flowering curve
1200
800
c
400
d
June
July
Figure 5. A schematic illustration of selection pressures on the flowering curve indicated by the study of
ovule fate in Frangula alnus. (a) Fruit set was higher in early and peak phases in the phenological experiment. (b) Seed size were postively correlated to late flowering. (c) Risks of not being dispersed increased with time in the fruiting phase. (d) Fruit set reached a local minimum two weeks after the flowering peak in the descriptive data set. (Paper V)
flowering and fruit set rendered mixed support from experimental and descriptive data
sets. Flowering time was positively related to seed size, that is, later opening flowers
developed into fruits with higher total vivid seed mass (paper V). The opposite rela-
27
Adaptation and constraint in the plant reproductive phase
10
9
fruit type changes
No. phylogenetically independent
11
„ evolving fleshy fruit
… loosing fleshy fruit
8
7
6
5
4
3
2
1
0
0-10
11-20
21-30
31-40
41-50
51-60
61-70
71-80
> 80
Clade age (Ma)
Figure 6. Historical distribution of origins and losses of fleshy fruit types. (Paper II)
tions to flowering time, between fruit set and seed mass, were confirmed in regression
analyses of 2nd-order polynomial (curvilinear) functions.
Seed size did affect juvenile size, but neither germination nor juvenile survival
were related to seed size in both greenhouse, common garden, and field experiments
(paper V).
Assuming that these different components of reproductive success (fruit set,
seed mass, dispersal, germination, juvenile size, juvenile survival) translate into selection pressures, Figure 5 illustrates their contributions to the selective regime moulding
the flowering curve.
Fleshy fruits — In paper II, we examined origins and losses of fleshy fruit types in
PIMPs. The historical distribution of fleshy fruit origins was bimodal (Figure 6), peaking around the transitions from Paleocene to Eocene (~55 Ma) and Oligocene to Miocene (~25 Ma). Figure 6 was based on the oldest endpoints of the time interval suggested to encompass a fruit type change, and thus the distribution curve may be biased
for older fruit type changes. Despite the modal peaks, Figure 6 suggests a continuous
distribution of origins and losses of fleshy fruit types during the last 80 million years.
Evolutionary changes to fleshy fruit type were also correlated with habitat
change (paper II), such that fleshy fruited clades colonized vegetation types that were
28
Kjell Bolmgren
1.25
more closed
0.75
Derived fleshy fruit
Closedness index change
1.00
0.50
0.25
0.00
-0.25
-0.50
-0.75
-1.00
more closed
more open
-1.25
-1.25 -1.00 -0.75 -0.50 -0.25 0.00
0.25
0.50
0.75
1.00
1.25
1 case
2 cases
3 cases
4 cases
Closedness index change
Ancestral non-fleshy fruit
Figure 7. Changes in habitat light conditions, as compared to an outgroup, for clades evolving fleshy
fruit type versus their sister clades retaining the ancestral non-fleshy fruit type. Habitats were classified as
open, semi-open, and closed according to the prevailing vegetation type. (Paper II)
considered more closed than the habitats colonized by their dry-fruited sister clades
(Figure 7).
Fleshy fruit size was studied in paper IV and V. Using the reconstructed phylogenies from paper III, I analysed interspecific allometric relations in the Rhamnus
s.l. clade, by TIPS and PICs. The independent contrast analyses (PICs) in paper IV
suggested an allometric relationship between fleshy fruit size and plant mature height
in all eight, topologically different, phylogenetic hypotheses of Rhamnus s.l. On the
other hand, leaf length was not correlated to fruit size nor plant mature height in the
PICs analyses. TIPS were analysed using different monophyletic subclades within
Rhamnus s.l. Allometric correlations with fruit size revealed at the Rhamnus s.l. level,
prevailed in Rhamnus s.str. but not in its sister genera Frangula (Figure 8).
In the population study of Frangula alnus (paper V), fruit diameter was positively correlated with plant size (see also Table 1). Additional analyses (K. Bolmgren,
unpublished data) suggested positive correlations for both fruit diameter and plant size
with mean vivid seed mass per fruit (Table 1), and for individual fruits, fruit diameter
was positively correlated with mean vivid seed mass and number of vivid seeds (Figure 9).
29
Adaptation and constraint in the plant reproductive phase
Cervispina
R = 0.66**
N = 22
Rhamnus s.str.
Alaternus
R = 0.65***
n.s
N = 40
N=3
Rhamnus s.l.
Eurhamnus-Pseudalataternus
R = 0.37**
R = 0.76**
N = 69
N = 12
Frangula
n.s.
N = 29
10.
A.
9.0
7.5
1
2
3
6.0
15
25
35
Mean vivid seed mass per fruit (mg)
Fruit diameter (mm)
Fruit diameter (mm)
Figure 8. Fruit size and plant mature height correlations from the TIPS analyses, which were performed
on different monophyletic clades within Rhamnus s.l. The hierarchical topology allowed for analyses at
the supergeneric level (Rhamnus s.l.), the generic level (Rhamnus s.str. and Frangula), and the section
level (Cervispina, Alaternus, and Eurhamnus-Pseuadalaternus). *P<0.05, **P<0.01, ***P<0.001.
(Paper IV)
B.
10
9
8
1
2
3
No. of vivid seeds per fruit
Figure 9. Fruit diameter as a function of (A) mean vivid seed mass per fruit (P-M correlations; N1 vivid seed
-6
-6
per fruit = 216, R1 vivid = 0.53, p<10 ; N2 vivid seeds per fruit = 335, R2 vivid = 0.59, p<10 ; N3 vivid seeds per fruit =
31, R3 vivid = 0.55, p=0.001) and (B) number of vivid seeds per fruit (ANOVA; df: 2, 581; p<10-6) in
Frangula alnus 2000. (Paper V)
30
Kjell Bolmgren
Key innovations — No association between biotic pollination and higher species richness was found, when compared to wind pollinated sister clades (paper I). On the other
hand, evolution of fleshy fruit type was associated with more species-rich clades (paper II). However, this association was only valid when PIMPs characterized by woody
growth forms were sampled (test 2a, Table 2), and particularly so when fleshy fruit
types were the derived state (test 2b, Table 2). Among herbaceous plants, non-fleshy
fruit types were associated with higher species richness (test 3a, Table 2), and the
tendency was that this association was valid only when non-fleshy fruit types were the
derived state (test 3c, Table 2) Change per se did not result in higher species richness
(test 2c and 3b, Table 2).
Table 1. Correlation coefficients for plant and fruit characteristics of Frangula alnus. *P<0.05,
**P<0.01, ***P<0.001. (Paper V)
No. of
annual shoots
per plant
No. of annual
shoots per plant
Fruit diameter
No. of
vivid seeds
per fruit
Total
vivid seed
mass per fruit
Mean
vivid seed
mass per fruit
-
Fruit diameter
0.50*
-
No. of vivid
seeds per fruit
n.s.
n.s.
-
Total vivid seed
mass per fruit
n.s.
n.s.
0.76***
-
Mean vivid seed
mass per fruit
0.53*
0.49*
n.s.
n.s.
-
Table 2. Results of one-tailed sign tests of the correlation between extant species richness and fruit type.
p is the cumulative p-value (Sokal and Rohlf 1995). (Paper II)
Test
1
2a
Growth forms
All
‘Woody’ PICs
Prediction
p
fleshy > non-fleshy
0.23
fleshy > non-fleshy
0.01
0.01
2b
Woody, with dry ancestor
fleshy > non-fleshy
2c
Woody, with fleshy ancestor
fleshy > non-fleshy
0.34
non-fleshy > fleshy
0.02
3a
‘Herbaceous’ PICs
3b
Herbaceous, with dry ancestor
non-fleshy > fleshy
0.19
3c
Herbaceous, with fleshy ancestor
non-fleshy > fleshy
0.06
31
Adaptation and constraint in the plant reproductive phase
Discussion
Phenology — In the comparison between biotically and wind pollinated plants (paper
I), two anticipated phenological patterns appeared: biotic pollination was associated
with wider phenological spread; and wind pollinated trees flowered earlier in the season. As this study was based on PIMPs, the direction of phenological change is not
known. That is, whether the biotically pollinated taxa have diverged more than random
in flowering times or if the wind pollinated taxa have evolved a more narrow spread
than is expected by random is not possible to conclude from this study.
Previous propositions have suggested that reproduction in wind pollinated
populations is favoured by a more narrow flowering curve, as it amplifies the mass
release of pollen characteristic of wind pollinated plants (Whitehead 1969; Faegri and
van der Pijl 1979). If wind pollinated trees generally have a more narrow flowering
curve (cf Rabinowitz et al. 1981) more species may be packed into a temporal niche
space. Moreover, results by Linder and Midgley (1996) indicate that wind pollinated
species may be less harmed by interspecific flowering overlap, which would further
reduce phenological spread.
Wider phenological spread is one way to generate reproductive isolation between related taxa, and thus part of the general conception that biotic pollination has
enhanced speciation in angiosperms. Some initial suggestions of such temporal niche
differentiation (e.g. Stiles 1977) were criticized on methodological grounds (for review, see Gotelli and Graves 1996). In paper I, phenological spread was measured as
the standard deviation of flowering onset, which means that the patterns found may
have been generated by microevolutionary processes, but also by ‘quantum leaps’.
Plausible reasons for flowering time ‘quantum leaps’ could, for example, be changes
in germination time from autumn to spring, changes in growth form, or changes in
fruit type.
As with phenological spread, the study in paper I did not reveal which directional change that lead to earlier flowering in wind pollinated trees. But, in contrast to
the study of phenological spread, we do know the absolute seasonal position of the
flowering times. Wind pollinated trees flowered early in the season which gives further support to the previously proposed adaptive and mechanistic interpretations of
spring flowering times for wind pollinated trees (Whitehead 1969; Heinrich 1976).
32
Kjell Bolmgren
The comparison of Rhamnus s.l. species resulted in an anticipated correlation
between seasonal length and flowering times (paper IV). Still, flowering dates were
relatively conserved, gathered within a week despite a four month difference in seasonal lengths. Assuming that the temperature sum based correlations indeed are local
adaptations, the conserved flowering dates are puzzling. Of course, it may just be a
coincident, but considering the different selection pressures acting on flowering
phenology in an insect-pollinated, bird-dispersed, temperate plant (cf Figure 5), stabilizing selection may also be an alternative. Most phenological strategies are probably
moulded by several, differently directed selection pressures (Brody 1997; Pico and
Retana 2000; Lacey et al. 2003). Apart from the effects of the mutualistic interactions
(pollination and frugivory), phenology was also correlated to seed size in the local
study of Frangula alnus (paper V). This seed size correlation suggests that recruitment
processes may be part of reproductive phenology evolution in a more complex way
than has generally been considered (Ollerton and Diaz 1999; Lacey et al. 2003).
Fleshy fruits — Functionally analogous fleshy ‘fruits’ may be considered the plesiomorphic fruit type for seed plants (Herrera 2002b), but among angiosperms several
independent evolutions of fleshy fruits have occurred (e.g. paper II; Herrera 1989).
The sudden rise in abundance of fleshy fruited taxa at the Late Cretaceous–Early Paleocene boundary has been an issue in itself (Tiffney 1984; Eriksson et al. 2000), but it
has also been used as an explanation for conserved fleshy fruits (Tiffney 1984; Jordano 1987; Eriksson and Bremer 1992; Jordano 1995a; Eriksson et al. 2000). That is,
particular conditions, for example a unique period of global warming and/or the radiation of passerines, changed the adaptive landscape profoundly, giving frugivorous seed
dispersal fitness advantages during this particular period in angiosperm history. Paper
II supported the correlation between fleshy fruit evolution and habitat change, but also
a continuous distribution of fleshy fruit origins during the last 80 My. The historical
distribution of origins and losses of fleshy fruit types was also bimodal with one peak
more or less coinciding with the previously suggested peak in the Global warming
period 50 Ma (Janis 2003). Previous studies have concluded that abundances of fleshy
fruited plants peaked in Paleocene–Eocene (Eriksson et al. 2000), and paper II further
suggest that independent origins of fleshy fruits peaked 55 Ma (Figure 6). This connection between abundance and evolutionary origins of fleshy fruited plants was further manifested by the correlation between fleshy fruit types and higher species richness among woody plants (paper II). So, not only was the evolution of fleshy fruits
33
Adaptation and constraint in the plant reproductive phase
correlated with more closed vegetation types, fleshy fruits also seems to be a key innovation under conditions related to these habitats (cf Tiffney and Mazer 1995).
The correlations between fleshy fruit types, diversification effects, and habitat
types, suggest that selection for/on fleshy fruits may be stronger under these habitat
conditions. Few studies exist explicitly analysing demographic effects of fleshy fruit
characteristics and fleshy fruit dispersal in different habitats. Piper (1986) found mixed
responses to different light conditions, and interpreted large seeded species as more
shade tolerant. Herrera et al. (1994) found varying dispersal and recruitment patterns
for the same species in different habitats, while Wenny and Levey (1998) is the only
study I know of that have shown a positive effect of directed dispersal to favourable
recruitment sites by a frugivorous bird. Increased seed size affects several recruitment
processes positively, and may be comparatively more important in shady habitats
(Eriksson and Jakobsson 1998; Ehrlén and Eriksson 2000; Leishman et al. 2000; Jakobsson and Eriksson 2002). At a general level, vertebrate dispersed fruits have larger
seeds, though the seed size range and overlap with other fruit types is large (Hughes et
al. 1994), and fleshy fruited plants have been associated with communities characterized by higher stature (Willson et al. 1990; Guitian and Sanchez 1992; Jakobsson and
Eriksson 2002). In Frangula alnus (Figure 9) fruit size was correlated both with seed
size and seed number, implying that the selective regime of seed driven fruit size evolution may incorporate the frugivores. Frugivores drop larger fruits more often (Jordano 2000) and can change feeding behaviour from swallowing to pecking, and thus
may not disperse seeds (Rey et al. 1997). Larger fruits also face a reduced frugivore
guild (Wheelwright 1985). Moreover, the larger of the main seed dispersing frugivores
of F. alnus fruits were the earliest autumn migrators potentially placing an additional
pressure on the evolution of larger seeds. On the other hand, paper V did not suggest
any selection pressure for larger seeds in F. alnus. Seed size in F. alnus affected juvenile size, but neither seed size nor juvenile size had any general effects in the early
recruitment phase (paper V).
Fruit size variation may also be an allometric effect. Herrera (2002a) found
such relations between leaf and fruit sizes among Iberian fleshy fruited plants. Similarly, a positive correlation between plant height and fruit diameter was found among
species in Rhamnus s.l. (paper IV) and within species in F. alnus (paper V), but no
interspecific allometric relations to fruit size was found within Frangula (paper IV).
Allometric relations may, apart from being a phylogenetic constraint (further discussed
below), express simultaneous selection pressures due to abiotic conditions. For exam-
34
Kjell Bolmgren
ple, Herrera (2002a) suggested that water deficiency could lead to an evolutionary
parallel reduction in both leaf size and fruit size.
Constraints — A key innovation is a feature that yields comparatively rapid radiation
within a phylogenetic lineage, releasing the lineage from ancestral diversification
constraints. To be able to test hypotheses on key innovations, the present thesis have
adopted the additional criteria that key innovations must be phylogenetically repeated
(Mitter et al. 1988; McKitrick 1993; Miles and Dunham 1993).
In contrast to previous studies (Eriksson and Bremer 1992; Ricklefs and Renner
1994; Dodd et al. 1999), biotic pollination was not associated with higher species
richness when compared to wind pollinated clades. The main reason for this, perhaps,
unexpected result may have been that the PIMPs sampled had to be geographically
overlapping. Thereby the question at stake was merely if wind and biotic pollination
differ in effects on diversification, and not whether biotic pollination is associated with
angiosperm diversity. Considering the present results and that wind pollination becomes more common when moving polewards (Regal 1982), the reason why biotic
pollination may be associated with angiosperm radiation is that biotic pollination
dominates in the species-rich tropical regions.
Fleshy fruits were not found to be a global key innovation (paper II), which is a
result congruent with previous studies (Eriksson and Bremer 1992; Ricklefs and
Renner 1994; Tiffney and Mazer 1995). The result changed, though, when growth
form was controlled for, as fleshy fruits were associated with higher species richness
in woody plants. Fleshy fruits are expensive fruits reducing the total number of seeds
produced, and may therefore not pay-off for smaller (herbaceous) plants (Tiffney and
Mazer 1995).
Paper I, II, and IV examined and found anticipated courses of evolution for
flowering phenology in relation to pollination syndromes and seasonal conditions, and
for fleshy fruits in relation to habitat change. However, these studies do not completely
rule out the existence of phylogenetic constraints. They simply suggest that natural
selection for adaptive change may overpower phylogenetic constraints to the extent
that we can detect the anticipated outcomes. Based on the results from paper I, where
phenology patterns supported adaptive hypotheses at a global scale, niche related
phenology evolution must be considered more important than just a ‘fine-tuning’ process (Kochmer and Handel 1986, p. 319). Further, the differences in flowering times
between sister clades indicate that previous interpretations of conserved flowering
35
Adaptation and constraint in the plant reproductive phase
time rank orders (Kochmer and Handel 1986) may have been unnecessarily biased
towards phylogenetic constraints. Such patterns may equally well be interpreted as an
outcome of phylogenetic niche conservatism (Harvey and Pagel 1991; Lord et al.
1995).
Ecotypic differentiation of flowering times to variation in seasonal conditions,
for example, along a latitude or altitude transects, is a much supported pattern (e.g.
Clausen et al. 1948; Reader 1983), and the adaptability of the seasonal sequence of
phenological phases to make them fit into local conditions may be an important constraint in migration processes. No such correlation between local seasonal length and
flowering time, measured as temperature sums, was found in the two intraspecific data
sets of Frangula alnus and Rhamnus cathartica (paper IV). This unexpected outcome
may be interpreted as an indication of phylogenetic constraints, although such a conclusion of phylogenetic constraints may be unwarranted if the preconditions (fitness
differences, selection pressure) have not been examined (Antonovics and van
Tienderen 1991). Similarly, Jordano (1995a) used a lack of an anticipated outcome to
suggest that the evolution of fleshy fruits has been phylogenetically constrained. The
underlying assumption in Jordano’s study was that a close match in the fruit–frugivore
interaction would support an adaptive process. Thus, the lack of such a close match
falsified the generality of tight interactions. Along the same line of reasoning, Jordano
(1995a) suggested that frugivores are generally week selective agents on fleshy fruit
characteristics, except for seed size. A lot of fruit character variation was attributed to
phylogenetic affinities, thus confirming phylogenetic effects, but as long as no fitness
differences and no constraining mechanisms are presented, general claims of phylogenetically constrained character evolution must be considered with caution.
Allometry was found to be a potential mechanism underlying phylogenetically
constrained fleshy fruit size evolution in Rhamnus s.l., as fruit size covaried with plant
mature height (paper IV). Allometric effects have recently been proposed as an additional explanation of fleshy fruit size variation (Herrera 2002a). As a phylogenetic
constraint, the allometric mechanism within Rhamnus s.l. seems rather week, considering that the allometric relation vanished within Frangula, while it prevailed in its monophyletic sister clade Rhamnus s.str.
The final paper of this thesis (paper V) considered functional constraints, that is
counteracting selection pressures, which Schwenk (1995) argued should not be regarded as a phylogenetic constraint at all. When disentangling the different selective
and constraining forces moulding the evolution of a character, a ‘liberal’ view of the
36
Kjell Bolmgren
constraint concept might be useful, at least when approaching the study system. Experimental and descriptive examination of the relation between phenology and components of reproductive success indicated a complex pattern of selection pressures on
the flowering curve of Frangula alnus (Figure 5). In general the early part of the curve
favours fruit set and dispersal, while increasing seed size is favoured after the flowering peak. Thus, fruit set, and thereby seed number, and seed size were inversely correlated to flowering time in F. alnus. Even if seed size variation is just a result of the
trade-off between seed number and seed size (Shipley and Dion 1992; Jakobsson and
Eriksson 2000), selection for a phenological strategy leading to increased fruit set may
be counteracted by selection for larger seeds. For example, within the population of F.
alnus examined in paper V, a retained seed size range may be accomplished by a selection for a wider flowering curve. In the special case of F. alnus, however, seed size
was only found to affect juvenile size in the recruitment phase, while neither germination nor juvenile survival was affected by seed size under the conditions employed.
37
Adaptation and constraint in the plant reproductive phase
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44
Kjell Bolmgren
Svensk sammanfattning
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.
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Adaptation and constraint in the plant reproductive phase
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.
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