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First published online July 20, 2007
Journal of Experimental Biology 210, 2667-2675 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005751
In ovo temperature manipulation influences embryonic motility and growth of limb tissues in the chick (Gallus gallus)
Department of Veterinary Basic Sciences, The Royal Veterinary College, Royal College Street, London, NW1 0TU, UK
* Author for correspondence (e-mail: chhammond{at}rvc.ac.uk)
Accepted 16 May 2007
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Key words: chick, movement, temperature, growth, incubation, muscle, bone
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) but also, more
recently, in the development of avians
(Maltby et al., 2004) and
reptiles (Booth, 1998;
Booth, 2006). The effects of
incubation temperature have been examined on the growth of long bones in chick
(Brookes and May, 1972) and on
muscle in fish and turkeys (Johnston,
2006; Maltby et al.,
2004). Whilst it is clear that temperature can influence the
development both of muscle and of bone, the mechanisms by which this is
occurring are unclear.
In addition to the general developmental biology interest in studying the
effects of environment on the development of the chick musculoskeletal system,
there are important welfare implications in this work. A huge and growing
number of chicks are bred each year for their meat, with 860 million chicks
per year in the UK (Defra,
2006). The majority are intensively farmed in order to elicit the
highest weight gain in the shortest time. There have been a number of reports
showing the correlation between rapid growth rates and the incidence of leg
disorders (Kestin et al.,
2001; Kestin et al.,
1992), with further reports showing that this affects the
behaviour of the birds and their ability to walk
(Vestergaard and Sanotra,
1999; Weeks et al.,
2000). It would therefore be of great potential benefit to
manipulate the growth and development of support tissues such as leg muscle
and bone by making simple changes to incubation regimes such that chickens are
better able to support greater weights and thereby reduce the incidence of
abnormalities.
A problem with investigating the effects of temperature in chicks is that
the scope for altering the incubation temperature of poultry eggs is
relatively small. In turkeys, increasing the incubation temperature by 1°C
throughout the duration of incubation causes a significant reduction in
hatchability, whereas shorter periods of around 4 days spent at the higher
temperature do not cause decreases in viability
(French, 2000). In chick
embryos, the period between embryonic day 4 (ED4), roughly HH23 on the
Hamburger and Hamilton staging series
(Hamburger and Hamilton,
1951), and ED7 (roughly HH30) corresponds to the time when the
primary muscle fibres have been laid down in the trunk and is just prior to
the formation of the secondary muscle fibres, which begins at ED8
(Crow and Stockdale, 1986;
Lee et al., 2004). It is a
time when there is a great deal of proliferation among myoblasts, followed by
differentiation. It is also the time that the limb buds form and grow and when
the undifferentiated cells of the limb mesenchyme start to differentiate as
muscle, cartilage and skin (reviewed in
Christ and Brand-Saberi,
2002). From ED5, the limb muscle masses undergo cleavage, and the
final muscle pattern is apparent by ED7.5 or HH30
(Kardon, 1998;
Pautou et al., 1982). Thus, it
is a critical time in limb development, and as such we hypothesize that
intervention at this time would give the greatest changes to the development
of limb tissues. Interestingly, it has been shown that raising temperature by
1°C from ED5 to ED8 in turkeys caused an increase in semitendinosus muscle
fibre number at 16 days posthatch, without a concomitant decrease in
hatchability (Maltby et al.,
2004). Comparison of the stages of turkey development
(Mun and Kosin, 1960) with
those of chick development (Hamburger and
Hamilton, 1951) showed that ED5 in turkeys corresponds to chick
HH20, approximately ED3.5, while ED8 in turkeys corresponds to HH29, which is
approximately ED6.5. We therefore chose ED4–7 as the time period that
best corresponded to the time reported to be most successful in turkeys and
also the time likely to have the greatest effect on limb development. We
hypothesize that temperature might control the balance between proliferation
and differentiation not only in the muscles but also in the growing bones of
the limb, supplying more cells to the tissues to promote future growth.
Small differences in incubation temperature, applied throughout incubation,
have been previously shown to influence growth of the long bones in the chick
leg (Brookes and May, 1972).
Additionally, short-term changes in temperature, in which high deviations from
normal temperature are applied, influence embryonic bone development in the
rat, probably through activation of heat shock
(Harrouk et al., 2005;
Kimmel et al., 1993). However,
it is not known whether a small change in temperature applied during early
incubation would be sufficient to change bone growth throughout development or
whether any change would be diminished by the later stages of development.
Importantly, the choice of our experimental time period (ED4–7), coming
at a time when, in the trunk, the sclerotome of the somites has condensed and
the cartilage model for the vertebrae has been laid down
(Christ et al., 2004),
suggests that our manipulations may be unlikely to interfere with trunk
skeletal patterning.
One way in which temperature might influence the growth and development of
the limb tissues could be by changing the motility of the chick, such that
differentiation of myoblasts might be promoted through muscle stretch
(Otis et al., 2005). It has
been reported that decrease of temperature reduces metabolic activity and
diminishes motor activity (Oppenheim and
Levin, 1975). It was therefore of interest to investigate whether
the converse is also true; whether increased temperature could increase the
motor activity of the chick.
In this study, we demonstrate that increasing the temperature of chick incubation by as little as 1°C for 3 days during early incubation has a significant effect on the motility and body mass of the chick embryo and on the growth of limb muscle and bone, coupled with a decrease in adipocyte size. We propose that the increased movement in the chicks raised at higher temperature may explain the effects seen on the growth of the musculoskeletal system.
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60–70% throughout embryonic growth in the case of controls.
Approximately half of the eggs were transferred to an identical incubator set
to 38.5°C from ED4 to ED7 before being returned to the control incubator
(Fig. 1). Temperatures within
the incubators were measured with a Squirrel Logger (Grant Instruments Ltd,
Cambridge, UK), with 10 probes each recording the temperature at a different
position within the incubator every 5 min. Prior to experiments, incubators
were mapped to see if any positions within the incubator deviated by more than
0.3° from the set temperature at any time over a 3-day period. Any
positions that showed deviation, such as the corners of the lowest shelf, were
not utilised for further experiments. During the experiments, temperatures
continued to be monitored, and any eggs judged to have experienced a
temperature that was out of the range of set temperature ±0.3°C
were removed from the experiment.
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). After
observation, the egg was resealed and replaced in the appropriate incubator.
All measurements in this paper were taken by the same researcher, although a
random sample were blinded and recorded by an independent researcher to ensure
validity of the measurements.
Sampling
Embryos from ED7 to ED18 were killed by decapitation, weighed and samples
taken as per the scheme in Fig.
1. The tissues were isolated and processed as detailed below.
Skeletal development
Embryos for skeletal staining were fixed in 96% ethanol for 2 days, then
stained with Alcian Blue and Alizarin Red to show cartilage and mineralized
bone, respectively, as previously described
(Lamb et al., 2003). The
length of the bones was measured on a dissecting microscope, with the
measurements calibrated using a 1 mm graticule.
Adipocyte morphology
Pectoral fat pads from chicks at ED15 and ED18 were fixed in buffered
formalin (BDH, Poole, UK) and were processed for wax embedding in a Shandon
Citadel 2000 automatic tissue processor (Shandon Scientific Ltd, Shandon, UK)
to preserve their delicate morphology. 5 µm-thick sections were cut using a
Microm HM360 microtome (Microm International, Bicester, UK). Sections were
stained with haematoxylin and eosin for subsequent measurements.
The Kontron image analysis software (Zeiss, Oberkochen, Germany) was used to determine mean adipocyte cross-sectional areas by taking high-magnification pictures, picking frames at random and counting the number of adipocytes per frame. The total number of frames was such that more than 30% of the adipocytes in the pectoral fat pad would be measured (more than 1000 cells were measured per age per chick).
Muscle morphology
Tissue for histological analysis, with the exception of fat, which was
processed as described above, was snap frozen in isopentane cooled in liquid
nitrogen. Cryosections at 15 µm were taken on a Bright Crysotat at
–20°C (Bright Instruments, Huntingdon, UK). Sections were adhered to
Superfrost slides (Fisher Scientific, Loughborough, UK), airdried and stored
at –20°C until required.
Haematoxylin and eosin staining was performed as previously described
(Heywood et al., 2005). Within
cross sections of the leg, the gastrocnemius muscle was identified. For
myofibre and myonuclear quantification, high-magnification pictures were
taken, choosing frames at random but discarding any that contained large blood
vessels, as blood vessels have more haematoxylin-stained nuclei per area than
do muscle. The number of myofibres and myonuclei were counted in a number of
frames, which totalled 8–12% of the total area of the muscle. The
numbers for each animal were averaged to a number per unit area, then the
number of myonuclei was divided by the number of myofibres to give a ratio of
nuclei per fibre.
Immunohistochemistry
Immunohistochemistry was carried out essentially as previously described
(Groves et al., 2005).
Briefly, sections were rehydrated in PBS+0.1% Tween20 (PBST), blocked in
PBST+5% goat serum and incubated in 1/200 CB-1 Antibody (DSHB, Iowa City, IA,
USA) diluted in the blocking reagent overnight at 4°C. The primary
antibody was detected with biotin-conjugated goat-derived anti-mouse IgG
(Vector, Peterborough, UK), Vectastain ABC Elite Peroxidase kit (Vector) and
visualized using 0.5 mg ml–1 of diaminobenzidine.
Photography
Light photomicrographs were taken using the KS300 system and sections were
analysed using Zeiss KS300 image analysis software (Image Associates, UK).
Micro computer tomography (Micro-CT)
Bones for microCT analysis were stripped of adherent muscle and other
tissue, then fixed in neutral buffered formalin. Scans were performed on a
SkyScan 1172 high resolution micro-CT (SkyScan, Kontich, Belgium), using the
software provided by the company. The bones were scanned with a pixel size of
13 µm, with the picture size set to 1024x768 pixels, the camera
position set to near, and with a 0.5 µm filter. Scans were reconstructed in
the NRecon 14.4.0 software supplied with the SkyScan and analysed with the
CTAnalyse software supplied by the manufacturer.
Statistical analysis
Statistics were performed using SPSS software (Chicago, IL, USA). Data was
analysed to ensure a normal distribution within groups, then Student's
t-tests were used to compare differences in each parameter between
the two temperature groups. All data displayed on graphs are presented as
means ± s.e.m.
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), which
would lead to the introduction of another variable, that of shell size, to the
experiments. On ED6 and ED7, the embryos incubated at 38.5°C made
significantly more movements over the measured period than the controls
(Fig. 2). Moreover, those
embryos that had been incubated at the higher temperature continued to move
more than the controls on ED11, 4 days after the eggs had been returned to the
control incubator (Fig. 2).
Therefore, not only does higher temperature induce the embryos to move more
during the period spent at high temperature but also somehow makes changes to
the behaviour of the embryo such that they continue to be more active long
after their return to control conditions. We therefore wanted to see what
effect these sustained movements were having on the growth and development of
the chick.
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), after which
point the extent of the mineralized portion of the bone increases towards the
joints. At none of the stages examined did we see any differences in the
timing of the onset or the extent of mineralization (measured as a percentage
of the length of the bone stained red by Alizarin Red) between the two
temperature regimes (Fig. 4C,D
and data not shown). In addition to looking at the length and mineralization
of the bone, we investigated the structure of the mineralized portions of the
tibia and femur bones later in development at ED15 and ED18 by micro-CT. We
saw no difference in the extent, or the structures, of the mineralized portion
of the femur and tibia bones between the two groups
(Fig. 4E,F and data not
shown).
Chicks raised at the higher temperature have more muscle fibres and nuclei in the gastrocnemius than do controls
We examined the number of myofibres per 150 000 µm2, the
number of myonuclei (per 150 000 µm2) and the ratio between the
two in the gastrocnemius muscle at ED18. The gastrocnemius is an important
muscle in chickens both for postural stability and for walking. Both the mean
number of myofibres and the mean number of myonuclei per cross-sectional area
at ED18 were higher in the chicks raised at the higher temperature than in the
chicks raised at 37.5°C throughout
(Fig. 5A,D,E). This appears to
be due to two factors: a small decrease in the size of the myofibres and a
small reduction in the amount of connective tissue seen in each frame
(Fig. 5D–G). In addition
to the numbers of myofibres and myonuclei per unit area, the total mass of the
gastrocnemius muscle is significantly higher in the chicks raised on the
experimental temperature regime (Fig.
5B). Together, these results suggest that the total number of
myonuclei and myofibres in the gastrocnemius muscle will be much higher in the
temperature-manipulated chicks than in the controls. Interestingly, the ratio
of nuclei per fibre was also increased in the chicks raised at 38.5°C,
from a mean of 0.81 nuclei visibly associated with each fibre to just over 1
nucleus per fibre (Fig.
5C).
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), which
would lead to the introduction of another variable to the experiments.
Additionally, the number of limb movements appears to peak around this period
(ED11–12) before declining dramatically by ED15
(Bradley, 1999;
Bradley et al., 2005).
The effects of movement have been widely studied during the in ovo
development of the chick because of the ability to control the environment of
the chick independently of maternal influence and because of the ease of
studying movements in ovo by windowing eggs. The first muscle
contractions in chicks begin early in development, around ED3
(Bekoff, 1981;
Bekoff, 1992;
Bekoff, 2001). A number of
different drugs have been used, by injection, to control the movement of the
chick. Two drugs have been widely utilized to induce paralysis, namely
pancurium bromide (PB), to induce flaccid paralysis, and decamethonium bromide
(DMB), to induce rigid paralysis, while a third drug, 4-aminopyridine (4-AP),
has been used to induce hyperactivity
(Pitsillides, 2006). With
respect to temperature, it has been reported that decrease of temperature
reduces metabolic activity and diminishes motor activity
(Oppenheim and Levin, 1975).
Conversely, in another paper, it was stated that cooling embryos between days
5 and 15 resulted in no change in embryonic motor activity unless the embryos
are cooled to 22°C, although a cessation in amnion contractions was noted
(Nechaeva and Turpaev, 1991).
Our results are more in agreement with those of Oppenheim and Levin and show
that a small rise in the temperature of incubation can have a significant and
sustained effect on the motility of the embryo. Indeed, the fact that the
embryos show increased activity after a return to the control temperature
suggests that the time spent at higher temperature programmes the later
motility of the chick. This could be through changes to the pattern of muscle
innervation or to the metabolism of the muscles. Interestingly, a recent paper
on Atlantic salmon has demonstrated that changing the incubation temperature
of salmon larvae during the period between fertilization and hatching leads to
changes in the motility of the fish, which are maintained until at least 21
weeks after first feeding (the latest stage examined)
(Albokhadaim et al., 2007).
Since, in this paper, fish activity was stimulated by feeding, the changes in
the motility between the groups could be related either to changes in muscle
development or to changes in appetite regulation
(Albokhadaim et al., 2007).
Temperature, movement and long bone growth
Increased temperature throughout the incubation period has been
demonstrated to cause increased long bone length in chicks
(Brookes and May, 1972). While
it has also been demonstrated that short periods spent at high temperature can
cause changes to bone development in rodents
(Harrouk et al., 2005;
Kimmel et al., 1993), these
studies have used non-physiological temperatures of 42°C, which cause rib
fusions and vertebrae truncations and are likely to be due to the effects of
heat shock during segmentation. It still remained unclear whether a relatively
short exposure to a temperature within a physiological range could have
effects on bone growth that would be sustained throughout later development.
That our embryos did not show a significant difference in leg bone length
until ED12, 5 days after a return to the control temperature, is interesting
and, as in the case of the increased motility, suggests that the early time
spent at higher temperature is programming later bone development. This could
be achieved by changes in the balance between proliferation and
differentiation in the long bone cartilage model, with different proportions
of chondrocytes in the different zones of the growth plate at each stage,
which are under the control of various signalling pathways (reviewed in
Kronenberg, 2003). It is
possible that an extra round of proliferation at an early stage, such as
during the period spent at higher temperature, would not become apparent until
much later in development when those extra cells have already differentiated.
The other possibility is that we do not see any changes in leg bone length in
the earlier stages because extra leg growth could be secondary to another
effect that is sustained through later development, of which one possible
candidate might be movement.
Our results showing that the embryos that were more motile had longer leg
bones than controls also concur with previous reports showing that paralysis
of chicks during embryonic development by either PB or DMB leads to long bones
that are shorter than controls (Bertram et
al., 1997; Hogg and Hosseini,
1992; Hosseini and Hogg,
1991a; Hosseini and Hogg,
1991b; Lamb et al.,
2003). The effects of increased motility on chick development have
been less well characterized, although treatment of embryos with the
hyperactivity-inducing drug 4-AP led to increased chick body mass at ED15 and
ED16, along with increased tibial length at these times, although the
differences were not significant at ED20
(Heywood et al., 2005).
Similar experiments showed that the balance of insulin-like growth factors
(IGFs) can be altered in leg muscles by motility-inducing drugs
(McEntee et al., 2006). It is
interesting that our temperature experiments have yielded results that closely
correlate with the results of inducing motility. Indeed, in our
temperature-treated embryos, the differences in both body mass and long bone
length appear to continue to diverge throughout development and are larger
than the effects seen following 4-AP treatment, despite the early nature of
our intervention. This may suggest that the chicks are more susceptible to
alterations to their incubation environment early in development than they are
at later stages. The mechanism behind the increased motility remains unclear,
but possibilities could be a change in the timing and pattern of muscular
innervation in the embryonic limbs or an acceleration in the establishment of
functional motor units within the muscle.
Temperature and increased embryonic movement leads to increases in the number of leg myonuclei
It has been shown that raising the temperature of incubation for a short
period during the development of turkeys can lead to an increase in the number
of myonuclei in the semitendinosus posthatch
(Maltby et al., 2004). We show
that increased incubation temperature leads to increased numbers of myonuclei
and increased myofibre number. Since there is an apparent decrease in the size
of the myofibres in addition to an increase in their numbers in the chicks
raised at 38.5°C, it suggests that there may be a temperature-dependent
change in the balance between the numbers of myoblasts undergoing
proliferation and those undergoing differentiation and hypertrophy, with
differentiation and growth delayed in favour of increased proliferation.
Interestingly, a recent paper on the effects of incubation temperature on
muscle development in larval haddock showed that incubating the fish at higher
temperature resulted in an increase in the number of myofibres in the deep
myotome 28 days after hatch (Martell and
Kieffer, 2007). Taken together, this suggests that diverse species
may exhibit similarities in their effects to altered incubation temperature,
which are sustained for long periods after the time spent at higher
temperature. The effects of altered temperature could perhaps be leading to
subtle changes in the balance between the phases of proliferation and
differentiation in the different cell populations.
However, an alternative explanation for the fact that changes to the muscle
and bone are seen much later in development may be offered by the fact that
this correlates with increased embryonic motility. The hyperactivity of the
embryos could provide a link between the changes that we are making early and
the effects, which we only see manifested later. Indeed, the only effect that
we see both during the time spent at increased temperature and during later
development is the hyperactivity of the embryos raised at higher temperature.
This would suggest that the change in movement could be driving the changes in
the development of the muscle and bone. This idea fits with the results of
Heywood et al., who demonstrated that artificially increasing embryonic
movement by in ovo injection of 4-AP leads to increased numbers of
myonuclei at ED20 (Heywood et al.,
2005). This may be caused by motility-driven changes in IGF
expression in the chick, as has been shown following injection of 4-AP
(McEntee et al., 2006).
However, there are numerous signalling pathways and other growth factors
operating in the chick limb during embryonic development such as the FGF
(fibroblast growth factor), Shh (Sonic hedgehog), Wnt and BMP (bone
morphogenic protein) signalling pathways, with their associated growth
factors, which could also be influenced by either temperature or mechanical
stretch (reviewed in Duprez,
2002).
While the results are in agreement with those of Heywood et al.
(Heywood et al., 2005), it is
interesting to speculate as to whether the effect of movement on muscle
development is a primary effect or is secondary to the effect of
temperature/movement on long bone development. Indeed, in papers where the
effect of paralysis on long bone development has been studied, it has been
postulated that the main force in driving the increase in muscle fibre length
is the growth of the skeletal elements
(Hall and Herring, 1990). This
is interesting given that stretch in muscles is linked to muscle growth.
Stretch-induced hypertrophy has been linked to changes in IGF signalling
(Goldspink, 1999) and leads to
increases in the expression of myogenic regulatory factors (MRFs)
(Lowe and Alway, 1999). In
culture systems, biaxial or uniaxial, stretch of the muscle cultures has been
demonstrated to increase myoblast proliferation through a number of pathways
(Kumar et al., 2004;
Otis et al., 2005). It is
possible that the increased bone length subjects the muscle fibres to greater
stretch forces and therefore promotes myogenic proliferation. If so, an
increase of temperature during early development leads to increased embryonic
motility, which in turn promotes increased growth of the bone and then the
muscle of the limb. In avian mutants that show defective motility, such as the
cn/cn mutant, muscle growth is severely limited
(Oppenheim et al., 1997).
Conversely, it has been reported that skeletal muscle can itself model bone
development. In
Myf5–/–;Myod–/–
double-mutant mice, lacking striated muscle, a number of bone defects have
been characterized, including fused vertebrae and long bone truncations
(Rot-Nikcevic et al., 2006).
This suggests that the forces that muscle exerts on the bone, as well as the
forces that bone exerts on muscle are required for normal growth and
patterning of both tissues.
The increase both in the number of myofibres and the nuclei:fibre ratio in
the temperature-treated chicks has interesting implications for the long-term
growth, posthatch, of these chicks. As the number of muscle fibres in amniotes
is fixed at the time of birth or hatch
(Goldspink, 1972), an increase
in the number of fibres in a particular muscle will allow that muscle to grow
more by hypertrophy than controls. Increases in hypertrophy of these fibres
are also likely to be driven by the increased nuclei:fibre ratio for two
reasons. Firstly, because it is likely that a proportion of the extra nuclei
seen in the group raised at higher temperature are satellite cells, the
proliferation of which provides most of the additional myonuclei required
posthatch for muscle growth (Campion,
1984). Secondly, because typically after birth/hatch, most fibres
tend to have a set nuclear domain size, which is the volume of cytoplasm that
can be supported by each nucleus (Brack et
al., 2005). The increase in the number of nuclei in each fibre
should increase the size to which the fibre can grow. Taken together, these
changes suggest that the chicks grown at this brief higher temperature regime
are likely to continue to show increased leg muscle growth later in life.
Adipose tissue begins to form in the chick around ED12
(Speake et al., 1996). Since
the chick egg is a sealed system, the amount of fat and protein available for
the growth of the embryo is fixed at the time the egg is laid. Since those
embryos raised at the higher temperature for a number of days show increased
motility and growth during the stages of development studied, it would seem
apparent that in order to achieve these phenomena the embryo must be expending
more energy than the control embryos. It is therefore unsurprising that that
these embryos have smaller adipocytes in the latter stages of development. It
might also be predicted, from these results, that the mass of the yolk might
be reduced in the later stages of development. It would be interesting in
future studies to examine whether this is the case and, if so, whether this
would have any effect on the timing of hatching. Previous studies have shown
that decreasing temperature can cause delayed hatch times
(Suarez et al., 1996), so it
might be predicted that our temperature regime might subtly reduce the length
of incubation.
In conclusion, increasing the temperature of incubation by 1°C for 3
days in early development affects a number of parameters during embryonic
growth, namely embryonic motility, body mass, long bone length and
gastrocnemius size and nuclear number. The fact that such a small change in
temperature in early development leads to continued divergence between the
groups throughout later development suggests that the stage between ED4 and
ED7 may be a critical window during which the tissues of the limb are more
susceptible to change. This study demonstrates that small temperatures can
cause significant changes that persist long after their application in chick,
as is the case in fish species such as haddock and salmon
(Martell and Kieffer, 2007;
Albokhadaim et al., 2007).
Additionally, these results also illustrate the importance of keeping a
constant incubation environment when carrying out other experiments in
developmental biology, otherwise the effect of the experiment could be masked
by changes caused by a fluctuation in the temperature of incubation.
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Acknowledgments |
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