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High altitude frogs (Rana kukonoris) adopt a diversified bethedging strategy in the face of environmental unpredictability

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Environmental unpredictability can influence strategies of maternal investment among eggs within a clutch. Models predict that breeding females should adopt a diversified bet-hedging strategy in unpredictable environments, but empirical field evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg size along an altitudinal gradient in a frog species (Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch variability in egg size increased as the environment became variable (e.g., lower mean monthly temperature and mean monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs that were smaller and more variable in size. We provide support for a diversified bet-hedging strategy in high-altitude environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality. This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime fitness by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg size due to physiological constraints imposed by environmental conditions (e.g., duration of the active season, food availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future climatic changes. © 2018, Asiatic Herpetological Research Society. All rights reserved.
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Asian Herpetological Research 2018, 9(1): 43–49
DOI: 10.16373/j.cnki.ahr.170073
1. Introduction
Given finite resources, mothers generally make an
energetic trade-off between current reproductive
investment and somatic maintenance (Stearns, 1992).
This strategy serves to enhance tness by ensuring future
reproductive potential by producing offspring that vary
in size and quality (e.g., many small or fewer larger)
based on the environmental conditions of the habitat. The
outcome is a balance between the benefits of increased
fecundity and high offspring quality (Morrongiello et al.,
2012). A mother’s best option should be to produce as
many offspring of optimal size as is possible, which is
adjusted depending on environmental cues (Einum and
Fleming, 2004). Such resource allocation within eggs
of a clutch is influenced by the environmental variation
(Einum and Fleming, 2004; Morrongiello et al., 2012).
Empirical support for these patterns is widespread among
diverse taxa including plants (Vaughton and Ramsey,
1998), insects (Zovi et al., 2008), fishes (Johnston and
High Altitude Frogs (Rana kukonoris) Adopt a Diversified Bet-
hedging Strategy in the Face of Environmental Unpredictability
Wei CHEN1*, Liqing PENG1, Lichun JIANG1, David A. PIKE2, Christopher R. FRIESEN3
and Gregory BROWN3
Abstract Environmental unpredictability can inuence strategies of maternal investment among eggs within a clutch.
Models predict that breeding females should adopt a diversied bet-hedging strategy in unpredictable environments,
but empirical eld evidence from Asia is scarce. Here we tested this hypothesis by exploring spatial patterns in egg
size along an altitudinal gradient in a frog species (Rana kukunoris) inhabiting the Tibetan Plateau. Within-clutch
variability in egg size increased as the environment became variable (e.g., lower mean monthly temperature and mean
monthly rainfall at higher altitudes), and populations in environments with more unpredictable rainfall produced eggs
that were smaller and more variable in size. We provide support for a diversied bet-hedging strategy in high-altitude
environments, which experience dynamic weather patterns and therefore are of unpredictable environmental quality.
This strategy may be an adaptive response to lower environmental quality and higher unpredictable environmental
variance. Such a strategy should increase the likelihood of breeding success and maximize maternal lifetime tness
by producing offspring that are adapted to current environmental conditions. We speculate that in high-altitude
environments prone to physical disturbance, breeding females are unable to consistently produce the optimal egg
size due to physiological constraints imposed by environmental conditions (e.g., duration of the active season, food
availability). Species and populations whose breeding strategies are adapted to cope with uncertain environmental
conditions by adjusting offspring size and therefore quality show a remarkable degree of ability to cope with future
climatic changes.
Keywords altitude, bet-hedging strategy, environmental quality, egg size, within-clutch variation, unpredictable
* Corresponding author: Dr. Wei CHEN, from Ecological Security and
Protection Key Laboratory of Sichuan Province, Mianyang Normal
University, Mianyang, China, with his research focusing on the ecology
and adaptive evolution of amphibians.
Received: 20 September 2017 Accepted: 13 December 2017
1 Ecological Security and Protection Key Laboratory of Sichuan Province, Mianyang Normal University, Mianyang
621000, China
2 Department of Biology, Rhodes College, Memphis Tennessee 38111, USA
3 School of Life and Environmental Sciences, University of Sydney, New South Wales 2006, Australia
Asian Herpetological Research44 Vol. 9
Leggett, 2002; Morrongiello et al., 2012; Marshall and
Burgess, 2015), amphibians (Räsänen et al., 2008), and
birds (Tremblay et al., 2003).
In addition to trade-offs between the size and number
of offspring produced, breeding females often vary
offspring size within a clutch based on the environmental
cues they experience throughout ontogeny (Kaplan and
Cooper, 1984). When environments vary predictably
with the seasons, females are likely to lay eggs that
are of optimal size, and thus that are similar within
and among clutches (Kaplan and Cooper, 1984). When
environments vary unpredictably among years through
evolutionary time, females should instead evolve a bet-
hedging breeding strategy that increases geometric-
mean fitness (Philippi and Seger, 1989; Simons, 2011,
2014). When using a conservative bet-hedging strategy,
females may produce offspring that are larger but less
variable in size because large eggs may have greater
probability of survival in unpredictable environments, as
compared to a stable environment (Shine, 1978; Travis,
1980). This strategy can result in greater reproductive
success in years when environmental quality is poor,
especially if larger offspring have a size-based survival
advantage in these conditions (Einum and Fleming,
2004). Alternatively, females can also employ a
diversified bet-hedging strategy to produce a range of
offspring sizes, which spreads the risk of incorrectly
predicting future environmental conditions to ensure
at least some offspring survive, regardless of future
conditions (Capinera, 1979; Kaplan and Cooper, 1984;
Parker and Begon, 1986; Einum and Fleming, 2004;
Simons, 2011). According to the imperfect information
hypothesis, the degree of within-clutch variability in egg
size will decrease relative to average egg size (Koops et
al., 2003), and environmental quality also inuences the
degree of egg size variation by desiccation stress and/or
temperature and climate variability (Morrongiello et al.,
2012; Marshall and Burgess, 2015; Shama, 2015).
High altitude environments are ideal for testing the
predictions of bet-hedging models because of the high
degree of environmental variation and unpredictability
that occurs over small spatial scales. Animals living at
higher altitudes usually face harsher and less predictable
environments compared to ones living at lower altitudes
(Duellman and Trueb, 1986; Morrison and Hero, 2003;
Chen et al., 2013). These environmental conditions should
result in population divergence of reproductive strategies
along altitudinal gradients that are most suited to local
conditions. Most amphibians show variation in life history
traits among populations at different altitudes, including
shorter breeding seasons and activity periods, larger eggs
and longer juvenile stages, and larger body sizes at all
life stages being associated with high altitudes (reviewed
by Morrison and Hero, 2003). The shorter and more
variable activity periods of high-altitude environments
can directly constrain foraging time and therefore reduce
energy accumulation (Morrison and Hero, 2003; Chen
et al., 2011). Stored energy will determine breeding
investment strategies of explosive breeding species,
based on an assessment of environmental quality (Wells,
2007). However, it is difficult for selection to optimize
any one life history trait in a vicissitudinous environment
(Morrison and Hero, 2003), and therefore selection
may favor bet-hedging strategies. The Tibetan Plateau,
which experiences highly variable seasonal temperature
and rainfall patterns, provides an ideal location to test
the hypothesis that unpredictable environments select
for within clutch variation in egg size as predicted by
theoretical work on bet-hedging strategies (McGinley
et al., 1987; Einum and Fleming, 2004; Marshall et al.,
We investigated within clutch variation in egg-size
of Rana kukunoris, a frog species distributed along an
altitudinal gradient on the Tibetan Plateau, to test the
following predictions: within-clutch variation in egg
size will be (1) positively associated with altitude; (2)
negatively associated with mean egg size and positively
associated with clutch size; (3) negatively associated
with environmental quality, and (4) negatively associated
with environmental predictability. We also carried out
an experiment to investigate the influence of body size
on desiccation and survival of tadpoles. Such trade-offs
could help understand how maternal breeding strategies
are adapted to unpredictable environmental conditions,
and therefore provide a glimpse of reproductive tactics
that may continue to be successful under future climatic
2. Materials and Methods
Study species The plateau brown frog, R. kukunoris, is
endemic to high-altitude regions of the eastern Tibetan
Plateau, and is one of the few frog species that reaches
high elevation (2000–4400 m, Chen et al., 2011). Upon
emergence from hibernation in the spring, explosive
breeding takes place in shallow temporary ponds, where
desiccation and freezing can determine larval survival (Lu
et al., 2008). Egg clutches are deposited on the margins of
water bodies, which often freeze over during the night (Lu
et al., 2008); this, combined with drying of water bodies
Wei CHEN et al. Breeding Strategy of a High-altitude FrogNo. 1 45
during the breeding season can result in larval mortality
(Chen, personnel observation). After reproducing, females
only have a short activity period during which to store
energy for the next reproductive bout, prior to ceasing
activity for the next winter (Lu et al., 2008; Chen et al.,
2011, 2013). Female frogs are the larger sex, and clutch
size is positively correlated with female body size, with
females at higher altitudes producing larger clutches of
eggs (Chen et al., 2013).
Data collection We collected data from six R .
kukunoris populations (breeding ponds) along the eastern
Tibetan Plateau spanning a 255-km latitudinal gradient and
ranging in altitude from 2035 to 3494 m above sea level
(Figure 1, Table 1). During 2010-2015 we searched for
freshly laid egg clutches at breeding ponds. We counted
the number of eggs in a small sample of each clutch (ca.
5 g), which was weighed (to 0.01 g) and used to estimate
clutch size based on mass of the entire clutch. We
quantied egg size by measuring the diameter of 10–30
eggs from digital photographs of each clutch (Abramoff
et al., 2004). To ensure that egg size measurements were
comparable within and among populations (Räsänen et
al., 2008), all clutches were sampled and measured prior
to eggs reaching Gosner Stage 12 (Gosner, 1960). We
adopted coefcient of variation (CV) in egg diameter as a
measure of egg size variation that describes the standard
deviation as a percentage of the mean (Quinn and
Keough, 2002).
In order to explore the effects of environmental
conditions on egg size, we used mean monthly
temperature (MMT) and mean monthly rainfall (MMR)
to describe environmental quality of each site from
Figure 1 Map showing the distribution of our sampling sites for Rana kukunoris in the Tibetan Plateau.
Asian Herpetological Research46 Vol. 9
1980 – 2010 (from data. cma. cn). These variables can
mirror different aspects of environmental quality. For
example, in frogs, MMT is related to activity period
and metabolism, whereas MMR can determine food
availability and thus potential for energy accumulation
and storage (Wells, 2007). For three populations in
close proximity to local weather stations (< 20 km),
we also used mean monthly rainfall and mean monthly
temperature to calculate Colwell’s predictability indices
for rainfall and temperature (Colwell, 1974).
Tadpole Survival under Desiccation Experimental
Design We captured adult frog pairs in amplexus from
ponds at an altitude of 3462 m, and took these animals
back to Mianyang Normal University. We obtained
fertilized eggs by injecting pairs of frogs with synthetic
gonadotropins (10 IU/ml chorionic gonadotropin). We
measured the egg size and body size of the females, after
the eggs were laid.
We used 20 replicates of 10 fertilized eggs each (one
from each clutch, Gosner stage 10; Gosner, 1960) of
different sizes and placed them into a plastic box (20
cm×10 cm×5 cm) containing aged water maintained at
20°C. After 7 days, the numbers of hatched eggs (Gosner
stage 18–20) were recorded. At this time, all eggs had
either hatched or were clearly inviable. To measure the
impact of egg size on larval life, we maintained the
tadpoles in the same boxes for two weeks post-hatching
with a room temperature of 20°C, and we feed the
tadpoles in each box with sh food every three days and
change the water every three days. In order to investigate
the inuence of drought on tadpoles of different size, 40
tadpoles with different body lengths were haphazardly
selected to be placed onto dry copy paper, and have
survival time recorded as a function of desiccation.
Statistical methods First, we explored the relationships
between altitude and egg size variation using General
linear models (Glms) with altitude and latitude as
covariates, and CV as the dependent variable. We then
investigated the correlation between CV and clutch size
as well as CV and mean egg size in another independent
model. To explore the effect environmental quality on
egg size, we also explored the relationship between
environmental quality (mean monthly temperature and
rainfall) and CV using the same models. We explored the
relationships between both within-clutch variability of egg
size and egg size and environmental predictability using
linear regressions using stepwise discriminant function.
We explored the correlation between egg size and
survival rate, between egg size and tadpole performance,
and between body size of tadpoles and their survival rate
using the Spearman’s correlation coefcients.
Prior to analyses, we log10-transformed all variables
to better attain normality and improve homogeneity of
variance. All analyses were conducted using IBM SPSS
Statistics version 24.
3. Results
Field Data In total, we measured 410 clutches from six
populations spanning a 255-km latitudinal gradient and
ranging in altitude from 2035 to 3494 m above sea level.
Egg size showed significant variation within a clutch
(CV range 1.72%–12.73%), among clutches (t = 56.967,
df = 409, P < 0.001), and among populations (F5, 404 =
30.357, P < 0.001, Table 1). Body size of females was
not correlated with the degree of egg-size variation within
a clutch (Spearman’s correlation: rs = -0.416, n = 17, P =
The results from Glms revealed that altitude (F1, 407 =
5.984, P = 0.015), latitude (F1,407 = 12.659, P < 0.001)
can both influence the egg-size variation (Table 2).
The degree of egg-size variation did not increase with
increasing clutch size (F1, 398 = 1.470, P = 0.226), and this
was also the case for mean egg size (F1, 398 = 0.122, P =
0.727), despite signicant variation in the degree of egg-
size variation among populations (F5, 398 = 31.436, P <
0.001). However, the degree of egg-size variation within
a clutch was affected by environmental quality (Table
2), including temperature and rainfall (mean monthly
temperature F1, 407 = 57.117, P < 0.001, rainfall F1, 407 =
56.614, P < 0.001). Differences in the estimates of
Altitude (m) Latitude (degrees) Number of clutches (n) Mean egg size (mm) Std. Deviation Range (mm) Egg variation (CV%)
2035 33.16 46 2.07 0.14 1.76-2.44 6.92
3038 34.8 11 2.34 0.12 2.15-2.59 5.3
3061 32.78 45 2.17 0.15 1.91-2.61 7.1
3189 34.1 35 2.02 0.21 1.54-2.49 10.24
3462 34.82 189 1.97 0.13 1.62-2.36 6.66
3493 34.3 84 2.36 0.19 1.98-2.76 7.88
Table 1 Study site details for six high-altitude populations of Rana kukunoris in the Tibetan Plateau, including altitude, latitude and sample
sizes and clutch attributes.
Wei CHEN et al. Breeding Strategy of a High-altitude FrogNo. 1 47
variation were unaffected by sample size variation among
In general, when we considered environmental
predictability, only rainfall remained in the final model
and rainfall change exerted significant influence on egg
size variation in a clutch (B = -5.769, t = -7.267, P <
0.001). Clutch size was not significantly associated
with these variables (B = 0.346, t = 0.945, P = 0.345).
Females inhabiting more predictable environments laid
large eggs (B = 1.341, t = 8.691, P < 0.001) but that were
less variable in egg size (Figure 2), whereas females
inhabiting more unpredictable environments laid small
eggs but more variable egg sizes, subbestinga diversied
bet-hedging strategy of energy allocation to offspring.
Desiccation Experiment At Gosner stage 25, the
survival rate of tadpoles was not dependent upon initial
egg size (rs = -0.18, n = 20, P = 0.941), but there were
obvious differences in the developmental speed of
tadpoles; tadpoles from larger eggs grew faster than those
from smaller eggs (rs = 0.584, n = 20, P = 0.007). We also
found the large tadpoles from large eggs survived longer
than the small tadpoles when in a desiccating environment
(Pearson’s correlation r = 0.775, n = 40, P < 0.001; Figure
3), indicating that the offspring from large eggs are more
likely to survive simulated harsh conditions.
4. Discussion
Altitude is an important environmental factor that affects
many life history traits of amphibians, including the
duration of the breeding season, size and age at sexual
maturity, lifespan, egg number and size, and development
and growth of offspring (Morrison and Hero, 2003).
Therefore, many life history traits show altitudinal
clines in these characteristics (Morrison and Hero,
2003). Environmental unpredictability can also inuence
strategies of maternal investment among eggs within a
clutch (Duellman and Trueb, 1986; Morrison and Hero,
2003; Chen et al., 2013); our study revealed considerable
variation in egg size of R. kukunoris from Asia, both
within a clutch and among populations differing in
altitude and latitude. We also detected an obvious
altitudinal cline of egg-size variation within a clutch,
but no correlation between egg-size variation within
a clutch and mean egg size. Interestingly, our results
showed that breeding females produce small, but more
variable offspring sizes in unpredictable environments.
Similar within-clutch variability of eggs has also been
documented in tropical tree frogs form Santa Cecilia,
Ecuador (Crump, 1981).
The imperfect information hypothesis (Koops
et al., 2003) predicts the degree of within-clutch
variability of egg size will be negatively related to
average egg size. Our results did not support this
prediction because the degree of egg-size variation was
not significantly correlated with mean egg size in R.
kukunoris. We also documented a consistent pattern of
females producing a greater range of size variation with
eggs, indicating that females are fairly consistent in how
they divide resources among eggs. This pattern has also
been documented in other animals (Koops et al., 2003;
Semmens, 2008).
Our results also provide empirical support for
the predictive models developed by Marshall et al.
(2008), which stipulate that a diversified bet-hedging
strategy will occur as an adaptive strategy when
future offspring environments are unpredictable. We
found that female R. kukunoris in these increasingly
unpredictable environments produced smaller eggs
that are more variable in size. Similar patterns of
within-clutch egg size variation with diversified bet-
hedging strategy are found across taxa including brook
trout Salvelinus fontinalis (Koops et al., 2003), common
jollytails Galaxias maculatus (Semmens, 2008), quacking
frogs Crinia georgiana (Dziminski et al., 2009) and
tree frogs (Crump, 1981). The Tibetan Plateau is a
variable and unpredictable environment (Colwell index
values 0.89). In this environment, precipitation is an
important factor affecting the persistence of habitat and
breeding ponds and the survival of offspring, which likely
Parameter B t Sig. 95% CI
Lower Upper
Model 1
Altitude 0.00006 2.44613 0.01486 0.00001 0.00011
Latitude 0.05385 3.55794 0.00042 0.0241 0.0836
Model 2
Mean Monthly Temperature -0.19302 -7.55762 < 0.001 -0.24322 -0.14281
Mean Monthly Rainfall -1.96632 -7.52425 < 0.001 -2.48004 -1.45259
Table 2 Parameter estimates and test statistics from General linear models describing within-clutch egg-size variation. Model 1 and model 2
are the results testing the altitudinal cline and environmental quality, respectively. CI: Condence Interval for Mean.
Asian Herpetological Research48 Vol. 9
acts as strong selective forces on the breeding allocation
strategies of females. We thus speculate that adopting
a diversified bet-hedging strategy may be optimal and
adaptive in these low quality high-altitude environments
by increasing geometric-mean fitness (Simons, 2011,
2014), because the large tadpoles from larger eggs survive
longer in desiccating environments (Figure 2).
Within-clutch variation in offspring size has also been
attributed to the physiological or developmental inability
of females to precisely allocate resources evenly among
individual offspring (McGinley et al., 1987; Fox and
Czesak, 2000; Einum and Fleming, 2004), the inuence
from mothers on offspring environment (van den Berghe
and Gross, 1989), or sibling competition (Einum and
Fleming, 2002). Even so, we cannot rule out the effects
of phenotypic plasticity on egg-size variability, because
the concurrent evolution between predictable and
unpredictable components in environmental variance
is expected (Shama, 2015). In our study, we lack the
morphological data on female body condition before
oviposition, and were therefore unable to test whether
condition influences egg-size variability. Thus the exact
causes of egg-size variation within a clutch require further
Acknowledgments We thank Richard SHINE and
Dustin MARSHALL for comments on an early draft of
the manuscript. This study was funded by the Natural
Sciences Foundation for Distinguished Young Scholar of
Sichuan (grant number 2016JQ0038), Key Foundation
of Sichuan Provincial Department of Education
(grant number 18ZA0255) and the National Sciences
Foundation of China (grant number 31670392). All eld
and laboratory work was conducted under permission
from Mianyang Normal University.
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and enemies. Ecology, 89: 1388–1398
... For anurans species with a biphasic life cycle, reproduction is an annual key event that is conditioned by the characteristics of the environment where the different species will develop their larval phase (Wells 2007). In habitats where climate varies regularly, and this variation can be predicted, reproductive events may occur in favorable periods; meanwhile, in habitats where changes in climate conditions are unpredictable, the detection and reaction to favorable changes can be essential to increase reproductive success and offspring survival (Caro et al. 2016;Chen et al. 2018). In such cases, spawning in rain-filled ponds of unpredictable duration is expected to be synchronized with rainfall and occur more than once per season in favorable years and (or) be avoided in unfavorable years. ...
... Fast hatching would be beneficial in the shallow ponds where M. rubriventris develop as long as it allows the hatchlings to be washed into stable ponds of standing water (Laufer et al. 2015), or to ensure a long period of larval development before the pond dries. However, environmental quality also influences the degree of egg size variation by desiccation stress and (or) climate variability (Chen et al. 2018). A bet-hedging breeding strategy (risk spreading) should then evolve when environments vary unpredictably over years (Song et al. 2020). ...
... A bet-hedging breeding strategy (risk spreading) should then evolve when environments vary unpredictably over years (Song et al. 2020). The high risk of desiccation in temporary and unpredictable aquatic systems due to short hydroperiods should select for the production of smaller eggs and variable offspring sizes (Chen et al. 2018). Smaller eggs will result in shorter developmental periods, but larger eggs may have a greater probability of survival. ...
Anuran amphibians that breed in ephemeral ponds of unpredictable environments have mechanisms to tolerate or avoid associated risks of egg and tadpole mortality, such as selection of oviposition sites, plasticity in larval development, and resistance of eggs to desiccation. The Red-belly Toad Melanophryniscus rubriventris (Vellard 1947) breeds in temporary ponds in the Andean Yungas under unpredictable events of flooding and droughts of reproductive sites. To determine whether this species possesses any developmental mechanisms to deal with the environmental conditions, we experimentally evaluated the resistance of eggs subjected to different times of exposure to air and the tadpoles to different levels of pond desiccation. The species has not developed mechanisms of resistance of its eggs or phenotypic plasticity to the recurrent risks of pond desiccation, and mass mortality is a common event. In such a context explosive breeding highly synchronized with rainfall, together with fast larval development, seems to be vitally important at these places where the duration of ponds is short and unpredictable.
... The high-altitude adaptation allows an excellent phenomenon for examining how the animals cope with environmental stressors and accumulating genetic alterations and other physiological systems (Hutchison et al. 1976;Weber et al. 2002). The frogs are evident to acquire different genetic mechanisms correlated with the elevation distribution and high-altitude adaptation compared to other endotherms (Chen et al. 2013;Yang et al. 2016;Chen et al. 2018). Due to the high-altitude adaptation the physiological traits (body size and body mass), behavior such as vocal response are also switched among anurans and often hypothesized with different ecogeographical rules (Hu et al. 2011;Meenderink et al. 2017;von May et al. 2017). ...
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The molecular information of lesser-known bullfrog, Hoplobatrachus litoralis is restricted from Bangladesh (type locality) and Myanmar. The morphological observation further evidenced the range-extension of this species from India and Myanmar. Here, we collected the H. litoralis specimen from the Dampa Tiger Reserve, Mizoram state and provides a new altitude record (268m) and range-extension in northeast India. The DNA barcoding with mitochondrial Cytochrome b gene discriminates H. litoralis from other congeners with sufficient genetic distance (13.9% to 27.8%). The Bayesian phylogeny revealed monophyletic clustering of all five Hoplobatrachus species and showed the sister relationship of H. litoralis and H. tigerinus. The generated sequences of H. litoralis from northeast India depicted shallow divergence (1.5%) from the sequences generated from Bangladesh, indicates the possible genetic variability due to the alteration of the ecological niche. We suggested further physiological and molecular study with extensive sampling of this species to confirm their actual range distribution, high-altitude adaptation, and gene flow.
... Specifically, later birth-order daughters produce turions earlier in a northern latitude (Ontario) population (Mejbel & Simons, 2018). Here, because our goal is to isolate latitude as a source of variation in turion production, we used a stan- where environments are less predictable (Chen et al., 2018). To test this hypothesis, a design could include early and late (e.g., 3rd and 7th) birth-order daughters, although this would be logistically difficult, requiring multiple thermogradient runs, and staggering of frond introduction times because late birth-order daughters are produced after early ones. ...
Variable environments may result in the evolution of adaptive phenotypic plasticity when cues reliably indicate an appropriate phenotype‐environment match. Although adaptive plasticity is well established for phenological traits expressed across environments, local differentiation in norms of reaction is less well studied. The switch from the production of regular fronds to overwintering “turions” in the greater duckweed Spirodela polyrhiza is vital to fitness and is expressed as a norm of reaction induced by falling temperatures associated with the onset of winter. However, the optimal norm of reaction to temperature is expected to differ across latitudes. Here, we test the hypothesis that a gradient in the length and predictability of growing seasons across latitudes results in the evolution of reaction norms characterized by earlier turion production at higher latitudes. We test this by collecting S. polyrhiza from replicate populations across seven latitudes from Ontario to Florida, and then assessing differentiation in thermal reaction norms of turion production along a common temperature gradient. As predicted, northern populations produce turions at lower birth order and earlier; a significant latitude‐by‐temperature interaction suggests that reaction norm differentiation has occurred. Our results provide evidence of differentiation in reaction norms across latitudes in a phenological trait, and we discuss how the adaptive significance of this plasticity might be further tested.
... Rana kukunoris Nikolskii, 1918, is endemic to the eastern Tibetan plateau (Xie et al., 2000), and the species is an explosive breeder with a pure capital breeding strategy (Lu et al., 2008;Chen et al., , 2013aChen et al., , 2018. The species is sexually size-dimorphic with females being the larger sex Feng et al., 2015). ...
Organisms living in extreme environments, such as amphibians inhabiting the Tibetan plateau, are faced with a magnitude of potentially strong selection pressures.With an average elevation exceeding 4500 m, the Tibetan plateau is mainly characterized by low temperatures, but little is known about the influence of this factor on the growth, development, and behaviour of amphibian larvae living in this environment. Using a common garden experiment, we studied the influence of temperatures on the early growth and development of tadpoles of the Tibetan brown frog (Rana kukunoris) endemic to the eastern Tibetan plateau. We discovered that temperature had a significant influence on early growth and development of the tadpoles, with those undergoing high-temperature treatment growing and developing faster than their siblings from a low-temperature treatment. However, high-altitude individuals grew faster than low-altitude individuals at low temperatures, while the opposite was true at high temperatures. These results support the temperature adaptation hypothesis, as tadpoles’ growth and developmental rates were maximized at the temperatures experienced in their native environments. These results suggest that variation in ambient temperature, combined with evolutionary adaptation to temperature of local environments, is probably one of the most critical environmental factors shaping altitudinal differences in the growth and development of amphibian larvae on the Tibetan plateau.
... Variation in organ structure probably provides important clues on local adaptation of the morphology, physiology and behavior in organisms across environmental gradients and reflects the pressure target of natural selection during the evolutionary process (Liao & Chen, 2012;Jin et al., 2016;Lou et al., 2016;Alton et al., 2017;De Melo & Masunari, 2017;Lüpold et al., 2017;Shultz & Burns, 2017;Tanner et al., 2017;Zhong et al., 2017a;Chen et al., 2018;Inostroza-Michael et al., 2018;Liao et al., 2018;Qin et al., 2018;Tang et al., 2018;Wang & Liao, 2018;Wu et al., 2018;Huang et al., 2019;Mai & Liao, 2019). Different organs (e.g., digestive tract, muscles, livers, heart and lungs) in animals commonly display phenotypic adaptation to increasing altitude (Piersma et al., 1999;Hammond et al., 2001;Naya et al., 2009;Jin et al., 2015;Liao et al., 2015Liao et al., , 2016aMa et al., 2016;Wang et al., 2017;Zhong et al., 2017b;Yang et al., 2018). ...
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Variation in organ structure likely provides important clues on local adaptation and reflects the pressure target of nature selection. As one of the important organs, the skin plays a key role in adapting to complex environments by reducing water loss or increasing water absorption. Nevertheless, variation in the skin structure across different populations in a single species of anurans remains enigmatic. Here, we studied geographical variation in the skin structure of male Andrew's toads (Bufo andrewsi) across ten populations using histological methods. We quantified thickness of the skin, the epidermis, the loose layer, the compact layer, and of the epidermis, area of granular glands (GGs) and of ordinary mucous glands (OMGs), width of the calcified layer, and number of capillary vessels. We found that the thickness of the skin, dermis and loose layer in dorsal skin increased with latitude whereas the area of granular glands decreased with altitude. Moreover, the width of the calcified layer in ventral skin decreased with latitude among populations. Our findings suggest that geographical variation in skin structure in male B. andrewsi is likely to reduce water loss or make water absorption occur faster in complex high-latitude environments, improving local adaptation.
Life-history theory suggests that male anurans living in harsh and unpredictable environmental conditions (e.g., low temperature and/or high seasonality) should decrease reproductive investment because of short periods of activity and poor productivity. Although geographic variations in female life-history traits have been investigated intensively across a wide range of taxa, similar studies in males have been scarce. Here, we examined geographic variation in male testis mass of the brown frog ( Rana kukunoris ) across seven different altitudes on the eastern Tibetan plateau, and tested the hypothesis that relative size of testis mass should increase with increasing temperature and/or decreasing seasonality. In this study, we found male body condition, age and testis mass did not increase with temperature and temperature seasonality, which do not conform to our previous hypothesis, revealing that differences in temperature and temperature seasonality across populations could not drive the evolution of testis size. However, we found a positive correlation between testis mass and body condition or age when controlling for population and the effect of temperature and temperature seasonality, indicative of a condition-dependent expression of testis size. In addition, a correlation between testis mass and operational sex ratio was not significant, suggesting that male–male competition did not lead to increasing levels of sperm competition.
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Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within-clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17°C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21°C), implying selection for different-sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within-female egg size variability, especially at 21°C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21°C had larger mean body sizes if their mother developed at 21°C, but this TGP benefit was not present for offspring of 17°C mothers reared at 17°C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21°C. In summary, stickleback mothers may have used both TGP and diversified bet-hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty. This article is protected by copyright. All rights reserved. This article is protected by copyright. All rights reserved.
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Adaptive phenotypic plasticity evolves when cues reliably predict fitness consequences of life-history decisions, whereas bet hedging evolves when environments are unpredictable. These modes of response should be jointly expressed, because environmental variance is composed of both predictable and unpredictable components. However, little attention has been paid to the joint expression of plasticity and bet hedging. Here, I examine the simultaneous expression of plasticity in germination rate and two potential bet-hedging traits – germination fraction and within-season diversification in timing of germination – in seeds from multiple seed families of five geographically distant populations of Lobelia inflata (L.) subjected to a thermal gradient. Populations differ in germination plasticity to temperature, in total germination fraction and in the expression of potential diversification in the timing of germination. The observation of a negative partial correlation between the expression of plasticity and germination variance (potential diversification), and a positive correlation between plasticity and germination fraction is suggestive of a trade-off between modes of response to environmental variance. If the observed correlations are indicative of those between adaptive plasticity and bet hedging, we expect an optimal balance to exist and differ among populations. I discuss the challenges involved in testing whether the balance between plasticity and bet hedging depends on the relative predictability of environmental variance.
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Examines the effect of spatial and temporal environmental variability on the optimal offspring size(s) through the use of mathematical models. Environmental variability does not necessarily favor the production of a range of offspring sizes by a parent. Most often, parental fitness is maximized by investing equally in all young. Considerable variation in offspring size has, however, been documented for both plants and animals. Factors that may prevent an organism from making equal-sized young are discussed.-from Authors
Prologue Part I: Evolutionary explanation Demography: age and stage structure Quantitative genetics and reaction norms Trade-offs Lineage-specific effects Part II: Age and size at maturity Number and size of offspring Reproductive lifespan and ageing Appendices Glossary References Author index Subject index.
Environmental predictability is predicted to shape the evolution of life histories. Two key types of environmental predictability, seasonality and environmental colour, may influence life-history evolution independently but formal considerations of both and how they relate to life history are exceedingly rare. Here, in a global biogeographical analysis of over 800 marine invertebrates, we explore the relationships between both forms of environmental predictability and three fundamental life-history traits: location of larval development (aplanktonic vs. planktonic), larval developmental mode (feeding vs. non-feeding) and offspring size. We found that both dispersal potential and offspring size related to environmental predictability, but the relationships depended on both the environmental factor as well as the type of predictability. Environments that were more seasonal in food availability had a higher prevalence of species with a planktonic larval stage. Future studies should consider both types of environmental predictability as each can strongly affect life-history evolution.
Reproducing females can allocate energy between the production of eggs or offspring of different size or number, both of which can strongly influence fitness. The physical capacity to store developing offspring imposes constraints on maximum clutch volume, but individual females and populations can trade off whether more or fewer eggs or offspring are produced, and their relative sizes. Harsh environments are likely to select for larger egg or offspring size, and many vertebrate populations compensate for this reproductive investment through an increase in female body size. We report a different trade-off in a frog endemic to the Tibetan Plateau, Rana kukunoris. Females living at higher altitudes (n = 11 populations, 2000–3500 m) produce larger eggs, but without a concomitant increase in female body size or clutch size. The reduced diel and seasonal activity at high altitudes may impose constraints on the maximum body size of adult frogs, by limiting the opportunity for energy accumulation. Simultaneously, producing larger eggs likely helps to increase the rate of embryonic development, causing tadpoles to hatch earlier. The gelatinous matrix surrounding eggs, more of which is produced by large females, may help buffer developing embryos from temperature fluctuations or offer protection from ultraviolet radiation. High-altitude frogs on the Tibetan Plateau employ a reproductive strategy that favours large egg size independent of body size, which is unusual in amphibians. The harsh and unpredictable environmental conditions at high altitudes can thus impose strong and opposing selection pressures on adult and embryonic life stages, both of which can simultaneously influence fitness.
Life history theory predicts that organisms inhabiting environments with relatively poor conditions for the growth and survival of their offspring should produce fewer and larger offspring. We examined egg size (an index of offspring size) of all iteroparous, broadcast-spawning, freshwater fish-the walleye (Stizostedion vitreum)-from 34 populations across 26degrees of latitude in order to determine whether egg size varied with respect to environinental indices of juvenile habitat quality. Variation among populations (among environments) was compared to variation within populations (among females). Within Populations, egg size generally increased with maternal size and age. Slopes of these relationships were much more variable among populations (cv > 100%) than interannually within populations (cv < 50%). Egg size vs. female size/age correlations were stronger in populations closer to the northern and southern limits of the walleye range. Egg size was also related to maternal growth history, but the effects of recent growth (previous year) were inconsistent. Egg size varied much less than fecundity among females of the same Population. For a standard size/age of female, predicted egg size was more variable among populations (cv > 10%) than interannually within Populations (cv < 5%), but only slightly more variable than among females within populations (mean cv = 8.5%). Nevertheless, among-population variability in egg size was related to environmental conditions. Mean egg size decreased with increasing latitude/decreasing mean annual temperature, contrary to our predictions. However, as predicted, egg size decreased with increasing lake productivity following adjustment for the latitudinal/temperature effect. These results suggest that egg size in fishes may be influenced by multiple environmental factors across populations, as well as by maternal effects within populations.
Predictions concerning egg size and the associated within-clutch variability component were tested with tropical treefrogs, genus Hyla. It was expected that species breeding in temporary versus permanent aquatic breeding sites would exhibit significant differences in clutch parameters as a result of differing selective forces in these contrasting environments. Although the intraclutch variability in egg size, as measured by CV, was not significantly different between the two groups, there was a significant difference in the shape of the distribution of values around the mean, as measured by kurtosis values (g2). The clutches from species breeding in temporary ponds tended towards platykurtosis; this distribution is interpreted as "bet-hedging" as a response to environmental uncertainty. The clutches from species breeding in permanent ponds tended towards leptokurtosis; this distribution is interpreted to be the result of stabilizing selection around an optimal egg size in the more predictable environment....
The functions of plant and insect propagule size are considered in the context of environmental heterogeneity. Qualitative phenetic characteristics associated with individuals and populations, such as development time, reproductive capacity, and survival probability, are generally correlated with propagule size. Optimal propagule size, i.e., that which confers increased fitness, varies with environmental conditions. Thus, the traditional view that progeny from large propagules are qualitatively superior or more vigorous is subject to qualification. Phenetic variation appears to result in production of progeny that are able to cope effectively with unpredictable but recurrent instabilities in their environment.