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First published online September 14, 2007
Journal of Experimental Biology 210, 3415-3421 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005652
Rapid assimilation of yolk enhances growth and development of lizard embryos from a cold environment
Department of Ecology and Organismal Biology, Indiana State University, Terre Haute, IN 47809, USA
* Author for correspondence (e-mail: mangilletta{at}indstate.edu)
Accepted 12 June 2007
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Summary |
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Key words: countergradient variation, growth rate, Sceloporus, tradeoff, yolkectomy
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Conover and Schultz,
1995). Most documented cases of countergradient variation
(sensu Levins, 1968)
have resulted from the evolution of a greater capacity for growth in colder
environments (Berven et al.,
1979; Conover et al.,
1997; Conover and Present,
1990; Jonassen et al.,
2000). The maintenance of a low capacity for growth in warm
environments seems counterintuitive because large size can confer greater
survival and fecundity (Roff,
2002; Stearns,
1992). The resolution of this paradox requires us to understand
the tradeoffs between growth and other functions that affect the fitness of
organisms (Billerbeck et al.,
2001; Gotthard,
2001; Lankford et al.,
2001). To identify potential tradeoffs, we must first determine
the proximate mechanisms by which certain genotypes achieve rapid growth
(Angilletta et al., 2003;
Present and Conover,
1992).
Embryos constitute a simplified biological system in which to investigate
the proximate sources of variation in growth rate. Most embryos reside within
eggs than contain a fixed supply of resources. Moreover, embryos expend little
energy on locomotion and no energy on reproduction. Consequently, embryos
consume most of their available energy for growth and respiration.
Countergradient variation in embryonic growth can arise in two ways: embryos
from colder environments either have more energy for growth or use their
energy more efficiently. In some species, mothers in colder environments
provision their embryos with larger supplies of energy
(Angilletta et al., 2006b;
Atkinson et al., 2001). By
manipulating the energy available to embryos, we can isolate the effects of
maternal energy allocation and embryonic growth efficiency
(Oufiero and Angilletta,
2006). Embryos could grow more efficiently by assimilating yolk
more rapidly or by reducing costs of growth and maintenance. Either strategy
would enhance fitness in a cold environment, where the poor potential for
thermoregulation and activity limits growth after hatching (see
Oufiero and Angilletta, 2006).
Still, both strategies should impose an energetic tradeoff that could
negatively impact the survival of the embryo or its performance after
hatching. Such tradeoffs would favor submaximal growth in environments where
the costs of rapid growth outweigh the benefits.
In this paper, we report the proximate causes of countergradient variation
in embryonic growth of the eastern fence lizard (Sceloporus
undulatus), with emphasis on the likely tradeoffs that constrain the
evolution of growth rates along geographic clines. Recently, Oufiero and
Angilletta discovered that S. undulatus has evolved countergradient
variation at least twice along latitudinal clines
(Oufiero and Angilletta,
2006). Although embryos from colder environments generally have
more yolk (Angilletta et al.,
2006b), countergradient variation persisted after controlling for
differences in egg size between populations. From this result, Oufiero and
Angilletta concluded that the physiological capacity for growth must have
diverged between populations. To determine the proximate mechanisms that
underlie differences in embryonic growth efficiency, we compared the
energetics of embryos from two of the populations studied previously. As in
previous experiments (Sinervo,
1990; Sinervo et al.,
1992), we removed yolk from eggs (yolkectomy) to manipulate the
energy available to embryos and ameliorate natural differences between
populations. Additionally, we controlled the duration of growth by measuring
energetics during a fixed period of development. Our results clearly show that
embryos from the cold environment fueled their rapid growth by assimilating
more yolk, potentially leaving less yolk available for juvenile growth.
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Materials and methods |
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Collection and husbandry
During the spring of 2005, we collected gravid females of Sceloporus
undulatus (Bosc and Daudin) from Edgefield County, South Carolina, USA
(SC) (122–137 m) and Montgomery, Giles, and Craig Counties, Virginia,
USA (VA) (884–1128 m). Mean annual air temperature of the area in SC
(18.0°C) greatly exceeds that of the area in VA (11.0°C). Both
populations belong to the eastern clade of S. undulatus, as described
by Leaché and Reeder (Leaché
and Reeder, 2002).
Lizards were placed individually in cloth bags and were stored in an insulated container for up to 72 h while being transported to Indiana State University. In the laboratory, lizards were placed in glass terraria (38 liters) with a substrate of fine sand. Terraria were kept in an environmental chamber set at a temperature of 25±1°C and a light cycle of 12 h:12 h L:D. An incandescent bulb (40 W) was placed at one end of each terrarium to enable lizards to thermoregulate. Lizards were fed domestic crickets (Acheta domesticus) to satiation every other day. Water was available at all times.
Acquisition of eggs
We acquired eggs by hormonally inducing females to oviposit. Controlling
the timing of oviposition served two purposes. First, we could weigh eggs
immediately after laying to avoid changes in mass caused by water flux.
Second, we could coordinate dates of oviposition among females to synchronize
measures of embryonic respiration. Oviposition was induced with an
intracoelomic injection of 
0.5 ml of oxytocin (20 USP; The Butler Company,
Columbus, OH, USA). Although this procedure probably reduced the initial stage
of development for some embryos (Parker et
al., 2004), we have no reason to believe that hormonal induction
would have affected mean developmental stage more in one population than the
other (see Oufiero and Angilletta,
2006). After induction, each lizard was placed in a plastic
container (4 liters) with a substrate of moist sand. These containers were
kept in a dark incubator set at 30°C. We monitored females closely for up
to nine hours or until palpation revealed that all eggs had been deposited.
Freshly laid eggs were assigned unique marks for identification and were
weighed to the nearest 0.01 mg.
Manipulation of egg size
Eggs received one of three treatments: (1) incubation after removal of yolk
(yolkectomized eggs), (2) incubation after a sham manipulation (sham eggs) or
(3) incubation without manipulation (control eggs). Females from VA generally
produce larger eggs than females from SC
(Oufiero and Angilletta,
2006). Therefore, eggs from VA received yolkectomy, sham and
control treatments (12, 13 and 11 eggs, respectively), but eggs from SC
received only sham and control treatments (17 and 19 eggs, respectively). To
avoid pseudoreplication, only one egg from each clutch was randomly assigned
to each treatment; uneven sample sizes reflect mortality of eggs in some
treatments. Additionally, one egg from each clutch was frozen at
–60°C on the day of oviposition. These eggs were used to estimate
the energy available to embryos (see below). To yolkectomize eggs, we used a
syringe to aspirate 30–100 mg of yolk (60±20 mg, mean ±
s.d.), depending on the initial mass of the egg. Sham eggs were pierced with a
needle but no yolk was removed. Control eggs were handled briefly but were
incubated without further manipulation.
Incubation of eggs
Eggs were incubated in plastic containers (10x10x6 cm)
containing a substrate of fine sand (100% silica). The water content of the
sand was maintained at 1% of total mass, yielding a water potential of
–10 kPa (Oufiero and Angilletta,
2006). To avoid conflating effects of incubation and source
environments, no more than one egg from each population was incubated in each
container. These containers were kept in two programmable incubators (Model KB
115; Brinkman Instruments, Westbury, NY, USA), which maintained a daily cycle
of temperatures ranging from 20 to 34°C [see
fig. 3 of
(Oufiero and Angilletta,
2006)]. This thermal cycle resembles those of natural nests in New
Jersey and Virginia (Angilletta et al.,
2005; Warner and Andrews,
2002). Although we do not know the temperatures of nests in SC,
differences in growth and development between populations did not depend on
incubation temperature in a previous experiment
(Oufiero and Angilletta,
2006). We shuffled the containers within and between incubators
every 2 days to minimize effects of thermal gradients; nevertheless, gradients
in temperature within each incubator were trivial (
0.5°C), as
verified by temperature loggers that we placed inside containers (Thermochron
iButton; Maxim Integrated Products, Sunnyvale, CA, USA). Every 4 days, we
replaced water that had evaporated from each container to minimize changes in
water potential during development.
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Embryonic respiration
For a subset of embryos, we estimated the energy expended on maintenance
and development from measures of respiration. At set intervals throughout
incubation, we recorded the oxygen consumption of embryos by closed-system
respirometry (Model TR-3; Sable Systems, Las Vegas, NV, USA). These recordings
began one day after oviposition and were repeated every 4 days until eggs were
sacrificed.
Each recording lasted 24 h, such that respiration could be summed over an entire thermal cycle. Prior to a recording, eggs were removed from their containers, cleaned of adhering sand and weighed to the nearest 0.01 mg. Each egg was placed on a piece of sterile cotton in a plastic dish. To prevent dehydration during respirometry, 1 ml of distilled water was added to the cotton. The dish was then positioned inside a clean, glass chamber (250 ml). Sealed chambers were placed in the same programmable incubators that housed the incubation containers. To ensure that embryonic temperatures equaled the air temperature of the incubator, chambers were placed in the incubators at least 1 h prior to measures of respiration. During this time, we calibrated the oxygen analyzer (Model FC-1; Sable Systems) with a gas of known concentration. Recordings always commenced at 16.00 h. Initially, all chambers were flushed sequentially with air purged of water and carbon dioxide by a gas generator (Model 75-45; Parker Hannifin Corp., Haverhill, MA, USA). Each chamber was flushed again at 12 and 24 h after the initial flush. At each flush, all air from the chamber was passed through the oxygen analyzer at a known rate. A computer controlled the sequential flushing of chambers to ensure that each chamber was sealed for a precise duration between recordings. Given our measures of oxygen concentration and flow rate, we could calculate the total volume of oxygen consumed while the chamber was sealed. Daily energy expenditure was calculated as the sum of oxygen consumption during the sequential 12-h periods. Although each recording ended at 04.00 h, eggs were not returned to their incubation containers until 08.00–10.00 h. Thus, eggs spent about 40 h within chambers during each recording. Nevertheless, these eggs developed similarly to eggs incubated without measures of respiration.
Total respiration was estimated by integrating rates of energy expenditure
over incubation. Each recording was analyzed by a computer program (CONVOL;
Sable Systems) to generate a daily rate of oxygen consumption (ml
day–1). These rates were converted to energy expenditure (J
day–1) by assuming that embryos catabolized protein and lipid
in equal quantities [19.05 J ml–1 of O2
(Nagy, 1983)] – an
assumption supported by the energy densities of eggs
(Oufiero et al., 2007) and the
respiratory quotients of embryos (Thompson
and Russell, 1998; Thompson
and Russell, 1999; Thompson
and Stewart, 1997). Because we made repeated measures of
respiration, we fit a linear model to each embryo's change in daily
respiration. All models described respiration extremely well (median
r2=0.95; range=0.70–0.99). By integrating the fitted
models, we obtained each embryo's total respiration during incubation (J).
In our analyses, we included only eggs that appeared to contain healthy embryos throughout incubation. For the population from VA, we included 7, 8 and 5 eggs from the yolkectomy, sham and control treatments, respectively. For the population from SC, we included 9 and 10 eggs from the sham and control treatments, respectively.
Developmental stages
After 48 days of incubation, we determined the developmental stages of
embryos by microscopy. Eggs were warmed from –60 to –2°C in
pre-weighed aluminum pans. Each egg was cut superficially on one side, and the
shell was separated from the embryo and membranes. Once the embryo had thawed
to room temperature, the yolk sac and chorioallantoic membrane were separated
from the embryo. Because eggs frozen at oviposition lacked discernable
embryos, these eggs were separated into shell and internal contents only.
Shells, yolk sacs and embryos were weighed individually to the nearest 0.01
mg. Embryos were placed on ice and were examined with a dissecting microscope
(Model DP12; Olympus, Center Valley, PA, USA). Developmental stages were
scored using the system of DuFaure and Hubert
(DuFaure and Hubert, 1961).
Because some embryos were between discrete stages, we scored development to
the nearest half stage. Scoring by half stages was based on the following
criteria: (1) the degree to which digits and scales had developed on the
hands, (2) the degree to which pigment and scales had developed on the head
and (3) the degree to which eyelids had formed. Embryos at half-stages
displayed either incomplete development of stage-defining characteristics or a
combination of characteristics from two sequential stages. After dissection,
the components of each egg were dried to a constant mass at 50°C.
Energetics of embryos
To estimate the assimilation and expenditure of energy, we determined the
caloric contents of yolk sacs and embryonic tissues via bomb
calorimetry. Dry samples were homogenized and pressed into one or two pellets
weighing at least 20 mg. Prior to calorimetry, these pellets were stored in
nitrogen-filled vials at –60°C. Some samples of embryonic tissue
were too small to combust directly (<20 mg); these samples were mixed with
benzoic acid to yield samples that were large enough to combust. After
combusting the mixed samples, we used their energy density and the energy
density of benzoic acid to calculate the energy density of the embryo. Shells
were not formed into pellets because they contained mostly minerals that would
not combust. Samples were combusted in a semimicro bomb calorimeter (Model
1420; Parr Instruments Company, Moline, IL, USA). The calorimeter was
calibrated with benzoic acid several times per day. After combustion, the
energy density of each sample was multiplied by its dry mass to yield its
energy content. Hereafter, we refer to the energy contents of embryos and yolk
as embryonic growth and residual yolk, respectively.
The energy available to each embryo was estimated from calorimetry of the
eggs frozen at oviposition. Because we froze one egg from each clutch, we
could use its yolk to estimate the energy available to its siblings. This
method avoids the accumulation of error inherent in summing components of an
energy budget (Thompson et al.,
2001) and provides accurate estimates of energy availability in
S. undulatus (dry masses generally differ by less than 5% between
sister eggs; C. E. Oufiero and M.J.A., unpublished data). To estimate the
energy available to a yolkectomized egg, we assumed yolk comprised equal
quantities of lipid and protein (Thompson
and Speake, 2002) and calculated the energy removed by yolkectomy
(see Oufiero and Angilletta,
2006).
Statistical analyses
We used analysis of covariance (ANCOVA) to examine the effects of
population on developmental stage, embryonic growth and residual yolk. In each
model, the effect of treatment (yolkectomy, sham or control) was nested within
the effect of population (VA or SC). The initial energy in each egg was used
as a covariate. A similar analysis was used to compare respiration between
populations and among treatments. For our comparison of total respiration (J),
we used embryonic growth (J) as a covariate; therefore, a significant
difference between populations would indicate a difference in the cost of
growth, defined as the slope of the relationship between growth and
respiration (Wieser, 1994).
Additionally, we compared rates of respiration near the end of incubation (day
45), using embryonic dry mass as a covariate. Prior to each analysis, we
assessed whether slopes of the relationship between the covariate and the
dependent variable differed between populations; when slopes differed, we
based our conclusions on a model that included the interaction between the
effects of the covariate and the population (see
Engqvist, 2005). All analyses
were performed with Statistica 6.0 (StatSoft Inc., Tulsa, OK, USA).
Descriptive statistics are reported as means ± 95% confidence
intervals.
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Results |
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As expected from previous experiments
(Oufiero and Angilletta,
2006), embryos from VA developed and grew more rapidly than
embryos from SC, even when both had similar quantities of energy at
oviposition (see Fig. 1 and
Fig. 2). Embryos from VA were
about half a stage more developed after 48 days of incubation than were
embryos from SC (F1,66=5.74, P=0.02). In other
words, embryos from VA had better-defined scales on their hands, more
pigmentation on their fingers and greater development of their eyelids.
Furthermore, embryos from VA contained 60% more energy in their tissues than
embryos from SC (F1,66=28.99, P<0.00001). The
relatively rapid growth of embryos from VA resulted from a greater
assimilation of yolk rather than a reduction in maintenance. Embryos from VA
had less residual yolk after 48 days of incubation than embryos from SC
(Fig. 3), even after adjusting
residual yolk for initial energy (F1,66=15.45,
P<0.001). The difference in mean residual yolk between populations
was nearly energetically equivalent to the difference in growth (see
Fig. 2 and
Fig. 3). Still, the rapid
assimilation of energy by embryos from VA appears to have imposed an energetic
cost (Fig. 4). Based on our
ANCOVA, the `cost of growth' (sensu
Wieser, 1994) was
approximately half a Joule of respiration per Joule of tissue
(ß=0.57±0.27; F1,33=19.12,
P<0.001). But even after we adjusted for variation in embryonic
growth, the total respiration of embryos from VA exceeded that of embryos from
SC (F1,33=6.79, P=0.01). Moreover, embryos from
VA respired more than embryos from SC on day 45 (separate slopes ANCOVA;
F1,31=5.34, P=0.03). Because both comparisons
were made after adjusting respiration for embryonic growth, these differences
indicate a relatively high cost of growth for the rapidly growing embryos from
VA.
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Discussion |
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). However, incubation periods may not reflect
developmental rates because an embryo could remain in the egg after reaching
its final developmental stage. By directly measuring development during a
fixed period, we found that embryos from a cold environment (VA) had reached a
later stage than embryos from a warm environment (SC). Moreover, embryos from
VA had deposited more energy within their tissues than embryos from SC. This
countergradient variation in growth and development resembles that documented
in other species of animals, including insects
(Neat et al., 1995),
crustaceans (Lonsdale and Levinton,
1985), fish (Conover,
1990; Imsland et al.,
2000b; Purchase and Brown,
2000), amphibians (Berven,
1982) and reptiles (Qualls and
Shine, 1998). For most of these species, biologists have yet to
identify the proximate and ultimate mechanisms that gave rise to these
patterns.
Two proximate mechanisms can lead to countergradient variation along
thermal clines: genotypes from cold environments either assimilate more energy
or grow more efficiently than genotypes from warm environments. In certain
species, we know that greater assimilation by rapidly growing genotypes
generates countergradient variation
(Conover and Present, 1990;
Jonassen et al., 2000;
Nicieza et al., 1994). In
other species, this phenomenon appears to result from differences in the
allocation of energy between growth and maintenance
(Imsland et al., 2000a;
Imsland et al., 2000b;
Malloy and Targett, 1994;
Neat et al., 1995). In S.
undulatus, embryos from VA grew faster than embryos from SC by
assimilating energy more rapidly. Rapid assimilation of yolk by embryos from
VA could explain their correspondingly high rates of respiration. During the
48 days of incubation, embryos from VA expended 8% more energy on respiration
than embryos from SC (see Fig.
4A). Presumably, a relatively high rate of respiration reflects a
greater need to generate ATP for maintenance, development and growth. For
example, rapid growth and development should require extensive extra-embryonic
membranes for transferring nutrients and wastes. The maintenance and function
of membranes directly limits the capacity for anabolism and constitutes a
major cost of living (Else and Hulbert,
2003). Other likely sources of variation in respiration between
populations include protein turnover and tissue remodeling associated with
development.
Although metabolic costs were relatively high for rapidly growing embryos,
a reduction in the incubation period resulting from rapid development helps to
compensate for this expense. In other words, an individual that hatches
earlier will need less energy to maintain itself as an embryo
(Angilletta et al., 2006a). We
can use our measures of respiration to conservatively estimate the energy
saved by rapid development. Towards the end of the 48 days of incubation,
embryos from VA expended about 40 J day–1. Because lizards
from VA complete incubation as many as 8 days earlier than lizards from SC do
(Oufiero and Angilletta,
2006), the savings could amount to 320 J. This conservative
estimate does not account for the fact that rates of respiration during
development would ultimately exceed 40 J day–1
(Angilletta et al., 2000). To
put this energetic saving in perspective, the mean respiration of an embryo
from VA exceeded that of an embryo from SC by only 100 J during the first 48
days of incubation. Therefore, we believe the energetic savings resulting from
rapid development more than compensate for the higher rate of energy
expenditure.
High rates of energy assimilation by embryos should lead to tradeoffs that
affect fitness. In other life stages, greater assimilation carries a cost of
predation risk (Gotthard,
2000; Lankford et al.,
2001). In embryos, costs of assimilation could arise in different
ways. For example, residual yolk can enhance growth or survival after hatching
(Ji and Sun, 2000;
Ji et al., 1997;
Pandav et al., 2006;
Troyer, 1987). In a companion
study (P. H. Niewiarowski, M.J.A. and M.A.S., manuscript in review), we
measured the growth of hatchlings from VA and SC over a period of 60 days. We
found that lizards from VA grew slower after hatching than lizards from SC. To
our surprise, this difference between populations was inconsistent with the
variation among individuals; within both populations, lizards that grew
rapidly as embryos also grew rapidly as hatchlings. At present, we do not know
the cause of these complex patterns. Nevertheless, we suspect the tradeoffs
imposed by rapid embryonic growth occur primarily in natural environments.
Hatchlings with low energy reserves would need to forage more intensely during
the first few days of life, when their inexperience with predators and
ignorance of their surroundings make them particularly vulnerable. This cost
of embryonic growth cannot be observed in an artificial environment with
unlimited food and no predators.
If rapid embryonic growth does impose a cost, we should detect this cost
through field experiments. First, we could release hatchlings from VA and SC
into natural environments and compare their growth and survival
(Sinervo, 1990;
Warner and Andrews, 2003).
Second, we could directly manipulate the residual yolk of hatchlings to assess
whether energy assimilation during the embryonic stage trades off with
physiological performance during the juvenile stage. By directly manipulating
residual yolk, rather than egg size, we could avoid confounding the effects of
residual yolk and hatchling size. For example, Troyer cleverly removed iguanas
from their shells and tied off their yolk sac to prevent further absorption;
these manipulated animals grew less than sham-manipulated and unmanipulated
animals (Troyer, 1987).
Similarly, Radder and colleagues (Radder
et al., 2007) surgically removed residual yolk from hatchling
lizards. In contrast to Troyer (Troyer,
1987), these investigators observed no differences in growth among
manipulated, sham-manipulated and unmanipulated lizards. Unfortunately, these
procedures only decrease residual yolk, whereas manipulations of egg size
could either increase or decrease residual yolk. Still, we could reduce the
residual yolk of lizards from SC to determine whether manipulated individuals
suffer poor performance. Such experiments could reveal tradeoffs between
embryonic growth and juvenile performance that maintain countergradient
variation.
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Acknowledgments |
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References |
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