Download Ecology and Evolution of Adaptive Morphological Variation in Fish

Ecology and Evolution of Adaptive Morphological
Variation in Fish Populations
Richard Svanbäck
Umeå 2004
Department of Ecology and Environmental Science
Umeå University
SE-901 87 Umeå
Sweden
AKADEMISK AVHANDLING
Som med vederbörligt tillstånd av rektorsämbetet vid Umeå Universitet för
erhållande av filosofie doktorsexamen i ekologi kommer att offentligen försvaras
fredagen den 19:e mars kl. 10.00 i Stora Hörsalen, KBC.
Examinator: Professor Lennart Persson, Umeå Universitet
Opponent: Professor Beren W. Robinson, Department of Zoology, University of
Guelph, Ontario, Canada.
ISBN 91-7305-583-2
© Richard Svanbäck 2004
Printed by VMC, KBC, Umeå University, Sweden
Cover: Trehörningen, Umeå
Photo by Richard Svanbäck
Organisation
Umeå University
Dept. of Ecology and Environmental Science
SE-901 87 Umeå
Document name
Doctoral Dissertation
Date of issue
Mars 2004
Author Richard Svanbäck
Title Ecology and Evolution of Adaptive Morphological Variation in Fish
Populations
Abstract
The work in this thesis deals with the ecology and evolution of adaptive individual
variation. Ecologists have long used niche theory to describe the ecology of a
species as a whole, treating conspecific individuals as ecological equivalent.
During recent years, research about individual variation in diet and morphology has
gained interest in adaptive radiations and ecological speciation. Such variation
among individual niche use may have important conservation implications as well
as ecological and evolutionary implications. However, up to date we know very
little about the extension of this phenomenon in natural populations and the
mechanisms behind it.
The results in this thesis show that the extension of individual diet
specialization is widely spread throughout the animal kingdom. The variation in
diet is mainly correlated to morphological variation but not always. Furthermore,
this variation in diet and morphology among individuals could be both genetically
determined and environmentally induced and it mainly comes from trade-offs in
foraging efficiency between different prey types.
The results from a number of studies of perch also show that individual perch
differ in morphology and diet depending on habitat, where littoral perch has a
deeper body compared to pelagic perch. This difference in morphology
corresponds to functional expectations and is related to foraging efficiency tradeoffs between foraging in the littoral and pelagic zone of a lake. The variation in
morphology in perch is mainly due to phenotypic plasticity but there are also small
genetic differences between the littoral and pelagic perch. Two separate studies
show that both predation and competition may be important mechanism for the
variation in morphology and diet in perch.
In conclusion, the results in this thesis show that individual variation in diet
and habitat choice is a common phenomenon with lots of ecological and
evolutionary implications. However, there are many mechanisms involved in this
phenomenon on which we are just about to start learning more about, and only
further research in this area will give us the full insight.
Key words competition, functional morphology, individual specialization, interindividual variation, intra-population variation, morphological variation, ontogeny,
Perca fluviatilis, perch, phenotypic plasticity, predation, trade-offs.
Language English
Signature
ISBN 91-7305-583-2
Number of pages 35
Date 2004-02-07
Contents
Introduction
Morphological variation and habitat use in fish populations
7
9
Objectives
11
Methods
12
Species studied
12
Defining Individual Specialization
12
Major results and discussion
14
The ontogeny of foraging specialization
16
Divergent natural selection
17
Phenotypic plasticity and genetics in adaptive morphological variation
18
The effect of predation on adaptive variation and diet specialization
19
Density dependent changes in individual diet specialization
21
Concluding remarks and future perspectives
22
Acknowledgements
25
References
25
Acknowledgements
34
Appendices (papers I-VI)
LIST OF PAPERS
This thesis is based on the following papers that will be referred to by the
corresponding Roman numerals
I
Bolnick, D.I., Svanbäck, R., Fordyce, J.A, Yang, L.H., Davis, J.M.,
Hulsey, C.D. and Forister, M.L. (2003) The ecology of individuals:
incidence and implications of individual specialization. American
Naturalist 161: 1-28.
II
Svanbäck, R. and Eklöv, P. (2002) Effects of habitat and food resources
on morphology and ontogenetic growth trajectories in perch. Oecologia
131: 61-70.
III
Svanbäck, R. and Eklöv, P. (2003) Morphology dependent foraging
efficiency in perch: a trade-off for ecological specialization?. Oikos 102:
273-284.
IV
Svanbäck, R. and Eklöv, P. Genetic variation and phenotypic plasticity:
causes of morphological variation in Eurasian perch. Manuscript
V
Eklöv, P. and Svanbäck, R. Predation favors adaptive morphological
variation in perch populations. Manuscript
VI
Svanbäck, R. and Persson, L. Individual diet specialization, niche width
and population dynamics: implications for trophic polymorphisms. Journal
of Animal Ecology, provisionally accepted.
Papers I, II and III are reproduced with the permission from the publishers.
Ecology and Evolution of Adaptive Morphological
Variation in Fish Populations
Introduction
”Natural selection … leads to divergence of character, for more living beings can be
supported on the same area the more they diverge in structure, habitat and constitution”
(Darwin, C. 1859)
If intra-specific competition is strong, then an individual that is able to efficiently
use a new resource may experience reduced intra-specific competition and gain
higher fitness (Wilson and Turelli 1986). Expansion of the population niche width
and adaptations to novel resources has theoretically been shown to be one of the
causes of resource polymorphisms and ultimately sympatric speciation (e.g. Smith
and Skúlason 1996, Dieckman and Doebeli 1999, Doebeli and Dieckman 2000).
The expansion of the population niche width is thought to be due to increased intraspecific competition or reduced inter-specific competition, and support for this
stems largely from observational studies of character release and displacement
(Grant 1972, Robinson and Wilson 1994, Robinson and Schluter 2000).
In the late fortieth, Svärdson (1949) observed that habitat variation in a
species is low when inter-specific competition is dominant whereas if intra-specific
competition dominates then habitat variation is much greater. In the mid sixtieth,
Van Valen (1965) developed the “niche variation hypothesis”. Both Svärdson and
Van Valen proposed that niche expansion in the absence of inter-specific
competition was achieved by increased between-individual variation in resource
and habitat use. Roughgarden (1972, 1974) provided further support for the role of
between-individual variation by theoretical work. After a few supportive (e.g.
Rothstein 1973, Grant et al. 1976, Bernstein 1979), and a few negative tests (e.g.
Soulé and Stewart 1970, Soulé 1972, Patterson 1983), the discussion of individual
variation trailed of in the 1980s. However, the discussion of intra-specific niche
variation has recently revived with renewed interest in resource polymorphism,
adaptive radiation, and ecological speciation (e.g. Smith and Skúlason 1996,
Doebeli and Dieckman 2000, Mousseau et al. 2000, Schluter 2000).
Between-individual niche variation can occur in several ways, including
ecological sex dimorphism (e.g. Shine 1989, 1991), ontogenetic niches (e.g. Polis
1984, Werner and Gilliam 1984), and discrete polymorphisms (e.g. Smith and
Skúlason 1996). These cases of niche differentiations are correlated to discrete
morphological differences between the foragers. Between-individual niche
variations have also been shown to occur where there are no obvious discrete
morphological differences between the foragers, and such “individual
7
specialization” may sometimes exceed differences between conventional species
(e.g. Werner and Sherry 1987, West 1986, 1988, Ehlinger and Wilson 1988).
The feeding specialization among individuals may to some extent reflect
morphological and behavioral constraints (e.g. Wainwright 1988, Ehlinger and
Wilson 1988) but they may also be a consequence of learning (e.g. Heinrich 1976,
Werner and Sherry 1987). The morphological and behavioral constraints in
handling time efficiency and search efficiency give rise to foraging efficiency
trade-offs (e.g. Lewis 1986, Milinski 1987, Ehlinger and Wilson 1988, Robinson
2000). The trade-offs in foraging on different food resources that may lead to
phenotypically divergent populations are hypothesized to be a primary cause of
trophic polymorphisms and adaptive radiations (e.g. Ehlinger and Wilson 1988,
Schluter 1993, Smith and Skúlason 1996, Robinson et al. 1996). For example,
observations on a Galapagos finch species, the medium ground finch (Geospiza
fortis) has revealed that individuals with different beak sizes feed in different ways.
The efficiency that the medium ground finch display in cracking seeds varies
depending on beak size, and in the dry season, when food supply is likely to be
limiting and most mortality to occur, they feed on seeds of different sizes and
hardness in proportion to their beak sizes (Grant et al. 1976, Price 1987). The same
correlations between beak size and diet has been found for other seed-eating
finches elsewhere (Smith 1987, 1993, Benkman 1993, Diaz 1994,). The foraging
efficiency trade-offs leading to differential energy intakes will have consequences
for the foragers’ fitness. It is hypothesized that the functional trade-offs in handling
seeds of different sizes and hardness are responsible for the adaptive radiation in
Galapagos finches and other seed eating finches elsewhere (e.g. Grant 1986, Smith
1987).
Genetic divergence between populations due to local adaptations or
environmentally induced morphological changes are the two processes that have
been ascribed to cause differences in trophic morphology. Genetic divergence
through local adaptations have long been recognized to create great morphological
variation, but that plasticity may be a major component of phenotypic variation has
just recently attracted much attention. Many organisms can modulate their
morphology in response to environmental cues. Such plasticity is thought to be an
important adaptive strategy for populations experiencing variable environments
(Stearns 1989, Scheiner 1993), and it is likely that phenotypic plasticity plays an
important role in diversification (West-Eberhard 1989). For example, if the positive
correlation between the trait and fitness is exclusively due to nonheritable
environmental component, the trait may appear to be under directional selection
and yet not evolve. Such cases have been suggested for life history traits (Price et
al. 1988, Price and Liou 1989) and morphological characters (van Noordwijk et al.
1988, Alatalo et al. 1990). This has important consequences for our ability to
predict phenotypic changes when measuring natural selection.
8
“In an extremely small area … and where the contest between individual and individual
must be severe, we always find great diversity in its inhabitants.”
(Darwin, C. 1859).
As Darwin wrote in the “Origin of Species”, more recent models of so-called
”competitive speciation” hypothesize that competition is diversifying, (Rosenzweig
1978, Pimm 1979, Dieckmann and Doebeli 1999), i.e. that the gradual expansion
into a new niche occurs in response to competitive pressure within the old niche.
Trophic resource polymorphisms in fishes for example, are believed to have arisen
through intra-specific competition via character release (Robinson et al. 1993,
Robinson and Wilson 1994, Skulason and Smith 1995). Due to the absence of other
species such as competitors and predators, intra-specific competition has forced
individuals to inhabit new niches and thereby broaden the species’ niche width.
Just as competition is diversifying, predation is also an important
selective force in most natural communities. Besides its obvious impact on
abundance and size structure of prey populations, predation has commonly selected
for ecological, behavioral and morphological traits in prey (Lima and Dill 1990,
Harvell1990). Various morphological structures in prey organisms’ function as
efficient adaptations against predation, and these morphological defenses could be
either constitutive or environmentally induced. Furthermore, recent findings have
shown that predation may be involved in creating variation within a species
(Vamosi 2002, Abrams 2003).
So in order to understand the evolutionary ecology of a population or a
species, then individual differences are important to document, for it is the
variation among individuals that is the raw material on which natural selection acts.
Morphological variation and habitat use in fish populations
Many aspects of a fish's ecological niche can be indicated from its morphological
features. For example, body shape and fin dimensions are good indicators of the
habitat preference and swimming behavior of fishes (e.g. Keast and Webb 1966,
Webb 1984). There are three main categories of locomotion in fish that are highly
dependent on the body form of the fish (Webb 1984, Webb and Weihs 1986). The
three categories are cruisers, maneuverers and accelerators. Each of these has a
distinct structure and form optimal for the special activity. Most fish however, have
body and fin forms intermediate among those of specialists (Webb 1984).
Therefore, most fish are locomotor generalists in that they perform well in several
areas of locomotor patterns, although performance in each area is lower than that of
the relevant specialist. The locomotor pattern of cruisers is optimal for exploitation
of widely dispersed food (Webb 1984) and the optimal morphology of a cruiser
includes a fusiform shaped body with a slim caudal peduncle (Webb 1984, Webb
and Weihs 1986). Performance in maneuvers is affected by body and fin
morphology (Howland 1974, Webb 1976, 1983), and the optimal design for
maneuvering is to have a short, deep laterally compressed body with mid-lateral
pectoral fins (Webb 1982, 1984, Webb and Weihs 1986). In lake fish communities,
deep-bodied species are usually found in the more structurally complex littoral
9
habitat, whereas pelagic fish show more streamlined body morphology (e.g. Keast
and Webb 1966, Watson and Baloon 1984, Motta et al. 1995). Predators of locally
abundant and evasive prey require maximal acceleration (Webb and Skadsen 1980,
Rand and Lauder 1981, Vinyard 1982) to minimize the duration of interaction. The
optimal body form of an accelerator is characterized by Esox and consists of an
elongated body shape with a deep caudal peduncle and a large muscle mass (Webb
1984, Webb and Weihs 1986).
Many fish species exhibit considerable intraspecific variation in
morphology. This intraspecific variation can be divided into intra- and interpopulation variation. Inter-population variation is considered to be correlated with
differences in the availability of resources either through competition with other
species (Lindsey 1981, Magnan 1988) or by system specific differences in resource
conditions (e.g. Lavin and McPhail 1985, 1986, Mittelbach et al. 1992, Walker
1997). Intra-population variation in morphology of fish on the other hand is
thought to be correlated with habitat choice of individuals (Smith and Skúlason
1996), where intraspecific competition is thought to give rise to the pattern of
correlation between morphology and habitat choice (Wilson and Turelli 1986).
Resource polymorphisms in fish have attracted a lot of attention in the
past decade where most examples reflect segregation between the littoral and the
pelagic habitats of lakes (Smith and Skúlason 1996). In the cases of a littoralpelagic segregation of individuals it has been found that the littoral individuals
have a deeper body (e.g. Ehlinger and Wilson 1988, Snorrason et al. 1994,
Robinson et al. 1996), and longer pectoral and pelvic fins (Ehlinger and Wilson
1988, Bourke et al. 1997, Dynes et al. 1999). The pelagic fish on the other hand
have a more streamlined body with shorter pectoral and pelvic fins (Ehlinger and
Wilson 1988, Robinson et al. 1996, Bourke et al. 1997, Dynes et al. 1999).
The differentiation in morphology between the littoral and pelagic
habitats range from a more normal distribution of phenotypes where only the mean
values differ between the littoral and pelagic habitat (e.g. Ehlinger and Wilson
1988, Robinson et al. 1993, 1996) to clear bimodal non-overlapping morphologies
between the habitats (e.g. Mann and McCart 1981, Hindar and Jonsson 1982,
Pigeon et al. 1997). These stages of differentiation in morphology might represent
intermediate stages in speciation (Smith and Skúlason 1996) and in some cases it
has been found that the morphs differentiate not only morphologically but also
genetically (e.g. Hindar et al. 1986, Foote et al. 1989, Vuorinen et at. 1993).
10
Objectives
Despite the long history of the “niche variation hypothesis” we still lack knowledge
about the mechanisms that drives the population niche width. For example, tradeoffs in foraging efficiency are thought to be a mechanism behind differential
resource use but still we know little about the mechanisms behind the trade-offs.
The concept of character release predicts that the population niche width (or at
least the morphological variation) will increase in the absence of a competitor.
However, empirical studies of character release and polymorphisms in fish have
only considered the ontogenetic end stages, whereas most fish species grow several
orders of magnitude during their life. Furthermore, theories of competitive
speciation suggest that intra-specific competition is important in expansion of the
population niche width. Up to date, the theories of competitive speciation describes
a situation when the population is at a numerical equilibrium despite that most
populations in nature fluctuate in numbers through time. This has lead to that when
character release/displacement and resource polymorphisms are studied, analyzed
and discussed, this is performed in the absence of a population dynamic
perspective. Furthermore, the strong focus on competition as the driving force has
led to an ignorance of predation as a factor in driving niche variation.
The main objective of this thesis was to gain deeper knowledge about
individual variation in diet and habitat choice. More specifically, the ecological and
evolutionary causes and consequences of individual variation. The main questions
addressed in this thesis are:
•
•
•
•
•
•
How common are the patterns of individual diet specialization in nature
and what are the theory behind the mechanisms of individual specialization
(I)
Is the individual diet and habitat specialization related to morphological
variation (I, II and III)
Is the morphological variation within and between habitats related to
foraging efficiency trade-offs and if so how do they relate to growth rates
in nature (III)
Is the morphological variation between habitats related to genetic
difference or to phenotypic plasticity (I, and IV)
It is known that predation can influence habitat choice of the prey but what
is the effect of predation risk on individual diet specialization and
morphological development in prey (V)
Competition is said to be diversifying but what is the effect of population
dynamical feedbacks on individual diet choice (VI)
11
Methods
To study the ecology and evolution of adaptive individual variation several
different methods were used. This thesis consists of a review (paper I) and studies
on different temporal and spatial scales such as snap shot and long-term field
surveys (paper II, III, and VI), aquaria experiments (paper III), and outdoor pond
and common garden experiments (paper IV and V). Paper I was designed to
investigate the general pattern in nature whereas the other papers were designed to
answer more specific questions. To answer the more specific questions, Eurasian
perch (Perca fluviatilis) was chosen as study organism, based on the vast
background knowledge of the species’ ecology.
Species studied
Eurasian perch is one of the most common fish species in Eurasia (Svärdson 1976,
Johansson and Persson 1986). Perch is an ontogenetic omnivore and undergoes two
diet shifts over its life span. Perch spawn in the littoral zone and the 5-7 mm long,
newly hatched larvae shift habitats to the pelagic zone within a day (Byström et al.
2003). As the larval perch grow they get pigmented and develop into juveniles at a
size of approximately 20 mm. Due to their small size, juvenile perch are very
vulnerable to predation and therefore they shift back to the littoral zone after a few
weeks (Byström et al. 2003). Larval and juvenile perch mainly feed on
zooplankton (Craig 1978, Guma’a 1978, Coles 1981, Byström et al. 1998). With an
increase in size, perch gradually shift to macroinvertebrate feeding and finally as
large become piscivorous (Fig. 1) (Persson 1988). As adults, perch occupy both the
littoral and pelagic habitats of lakes and movements between these habitats are
relatively restricted (Eklöv 1997).
Zooplankton
Macroinvertebrates
Fish
Figure 1. Graphical description of the major diet categories and ontogenetic diet shifts in
perch.
Defining Individual Specialization
Roughgarden (1972, 1974) provided a quantitative framework for thinking about
intrapopulation niche variation. Roughgarden (1972) suggested that the size
12
component of the total niche width (TNW) of a population could be broken down
into two components; the variation in resource use within individuals (withinindividual component, WIC), and the variance between individuals (betweenindividual component, BIC) so that TNW = WIC + BIC. Roughgarden developed
this framework for a single continuous variable such as prey length, but later
Roughgarden (1979) proposed a measure that uses the Shannon-Weaver index as a
proxy for variance in discrete data. In both continuous and discrete cases, the
relative degree of individual specialization (IS) can be measured as the proportion
of TNW explained by within-individual variation (WIC/TNW). If all individuals
utilize the full range of the population’s niche this value approaches 1, whereas
smaller values indicate decreasing inter-individual overlap and hence higher
individual specialization. Originally Roughgarden developed this framework for
within- and between-phenotype variation (or between-sex variation, Ebenman and
Nilson 1982), but it can also be applied at the individual level (Bolnick et al. 2002).
As mentioned, intrapopulation niche variation can occur by subdividing the
population’s niche in a number of different ways, for example into sex, age, or
obvious distinct morphs.
The goal of paper I was to demonstrate that there also could be important
niche variation among individuals. Therefore we defined an “individual specialist”
as an individual whose niche is substantially narrower than its population’s niche
for reasons not attributable to its sex, age, or discrete (a priori) morphological
group. Note however that individual specialization is characterized not by a low
WIC per se but by a low WIC relative to TNW. Thus, in paper I we surveyed the
literature for examples of individual specialization on resources, such as prey taxa,
host plants or oviposition sites. When possible we noted the morphological
distribution, if it had a genetic basis, the timescale of consistency and if there were
any trade-offs associated with the individual specialization. Papers II, III, IV, V
and VI all intend to investigate various components and mechanisms behind
individual variation outlined from paper I.
13
Major results and discussion
“Hence I look at individual differences … as being the first step towards such slight
varieties as are barely thought worth recording in works on natural history. And I look at
varieties which are in any degree more distinct and permanent, as steps leading to more
strongly marked and permanent varieties; and at these latter, as leading to sub-species, and
to species.”
(Darwin, C. 1859).
As Darwin mention in the “Origin” (though not talking directly about diet
variation), individual diet specializations and discrete resource polymorphisms may
provide important stepping-stones for speciation. However, most empirical and
theoretical studies of resource use treat conspecific individuals as ecological
equivalent. Recently, ecological segregation with correlations between phenotype
and resource use has been documented in resource polymorphisms where we have
discrete morphs specializing on different resources (reviewed in Wimberger 1994,
Skúlason and Smith 1995, Smith and Skúlason 1996). Parallel to the research on
resource polymorphisms, researchers have documented cases where individuals
specialize on different resources without any distinct differences in morphology. In
paper I, we review the literature on individual specialization and found evidence
for individual specialization for 93 species distributed across a broad range of
taxonomic groups (Table 1). Although few studies actually had quantified the
degree to which individuals were specialized relative to their population, the
between individual variation sometimes comprised the majority of the population’s
niche width (paper I), where feeding behavior within a population can span those
of several families (e.g. Werner and Sherry 1987).
Table 1. Summary table of the number
of species in each taxonomic group
where individual specialization have
been noted (data from paper I, table 1).
Taxonomic
group
Number
of Species
Gastropods
Crustaceans
Insects
Fishes
Reptiles and amphibians
Birds
Mammals
5
5
18
29
5
20
11
Why would a group of individuals end up using different resources
despite sharing a common environment? The answer closest to hand is that
individuals will use different resources if they have different resource-use
14
efficiencies, reflecting variable morphological, behavioral or physiological
capacities to search and handle alternative resources. According to this, most of the
foraging specialization can be associated with morphological variation independent
of the magnitude (Robinson and Wilson 1994, Skúlason and Smith 1995, Smith
and Skúlason 1996, paper I). Yet, this poses a second problem; why does
phenotypic variation result in efficiency variation? In many cases where
individuals of different morphologies specialize in different niches, evidence has
been found for efficiency trade-offs between the alternate niches (e.g. Ehlinger and
Wilson 1988, Ehlinger 1990, Smith 1990, Robinson et al. 1993, Schluter 1993,
1995, Huckins 1997, Paper I, III). Without such trade-offs constraining efficiency
on different resources, phenotypic variation would not produce functional
variation, and all individuals would be equally capable of using all resources
(Taper and Case 1985).
Most cases of resource polymorphism and adaptive variation within fish
populations show that the segregation occurs between the littoral and pelagic
habitats. So in order to investigate the relationship between morphology and
habitat/diet specialization in perch we sampled perch from the littoral and pelagic
habitats of Lake Trehörningen (papers II and III). Lake Trehörningen is situated in
central Sweden (latitude 64° 00’ 50’’ N, longitude 20° 08’ 00’’ E) with a lake area
of 2.37 km2, and a maximum depth of 17 m. In addition to perch, Lake
Trehörningen also contains roach (Rutilus rutilus), pike (Esox lucius), and vendace
(Coregonus albula).
We have found in Lake Trehörningen and other lakes that perch
individuals from the littoral zone are deeper bodied and forage on littoral prey
types compared to the more streamlined individuals that forage on pelagic prey
types and are found in the pelagic zone (Paper II, III, Eklöv and Svanbäck
unpublished data). This difference in morphology corresponds to functional
expectations for fish species that occupy these habitats (e.g. Webb 1984). The
difference in morphology and diet of perch between the two habitats have also
been shown to reflect morphology dependent foraging efficiencies, where deeper
bodied individuals caught in the littoral zone had higher foraging efficiency in
experiments with structure. The more streamlined individuals from the pelagic
zone on the other hand had higher foraging efficiency in open water trials (paper
III).
The foraging efficiency trade-offs found in paper III were due to
behavioral differences in both searching for and attacking prey. The littoral perch
used slower search velocity than pelagic perch when foraging in open water, and
their search velocity was not much affected by foraging in vegetation. The search
velocity of the pelagic perch was on the other hand much affected by foraging in
vegetation, and pelagic perch thus ended up with slower search velocity in
vegetation trials compared to littoral perch. For pelagic prey types a higher search
velocity was related to a higher detection rate whereas for littoral prey types a
slower search velocity was related to higher detection rate (Svanbäck and Eklöv
2004). Furthermore, the littoral perch used a slower attack velocity while attacking
15
prey than pelagic perch did (paper III). For the pelagic macroinvertebrate
(Chaoborus sp.) in the vegetation trials and the littoral prey type used (mayfly
larvae) in both vegetation and open water, a slower attack speed was related to a
higher capture success whereas a higher attack speed was related to a higher
capture success in open water trials for Chaoborus sp. (Svanbäck and Eklöv 2004).
Overall, the differences in behaviors between littoral and pelagic perch resulted in
the differences in foraging efficiencies in perch from the two habitats (paper III,
Svanbäck and Eklöv 2004). The foraging efficiency results found in perch are
similar to those found in other fish species (Schluter 1993, Ehlinger 1990) and such
trade-offs in foraging efficiency has been suggested to be important in creating
intraspecific differences between morphologies in resource and habitat use (e.g.
Smith 1987, Ehlinger and Wilson 1988, Ehlinger 1990, Schluter 1993, 1995).
Other studies emphasize the importance of learning for foraging
specialization (e.g. Lewis 1986, Pietrewicz and Kamil 1979, Heinrich 1976,
Partridge 1976). For example, in a laboratory study of Pieris rapae, the cabbage
butterfly, Lewis (1986) found that the time required for individuals to find the
source of nectar in flowers decreased with successive attempts and that learning to
extract nectar from a second species inferred with the ability to extract nectar from
the first. There is no reason why learning should not aid in creating individual diet
specialization in perch and as such, learning should work in concert with
morphological variation.
The ontogeny of foraging specialization
A fundamental biological reality among most organisms is that they grow in size
during their ontogeny. The increase in size will affect fundamental ecological
properties such as energy demand, the ability to find and process food and the
ability to avoid predators (Werner 1988, Persson 1988). In fish, the increase in size
will affect morphological and behavioral properties. For example, as fish are gapelimited predators, a fish will be restricted in its prey use by the size of its gape
(Wainwright and Richard 1995). Whereas the habitat-morphology relation in paper
III only concerns the overall difference in morphology between the two habitats,
paper II analyzed the role of adaptive variation during ontogeny in perch. More
specifically, in paper II we investigated if there were any differences in
morphological trajectories during the ontogeny of perch collected from the two
habitats of Lake Trehörningen and how the diet choice related to the morphology.
We found in paper II that perch get relative deeper body morphology as
they grow. Such change in morphology during ontogeny will make larger perch
more adapted to benthic/littoral feeding compared to the smaller more streamlined
young perch (paper III). These factors affecting resource intake in fish may in turn
result in that only a small portion of the available resource spectra can be
processed.
The above discussion is reflected in the resource use of perch from Lake
Trehörningen. At small size classes, perch of both littoral and pelagic origin are
feeding on zooplankton (paper II). This makes the degree of individual
specialization very low (IS ~ 1, Fig. 2). The perch in the littoral zone then starts to
16
1
0.8
0.6
0.4
0.2
0
60
-6
9
70
-7
9
80
-8
9
90
-9
10 9
01
11 09
01
12 1 9
01
1 3 29
01
14 3 9
01
15 4 9
01
16 59
01
1 7 69
01
18 7 9
01
19 89
01
20 99
020
9
Individual specialization (IS)
feed on macroinvertebrates at intermediate sizes, whereas the pelagic perch keeps
on feeding on zooplankton (paper II) which makes the degree of individual
specialization increase (Fig. 2). At the largest size classes of perch caught in Lake
Trehörningen, all individuals in the littoral zone fed on fish whereas the pelagic
individuals fed either on fish or zooplankton keeping the degree of individual
specialization high. In other lakes we have found the same pattern of size and
individual specialization as in Lake Trehörningen. However, at larger size classes
than those caught in Lake Trehörningen, both littoral and pelagic perch fed on fish,
which therefore lowered the degree of individual specialization again (Svanbäck
and Eklöv, data).
Size class
Figure 2. The degree of individual specialization in perch from lake Trehörningen
depending on size class. Note that high IS (i.e. IS close to 1) means low degree of
specialization. The degree of individual specialization is calculated according to equations
1 and 2 in paper VI.
Divergent natural selection
In paper III we found strong effects of morphology on foraging efficiency of perch
in the laboratory (see also Svanbäck and Eklöv 2004). What evidence is there that
these effects are important for trophic polymorphism and fitness among fish
populations in the field? Divergent natural selection between and within
populations exploiting different resources is hypothesized to be a primary cause of
trophic polymorphisms and adaptive radiation (Lack 1947, Schluter and Grant
1984, Grant 1986, Schluter 1993, 1995, Skúlason and Smith 1995, Robinson et al.
1996, Smith and Skúlason 1996). An easy but weak test of this hypothesis has
been to look for correlations between morphology and resource use. This is a
pattern that we have found in many lakes for perch and other fish species like roach
(paper II and III, Eklöv and Svanbäck, data, Fransson, Eklöv and Svanbäck, data),
17
and there are several other studies showing a similar relationship (e.g. Grant 1986,
Smith 1987, Schluter and McPhail 1992, Hjelm et al. 2000). Furthermore, we
found correlations between, and trade-offs within morphology and resource use
efficiency (paper III, Svanbäck and Eklöv 2004), which is another criterion for
divergent natural selection (e.g. Smith 1987, Ehlinger 1990, Losos 1990, Benkman
1993, Schluter 1993). The resource use efficiency found in perch (paper III,
Svanbäck and Eklöv 2004) is hypothesized to give rise to the environmentdependent correlation between morphology and growth (fitness) that we observed
in paper III (Robinson et al. 1996, Schluter 1993, 1995).
In paper III, we found that the deeper bodied individuals from the littoral
zone grew faster than the more streamlined individuals whereas the opposite
pattern was found in the perch from the pelagic zone. Even though growth is not a
direct measure of fitness, growth rate is an important component of fitness in fishes
because size is correlated with a number of fitness components such as increased
reproductive success, reduced vulnerability to predation, increased over-winter
survival and increased success in competition (e.g. van den Berghe and Gross
1989, Ridgway et al. 1991, Mittelbach 1981, 1984, Lundvall et al. 1999, Werner
and Hall 1988, Post and Evans 1989, Merrett 1994). This finding would suggest
that the fitness trade-off appears to be concave, which would favor the evolution of
specialist phenotypes in each habitat (Schluter 1995, Robinson et al. 1996),
although factors such as temporal variation in resource abundance can influence
this outcome (Wilson and Yoshimura 1994). Similar patterns of growth has also
been found in pumpkinseed sunfish (Lepomis gibbosus) where the deeper bodied
individuals from the littoral zone grew faster than the more streamlined individuals
whereas the opposite pattern was found in the pumpkinseed sunfish from the
pelagic zone (Robinson et al. 1996).
Phenotypic plasticity and genetics in adaptive morphological variation
In forming a phenotype, two interacting processes act on the developmental
programme; the genome and the environment (Scheiner 1993). Genetic variation
for a fixed phenotype has been hypothesized to be favored in stable environments
(Hori 1993, Smith 1993) whereas phenotypic plasticity can be an important
adaptive strategy for coping with environmental variability (Stearns 1989, Scheiner
1993). In stable environments the selection regimes are rather constant (Dieckmann
and Doebeli 1999, Doebeli and Dieckmann 2000) which would favor genetic
variation for a fixed phenotype (DeWitt et al. 1998). Paper IV attempts to measure
the relative importance of genetic differences versus phenotypic plasticity in perch
from Lake Trehörningen. We performed a common garden experiment were adults
from the two lake habitats spawned separately and their offspring were raised in
enclosures with either open water or vegetation in an artificial pond.
In paper IV we found that the morphological variation in perch to a large
extent was determined by environmental factors and that the genetic variation only
contributed to a small amount to the morphological variation. In a similar
experiment, Robinson and Wilson (1996) showed that environment determined
most of the morphological variation for pumpkinseed sunfish, though the genetic
18
component influenced the variation more than in perch. Furthermore, in paper IV
we also found that the trade-offs in foraging efficiency found in paper III not only
have a morphological basis, but also that it might have a genetic basis. Perch from
littoral parents had a higher proportion of littoral prey types in their diet compared
to perch from pelagic parents independent of the environment they were grown in.
This fact might suggest that there are behavioral differences between littoral and
pelagic perch that is not transformed into morphological differences during one
season of growth. It might also suggest that the structural component of the habitat
have a bigger effect on morphological variation than the prey items have.
Correspondingly, Olsson and Eklöv (manuscript) have shown in an experiment,
combining structural complexity and diet, that structure had a bigger effect than
diet on morphological development in perch.
How come phenotypic plasticity dominates genetic variation in forming
perch body morphology? As discussed above, in size-structured populations, it is
common for individuals to exploit several niches sequential in the course of their
life history (Werner and Gilliam 1984). Because perch potentially undergoes two
niche shifts during its lifetime, i.e. from zooplanktivory to benthivory and then
from benthivory to piscivory (e.g. Persson 1988, Hjelm et al. 2000, paper II) and
the optimal morphology related to planktivory, benthivory and piscivory are not
related to each other (Webb 1984) it might be necessary to compromise between
the optimal forms in order to perform well in all three niches. Some degree of
plasticity will then aid in adapting to the new niche that the individual experience.
In addition to ontogenetic influences on diet choice, variation in resource
levels in both habitats will influence the diet choice of individuals. Such variations
in resource levels can be from fluctuating intensity of intra- and inter-specific
competition (Persson et al. 2000, paper VI), or due to environmental variations
(Grant 1986, Grant and Grant 2002). Furthermore, predation can be a major
selective factor (e.g. Reznick et al. 1990, Vamosi 2002) and besides selecting for
different morphologies, the presence of predators has shown to induce habitat shifts
in prey individuals (e.g. Eklöv and Diehl 1994, Persson and Eklöv 1995). The
density of predators or the predation pressure might also vary within or between
seasons (e.g. Persson et al. 2000, Eklöv and Svanbäck data). So not only might
intra-specific competition and inter-specific competition change through time,
predation pressure might also fluctuate through time.
However, we have in paper IV, but also in other studies of perch (paper
V, Hjelm et al. 2001, Olsson and Eklöv manus) shown that the response to the
environment is fast. These findings about phenotypic plasticity in perch
corroborate the results of paper II that the differences in morphological growth
trajectories between the littoral and pelagic perch might be due to phenotypic
plasticity.
The effect of predation on adaptive variation and diet specialization
There has been a long-standing debate whether intra-specific competition can be a
mechanism driving phenotypic divergence among species and also a process of
speciation. This debate has led to extensive research in this area and the evidence
19
so far support that this is a likely outcome (e.g. Schluter 2000, Bolnick 2001).
However, the debate has also lead to a neglect of other important ecological factors
for the adaptive divergence of species, such as the presence of predators (see
Abrams 2000, Abrams and Chen 2002). Predation has been shown in numerous
theoretical and empirical examples to have strong direct and indirect effects on
ecological interactions, but also on evolutionary important traits of organisms (Sih
et al. 1985, Lima and Dill 1990, Lima 1998, Vamosi 2002). Such direct and
indirect responses could for example involve morphological and behavioral
adaptations that reduce vulnerability to predators (Lima and Dill 1990, Brönmark
and Miner 1992). Furthermore, a reduction of competitors could potentially change
the selective regime connected to resource competition (Rundle et al. 2003).
However, the role of predation during resource polymorphisms and adaptive
variation has received limited attention.
The major aim with paper V was to experimentally test the prediction that
variation in predation risk could cause adaptive changes in phenotypic traits in a
fish population without necessarily affecting intraspecific competitive interactions.
The prediction lean on the assumption that food resource types varies among
habitats, and that a predator induced habitat shift in the prey would lead to
differential resource use and consequently shifts in adaptive characters.
A behavioral response to the presence of predators is to shift habitat to a
less risky habitat (Eklöv and Diehl 1994, Persson and Eklöv 1995). However, the
optimal habitat for escaping predation might not be the optimal habitat for
foraging. The prey individual might thereby end up in a safer habitat but with
morphology maladapted for foraging. In such a situation, it would be adaptive for
the prey individual to change its morphology to become more adapted to the new
feeding environment. The results of paper V suggest that the presence of predators
may be important for trophic polymorphisms. When the predation risk was higher
in one habitat, the prey fish shifted to the other habitat and fed on the specific food
resources found in this habitat. The restricted diet did in turn affect the phenotype
of the prey fish in a predicted way. When the open water environment was safer the
prey fish foraged in the open water and changed to a more streamlined
morphology, whereas the fish fed littoral preys and got deeper body morphologies
when the vegetated habitat was safer. There was no difference in prey mass
increase across treatments, indicating that the competition for resources was
probably weak and that the differential resource use of the prey fish probably
resulted from the restricted habitat use due to predation risk.
The restriction in habitat also reflected the diet and degree of individual
specialization. When the prey was restricted to one habitat due to differences in
predation pressure they all fed on the same food resource. In treatments with equal
predator densities in both habitats individual specialization was high, since some
individuals fed littoral resources and others pelagic resources. As a result of
differences in diet specialization among treatments we found that in treatments
with high degree of individual specialization, there was also a higher degree of
morphological variation. Thus, if there are unequal predation pressures among
habitats then morphological variation might be constrained in the same sense as a
20
competitor species would do (character displacement, see Robinson and Wilson
1994).
Density dependent changes in individual diet specialization
Theoretical analyses and empirical studies of diet choice, polymorphism and
sympatric speciation are usually restricted to only consider populations at
numerical equilibrium (e.g. paper I, Skúlason and Smith 1995, Smith and Skúlason
1996, Dieckman and Doebeli 1999; Doebeli and Dieckman 2000). In contrasts,
many populations fluctuate in density over time in relation to resource levels (e.g.
Grant 1986; Mittelbach et al. 1995; Smith et al. 1999; Persson et al. 2003; Grant
and Grant 2002; Klemola et al. 2002). Fluctuations in resource levels have been
related to external environmental factors (e.g. Grant and Grant 2002) or
intrinsically driven dynamics (e.g. Persson et al. 2003).
In paper VI, we studied a perch population that experienced intrinsic
cycling due to size-dependent inter-cohort competition and cannibalism, involving
a more than twenty fold change in the density of adult individuals (Person et al.
2000, 2003). The purpose of paper VI was to analyze the effect of intra-specific
competition on individual diet specialization in a population dynamical context.
The study was carried out in Lake Abborrtjärn 3, a small (9.3 ha, maximum depth
12 m) lake in central Sweden (latitude 64° 29’ N, longitude 19° 26’ E). In this
paper we focus on two main issues behind individual specialization. First, we
investigate the mechanisms (WIC and TNW) that may give rise to differences in
individual specialization. Second, we investigate the effect of population density on
diet choice in perch including feedbacks of perch consumption on resource levels.
When adult perch density was low, the abundances of benthic
invertebrate and YOY perch were high and dominated the diet of adult perch,
whereas the density of zooplankton was low due to predation from YOY perch.
Thus at low densities of adult perch the degree of individual specialization was
low. At high adult perch densities, benthic invertebrate abundance was lower and
zooplankton level was higher and some perch switched to feed on zooplankton
increasing individual specialization. This corroborates the results of Persson et al.
(2000) where it was found that adult perch were all found within the littoral zone at
low densities and with an increase in the adult population a larger proportion of the
population used the off-shore habitat as the preferred prey types (YOY perch and
macroinvertebrates) were scarce.
The results of paper VI show that individual specialization may fluctuate
with population density through feedback mechanisms via resource levels.
Expansions of population niche width and adaptations to novel resources have been
suggested to be one of the causes of resource polymorphisms and ultimately
sympatric speciation for equilibrium conditions (Smith and Skúlason 1996;
Dieckman and Doebeli 1999; Doebeli and Dieckman 2000; Claessen and
Dieckman 2002). However, there are only a few empirical studies that have looked
at the combination of population dynamics and evolutionary dynamics (for
21
examples see Tamarin and Krebs 1969; Gaines and Krebs 1971; Sinervo et al.
2000).
Fluctuations in density may have profound implications on the evolution
of resource polymorphisms. In our studied perch population all adult perch were
found within the littoral habitat at low adult densities (Persson et al. 2000). This
means that deeper bodied individuals will have the highest fitness in this phase
(Fig. 3) (Robinson et al. 1996; paper III). In contrast, at high adult densities the
same fitness scenario will be true for the ones staying in the littoral zone whereas
the slender-bodied individuals will have the highest fitness in the pelagic zone
(paper III) (Fig. 3). Thus, the fitness landscape for the adult population will
fluctuate with population density and depend on both density and frequency of
different phenotypes (Wilson and Turelli 1986, Svanbäck and Bolnick manuscript).
The fluctuating fitness landscape scenario therefore suggest that selection will
favor phenotypic plasticity rather than genetically determined morphologies in this
perch population as found in paper IV.
Figure 3. Hypothesized fitness landscapes for perch at low and high densities. At low
densities perch occupy only the littoral habitat whereas at high densities perch occupy both
habitats (Persson et al. 2000). The fitness should thus follow fluctuations in densities
between the right and the left graph, with many stages in between.
Concluding remarks and future perspectives
Although plenty examples of trophic polymorphism and adaptive variation in
freshwater fishes exist, we still know very little about the mechanisms that drive
this pattern. The most common explanation for trophic polymorphism is that this is
caused by a release in interspecific competition (Robinson and Wilson 1994,
22
Schluter 1994, Skúlason and Smith 1995). However, in the natural environment
both predation and competition is probably involved and it is likely that the
phenotypic response is affected by a trade-off between foraging gain and predation
risk. The trade-off between foraging and predation risk has been shown to be the
major factor influencing species interactions in ecological communities (Werner
and Anholt 1993, Lima 1998) and theoretical analyses show that this trade-off may
also lead to evolutionary branching and ultimately speciation (Abrams 2003).
In reality, individual variation and polymorphism are ends of a continuum
of increasingly discrete variation. This thesis focuses on the less discrete end of this
continuum, in which individuals cannot clearly be assigned to distinct
morphotypes. In this thesis I have shown that the occurrence of individual diet
specialization in nature is a widely distributed phenomenon and that it to a large
extent depends on trade-offs in foraging efficiency on alternate resources. I have
also shown that this trade-off in foraging efficiency is connected to morphological
characteristics of the forager. Furthermore, in a common garden experiment I have
shown that the morphological variation in perch connected to diet and habitat
choice in nature was mainly a result of phenotypic plasticity and only to a small
degree to genetic variation. The reason for such a large degree of phenotypic
plasticity in perch might be due to fluctuations in the level of competition or
changes in predation pressures through time.
In this thesis I have only grazed over a number of potential mechanisms
that might influence morphological variation and diet choice of individuals.
However, each paper in itself raises a couple of interesting questions for further
research. For example;
1) Paper II focuses a lot on the ontogenetic aspect of adaptive variation. Is
ontogenetic niche shifts a mechanism that promotes phenotypic plasticity
in adaptive characters? In a recent paper, Claessen and Dieckmann (2002)
found that diversification and speciation could occur along the axis of
optimal size for ontogenetic niche shift. Further research on ontogenetic
niche shifts in adaptive variation could possibly determine the effect and
importance of ontogenetic niche shifts in diversification.
2) The indication of disruptive selection in paper III raises the question; how
common is this pattern among fish populations in general and particularly
in perch populations? This aspect is interesting on its own, but also
competitive disruptive selection is supposed to be the main mechanism
behind resource polymorphisms and could eventually lead to sympatric
speciation.
3) Genetically determined phenotypes or phenotypic plasticity? Paper IV and
other research in this area show that there can be a varying degree to which
these two factors determine the phenotype of an individual. But what are
the proximate mechanisms behind this variation in adaptive variation and
resource polymorphisms?
4) Research on the effect and importance of predation in adaptive variation
and resource polymorphism is in its infancy. Paper V focuses on
23
behavioral responses and morphological changes in the prey as a function
of differences in predation pressure among habitats. However, there are
other ways predator-prey interactions can influence resource
polymorphisms. Predation may actually select for certain morphology as a
consequence of differences in escape ability between preys of different
morphologies. If so, is the escape ability – morphology correlation equal
among habitats, or are different morphologies adapted to escape predators
in different habitats? Furthermore, a prey individual can change its
morphology in response to the presence of predators as has been found in
crusian carp (Brönmark and Miner 1992). How would such morphological
response influence resource intake rate and how does it influence resource
polymorphisms and adaptive variation.
5) Population dynamics and evolutionary dynamics. Paper VI suggests that
population dynamics can influence the evolutionary dynamics in a
population. Other recent papers have suggested that evolutionary dynamics
can influence the population dynamics (Yoshida et al. 2003). However, the
interplay between population dynamics and evolutionary dynamics is also
in its infancy. Could the observed population dynamics in paper VI explain
the low degree of genetic variation found in perch (paper IV), or are there
other mechanisms driving the evolution of phenotypic plasticity? These
questions can only be answered with further empirical and theoretical
studies.
The occurrence of resource polymorphism is supposed to be higher in regions with
species poor faunas (Robinson and Schluter 2000). However, In lake Trehörningen
there are only a few other species present, but still we find the same kind of
adaptive variation in more species rich lakes in the Uppland region (Eklöv and
Svanbäck data). Moreover, both in Lake Trehörningen (Svanbäck data) and in
lakes in Uppland (Fransson, Eklöv and Svanbäck data) where we find differences
in morphology between littoral and pelagic perch, we also find similar differences
between littoral and pelagic roach. To spice it up even more, in Lake Erken I have
found evidence for that three different fish species show the same pattern of
adaptive variation at the same sampling time (Svanbäck data). So the real challenge
for future research in this area is to merge individual variation, population and
community dynamics, and evolutionary dynamics.
“Natural selection, as has just been remarked, leads to divergence of character and to much
extinction of the less improved and intermediate forms of life. On these principles, I
believe, the nature of the affinities of all organic beings may be explained”
(Darwin, C. 1859).
24
Acknowledgements
I would like to thank Mario Quevedo, Lennart Persson, and Jens Olsson for
comments on earlier drafts of this thesis summary. The work in this thesis has been
funded by grants from: STINT, JA Ahlstrands Fond, Hjerta-Rezius Stipendiefond,
Stiftelsen Oscar and Lili Lamms Minne, (to Richard Svanbäck), NSF Graduate
Research Fellowship (to D.I.B., C.D.H., L.H.Y., J.M.D., and M.L.F.), the ARCS
Foundation (to D.I.B.), the UC Davis Graduate Group in Ecology (to J.A.F.),
Swedish Council for Forestry and Agricultural Research (to Peter Eklöv), and the
Swedish Research Council and the Swedish Research Council for Environment,
Agricultural Sciences and Spatial Planning (to Peter Eklöv and Lennart Persson)
and the Turelli Memorial Fund to Uncover the Truth about Speciation and they are
all greatly acknowledged.
References
Abrams, P.A. 2000. Character shifts of prey species that share predators. American
Naturalist 156:S45-S61.
Abrams, P.A. 2003. Can adaptive evolution or behaviour lead to diversification of
traits determining a trade-off between foraging gain and predation risk?
Evolutionary Ecology Research 5:653-670.
Abrams, P.A., and Chen, X. 2002. The evolution of traits affecting resource
acquisition and predator vulnerability: Character displacement under real
and apparent competition. American Naturalist 160:692-704.
Alatalo, R.V., Gustafsson, L., and Lundberg, A. 1990. Phenotypic selection on
heritable size traits: environmental variance and genetic response. American
Naturalist 135:464-471.
Benkman, C.W. 1993. Adaptation of single resources and the evolution crossbill
(Loxia) diversity. Ecological Monographs 63:305-325.
Bernstein, R.A. 1979. Evolution of niche breadth in populations of ants. American
Naturalist 114:533-544.
Bolnick, D.I. 2001. Intraspecific competition favours niche width expansion in
Drosophila melanogaster. Nature 410:463-466.
Bolnick, D.I., Yang, L.H., Fordyce, J.A., Davis, J.M., and Svanbäck, R. 2002.
Measuring individual-level trophic specialization. Ecology 83:2936-2941.
Bourke, P., Magnan, P., and Rodríguez, M.A. 1997. Individual variations in habitat
use and morphology in brook charr. Journal of Fish Biology 51:783-794
Brönmark, C., and Miner, J.G. 1992. Predator-induced phenotypical change in
body morphology in crucian carp. Science 258:1348-1350.
Byström, P., Persson, L., and Wahlström, E. 1998. Competition between predators
and prey: juvenile bottlenecks in whole-lake experiments. Ecology 79:21532167.
25
Byström, P., Persson, L., Wahlström, E., and Westman, E. 2003. Size- and densitydependent habitat use in predators: consequences for habitat shifts in young
fish. Journal of Animal Ecology 72:156-168.
Claessen, D., and Dieckmann, U. 2002. Ontogenetic niche shifts and evolutionary
branching in size-structured populations. Evolutionary Ecology Research
4:189-217.
Coles, T.F. 1981. The distribution of perch, Perca fluviatilis L., throughout their
first year in Llyn Tegid, North Wales. Journal of Fish Biology 18:15-30.
Craig, J.F. 1978. A study of food and feeding of perch, Perca fluviatilis L., in
Windermere. Freshwater Biology 8:59-68.
Darwin, C. 1859. On the origin of species. John Murray, London.
DeWitt, T.J., Sih, A., and Wilson, D.S. 1998. Cost and limits of phenotypic
plasticity. Trends in Ecology and Evolution 13:77-81.
Diaz, M. 1994. Variability in seed size selection by granivorous passerines: effects
of bird size, bird size variability, and ecological plasticity. Oecologia 99:1-6.
Dieckmann, U., and M. Doebeli. 1999. On the origin of species by sympatric
speciation. Nature 400:354-357.
Doebeli, M., and Dieckmann, U. 2000. Evolutionary branching and sympatric
speciation caused by different types of ecological interactions. American
Naturalist 156:S77-S101.
Dynes, J., Magnan, P., Bernatchez, L., and Rodríguez, M.A. 1999. Genetic and
morphological variation between two forms of lacustrine brook charr.
Journal of Fish Biology 54: 955-972
Ebenman, B., and Nilsson. S.G. 1982. Components of niche width in a territorial
bird species: habitat utilization in males and females of the chaffinch
(Fringilla coelebs) on islands and mainland. American Naturalist 199:331344.
Ehlinger, T.J. 1990. Habitat choice and phenotype-limited feeding efficiency in
bluegill: individual differences and trophic polymorphism. Ecology 71:886896.
Ehlinger, T.J. and Wilson, D.S. 1988. Complex foraging polymorphism in bluegill
sunfish. Proceedings of the National Academy of Science, USA 85:18781882
Eklöv, P. 1997. Effects of habitat complexity and prey abundance on the spatial
and temporal distribution of perch (Perca fluviatilis) and pike (Esox lucius).
Canadian Journal of Fisheries and Aquatic Science 54:1520-1531.
Eklöv, P., and Diehl, S. 1994. Piscivore efficiency and refuging prey: the
importance of predator search mode. Oecologia 98:344-353.
Foote, C.J., Wood, C.C., and Withler, R.E. 1989. Biochemical genetic comparision
of sockeye salmon and kokanee, the anadromous and nonanadromous forms
of Oncorhynchus nerka. Canadian Journal of Fisheries and Aquatic Science
46:149-158.
Gaines, M.S., and Krebs, C.J. 1971. Genetic changes in fluctuating vole
populations. Evolution 25:702-723.
26
Grant, P.R. 1972. Convergent and divergent character displacement. Biological
Journal of the Linnean Society 4:39-69.
Grant, P.R. 1986. Ecology and evolution of Darwin’s finches. Princeton University
Press, Princeton, New Jersey, USA.
Grant, P.R., and Grant, B.R. 2002. Unpredictable evolution in a 30-year study of
Darwin’s finches. Science, 296:707-711.
Grant, P.R., Grant, B.R., Smith, J.N.M., Abbott, I.J., and Abbott. L.K. 1976.
Darwin's finches: Population variation and natural selection. Proceedings of
the National Academy of Sciences 73:257-261.
Guma’a, S.A. 1978. The food and feeding habits of young perch, Perca fluviatilis,
in Windermere. Freshwater Biology 8:177-187.
Harvell, C.D. 1990. The ecology and evolution of inducible defenses. The
Quarterly Review of Biology 65:323-340
Heinrich, B. 1976. The foraging specializations of individual bumblebees.
Ecological Monographs 46:105-128.
Hindar, K. and Jonsson, B. 1982. Habitat and food segregation of dwarf and
normal arctic charr (Salvelinus alpinus) from Vagnsvatnet Lake, Western
Norway. Canadian Journal of Fisheries and Aquatic Science 39:1030-1045
Hindar, K., Ryman, N., and Ståhl, G. 1986. Genetic differentiation among local
populations and morphotypes of Arctic charr, Salvelinus alpinus. Biological
Journal of the Linnean Society 27:269-285
Hjelm, J., Persson, L., and Christensen, B. 2000. Growth, morphological variation
and ontogenetic niche shifts in perch (Perca fluviatilis) in relation to
resource availability. Oecologia 122:190-199.
Hjelm, J., Svanbäck, R., Byström, P., Persson, L. and Wahlström, E. 2001. Dietdependent body morphology and ontogenetic reaction norms in a juvenile
omnivore. Oikos 95:311-323.
Hori, M. 1993. Frequency-dependent natural selection in the handedness of scaleeating cichlid fish. Science 260:216-219.
Howland, H.C. 1974. Optimal strategies for predator avoidance: the relative
importance of speed and manoeuvrability. Journal of Theoretical Biology
47:333-350.
Huckins, C.J.F. 1997. Functional linkages among morphology, feeding
performance, diet, and competitive ability in molluscivorous sunfish.
Ecology 78:2401-2414.
Johansson, L., and Persson, L. 1986. The fish community of temperate, eutrophic
lakes. Pages 237-266 in B. Reimann, and M. Søndergaard, eds. Carbon
dynamics of eutrophic, temperate lakes: the structure and functions of the
pelagic environment. Elsevier, Amsterdam, The Netherlands.
Keast, A. and Webb, D. 1966. Mouth and body form relative to feeding ecology in
fish fauna of a small lake, Lake Opinicon, Ontario. Journal of the Fisheries
Research Board of Canada 23:1845-1874
Klemola, T., Tanhuanpää, M., Korpimäki, E. and Ruohomäki, K. 2002. Specialist
and generalist natural enemies as an explanation for geographical gradients
in population cycles of northern herbivores. Oikos 99:83-94.
27
Lack, D. 1947. Darwin’s finches. Cambridge University Press, Cambridge, UK.
Lavin, P.A., and McPhail, J.D. 1985. The evolution of freshwater diversity in the
threespine stickleback (Gasterosteus aculeatus): site-specific differentiation
of trophic morphology. Canadian Journal of Zoology 63:2632-2638
Lavin, P.A., and McPhail, J.D. 1986. Adaptive divergence of trophic phenotype
among freshwater populations of the threespine stickleback (Gasterosteus
aculeatus). Canadian Journal of Fisheries and Aquatic Science 43:2455-2463
Levins, R. 1968. Evolution in changing environments: some theoretical
explorations. Princeton University Press, Princeton.
Lewis, A.C. 1986. Memory constraints and flower choice in Pieris rapae. Science
232:863-865.
Lima, S.L. 1998. Stress and decision making under the risk of predation: recent
developments from behavioral, reproductive, and ecological perspectives.
Advances in the study of Behavior 27:215-289.
Lima, S.L. and Dill, L.M. 1990. Behavioural decisions made under predation: a
rewiev and prospectus. Canadian Journal of Zoology 68:619-640.
Lindsey, C.C. 1981. Stocks are chameleons: Plastisity in gill rakers of coregonid
fishes. Canadian Journal of Fisheries and Aquatic Science 38:1497-1506
Losos, J.B. 1990. The evolution of form and function: morphology and locomotor
performance in west indian Anolis lizards. Evolution 44:1189-1203.
Lundvall, D., Svanbäck, R., Persson, L. and Byström, P. 1999. Size-dependent
predation - the interactions between predator foraging and prey avoidance
abilities. Canadian Journal of Fisheries and Aquatic Sciences 56:1285-1292.
Magnan, P. 1988. Interactions between Brook charr, Salvelinus fontinalis, and
nonsalmonid species: ecological shift, morphological shift, and their impact
on zooplankton communities. Canadian Journal of Fisheries and Aquatic
Science 45:999-1009
Mann, G.J. and McCart, P.J. 1981. Comparison of sympatric dwarf and normal
populations of least cisco (Coregonus sardinella) inhabiting trout lake,
Yukon Territory. Canadian Journal of Fisheries and Aquatic Science 38:240244.
Merrett, N.R. 1994. Reproduction in the North-Atlantic Ichthyofauna and the
relationship between fecundity and species sizes. Environmental Biology of
Fishes 41:207-245.
Milinski, M. 1987. Competition for non-depleting resources: the ideal free
distribution in sticklebacks. Pages 363-388 in A.C. Kamil, J.R. Krebs, and
H.R. Pulliam, eds. Foraging Behavior. New York, Plenum Press.
Mittelbach, G.G. 1981.Foraging efficiency and body size: A study of optimal diet
and habitat use by bluegills. Ecology 62:1370-1386.
Mittelbach, G.G. 1984.Predation and resource partitioning in two sunfishes
(Centrarchidae). Ecology 65:499-513.
Mittelbach, G.G., Osenberg, C.W., and Wainwright, P.C. 1992. Variation in
resource abundance affects diet and feeding morphology in the pumpkinseed
sunfish (Lepomis gibbosus). Oecologia 90:8-13
28
Mittelbach, G.G., Turner, A.M., Hall, D.J., and Rettig, J.E. 1995. Perturbation and
resilience: a long-term, whole-lake study of predator extinction and
reintroduction. Ecology 76:2347-2360.
Motta, P.J., Clifton, K.B., Hernandez, P., and Eggold, B.T. 1995.
Ecomorphological correlates in ten species of subtropical seagrass fishes:
diet and microhabitat utilization. Environmental Biology of Fishes 44:37-60.
Mousseau, T.A., Sinervo, B., and Endler J.A. 2000. Adaptive genetic variation in
the wild. Oxford University Press, New York
Partridge, L. 1976. Individual differences in feeding efficiencies and feeding
preferences of captive great tits. Animal Behaviour 24:230-240.
Patterson, B.D. 1983. Grasshopper mandibles and the niche variation hypothesis.
Evolution 37:375-388.
Persson, L. 1988. Assymetries in Competetive and Predatory Interactions in Fish
Populations. Pages 205-218 in B. Ebenmann, and L. Persson, eds. SizeStructured Populations. Springer-Verlag, Berlin.
Persson, L., Byström, P. & Wahlström, E. 2000. Cannibalism and competition in
Eurasian perch: population dynamics of an ontogenetic omnivore. Ecology
81:1058-1071.
Persson, L., De Roos, A.M., Claessen, D., Byström, P., Lövgren, J., Sjögren, S.,
Svanbäck, R., Wahlström, E. & Westman. E. 2003. Gigantic cannibals
driving whole lake trophic cascades. Proceedings of the National Academy
of Science of the USA 100:4035-4039.
Persson, L., and Eklöv, P. 1995. Prey refuges affecting interactions between
piscivorous perch and juventle perch and roach. Ecology 76:70-81.
Pietrewicz, A.T., and Kamil, A.C. 1979. Search image formation in the blue jay
(Cyanocitta cristata). Science 204:1332-1333.
Pigeon, D.P., Chouinard, A., and Bernatchez, L. 1997. Multiple modes of
speciation involved in the paralell evolution of sympatric morphotypes of
lake whitefish (Coregonus clupeaformis, Salmonidae). Evolution 51:196205
Pimm, S.L. 1979. Sympatric speciation: a simulation model. Biological Journal of
the Linnean Society 11:131-139.
Polis, G. 1984. Age structure component of niche width and intraspecific resource
partitioning: can age groups function as ecological species? American
Naturalist 123:541-564.
Post, J.R., and Evans, D.O. 1989. Size-dependent overwinter mortality of youngof-the-year yellow perch (Perca flavescens): Laboratory, in situ enclosure,
and field experiments. Canadian Journal of Fisheries and Aquatic Science
46:1958-1968,
Price, T. 1987. Diet variation in a population of Darwin's finches. Ecology
68:1015-1028.
Price, T., Kirkpatric, M., and Arnold, S.J. 1988. Directional selection and the
evolution of breeding date in birds. Science 240:798-799.
Price, T., and Liou, L. 1989. Selection on clutch size in birds. American Naturalist
134:950-959.
29
Rand, D.M. and Lauder, G.V. 1981. Prey capture in the chain pickerel, Esox niger:
correlations between feeding and locomotor behavior. Canadian Journal of
Zoology 59:1072-1078
Reznick, D., Bryga, H., and Endler, J.A. 1990. Experimentally induced life-history
evolution in a natural population. Nature 346:357-359.
Ridgway, M.S., Shuter, B.J. and Post, E.E. 1991. The relative influence of body
size and territorial behaviour on nesting asynchrony in male smallmouth
bass, Micropterus dolomieui (Pisces: Centrarchidae). Journal of Animal
Ecology 60:665-681.
Robinson, B.W. 2000. Trade offs in habitat-specific foraging efficiency and the
nascent adaptive divergence of sticklebacks in lakes. Behavior 137:865-888.
Robinson, B.W., and Schluter, D. 2000. Natural selection and the evolution of
adaptive genetic variation in northern freshwater fishes. Pages 65-94 in T.
Mousseau, B. Sinervo, and J.A. Endler, eds. Adaptive genetic variation in
the wild. Oxford University Press, New York.
Robinson, B.W., and Wilson,. D.S. 1994. Character release and displacement in
fishes: A neglected literature. American Naturalist 144:596-627.
Robinson, B.W., and Wilson, D.S. 1996. Genetic variation and phenotypic
plasticity in a trophically polymorphic population of pumpkinseed sunfish
(Lepomis gibbus). Evolutionary Ecology 10:631-652.
Robinson, B.W., Wilson, D.S., Margosian, A.S., and Lotito, P.T. 1993 Ecological
and morphological differentiation of pumpkinseed sunfish in lakes without
bluegill sunfish. Evolutionary Ecology 7:451-464.
Robinson, B.W., Wilson, D.S., and Shea, G.O. 1996. Trade-offs of ecological
specialization: an intraspecific comparison of pumpkinseed sunfish
phenotypes. Ecology 77:170-178
Rosenzweig. M.L. 1978. Competitive speciation. Biological Journal of the Linnean
Society 10:275-289.
Rothstein, S. I. 1973. The niche variation model-is it valid? American Naturalist
107:598-620.
Roughgarden, J. 1972. Evolution of niche width. American Naturalist 106:683-718.
Roughgarden, J. 1974. Niche width: biogeographic patterns among Anolis lizard
populations. American Naturalist 108:429-442.
Roughgarden, J. 1979. Theory of Population Genetics and Evolutionary Ecology:
An Introduction. Macmillan, New York.
Rundle, H. D., Vamosi, S.M., and Schluter, D. 2003. Experimental test of
predation’s effect on divergent selection during character displacement in
sticklebacks. Proceedings of the National Academy of Science of the USA
100: 14943-14948.
Scheiner. S.M. 1993. Genetics and evolution of phenotypic plasticity. Annual
Review of Ecology and Systematics 24:35-68.
Schluter, D. 1993. Adaptive radiation in sticklebacks: size, shape, and habitat use
efficiency. Ecology 74:699-709.
Schluter, D. 1994. Experimental evidence that competition promotes divergence in
adaptive radiation. Science 266:798-801.
30
Schluter, D. 1995. Adaptive radiation in sticklebacks: trade-offs in feeding
performance and growth. Ecology 76:82-90.
Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford University Press,
New York.
Schluter, D., and Grant, P.R. 1984. Determinants of morphological patterns in
communities of Darwin's finches. American Naturalist 123:175-196.
Schluter, D., and McPhail, J.D. 1992. Ecological character displacement and
speciation in sticklebacks. American Naturalist 140:85-108.
Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: a review
of the evidence. Quarterly Review of Biology 64:419-461.
Shine, R. 1991. Intersexual dietary divergence and the evolution of sexual
dimorphism in snakes. American Naturalist 138:103-122.
Sih, A., Crowley, P., McPeek, M., Petranka, J., and Strohmeier, K. 1985.
Predation, competition, and prey communities: a review of field
experiments. Annual Review of Ecology and Systematics 16:296-311.
Sinervo, B., Svensson, E., and Comendant, T. 2000. Density cycles and an
offspring quantity and quality game driven by natural selection. Nature
406:985-988.
Skúlason, S., and T. B. Smith. 1995. Resource polymorphisms in vertebrates.
Trends in Ecology and Evolution 10:366-370.
Smith, G.R., Rettig, J.E., Mittelbach, G.G., Valiulis, J.L. and Schaak, S.R. 1999.
The effects of fish on assemblages of amphibians in ponds: a field
experiment. Freshwater Biology 41:829-837.
Smith, T.B. 1987. Bill size polymorphism and intraspecific niche utilization in an
African finch. Nature 329:717-719.
Smith, T.B. 1990. Resource use by bill morphs of an african finch: evidence for
intraspecific competition. Ecology 71:1246-1257.
Smith, T.B. 1993. Disruptive Selection and the Genetic Basis of Bill Size
Polymorphism in the African Finch Pyrenestes. Nature 363:618-620.
Smith, T.B., and Skúlason, S. 1996. Evolutionary significance of resource
polymorphism in fishes, amphibians, and birds. Annual Review of Ecology
and Systematics 27:111-133.
Snorrason, S.S., Skúlason, S., Jonsson, B., Malmquist, H.J., Jonasson, P.M.,
Sandlund, O.T., and Lindem, T. 1994. Trophic specialization in arctic charr
Salvelinus alpinus (Pisces; Salmonidae): morphological divergence and
ontogenetic niche shifts. Biological Journal of the Linnean Society 52:1-18.
Soulé, M. 1972. Phenetics of natural populations. III. Variation in insular
populations of a lizard. American Naturalist 106:429-446.
Soulé, M., and Stewart, B.R. 1970. The "niche-variation" hypothesis: a test and
alternatives. American Naturalist 104:85-97.
Stearns, S.C. 1989. The evolutionary significance of phenotypic plasticity.
BioScience 39:436-445.
Svanbäck, R. and Eklöv, P. 2004. Morphology in perch affects habitat specific
feeding efficiency. Functional Ecology in press.
Svärdson, G. 1949. Competition and habitat selection in birds. Oikos 1: 157-174.
31
Svärdson, G. 1976. Interspecific population dominance in fish communities.
Report from the Institute of Freshwater Research, Drottningholm 56:144171.
Tamarin, R.H., and Krebs, C.J. 1969. Microtus population biology. II. Genetic
changes at the transferrin locus in fluctuating populations of two vole
species. Evolution 23:183-211.
Taper, M.L., and Case, T.J. 1985. Quantitative genetic models for the coevolution
of character displacement. Ecology 66:355-371.
Vamosi. S.M. 2002. Predation sharpens the adaptive peaks: survival trade-offs in
sympatric sticklebacks. Annales Zoologici Fennici 39:237-248.
van den Berghe, E. P., and Gross, M. R. 1989. Natural selection resulting from
female breeding competition in a pacific salmon (Coho: Oncorhynchus
kisutch). Evolution 43:125-140.
van Noordwijk, A.J., van Baalen, J.J., and Scharloo, W. 1988. Heritability of body
size in natural population of the great tit and its relation to age and
environmental conditions during growth. Genetic Research 51:149-162.
Van Valen, L. 1965. Morphological variation and width of ecological niche.
American Naturalist 99:377-390.
Vinyard, G.L. 1982. Variable kinematics of Sacramento perch (Archoplites
interruptus) capturing evasive and nonevasive prey. Canadian Journal of
Fisheries and Aquatic Science 39:208-211
Vuorinen, J.A., Bodaly, R.A., Reist, J.D., Bernatchez, L., and Dodson, J.J. 1993.
Genetic and morphological differentiation between dwarf and normal size
forms of lake whitefish (Coregonus clupeaformis) in Como Lake, Ontario.
Canadian Journal of Fisheries and Aquatic Science 50:210-216
Wainwright, P.C. 1988. Morphology and ecology: functional basis of feeding
constraints in caribbean labrid fishes. Ecology 69:635-645
Wainwright, P.C. and Richard, B.A. 1995. Predicting patterns of prey use from
morphology of fishes. Environmental Biology of Fishes 44:97-113
Walker. J.A. 1997. Ecological morphology of lacustrine threespine stickleback
Gasterosteus aculeatus L. (Gasterosteidae) body shape. Biological Journal
of the Linnean Society 61:3-50.
Watson, D.J., and Balon, E.K. 1984. Ecomorpholohical analysis of fish taxocenes
in rainforest streams of northern Borneo. Journal of Fish Biology 25:371384.
Webb, P.W. 1976. The effect of size on the fast-start performance of rainbow trout
Salmo gairdneri, and a consideration of piscivorous predator-prey
interactions. Journal of Experimental Biology 65:157-177
Webb, P.W. 1982. Locomotor patterns in the evolution of Actinopterygian fishes.
American Zoologist 22:329-342.
Webb, P.W. 1983. Speed, acceleration and manoeuvrability of two teleost fishes.
Journal of Experimental Biology 102:115-122
Webb, P.W. 1984. Body form, locomotion and foraging in aquatic vertebrates.
American Zoologist 24:107-120
32
Webb, P.W., and Skadsen, J.M. 1980. Strike tactics of Esox. Canadian Journal of
Zoology 58:1462-1469
Webb, P.W., and Weihs, D. 1986. Functional locomotor morphology of early life
history stages of fishes. Transactions of the American Fisheries Society
115:115-127
Werner, E.E. 1988. Size, scaling, and the evolution of complex life cycles. Pages
60-81 in B. Ebenman and L. Persson, eds. Size-Structured Populations.
Springer-Verlag, Berlin.
Werner, E.E., and Anholt, B.R. 1993. Ecological consequences of the trade-off
between growth and mortality rates mediated by foraging activity. American
Naturalist 142:242-272.
Werner E.E., and Gilliam, J.F. 1984. The ontogenetic niche and species
interactions in size-structured populations. Annual Review of Ecology and
Systematics 15:393-425.
Werner, E.E., and Hall, D.J. 1988. Ontogenetic habitat shifts in bluegill: the
foraging rate-predation risk trade-off. Ecology 69:1352-1366.
Werner, T.K., and Sherry, T.W. 1987. Behavioral feeding specialization in
Pinaroloxias inornata, the “Darwin’s Finch” of Cocos Island, Costa Rica.
Proceedings of the National Academy of Science of the USA 84:5506-5510.
West, L. 1986. Interindividual variationin prey selection by the snail Nucella
(=Thais) emarginata. Ecology 67:798-809.
West, L. 1988. Prey selection by the tropical snail Thais melones: a study of
interindividual variation. Ecology 69:1839-1854.
West-Eberhard, M. J. 1989. Phenotypic plasticity and the origins of diversity.
Annual Review of Ecology and Systematics 20:249-278.
Wilson, D.S., and Turelli, M. 1986. Stable underdominance and the evolutionary
invasion of empty niches. American Naturalist 127:835-850.
Wilson, D.S., and Yoshimura, J. 1994. On the coexistense on specialists and
generalists. American Naturalist 144:692-707.
Wimberger, P. H. 1994. Trophic polymorphisms, plasticity, and speciation in
vertebrates. Pages 19-43 in D.J. Stouder, and K. Fresh, eds. Advances in Fish
Foraging Theory and Ecology. Belle Baruch Press, Columbia, SC.
Yoshida, T., Jones, L.E., Ellner, S.P., Fussmann, G.F., and Hairston Jr., N.G. 2003.
Rapid evolution drives ecological dynamics in a predator-prey system.
Nature 424: 303-306.
33
Acknowledgements
The time as a graduate student has been an informative and memorable period of
my life. During this time I have had the privilege to do research at three different
Universities in two countries, namely Umeå University, UC Davis and Uppsala
University. Thus, I have experienced summer (?) fieldwork with snowfall but I
have also experienced warm winter days wearing shorts and t-shirt. This also
means that I have had the pleasure to interact with a lot of people both through
research but also private.
Research is never a result of the work of a single individual only, and behind every
project there is always an effort of a team. The studies in this thesis are no
exception! The most important persons for a graduate student are the supervisors.
With no doubt, Peter Eklöv has been the most scientific influential person for me
during this time. Tanks Peter for excellent supervision! Not only for your
constructive criticisms on manuscripts, your enthusiasm and your scientific
sharpness but also for always having time to listen to and discuss all my crazy new
ideas. Thanks for providing me with a rich scientific environment.
I cannot imagine having a better co-supervisor than Lennart Persson. Thank you
Lennart for shearing your scientific clearness, your enthusiasm and splendid
supervision. I’m very grateful for being part of the “Åmsele” project and the days
up there in snow or sunshine.
Though not formally a supervisor, Peter Wainwright has had a big influence on my
scientific training. Thank you Peter for letting me come to your lab and do
research. Thanks for your passion for science, your scientific guidance but
foremost for teaching me how to become famous. Thanks for opening the door to
functional morphology for me, now all I need is a high-speed video camera.
The people that have kept me going and made this period really pleasant are
foremost graduate students and post-docs in three different groups: the “Umeå fish
lab”, the “Davis fish lab”, and the “Uppsala fish lab”. The Umeå fish lab with
members like Bent Christensen, Erika Westman, Eva Wahlström, Joakim Hjelm,
and Pär Byström made my transition from undergraduate to graduate student easy
and funny. Special thanks to Pär for excellent supervision during my masters
project, Eva for mentoring me through teaching and research, Jocke for being a
good roommate but also for all discussions regarding morphology. After I started
as a graduate student Arne Schröder, Emma Lindgren, Felipe Gonzalez, Jens
Andersson, and Johan Lövgren have joined and enriched the Umeå fish lab, thanks
for all the good times. I owe many thanks to the Davis fish lab (Andrew Carroll,
Dan Bolnick, Darrin Hulsey, Justin Grubich, Lara Ferry-Graham, Tom Near, Tom
Waltzek) for making my six months in Davis memorable. I cannot imagine any
better lab in Davis, cheers duds. I also owe many thanks to the newly formed fish
lab in Uppsala: Antonia Liess, Jens Olsson, Henrik Ragnarsson, Marcus Sundbom,
34
and Mario Quevedo. Without you as support during these last years, life and
research wouldn’t have been the same. Special thanks to Jens and Ulf Westerlund
for good times both on and off work. To reiterate, I will always be thankful to the
past and present fish lab members in Umeå, Davis and Uppsala for making my
time in each place pleasant with interesting scientific discussions and recreational
activities.
Special thanks also to: Göran Arnquist for always putting up with all my questions
and having time to discuss geometric morphometrics and statistical questions. All
the administrative personnel, especially Sussi Mikaelsson and Ylva Linghult, for
all the help with bills and other administrative stuff. Jörgen Naalisvaara, Johan and
Kara Barker-Åström, Tuulikki Rooke and Fredrik Dahl, Tina Nilsson and Phil
Buckland for housing me during my frequent visits to Umeå during these last
years, but also for being good friends.
The papers in this thesis would not have been what they are without all coauthors,
field and laboratory assistants, and everyone giving constructive criticisms on
various drafts. I owe you all a great deal.
Finally, on a more personal level, I would like to thank my parents, sisters and
other close relatives and friends for all encouragement and support you have
offered me during the last years. My mother and father deserve special thanks for
always allowing me to make my own choices and supporting them. I would
definitively not be here otherwise.
35