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LOCAL ADAPTATION OR
ENVIRONMENTAL INDUCTION?
CAUSES OF POPULATION
DIFFERENTIATION IN ALPINE
AMPHIBIANS
Claude MIAUD1 & Juha MERILÄ2
University of Savoie, UMR CNRS 5553 Laboratory of Biology of Alpine
Populations, F-73 376 Le Bourget du Lac, France
E-mail: [email protected]
2
Department of Population Biology, Evolutionary Biology Centre, University of
Uppsala, Norbyvägen 18d, SE-75 236 Uppsala, Sweden
E-mail: [email protected]
1
Abstract
Many amphibian species have wide altitudinal and latitudinal distribution
ranges, and hence, different populations of the same species may face very different environmental constraints and selection pressures. Although the potential differences in selective regimes along altitudinal and latitudinal gradients are
still largely unknown, a number of studies have documented conspicuous phenotypic differentiation along these gradients. We reviewed the evidence for
among population genetic differentiation (past adaptation) and within population genetic variation (potential for future adaptation) in different life history
traits in amphibians, focusing mainly in studies conducted with the Common
Frog, Rana temporaria, and with the Alpine Newt, Triturus alpestris. Except for
larval traits, the evidence for genetic basis of population differentiation, as well
as for heritability of different traits, is limited. This is especially true for traits
expressed only in adults, such as age of maturity, fecundity and longevity, and
traits relating to tolerance to different types of environmental stresses (e.g.
nitrate, UV-B, pesticide tolerances). We suggest that due to the relative ease in
which the genetic basis of most traits in amphibians can be studied, they might
provide good model systems to study possible consequences of, and adaptation to, environmental changes expected to occur in forthcoming decades.
Key words: altitude, amphibians, environmental gradient, heritability, latitude,
local adaptation, phenotypic variation, Rana temporaria, Triturus alpestris
Received 15 November 2000; accepted 1 March 2001
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INTRODUCTION
A central thesis in evolutionary biology is that natural selection acting on
heritable phenotypic variation will
result in adaptation and differentiation among local populations inhabiting environments differing in their
selective regimes (Linhart & Grant
1996). Hence, to understand the
processes of evolution and local
adaptation, we need to understand
the factors and processes generating
and maintaining genetic variation,
how this variation is translated to the
phenotypic level, and how phenotypic expression of genetic variation in a
given trait will interact with other
traits and the environment to determine fitness (Stearns 1989). These
fundamental questions also are
important in the realm of applied
ecology: anthropogenic influences
such as elevated CO2-levels (Dixon et
al. 1999, Fitter et al. 2000), increased
ultraviolet-B (UV-B) radiation reaching the earth’s surface due to ozone
depletion (Blaustein et al. 1999,
Madronich et al. 1998), and shifts in
global climate (e.g. Hulme et al.
1999) are predicted to lead to rapid
environmental changes in the forthcoming decades (Chambers 1998,
Marchettini et al. 1999). Therefore,
knowledge about the genetic basis of
traits likely to be under selection in
changing environments will enable us
to predict population and ecosystem
responses to these environmental
changes (Kareiva et al. 1993, Bürger
& Lynch 1997, Mousseau et al.
2000).
For a given trait, the mean value of
the trait in a population (the mean
phenotype) is determined by genetic
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factors, environmental influences,
and interactions between the two
(genotype-environment interactions;
Falconer & Mackay 1996). Thus,
when discussing potential for adaptive differentiation among populations, the first step is to establish to
what degree the observed differences
among populations are of genetic
versus environmental origin (e.g.
Berven & Gill 1983, Conover &
Schultz 1995). One way to separate
between genetic differentiation and
direct environmental induction as a
cause of population differences in
life-history traits is to perform “common garden experiments,” in which
individuals from contrasting environments are reared in a common laboratory environment (Conover &
Schultz 1995; Figure 1). Another possibility is to conduct “reciprocal transplant experiments” in which individuals from different populations are
swapped to the environment of other
populations and their performance is
compared with those individuals
remaining in the population of origin
(Figure 1). The expectation from such
experiments is that if genetic adaptation has taken place, the differences
observed in nature will persist also in
the common environment (or in the
locality of transplantation), whereas if
environmental induction is the principal cause of population differences in
the wild, these differences will vanish
when the organisms are reared in a
common environment (Figure 1;
Conover & Schultz 1995).
Although the answer to the question
whether variation among populations
and species is mainly environmental
or genetic is crucial (Berven & Gill
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Figure legends
Figure 1: Schematic presentation of the
logic of (a) common garden and (b)
reciprocal transplant experiments. The
size of the circles represents the mean
phenotype in the two populations
inhabiting environments 1 and 2,
respectively, and the circles at the ends
of the arrows indicate the mean phenotype in the new environment. For both
(a) and (b), two possible outcomes are
pictured: one in which the initially
observed difference is genetically determined, another where the difference is
entirely of environmental origin. For
more complex outcomes, see Conover
& Schultz (1995).
1983), it does not necessarily give us
cues as to whether the populations
would be able to respond evolutionarily to further changes in their environment. In other words, although
there must have been genetic variation within at least one of the populations for two populations to have
diverged genetically, any future adaptation and evolution in a given trait in
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these populations depends on - apart
from selection acting on the trait in
question - whether there is (still) heritable genetic variation in the population (Falconer & Mackay 1996), and
how the expression of this variation is
influenced by environmental conditions (Hoffman & Merilä 1999). To
this end, to predict potential for
future adaptation we need some
knowledge about the proportion of
the phenotypic variation in the population that is attributable to the additive effects of genes, i.e. about the
trait’s heritability (h2; Falconer &
Mackay 1996).
The aim of this review is two-fold.
First, we review what is known today
about the (i) levels of heritable variation in different life history traits within amphibian populations, and (ii)
about the relative importance of
genetic versus environmental determinants of life history trait differentiation among amphibian populations
in the Alps. In our treatment, we will
focus primarily on life-history trait
variation in two model organisms: the
Common Frog Rana temporaria and
the Alpine Newt Triturus alpestris.
When no data are available from
these two species, information from
the Wood Frog Rana sylvatica - a vicariate species of Common Frog in
North America - will be included.
Second, being ectothermic and relatively poor disperses (e.g. Ward et al.
1992), amphibians are potentially
very sensitive to changes in levels of
abiotic stresses (e.g. temperature,
length of growth season) predicted to
occur over large areas in forth coming
decades (e.g. Beebee 1995, Meyer et
al. 1998, Hulme et al. 1999,
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Houlahan et al. 2000). To this end,
we will reflect upon the question how
the altitudinal and anthropogenic
gradients in the Alps could provide a
suitable model system to study biological responses to predicted environmental changes, and how the
data on alpine amphibians could be
utilised in this context.
The determinants of life history trait
variation in the Common Frog and
the Alpine Newt
As the starting point for our treatment, we will first briefly summarise
what is known about phenotypic
variation in adult life history traits
within and among different populations of the Common Frog and Alpine
Newt.
The Common Frog
The Common Frog is the most widely distributed, and one of the most
abundant anuran species of Europe
(Grossenbacher 1994, Gasc et al.
1997). It occurs from northern Spain
to the Barents Sea in the north, being
the only amphibian species with a
distribution reaching the North Cape
(Norway). To the south, it is increasingly restricted to mountainous
regions where populations can be
found at altitudes above 2 600 m
(Gasc et al. 1997).
Adult characteristics (viz. age structure, mean body size, growth patterns) have been described from several populations (reviewed in Miaud
et al. 1999). Table 1 summarises the
general comparisons between sexes
and populations differing in their
activity seasons (the activity period
decreases with increasing altitude and
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latitude). Both sexes show similar
trends in age, body size and growth
with respect to decreasing activity
period: age at maturity is delayed;
life-span is prolonged; and adult body
is increased (Table 1). The growth
coefficient increases when asymptotic size decreases, i.e. in populations in
which the asymptotic length is large
(short activity period), the growth
coefficient tends to be low (Miaud et
al. 1999, 2000).
The Alpine Newt
The range of the Alpine Newt is centred on the middle of Europe
(Grossenbacher 1994, Gasc et al.,
1997). The northern range limit is in
Denmark, and runs eastward to
Romania and Bulgaria via the
Carpathian and Balkan Mountains
(Gasc et al. 1997). As with the
Common Frog, the Alpine Newt
occupies a very broad altitudinal
range from sea level in the
Netherlands to 2500 m in the Alps.
Data on age, body length and growth
are now available from several lowland populations, and from the
French and Austrian Alps (reviewed in
Miaud et al. 2000). A general comparison of main life history features
between sexes and populations differing in their activity period is shown
in Table 1. Considering the comparison among sexes or populations, the
patterns are remarkably similar to
those observed in the Common Frog
(Table 1), although some details differ
(e.g. of age at maturity; Miaud et al.
1999, 2000). Nevertheless, what was
said above in the case of the
Common Frog also applies to the
Alpine Newt.
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(a) Comparisons between sexes within populations
Trait
Rana temporaria
Triturus alpestris
Age at maturity
Longevity
Body size at maturity
Mean body size
Asymptotic size1
Growth coefficient
Growth rate during the juvenile phase
Adult survival rate
males <
similar
males <
males <
males <
males <
males <
similar
similar
similar
males <
males <
males <
males <
males <
similar
females
females
females
females
females
females
(b) Comparisons between populations
Age at maturity
Longevity
Body size at maturity
Mean body size
Asymptotic size1
Growth coefficient1
Adult survival rate
increases
increases
increases
increases
increases
decreases
increases
females
females
females
females
females
short activity period:
increases
increases
increases
increases
increases
decreases
increases
1
Parameters derived from Von Bertanlanffy (1938) growth model
Table 1: Comparison of adult life history traits in the Common frog Rana temporaria and the Alpine newt Triturus alpestris. Comparison between (a) sexes and (b)
populations from Europe varying in altitude or latitude. Data from Miaud et al.
(1999, 2000).
In summary, both species show similar life history trait responses to
decreasing activity period (i.e. to
increasing altitude and latitude).
These responses could be caused
either by: 1) parallel evolution in
response to same environmental factors; 2) shared environmental influences; or 3) some combination of (1)
and (2). In order to differentiate
between these alternatives, it is necessary to investigate to what degree
variation in these adult life history
traits, as well as other traits, are of
genetic and environmental origin.
Timing of reproduction
Within population variation
Timing of reproduction is potentially a
trait of great importance for individ-
ual fitness, but we are not aware of
any amphibian study which would
have investigated the genetic basis of
this trait.
Among population variation
There is a great deal of variation
among different Common Frog populations in the timing of breeding
(e.g. Koskela 1973, Elmberg 1990,
Guyétant et al. 1995). We are not
aware of any studies which investigated a possible genetic component
to these differences in the Common
Frog and the Alpine Newt. However,
using a reciprocal transplant experiment, Berven (1982a) investigated
the possibility of a genetic component to population divergence in the
breeding time between two Wood
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Frog populations. Marked juveniles
were
transplanted
reciprocally
between a highland (1100 m) and
lowland (0 m) population in the
Shenandoah Mountains, Virginia,
USA, during three successive years.
Recaptures in the following breeding
seasons showed that there was no
difference in timing of breeding
between transplants and residents:
the timing of breeding was solely
environmentally determined. This
remains to be tested in Common Frog
and Alpine Newt. However, longterm data from a number of vertebrate species (Forchhammer et al.
1998), including amphibians (Beebee
1995, Forchhammer et al. 1998),
show marked changes in breeding
during recent decades. Whether
these changes reflect phenotypic
plasticity or genetically based evolution in response to changing climate
remains largely unexplored (but see:
Przybylo et al. 2000).
Fecundity
Within population variation
A positive correlation between body
size and egg number is well-documented in amphibians (Kaplan and
Salthe 1979), including Common
Frog (e.g. Joly 1991, Elmberg 1991,
Martin & Miaud 1999) and Alpine
Newt (C. Miaud, unpublished data).
However, there are no data available
on heritability of clutch size, neither
from the two focal species nor from
any other amphibian species.
Among population variation
Despite the fact that a number of
studies have documented amongpopulation variation in clutch size of
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the Common Frog (e.g. Kozlowska
1971, Cummins 1986, reviewed by
Joly 1991), next to nothing is known
about the relative importance of
genes and environment underlying
this variation. The same is true in the
case of the Alpine Newt. Berven
(1982a) compared the fecundity of
reciprocally transplanted juvenile
Wood Frogs when they started to
reproduce. Transplanted females
showed similar fecundity to their congeners in the parental population,
suggesting a genetic component to
fecundity/clutch size. However, the
possibility of maternal/carry over
effects (Falconer & MacKay 1996,
Rossiter 1996) on fecundity, as
demonstrated in other taxa (e.g.
Gustafsson & Schluter 1993), cannot
be strictly excluded.
Egg size
Within population variation
Although the relationship between
female body size and egg size is well
documented in the Common Frog
(e.g. Kozlowska 1971, Beattie 1977,
Cummins 1986, Augert & Joly 1993,
Martin & Miaud 1999) and in the
Alpine Newt (e.g. Brand &
Grossenbacher 1979, C. Miaud,
unpublished data), no information is
available on the genetic basis of egg
size variation in these species.
Among population variation
As in many other amphibians (Kaplan
1998), there is extensive among-population variation in egg size in
Common Frogs (e.g. Cummins 1986,
Laugen et al. 2001). For example,
Martin & Miaud (1999) compared
egg size in three populations (at 326,
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1318, and 2450 m) in the northwestern part of the Alps, and found that
egg size increased with increasing
altitude, corroborating earlier findings
by Kozlowska (1971), Brant &
Grossenbacher (1979), and Holms
(1982). Also, in the Alpine Newt, egg
size increases from low-to-highland
populations (C. Miaud, unpublished
data). Whether these patterns result
from phenotypic plasticity or genetic
divergence is not known for Common
Frog and Alpine Newt. In reciprocal
juvenile transplant experiments on
the Wood Frog (Berven 1982a), egg
size and in particular the relationship
between this trait and female body
size were functions of the parental
population, and not the environment
in which the transplanted individuals
matured. Nevertheless, by virtue of
the environmental effect on body size
(see below), this trait is indirectly
influenced by the environment
(Berven 1982a).
Rate of embryonic development
Within population variation
Despite the relative ease with which a
genetic component of the rates of
embryonic development could be
assessed, there appears to be no published study which has estimated heritability of this trait. However, there is
evidence for the genetic basis of
embryonic developmental rates in
Swedish Common Frog populations
from a common garden experiment
(M. Pahkala, A. Laurila & J. Merilä,
unpublished data). However, these
results are based on a full-sib design,
and maternal effects as a cause of
observed variation cannot be ruled
out.
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Among population variation
A number of studies have compared
developmental rates of eggs from
Common Frog populations originating from different altitudes using the
common garden approach (1500 vs.
2200 m, Angelier & Angelier 1968;
200 m vs. 1000 m, Kozlowska 1971;
50 vs. 800 m, Beattie 1977; 100 vs.
500 m, Holms 1982; 326 vs. 1318 vs.
2450m, Martin & Miaud 1999).
These studies confirmed a faster
development of high altitude eggs
over those from lower altitudes
(except Holms 1982), suggesting a
genetic capacity for faster egg development in high as compared to low
altitudes. These results support
counter-gradient selection hypothesis
(Levis 1968); eggs with faster development are selected at high altitudes
possibly because of their need to
develop faster (shorter growing season) and/or to counteract the negative effects of a colder climate on
developmental rates (Conover &
Schlultz 1995). In the Alpine Newt,
Brand and Grossenbacher (1979)
found that eggs from highland populations had a faster developmental
rate (and better tolerance to low temperature) than eggs from lowland
populations. Hence, it appears that in
both species, populations inhabiting
higher altitudes have evolved a
capacity for faster development than
those inhabiting lower altitudes.
These data are corroborated by latitudinal comparisons in the Common
Frog: embryos from northern Sweden
seem to be capable of faster development than those from southern
Sweden when reared in a constant
temperature (A. T. Laugen, A. Laurila
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and J. Merilä, unpublished data).
Larval developmental and growth
rate
Within population variation
There is evidence that larval developmental rates - or age at metamorphosis - is under genetic control in the
Common Frog. In a lowland population, Plytycz et al. (1984) demonstrated a genetic control of the larval
phase duration with tadpoles
obtained from controlled matings
(North Carolina II design; Kearsey &
Pooni 1996). Merilä et al. (2000a)
used a full-sib design and failed to
find evidence for genetic variation in
developmental rates in two Swedish
populations, but a low number of
families was used. However, a halfsib design (North Carolina I design;
Kearsey & Pooni 1996) applied to
individuals from one of these populations revealed a significant additive
genetic component to developmental
rate (Merilä et al. 2000b). In the
Wood Frog, Berven (1987) conducted experimental crosses with adults
of two populations, obtaining fulland half-sib families for both a lowland and mountain population. In
each of the populations, developmental rate was heritable.
Among population variation
A fair number of studies have investigated altitudinal and latitudinal variation in larval traits of the Common
Frog (Table 2). Using a common garden approach, Aebli (1966) compared the developmental rates of
Common Frog larvae among four
lowland (below 900 m) and highland
(above 1800 m) populations, and
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found that the larval period in a constant
temperature
experiment
increased in linear fashion from 59
days (highland) to 153 days (lowland). Holm (1982) reared tadpoles
from two populations - situated at
100 and 500 m, respectively - at constant temperature in the laboratory,
and found no effect of population of
origin on age at metamorphosis. In a
similar experiment, Brand and
Grossenbacher (1979) found that
tadpoles from 2550 m developed at a
faster rate and metamorphosed at a
larger size than those from 525 m.
Tadpoles obtained from controlled
matings of Common Frog originating
from two populations at 55°N and
68°N in Scandinavia were reared at
two temperatures and three food levels (Merilä et al. 2000a). Low temperature and low food level led to lowered growth rates and delayed metamorphosis, while high temperature
and high food level increased growth
rates and accelerated metamorphosis.
Tadpoles from the north metamorphosed earlier with a higher growth
rate than tadpoles from the south.
The clinal nature of this differentiation was later confirmed in a larger
experiment involving six different
populations along a latitudinal gradient across Scandinavia (Laugen et al.
2001). Hence, Common Frogs from
northern Sweden (Merilä et al.
2000a) and high elevation in the Alps
(see above; Martin & Miaud, unpublished data) have a genetic capacity
to complete their larval development
faster than Frogs from southern
Sweden and lowland populations.
Similar results have been obtained in
the Wood Frog: when tadpoles were
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39
Trait
Direction of difference
Reference
Growth rate
northern > southern
northern > southern
northern > southern
low > high altitude
low > high altitude
high = low altitude
southern > northern
southern > northern
Laugen et al. 2001
low > high altitude
high > low altitude
northern > southern
northern > southern
midlatitude > southern = northern
Merilä et al. 2000a
Johanssen et al. 2001
Laugen et al. 2001
Aebli 1966
Brand and Grossenbacher 1979
Holm 1982
Merilä et al. 2000a
Johanssen et al. 2001
Age at metamorphosis
southern > northern
Size at metamorphosis
Martin & Miaud, unpublished
Brand & Grossenbacher 1979
Merilä et al. 2000a
Johanssen et al. 2001
Laugen et al. 2001
Table 2: Comparison of larval life history traits among different Common Frog Rana
temporaria populations.
reciprocally transplanted between
two populations, the same duration
of the tadpole phase was observed in
transplants and residents but mountain to lowland transplants grew
faster and were larger (Berven
1982b). However, reciprocal crosses
between elevations were also performed (Berven 1982b) to separate
non-genetic maternal effects associated with egg size differences
between mountain and lowland populations from true genetic differences
in larval traits. Environmental effects
accounted for 88% of the variation in
the length of the larval period, while
only an insignificant (1%) part of the
variation was explained by genetic
origin. A significant maternal effect
on developmental time also was
demonstrated. Hence, as to genetic
basis of the differentiation in larval
developmental rates, the data from
different studies is conflicting.
Reciprocal crosses remain to be conducted in the Common Frog, and no
data on larval development in differ-
ent populations of Alpine Newt is yet
available.
Size at metamorphosis
Within population variation
Again, surprisingly little information is
available about the genetic basis of
metamorphic size in the Common
Frog, and no information in this
respect exists for the Alpine Newt.
Merilä et al. (2000a) found marginally significant family effects on size at
metamorphosis in the Common Frog,
but since this was a full-sib design,
these effects could result from maternal influences. Merilä et al. (2000b)
did not find any evidence for genetic
variation in metamorphic size using a
half-sib design. Both of these studies
were based on a very small number
of families, and larger designs are
clearly required to reach any confidence about the genetic basis of
metamorphic size. In Berven’s (1987)
experiments, size at metamorphosis
was strongly heritable (h2 = 0.66, S.E.
= 0.31) among mountain larvae while
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h2 was not significant among the
lowland larvae. There was, however,
a strong female component in the
lowland population, indicating that a
significant proportion of the variation
in larval size was female-dependent
(even if maternal effects through egg
size were not significant determinants
of larval body size, Berven 1987).
Among population variation
Egg masses of the Common Frog collected in 14 populations varying in
altitude (from 525 m to 2550 m in
the Alps) and reared in the laboratory
showed that tadpoles from the highland populations metamorphosed at
larger sizes than tadpoles from lowland
populations
(Brand
&
Grossenbacher 1979). However,
using a common garden experiment,
Merilä et al. (2000a) found that
metamorphic size did not differ
between one northern and one
southern Swedish population, but
after accounting for differences in
age at metamorphosis, metamorphs
from northern Sweden were larger
than those from southern Sweden
(Merilä et al. 2000a). An extended
study along the same latitudinal gradient revealed that size at metamorphosis was a positive function of latitude up to the mid-part of Sweden,
and negative thereafter (Laugen et al.
2001). Hence, the relationship
between season length and size at
metamorphosis may be more complex than previously anticipated.
Finally, a significant genetic component (20%) to the inter-elevation
variation in size at metamorphosis
was reported in the Wood Frog
(Berven 1982b). No data on larval
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size in different populations is yet
available for the Alpine Newt.
Age and size at maturity
Within population variation
We are not aware of any study that
has examined sources of within population variation in age and size at
maturity in the Common Frog or in
the Alpine Newt. However, since
metamorphic size is often correlated
with size at maturity in other species
(Smith 1987 Semlitsch et al. 1988,
Berven 1990, Amézquida & Lüddecke
1999), it is possible that a genetic
component to these traits also exists
in Common Frogs and Alpine Newts.
Among population variation
Augert & Joly (1993) found differences in age and size at maturity
between two neighbouring Common
Frog populations. Because professional fishermen mixed eggs and tadpoles from these two populations
each year, the differences in age and
size at maturity are likely to be due to
differences in local environmental
conditions (i.e. phenotypic plasticity).
On the contrary, in a reciprocal transplant study of juvenile Wood Frogs
between populations at different altitudes, Berven (1982a) found that
transplants matured at ages and sizes
intermediate to residents, suggesting
at least partial genetic control of
these traits. We are not aware of any
study which would have checked
whether this would also apply among
altitudinally or latitudinally separated
Common Frog populations.
In the Alpine Newt, Schabetsberger &
Goldschmid (1994) found that larvae
caught from a highland lake (1643
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m) and reared in the laboratory
reached the size of mature animals
within 2-3 years, while this size was
not reached before 10 years of age in
the field. This suggests that a major
part of the variation in size at maturity among Alpine Newt populations in
different altitudes may result from
phenotypic plasticity, but it does not
disprove the possibility of a genetic
component. In conclusion, it is clear
that more studies focusing on the
genetic vs. environmental determination of age and size at maturity are
needed in these amphibian species.
Other traits
We have focused on major life history traits which might be targets of
varying natural selection in different
habitats. These traits also may be
important in terms of adaptation to
changing environmental conditions.
However, we should also point out
that there is a whole suite of other
traits of potential relevance to adaptation to environmental changes.
These include, for example, tolerance
to low pH, high levels of ultraviolet
(UV-B) radiation and high concentrations of environmental pollutants,
such as nitrates and pesticides. Also,
changes in hydroperiod length and
predation pressure as a consequence
of climate change (e.g. Griffiths
1997) may render plastic responses to
pond dessication (e.g. Laurila &
Kujasalo 1999) and predation risk
(e.g. Lardner 2000) important for further adaptation. To this end, studies
of the genetic basis of stress responses and adaptation to local differences
in levels of these stressors would be
most illuminating. As to the physio-
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chemical stressors, we are aware of
only two studies addressing these
issues in the Common Frog. First,
Pahkala et al. (2001a) compared the
combined effects of low pH and high
levels of UV-B radiation between
southern and northern Swedish
Common Frog populations in a laboratory experiment. They found synergistic negative effects of UV-B radiation and low pH (see also: Long et al.
1995; Pahkala et al. 2001b), only in
the northern population. This suggests that the negative effects of UVB on embryonic development of the
Common Frog may be expressed only
in the presence of other stress factors,
and furthermore, in some but not in
all populations. Second, in an attempt
to test possible adaptation to varying
background levels of nitrate,
Johansson et al. (2001) compared
nitrate tolerance between two northern Swedish and two southern
Swedish populations of Common
Frogs. Their results suggest that
although all populations were highly
tolerant to nitrate, the southern
Swedish populations tolerated high
concentrations better than the northern Swedish populations. This difference is consistent with the interpretation that the southern Swedish tadpoles might have adapted to higher
background levels of nitrates in their
habitat. Similar comparisons using
other types of stressors, such as pesticides (e.g. Bridges and Semlitsch
2000), remain to be conducted. As to
the dessication and predation risk,
some data are available from the
Common Frog: at least in the lowland
populations studied so far, Common
Frog tadpoles appear able to speed
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up their development (at the cost of
smaller size at metamorphosis) when
facing a pond drying risk (Laurila &
Kujasalo 1999, Loman 1999, Merilä
et al. 2000b). However, it is unclear
whether this apparently adaptive
capacity is also present at high elevations or high latitudes, where the larvae seem to have been already
selected to maximise their developmental rates. Likewise, predator
induced (adaptive) morphological
changes occur in many lowland populations of Common Frog (Laurila
2000, Lardner 2000), but since these
responses are costly, it is not clear
whether they could also be expected
to have evolved at high altitudes and
high latitudes where the costs of
induced defences might be even
higher than in the lowland populations studied so far. Furthermore,
there are no studies focusing on the
question of the genetic basis of plastic responses in R. temporaria (but
see Merilä et al. 2000b) which would
be required to evaluate whether
these traits can evolve in response to
selection.
Conclusions
We have reviewed the currently
available data on life history trait variation in two model organisms - the
Common Frog and the Alpine Newt and propose here some possible
directions for future studies. First,
although the reviews above suggest
that local adaptation has taken place
at least in the case of the most thoroughly studied traits, and estimates
of genetic variability are available for
a few traits, studies on the genetic
and environmental determinants of
MIAUD, MERILÄ
variation (both within and among
populations) are typically conducted
on the aquatic stages (i.e. egg and
larval development). Even if these
traits are important determinants of
individual fitness, it is clear that information on the traits expressed in terrestrial phases (juveniles and adults)
are also of critical importance. For
instance, it is possible that selective
events taking place during terrestrial
phases are more important for population processes than those taking
place at larval stages. We also note
that nothing is known about the
genetics of behavioural traits, such as
male calling characters, dispersal
behaviour , or habitat choice (but see:
Laurila 2000), despite the fact that
Common Frog populations inhabiting
different environments have been
assumed to have diverged in mating
behaviour (Elmberg & Lundberg
1991). The same applies for tolerance
to different environmental stressors evidence is accumulating that different amphibian populations are differently sensitive to the same environmental stressors (e.g. Bridges &
Semlitsch 2000, Johanssen et al..
2001, Pahkala et al. 2001a, b), and
understanding the causes and consequences of this variation poses a challenge for further research. In particular, we propose that testing how populations from different altitudes may
differ in their responses to different
stressors might provide insights to the
question how forthcoming environmental changes will impact upon
amphibian populations, and what
kind of constraints (ecological and
genetic) there might be for evolution
of adaptive responses.
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Figure 2: (a) Schematic diagram of the
female life cycle for an amphibian with
both aquatic and terrestrial phases,
each (egg [N1], larvae [N2], juvenile
[N3- N4], and adult [N5]) with agespecific probabilities of survival (S) and
population size (N). Reproduction starts
with N5, fecundity (F), Juvenile survival
(S3) and adult survival (S4) are independent of age, and there is no senescence.
(b) The corresponding transition matrix
of this amphibian life cycle. N1 is the
size of the population at time t1 and N2
at time t2. The population growth
depends on (, the leading eigenvalue of
the average matrix M. If ( = 1, the population is stationary, decreases if ( < 1
and increases if ( > 1. Sensitivity analyses on the different parameters (F, S1 to
4) allows identification of factors that
most affect ( (i.e. population growth).
One potentially fruitful avenue for
future research would involve more
in-depth study of the impact of life
history variation on population
dynamics. In demographic ecology,
matrix projection models (e.g. Leslie
matrix, Ferriere et al. 1996) can be
used to determine the effects of the
Biota
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43
different phases in the life cycle on
the population growth rate (Fig. 2a,
b). Here, a central index that quantifies population growth or decline is
the leading eigenvalue ( of the average matrix (Fig. 2b). If ( > 1, matrix
theory predicts that, regardless of the
initial population size and structure,
the population will grow at a geometric rate given by (. The calculation
of stage-specific sensitivities or elasticities allows identification of factors
affecting population growth and persistence (Caswell 1978, Gaillard et al.
1998, Mills et al. 1999). Also, since (
is considered as one of the best estimate of fitness (McGraw & Caswell
1996), knowledge about the relative
importance of different life history
traits on ( (i.e. fitness) is thus clearly
informative about the adaptive
nature of life history trait variation
among different populations. Hence,
comparative analyses of selection on
life history traits, evaluation of the
genetic potential for evolutionary
change, and studies on the impact of
traits on demographic properties of a
population would all benefit from
such quantification of a trait’s impact
on the population growth rate
(Benton & Grant 1999). This
approach would be most interesting
to apply to different populations
along altitudinal and latitudinal clines,
since it would give us cues as to what
would be the most vulnerable lifestages in a given population, and
whether effects of various stressors
would differ among different populations. For example, in Alpine Newt,
the strong delay in age at maturity in
highland populations increases the
role of adult survival in population
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dynamics. Hence, we can hypothesise
that factors promoting adult survival
(e.g. body size) will be selected more
strongly in highland than in lowland
populations, whereas the opposite
may be true for the traits impacting
larval survival.
Another (related) direction concerns a
quantitative genetics approach: when
selection operates on a single trait,
the response to selection is roughly
proportional to the additive genetic
variance of the trait. If the same
genes influence the expression of different traits, then an evolutionary
change in one trait will lead to
changes in correlated traits (Falconer
& Mackay 1996). This can impede
the evolutionary process when there
is a conflict in the fitness consequences of selection operating on
correlated traits. Consequently,
understanding the constraints on the
evolution of systems of complex
characters requires information on
the magnitude and direction of
genetic correlation between characters. Quantitative-genetic methodology provides a useful, but data
demanding, means of elucidating
these issues (Mousseau et al. 2000).
However, the development of new
statistical methods and access to
hypervariable markers (e.g. Berlin et
al. 2000, Rowe & Beebee 2000) to
infer degree of genetic relatedness
among individuals will facilitate the
estimation of heritability of quantitative traits even in wild populations
(Ritland 2000a, b).
Finally, selection by multiple factors
on multiple traits, or parts of traits
(e.g. life history components such as
body size, fecundity, and survival)
MIAUD, MERILÄ
often gives rise to counterintuitive
results (Sinervo 2000). One possibility would be to start with suites of
traits with known interrelated adaptive functions. Path analysis gives
explicit predictions of what form the
correlations would take and then
allows measurement of natural selection (Scheiner et al. 2000). This
method consists of building an analytical model around a specific set of
causal relationships among traits that
determine fitness. Sinervo (2000)
conducted a five-year study (i.e. five
generations) on the lizard Uta stansburiana with controlled matings in
nature. Clutch size and egg-mass
were significantly heritable and a
negative genetic correlation was
found between the traits. A path analytic model describing the causal relationship between factors for year,
postlaying mass, clutch size, and egg
mass allowed him to address the
question of how natural selection acts
on the genetically based trade-off
between egg-mass and fecundity. A
pattern of multivariate selection was
determined to act on the trade-off: a
disruptive selection acted on variation
in clutch size (tended to pull the population average clutch size to extreme
values) and stabilizing selection acted
on egg-mass (limited variation in the
population). Such analyses could also
greatly improve our knowledge of
selection acting on amphibian life history traits along altitudinal / latitudinal gradients.
In conclusion, we have reviewed the
evidence for a genetic basis for population differentiation (past adaptation) of amphibian populations along
altitudinal and latitudinal gradients in
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Europe, as well as what is known
about the genetic basis of within
population variation in different life
history traits (potential for future
adaptation). Given the relative ease
with which the genetic basis of
among and within population variation of amphibians (at least in larvae)
can be studied, and because altitudinal and latitudinal gradients mimic in
many ways (e.g. temperature,
hydroperiod length, predator fauna,
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45
season length, etc.) the environmental changes caused by climatic
change, they could provide suitable
models for research evaluating effects
of global change on animal populations. To this end, we suggest that it
is also time to promote development
of interactions and collaborative projects between people with interests on
the interface between ecology,
genetics, ecotoxicology and evolutionary biology.
Acknowledgements
We thank Anssi Laurila and an anonymous referee for insightful suggestions for
the manuscript. Our research is supported by the French National Research
Council (CNRS) and the Swedish Natural Sciences Research Council (NFR).
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