Journal of Zoology
bs_bs_banner
Journal of Zoology. Print ISSN 0952-8369
Altitudinal variation in maternal investment and trade-offs
between egg size and clutch size in the Andrew’s toad
W. B. Liao1,2, X. Lu3 & R. Jehle4
1
2
3
4
Institute of Rare Animals and Plants, China West Normal University, Nanchong, China
Ecological Genetics Research Unit, Department of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland
Department of Zoology, College of Life Sciences, Wuhan University, Wuhan, China
School of Environment & Life Sciences, University of Salford, Salford, UK
Keywords
Bufo andrewsi; differentiation; reproductive
output; trade-offs.
Correspondence
Wen Bo Liao, Institute of Rare Animals and
Plants, China West Normal University, No. 1
of Shida Road, Nanchong City of China,
Nanchong 637000, China.
Email: liaobo_0_0@126.com
Editor: Mark-Oliver Rödel
Received 11 October 2013; revised 13
January 2014; accepted 13 January 2014
doi:10.1111/jzo.12122
Abstract
Environmental variation along altitudinal gradients can promote life-history trait
differentiation in ectothermic animals. Life-history theory predicts that increased
environmental stress results in a shift in reproductive allocation from offspring
quantity to quality and a stronger trade-off between egg size and clutch size. To
test this prediction, we investigated patterns of variation in life-history traits (i.e.
age, body size, clutch size and egg size) among four populations of Bufo andrewsi
from Baoxing County, western China, at different altitudes. We found that body
size, age, egg size and total reproductive output, but not clutch size, differed
between populations. Clutch size and total reproductive output increased with
female size and age. However, egg size decreased with female size and did not
change with female age. The egg size and clutch size trade-off was evident for all
populations except at lowest altitude, and the strength of trade-off between egg
size and clutch size increased with altitude. Our findings suggest that environmental constraints at high altitude select for investment in larger eggs at a cost of
offspring number.
Introduction
Geographical variation in life-history traits has intrigued evolutionary biologists and ecologists for decades, constituting
the base of many theoretical assumptions (Roff, 1992).
According to life-history theory, females will optimize their
allocation of resources between current and future reproduction, and between reproduction and growth as well as
maintenance (Williams, 1966; Stearns, 1992; Roff, 2002).
Environmental stress can be a major evolutionary force in
promoting differentiation in life-history traits. For example,
females may have to allocate more resources to growth at a
cost of reproduction because poor quality environments are
physiologically costly (Einum & Fleming, 1999; Räsänen
et al., 2008). Stressful environments are also expected to
favour investment in offspring quality at the expense of offspring number (Roff, 1992; Kaplan & Phillips, 2006). Moreover, environmental stress and resource availability also affect
the reproductive parameters, which depend upon female size
and age (Stearns, 1992). However, although a substantial
amount of data have been collated, an understanding of the
causes for geographical patterns of variation and covariation
in maternal investment frequently remains elusive. Therefore,
independent datasets from different populations across
various animal taxa help to understand the general patterns of
84
covariation among reproductive traits along environmental
gradients.
Offspring number and size, which simultaneously determine the maternal reproductive output, are two plastic lifehistory traits (Roff, 2002). In most animals, larger offspring
have better performance and hence a higher chance of survival
than smaller offspring (Stearns, 1992). However, females
cannot increase their offspring size without a concomitant
reduction in offspring number (Roff, 1992). The evolutionary
trade-off between offspring number and size is particularly
important for taxa that provide no parental care and development of young depends upon egg provisioning. Selection
should favour the individuals that allocate resources between
offspring number and size in such way that their annual offspring survival is maximized (Smith & Fretwell, 1974; Parker
& Begon, 1986; Fleming & Gross, 1990). However, the relationship between offspring size and number is determined by
complex interactions between numerous factors, and determinants of the trade-off are not always evident in natural populations (Berven, 1982; Liao & Lu, 2011a; Wang et al., 2011).
Amphibians respond to varying environments by changing
offspring number or size when resources are limited (e.g.
Räsänen et al., 2008). Studies across altitudes provide a good
approach to understand life-history evolution in stressful
environments (Kozłowska, 1971; Howard & Wallace, 1985;
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
W. B. Liao, X. Lu and R. Jehle
Maternal investment in a toad
Lüddecke, 2002). For example, ecological conditions at high
altitudes, such as colder temperatures, greater seasonality,
shorter breeding seasons and greater fluctuations in food
availability, favour increased investment per offspring as
a strategy to increase offspring survival (Berven, 1982;
Morrison & Hero, 2003). Indeed, across a wide diversity of
anurans, high-elevation populations are characterized by
smaller clutches of larger eggs, whereas low-elevation populations have larger clutches of smaller eggs (Cummins, 1986;
Morrison & Hero, 2003; Liao & Lu, 2011a). However, variation in the trade-off between offspring size and number
among and within populations remains poorly investigated.
The aim of this study was to investigate altitudinal variation in Andrew’s toad Bufo andrewsi life-history traits, focusing on a possible trade-off between egg size and egg number
within and among populations. To this end, we first explored
the relationships between altitude, female age and body size.
We then tested the prediction that females from high-altitude
environments invest in larger eggs than females from low altitude. We also tested the predictions that there is a trade-off
between investment in egg size and clutch size, and that
females should have smaller clutches and show a stronger
trade-off between egg and clutch size at high altitudes. Finally,
we extended the analyses to factors influencing variation in
egg size and number, and the relationship between the latter
two.
Materials and methods
Study species and study sites
Despite an ongoing debate about the taxonomic validity of
B. andrewsi as a species distinct from Bufo gargarizans (Macey
et al., 1998; Frost, 2013), we regard it as a full spcies for the
present study. Bufo andrewsi inhabits subtropical montane
regions of southern China between altitudes of 700 and
3000 m a.s.l. (Fei & Ye, 2001). The species has a relatively long
spawning period with egg laying extending from early February to mid-June (about 4.5 months). Egg clutches tend to be
laid in aggregates, and individual females release their entire
clutch with a single male (Liao & Lu, 2009). Mating is sizeassortative and parental care is absent (Liao & Lu, 2011b).
Fieldwork was conducted in Baoxing County, Sichuan
Province, south-western China (c. 102°48′–103°00′E, 30°19′–
30°47′N; Fig. 1). The area has an annual average temperature
of 5.9–7.2°C and an annual average precipitation of 700–
1300 mm (Liao & Lu, 2010). Specimens were collected from
four different localities along an altitudinal gradient (760,
1000, 1690 and 2100 m; Fig. 1). Climatic conditions at the
study sites differed systematically, with annual mean air temperatures being 14.1, 11.7, 10.2 and 8.8°C from lowest to
highest altitude site, respectively (Fig. 2; Liao & Lu, 2012).
The timing of spawning differed among localities (760 m: midJanuary to later March, 10 weeks; 1000 m: early February to
mid-April, 10 weeks; 1690 m: mid-March to mid-May, 8
weeks; 2100 m: mid-April to early June, 6 weeks). The species
is considered as a prolonged breeder sensu Wells (1977).
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
Figure 1 Map showing the location of study sites in Baoxing County in
western China, together with the four sites from where Andrew’s toad
Bufo andrewsi were sampled for this study.
Sampling
Amplexed toads were collected from four sites during the
breeding seasons of 2008–2013. Caught pairs were transported
to field laboratories near the sites and each pair was kept in
separate tanks (40 × 50 × 60 cm) filled with pond water to
allow ovipositing. Once oviposition was completed, snout–
vent lengths of males and females were measured using a
vernier caliper to the nearest 0.1 mm, and the total number of
eggs in each clutch was counted. One hundred eggs were
randomly sampled and placed on a glass plate for photographing. A Motic Images 3.1 digital camera mounted on a
Moticam2006 light microscope (Motic China Group Co., Ltd,
Xiamen, China) was used to take digitalized photographs
under 400× magnifications. The diameter of 100 eggs was
measured to the nearest 0.1 mm, not including jelly capsules
based upon their outlines. We calculated egg volume assuming
the volume of a sphere (Vs = 4/3πr3, where r is the radius).
Clutch volume was calculated by multiplying clutch size with
average egg volume for each clutch. The longest phalanges
from the right hind limb of all females were removed
for marking and stored in 10% neutral buffered
85
Maternal investment in a toad
W. B. Liao, X. Lu and R. Jehle
GLMMs where altitude was entered into the models as regressor, and the population as a random effect, including female
age and size (covariates), year, as well as their interactions
with altitude in the models. To test for the trade-off between
egg size and clutch size, the set of models included egg size or
clutch size, respectively, as well as female phenotype and their
interactions with altitude. Models were also chosen by testing
equalities of slopes (i.e. significant interaction terms) and their
difference from zero. All statistics are two-tailed and values
are presented as mean ± sd. All analyses were performed using
SPSS 17.0 (SPSS Inc., Chicago, IL, USA).
Results
Figure 2 Monthly mean air temperatures for 1951–2000 at the four
localities (data from Baoxing County Weather Office), from which Bufo
andrewsi were collected.
formalin for skeletochronology. After the experiments, all
individuals and egg strings were returned to the places where
they were collected.
Age determination
We used an improved method of paraffin sectioning and Harris’s haematoxylin staining to produce histological sections
used for ageing of adult females (Liao & Lu, 2010). Cross
sections (13 μm thick) of the phalanx with the smallest
medullar cavity and the thickest cortical bone were selected
and mounted on glass slides. Mid-diaphyseal sections were
chosen for counting numbers of lines of arrested growth
(LAG) under a light microscope. The numbers of LAGs were
demonstrated to be formed during the hibernating period
based upon recapture of four marked individuals; hence, the
counted LAGs can be treated as the actual age, barring
endosteal resorption. To account for the latter, we compared
the diameter of the smallest cross section among juvenile
(1-year old) toads lacking resorption to the diameter of the
resorption line in adults to estimate missing LAGs due to
endosteal resorption. If the resorption area in adults exceeded
smallest cross-section diameter in juveniles, we assumed that
the first LAG was missing, and added 1 year as true age.
Statistical analyses
We used general linear models (GLMs) and generalize linear
mixed models (GLMMs) to analyse the data, using logtransformed data on body size, age, clutch size, egg volume
and clutch volume. We started by simple GLMs treating
population as a factor to assess existing variation in all
response variables of interest. We then investigated the
relationships between response variables and altitude using
86
Except for clutch size, mean values of all life-history traits
differed significantly between populations (Table 1). Sampling
time did not affect altitudinal variation in all life-history traits,
except for body size (all P > 0.22). Although female age tended
to increase with altitude, this effect was not significant
(F1,2.171 = 10.90, P = 0.07). Female size increased with altitude
(F1,3.592 = 16.93, P = 0.048), and this relationship remained significant when female age and collection time was controlled
for (age: F1,97.942 = 45.50, P < 0.001; altitude: F1,3.683 = 8.71,
P = 0.046; collection time: F1,33.181 = 4.63, P = 0.06), suggesting
that altitudinal differences in body size were driven by female
age. The effect of age on size was verified by the analysis of
covariance (ANCOVA), which revealed that age (F1,105 =
44.07, P < 0.001) and population (F3,105 = 5.01, P = 0.003) significantly explained female size. The fact that the interaction
between age and population was not significant (F3,105 = 1.06,
P = 0.40) showed that the relationship between female size
and age was similar in all populations.
GLMM revealed that egg volume was negatively correlated
with female size and age, but not collect time (Table 2). There
was a positive relationship between egg volume and altitude
independent of the effects of female body size and age (Fig. 3).
The negative effects of female size and age on egg size significantly differed among populations (ANCOVA: size, t = −2.07,
P < 0.001; age, t = −2.29, P < 0.05; Fig. 4).
Clutch size was positively, strongly correlated with female
size and age, but not collection time (Table 2). Clutch size
decreased significantly with increasing altitude when removing
the effect of female size and age (Fig. 3). The positive effects
of female size and age on clutch size significantly differed
among populations (ANCOVAs: size, t = 13.02, P < 0.001;
age, t = 4.97, P < 0.001; Fig. 4).
Clutch volume positively correlated with female size and
age, but not with collection time (Table 2), suggesting a relatively higher investment in reproduction later in life. After
controlling for the effects of female phenotype, clutch volumes
significantly increased with altitude (Fig. 3). There were significantly different relationships between female size and
clutch volume (ANCOVAs: t = 10.03, P < 0.001) and between
age and clutch volume among populations (t = 4.03,
P < 0.001).
Clutch size was negatively correlated with egg volume when
accounting for female size within each population, except at
760-m altitude (Fig. 5; partial correlation analysis, r > −0.39,
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
W. B. Liao, X. Lu and R. Jehle
Maternal investment in a toad
Table 1 Comparisons of life-history traits of Bufo andrewsi from four altitudes in Baoxing County, China
Population
n
Age
SVL
Egg size (mm)
Clutch size
Egg volume (mm3)
Clutch volume (mm3)
760 m
1000 m
1690 m
2100 m
F
P
21
27
41
21
3.0 ± 0.9
3.9 ± 1.0
4.2 ± 1.2
5.1 ± 1.1
10.46a
<0.001
91.9 ± 3.8
97.1 ± 4.1
100.3 ± 5.4
102.9 ± 4.2
14.89a
<0.001
2.0 ± 0.1
2.1 ± 0.1
2.2 ± 0.1
2.4 ± 0.1
81.16a
<0.001
3440.0 ± 595.1
3574.6 ± 667.2
3655.1 ± 779.0
3887.2 ± 748.8
1.02
0.386
4.0 ± 0.5
4.4 ± 0.5
5.7 ± 0.7
6.9 ± 0.8
72.69a
<0.001
13 572.0 ± 1270.2
15 646.0 ± 2500.9
20 713.6 ± 4171.4
26 424.9 ± 3841.8
18.95a
<0.001
Note: F = test value of one-way analysis of variance for differences in population means. n = sample size.
a
P < 0.001.
SVL, snout–vent length.
Table 2 Analyses of covariance of egg size, clutch size and total reproductive output (clutch volume) in Bufo andrewsi females from four altitudinally
separated localities in Baoxing County, China
Random
Source of variation
Egg volume
Population
Residuals
Altitude
Female size
Female age
Collect time
Clutch size
Population
Residuals
Altitude
Female size
Female age
Collect time
Clutch volume
Population
Residuals
Altitude
Female size
Female age
Collect time
Fixed
VAR
SE
Z
0.0098
0.0025
0.0139
0.0003
0.704
7.107a
0.0010
0.0027
0.0072
0.0026
0.0014
0.0004
0.0060
0.0004
df
b
SE
F
P
1,3.164
1,101.952
1,101.503
1,101.081
0.0025
−0.0459
−0.1247
−0.0024
0.0002
0.0130
0.0567
0.0024
101.72
11.80
4.83
0.93
0.002
0.001
0.030
0.337
1,2.486
1,103.420
1,103.491
1,101.735
0.0033
0.0141
0.0319
0.0044
0.0002
0.0013
0.0065
0.0026
8.60
158.76
23.81
1.70
0.040
<0.001
<0.001
0.092
1,2.475
1,102.887
1,102.102
1,10.507
0.0012
0.0097
0.0209
0.0009
0.0014
0.0010
0.0056
0.0031
0.672
7.106a
1.090
7.034a
19.34
84.53
12.57
0.083
0.032
<0.001
0.001
0.773
Note: Back-transformed slopes (b) are given with their SE.
a
P < 0.001.
P < 0.05 in all cases). There was a negative relationship
between clutch size and egg size indicative of a trade-off across
altitudes (F1,104.986 = 30.09, P < 0.001; Fig. 4). The slopes of
clutch size on egg size tended to increase with increasing
altitude, but the difference was non-significant (Z = 1.21,
P = 0.23; population × egg size, F3,109 = 0.80, P = 0.70).
Discussion
The four populations of B. andrewsi exhibit significant
altitudinal variation in the examined life-history traits. Female
body size is positively correlated with altitude. A geographical
gradient in body size has previously been observed in other
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
amphibians (Miaud, Guyetant & Elmberg, 1999; Ma, Lu &
Merilä, 2009; Liao et al., 2010; Oromi, Sanuy & Sinsch, 2012).
Bergmann’s rule rationalizes the occurrence of large-scale patterns of variation in body size as a consequence of environmental factors (Bergmann, 1847; Rensch, 1950). This theory
has been widely supported in animal taxa (anurans: Lu, Li &
Liang, 2006; Liao & Lu, 2010; reptiles: Sacchi et al., 2007;
birds: Ashton, 2002; mammals: Ashton, Tracy & de Queiroz,
2000). Altitudinal variation in female body size among four
B. andrewsi populations follows Bergmann’s rule, consistent
with previous evidence considering six populations (Liao &
Lu, 2012).
Theory suggests that the positive relationship between
maternal size and investment into offspring is associated with
87
Maternal investment in a toad
W. B. Liao, X. Lu and R. Jehle
Figure 4 Regression coefficients (slope, b) for (a) effects of female
phenotype [age and snout–vent length (SVL)] on maternal investment
parameters (egg size, clutch size and total reproductive output [clutch
volume]) and (b) the relationship between clutch size and egg size in
four populations. * P < 0.05; ** P < 0.01; *** P < 0.001.
Figure 3 Altitudinal variation in maternal investment parameters [egg
size, clutch size and total reproductive output (clutch volume)]. Each dot
represents the residual mean value for a given population corrected for
the effect of female size.
advantages of larger individuals for egg production (Roff,
1992). For B. andrewsi, egg size decreases with increasing
body size, and further studies are needed to disentangle the
exact mechanisms causing this observation. Larger females
have higher total capacities in reproduction, as confirmed for
other anurans (reviewed in Duellman & Trueb, 1986; Roff,
1992). The reasons for this positive relationship between
female size, clutch size and reproductive output can be
explained by the fact that females in good body condition tend
to increase the number of offspring produced (Seigel & Ford,
1992).
Life-history theory emphasizes that animals should optimally partition limited resources between growth and
reproduction throughout life. For example, an increase in
88
Figure 5 Among-population variation in the trade-off between egg size
and clutch size. Each dot represents the residual mean value for a given
individual corrected for the effect of female size.
reproductive output, clutch size and egg size with increasing
age is expected if residual reproductive resources decrease
(Stearns, 1992), or if resources available for reproduction
increase as a result of diminishing needs to allocate resources
to growth (Roff, 1992). Like most ectotherms with indetermiJournal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
W. B. Liao, X. Lu and R. Jehle
nate growth, female B. andrewsi fit the von Bertalanffy’s
model (Liao & Lu, 2012), which describes rapid somatic
growth for earlier stages followed by slower growth thereafter.
This implies that a larger fraction of energy would be devoted
to reproduction as individuals become older (Jørgensen, 1992;
Czarnoleski & Kozlowski, 1998), thus resulting in age-specific
reproductive output. In B. andrewsi, clutch size and reproductive output increase with increasing female age, suggesting a
higher investment in reproduction than in growth and/or selfmaintenance. However, the clutch by-female data further
show significant differences between size and age and maternal investment among populations, suggesting that environmental influences such as temperature and seasonality affect
maternal investment of females.
That egg size increases with increasing altitude supports the
hypothesis that larger eggs are selected for decreasing breeding site temperature and shorter breeding seasons in highaltitude environments (Armbruster et al., 2001; Johnston &
Leggett, 2002). This finding is in accordance with previous
findings from intra-specific comparisons of species with wide
geographical ranges, supporting the idea that larger eggs are
produced in colder localities where egg survival is presumably
low (Berven & Gill, 1983). The reasons are that increasing
energetic requirements posed by physiological stress or limited
resources may be overcome by a larger amount of yolk and
nutrients (Komoroski, Nagle & Congdon, 1998). Moreover, a
lower loss of sodium resulting from a smaller surface-tovolume ratio of larger eggs is the major physiological impact
of low temperature stress in larvae (Roff, 2002).
Clutch size from our study tends to decrease with increasing
altitude, suggesting that investment in larger eggs come at a
cost of egg number, in line with basic life-history theory
(Stearns, 1992). It is possible that the observed variation in
clutch size among populations is a result of colder environments in high-altitude habitats, which are physiologically
stressful or resource-limited during clutch production
(Lüddecke, 2002; Roff, 2002).
Total reproductive investments of organisms are often ecologically constrained. For example, reduced investments with
increasing latitudes have frequently been observed in temperate anurans (Miaud et al., 1999). The pattern is generally
attributed to restrictions of a short reproductive period and
harsh climates experienced by northern species or populations, even if animals adaptively shorten or cancel the ovarian
resting period before vitellogenic growth (Miaud et al., 1999;
Lu, 2004). Because of similar environmental constraints
encountered by high-altitude animals, their life-history strategies are expected to be similar than at high latitude
(Kozłowska, 1971). However, relative investments increasing
with altitudes have been observed in frogs (Rana temporaria,
Elmberg, 1991; Hyla labialis, Lüddecke, 2002). In our study,
higher relative investments at high-altitude environments are
probably associated with female somatic condition, which
affects the number and growth of oocytes to be recruited into
a future clutch (Jørgensen, 1992; Lüddecke, 2002). Hence,
higher relative investments depend, in part, upon faster egg
growth and intrinsic female properties and, in part, upon the
environment.
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
Maternal investment in a toad
Before accounting for female size, egg number–size relationships in anurans may be negative (Cummins, 1986;
Lüddecke, 2002) or unrelated to each other (Tejedo, 1992).
When the effect of body size is removed, a negative correlation
is frequently observed (reviewed in Duellman & Trueb, 1986;
Willamson & Bull, 1995). This trade-off for a given female size
was also observed in three B. andrewsi populations. However,
inconsistent with the prediction that stronger trade-offs
between clutch size and egg size should be observed in stressful
environments (Olsen & Vøllestad, 2003), our data indicate
that the strength of the trade-off between clutch size and egg
size did not differ among populations. The particular mechanisms mediating such trade-offs may be explained by the
relative importance of resource acquisition variation and allocation that dictates the relationship among reproductive traits
(Reznick, Nunney & Tessier, 2000).
For B. andrewsi, higher altitude individuals experience
lower temperatures and shorter growth periods (Liao & Lu,
2012). The interpopulation trade-off characterized by larger
and relatively fewer eggs at high altitudes should be a result of
adaptation of larger offspring to harsh environments. This
idea is supported by theoretical (Smith & Fretwell, 1974;
Lloyd, 1987) and empirical (Roff, 1992; Räsänen, Laurila &
Merilä, 2005) studies, which show that stressful environments
promote larger maternal investment in per-individual offspring to improve the annual offspring survival. In anurans,
advantages of larger eggs at higher latitude or altitude have
been demonstrated previously (development rate: Riha &
Berven, 1991; Merilä et al., 2000; Laugen et al., 2003; size at
metamorphosis: Kuramoto, 1978; Kaplan & King, 1997;
juvenile survival: Berven, 1990; Altwegg & Reyer, 2003). Since
warmer conditions should be favourable for the growth of
young (Parichy & Kaplan, 1992; Einum & Fleming, 2000), the
survival advantage associated with producing smaller eggs by
female B. andrewsi could lie in increased fecundity, which
potentially maximizes the number of offspring surviving to
reproduction (Stearns, 1992).
In conclusion, our results support the idea that relationships between maternal investment and female phenotype are
adaptive among populations and thus result in offspring survival gains. In particular, our analyses show that female size
and age contribute to reproductive traits, allowing us to conclude that selection favours larger clutches and high reproductive investment in larger and older females. High-altitude
females have higher investments per offspring to compensate
for the increased mortality rates of their offspring than their
low-altitude counterparts. The trade-off between egg number
and size occurs due to resource limitation. Differences
between populations in this trade-off result from selective
advantages of larger eggs at high altitude. Moreover, we also
find that the trade-off between egg size and clutch size is
altered in the face of higher altitude.
Acknowledgements
We are thankful to Professor Juha Merilä from University
of Helsinki and Dr Jun Hua Hu from Chengdu Institute
of Biology, Chinese Academic of Science for the helpful
89
Maternal investment in a toad
comments in the paper. Financial support was provided by the
National Natural Science Foundation of China (31101633),
Sichuan Province Outstanding Youth Academic Technology
Leaders Program (2013JQ0016) and the Innovative Team
Foundation of China West Normal University. All animals
used in the study were treated humanely and ethically following all animal care guidelines applicable in China.
References
Altwegg, R. & Reyer, H.U. (2003). Patterns of natural selection on size at metamorphosis in water frogs. Evolution 57,
872–882.
Armbruster, P., Bradshaw, W.E., Ruegg, K. & Holzapfel,
C.M. (2001). Geographic variation and the evolution of
reproductive allocation in the pitcher-plant mosquito,
Wyeomyia smithii. Evolution 55, 439–444.
Ashton, K.G. (2002). Patterns of within-species body size
variation of birds: strong evidence for Bergmann’s rule.
Glob. Ecol. Biogeogr. 11, 505–523.
Ashton, K.G., Tracy, M.C. & de Queiroz, A. (2000). Is
Bergmann’s rule valid for mammals? Am. Nat. 156, 390–415.
Bergmann, C. (1847). Über die Verhältnisse der
Wärmeökonomie der Thiere zu ihrer Grösse. Gött. Stud. 1,
595–708.
Berven, K.A. (1982). The genetic basis of altitudinal variation
in the wood frog Rana sylvatica. I. An experimental analysis of life history traits. Evolution 36, 962–983.
Berven, K.A. (1990). Factors affecting population fluctuations
in larval and adult stages of the wood frog (R. sylvatica).
Ecology 71, 1599–1608.
Berven, K.A. & Gill, D.E. (1983). Interpreting geographic
variation in life-history traits. Am. Zool. 23, 85–97.
Cummins, C.P. (1986). Temporal and spatial variation in egg
size and fecundity in R. temporaria. J. Anim. Ecol. 55, 303–
316.
Czarnoleski, M. & Kozlowski, J. (1998). Do Bertalanffy’s
growth curves result from optimal resource allocation.
Ecol. Lett. 1, 5–7.
Duellman, W.E. & Trueb, D.L. (1986). Biology of amphibians:
New York: McGraw-Hill Inc.
Einum, S. & Fleming, I.A. (1999). Maternal effects of egg size
in brown trout (Salmo trutta): norms of reaction to environmental quality. Proc. Biol. Sci. 266, 2095–2100.
Einum, S. & Fleming, I.A. (2000). Selection against late emergence and small offspring in Atlantic salmon (Salmo salar).
Evolution 54, 628–639.
Elmberg, J. (1991). Ovarian cyclicity and fecundity in boreal
common frogs R. temporaria L. along a climatic gradient.
Funct. Ecol. 5, 340–350.
Fei, L. & Ye, C.Y. (2001). The colour handbook of amphibians
of sichuan: Beijing: China Forestry Publishing House.
Fleming, I.A. & Gross, M.R. (1990). Latitudinal clines: a
trade-off between egg number and size in Pacific salmon.
Ecology 71, 1–11.
90
W. B. Liao, X. Lu and R. Jehle
Frost, D.R. (2013). Amphibian species of the world: an online
reference: New York: American Museum of Natural
History.
Howard, J.H. & Wallace, R.L. (1985). Life history characteristics of populations of the long-toed salamander
(Ambystoma macrodactylum) from different altitudes. Am.
Midl. Nat. 113, 361–373.
Johnston, T.A. & Leggett, W.C. (2002). Maternal and environmental gradients in the egg size of an iteroparous fish.
Ecology 83, 1777–1791.
Jørgensen, C.B. (1992). Growth and reproduction, In Environmental physiology of the amphibians: 439–467. Feder, M.E.
& Burggren, W.W. (Eds). Chicago: University Chicago
Press.
Kaplan, R.H. & King, E.G. (1997). Egg size is a developmentally plastic trait: evidence from long-term studies in the
frog Bombina orientalis. Herpetologica 53, 149–165.
Kaplan, R.H. & Phillips, P.C. (2006). Ecological and developmental context of natural selection: maternal effects and
thermally induced plasticity in the frog B. orientalis. Evolution 60, 142–156.
Komoroski, M.J., Nagle, R.D. & Congdon, J.D. (1998). Relationships of lipids to ovum size in amphibians. Physiol.
Zool. 71, 633–641.
Kozłowska, M. (1971). Difference in the reproductive biology
of mountain and lowland common frog R. temporaria L.
Acta Biol. Cracov. Ser. Zool. 14, 17–32.
Kuramoto, M. (1978). Correlations of quantitive parameters
of fecundity in amphibians. Evolution 32, 287–296.
Laugen, A.T., Laurila, A., Räsänen, K. & Merilä, J. (2003).
Latitudinal countergradient variation in common frog
(R. temporaria) development rates – evidence for local
adaptation. J. Evol. Biol. 16, 996–1005.
Liao, W.B. & Lu, X. (2009). Sex recognition by male
Andrew’s toad B. andrewsi in a subtropical montane region.
Behav. Processes 82, 100–103.
Liao, W.B. & Lu, X. (2010). Age structure and body size of
the Chuanxi tree frog Hyla annectans chuanxiensis from
two different elevations in Sichuan (China). Zool. Anz. 248,
255–263.
Liao, W.B. & Lu, X. (2011a). A comparison of reproductive
output of the Omei Treefrog (Rhacophorus omeimontis)
between high and low elevations. Anim. Biol. 61,
263–276.
Liao, W.B. & Lu, X. (2011b). Proximate mechanisms leading
to large male-mating advantage in the Andrew’s toad,
B. andrewsi. Behaviour 148, 1087–1102.
Liao, W.B. & Lu, X. (2012). Adult body size = f (initial
size + growth rate × age): explaining the proximate cause of
Bergman’s cline in a toad along altitudinal gradients. Evol.
Ecol. 26, 579–590.
Liao, W.B., Zhou, C.Q., Yang, Z.S., Hu, J.C. & Lu, X.
(2010). Age, size and growth in two populations of the
dark-spotted frog Rana nigromaculata at different altitudes
in southwestern China. Herpetol. J. 20, 77–82.
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
W. B. Liao, X. Lu and R. Jehle
Lloyd, D.G. (1987). Selection of offspring size at independence and other size-versus-number strategies. Am. Nat. 129,
800–817.
Lu, X. (2004). Annual cycle of nutritional organ mass in a
temperate-zone anuran, Rana chensinensis, from northern
China. Herpetol. J. 14, 9–12.
Lu, X., Li, B. & Liang, J.J. (2006). Comparative demography
of a temperate anuran, R. chensinensis, along a relatively
fine elevational gradient. Can. J. Zool. 84, 1789–1795.
Lüddecke, H. (2002). Variation and trade-off in reproductive
output of the Andean frog H. labialis. Oecologia 130, 403–
410.
Ma, X., Lu, X. & Merilä, J. (2009). Altitudinal decline of
body size in a Tibetan frog. J. Zool.(Lond.) 279, 364–371.
Macey, J.R., Shulte, J.A. II, Larson, A., Fang, Z., Wang, Y.,
Tuniyev, B.S. & Papenfuss, T.J. (1998). Phylogenetic relationships of toads in the Bufo bufo species group from the
eastern escarpment of the Tibetan Plateau: a case of
vicariance and dispersal. Mol. Phylogenet. Evol. 9, 80–87.
Merilä, J., Laurila, A., Pahkala, M., Räsänen, K. & Laugen,
A.T. (2000). Adaptive phenotypic plasticity in timing of
metamorphosis in the common frog R. temporaria.
Ecoscience 7, 18–24.
Miaud, C., Guyetant, R. & Elmberg, J. (1999). Variations in
life-history traits in the common frog R. temporaria
(Amphibia: Anura): a literature review and new data from
the French Alps. J. Zool.(Lond.) 249, 61–73.
Morrison, C. & Hero, J.M. (2003). Geographic variation in
life-history characteristics of amphibians: a review. J. Anim.
Ecol. 72, 270–279.
Olsen, E.M. & Vøllestad, L.A. (2003). Microgeographical
variation in brown trout reproductive traits: possible effects
of biotic interactions. Oikos 100, 483–492.
Oromi, N., Sanuy, D. & Sinsch, U. (2012). Altitudinal variation of demographic life-history traits does not mimic latitudinal variation in natterjack toads (Bufo calamita).
Zoology 115, 30–37.
Parichy, D.M. & Kaplan, R.H. (1992). Maternal effects on
offspring growth and development depend on environmental quality in the frog B. orientalis. Oecologia 91, 579–586.
Parker, G.A. & Begon, M. (1986). Optimal egg size and
clutch size: effects of environment and maternal phenotype.
Am. Nat. 128, 573–592.
Räsänen, K., Laurila, A. & Merilä, J. (2005). Maternal investment in egg size: environment- and population-specific
effects on offspring performance. Oecologia 142, 546–553.
Journal of Zoology 293 (2014) 84–91 © 2014 The Zoological Society of London
Maternal investment in a toad
Räsänen, K., Söderman, F., Laurila, A. & Merilä, J. (2008).
Geographic variation in maternal investment: acidity affects
egg size and fecundity in Rana arvalis. Ecology 89, 2553–
2562.
Rensch, B. (1950). Die Abhängigkeit der relativen
Sexualdifferenz von der Körpergrösse. Bonn. Zool. Beitr. 1,
58–69.
Reznick, D., Nunney, L. & Tessier, A. (2000). Big houses, big
cars, superfleas, and the cost of reproduction. Trends Ecol.
Evol. 15, 421–425.
Riha, V.F. & Berven, K.A. (1991). An analysis of latitudinal
variation in the larval development of the wood frog
(R. sylvatica). Copeia 1991, 209–221.
Roff, D.A. (1992). The evolution of life histories: New York:
Chapman & Hall.
Roff, D.A. (2002). Life-history evolution: Sunderland: Sinauer
Associates.
Sacchi, R., Pupin, F., Pellitteri, D.R. & Fasola, M. (2007).
Bergmann’s rule and the Italian Hermann’s tortoises: latitudinal variations of size and shape. Amphib-Reptil. 28,
43–50.
Seigel, R.A. & Ford, N.B. (1992). Effect of energy input on
variation in clutch size and offspring size in a viviparous
reptile. Funct. Ecol. 6, 382–385.
Smith, C.C. & Fretwell, S.D. (1974). The optimal balance
between size and number of offspring. Am. Nat. 108, 499–
506.
Stearns, S.C. (1992). The evolution of life histories: Oxford:
Oxford University Press.
Tejedo, M. (1992). Absence of the trade-off between the size
and number of offspring in the natterjack toad
(B. calamita). Oecologia 90, 294–296.
Wang, Y.J., Ji, W.H., Zhao, W., Yu, N.N. & Liu, N.F.
(2011). Geographic variation in clutch and egg size for the
lizard Phrynocephalus przewalskii (Squamata: Agamidae).
Asian Herpetol. Res. 2, 97–102.
Wells, K.D. (1977). The social behaviour of anuran amphibians. Anim. Behav. 25, 666–693.
Willamson, I. & Bull, C.M. (1995). Life-history variation in a
population of the Australian frog Ranidella signifera: seasonal changes in clutch parameters. Copeia 1995, 105–113.
Williams, G.C. (1966). Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am. Nat.
100, 687–690.
91