Download Thyroid function and the development of endothermy

GENERAL AND COMPARATIVE
ENDOCRINOLOGY
General and Comparative Endocrinology 136 (2004) 17–22
www.elsevier.com/locate/ygcen
Thyroid function and the development of endothermy
in a marsupial, the Tasmanian bettong, Bettongia gaimardi
(Demarest 1822)
R.W. Rose* and Nur Kuswanti1
School of Zoology, University of Tasmania, Private Bag 5, Hobart, Tasmania 7001, Australia
Received 7 October 2003; revised 11 November 2003; accepted 20 November 2003
Abstract
The Tasmanian bettong (Bettongia gaimardi) is a small rat-kangaroo (marsupial) found only in Tasmania, Australia. The duration of pouch life is 15 weeks. Adults and older young display non-shivering thermogenesis and this paper examines the role of
thyroxine in the development of endothermy in pouch young. Free thyroxine (T4) concentrations varied throughout pouch life. The
mean ( SE) concentration was 6.2 1.9 pmol L1 in week 7, increased and peaked at 19.2 4.3 pmol L1 in week 12, and declined
to 5.6 0.4 pmol L1 by week 20. This was similar to adult levels (3.2 3.8 pmol L1 ). These concentrations showed significant
differences. From pouch week 12 onwards, T4 injection raised oxygen consumption. Maximum levels of VO2 after T4 injection
occurred at weeks 14–15. Although adult levels were lower, the increase in adult oxygen consumption after T4 injection was about
50%. Peak free T4 levels and metabolic responses to nor-adrenalin occur at week 12 and we hypothesize that thyroid hormone may
facilitate the development of adrenergic-receptors in this species. The data presented in the paper further attest to the likely important role of the thyroid gland in the development of endothermy in marsupial pouch young.
Ó 2003 Elsevier Inc. All rights reserved.
1. Introduction
In both eutherian and marsupial mammals, the thyroid gland plays a crucial role in the maturation of
physiological processes such as endothermy. At birth all
marsupials are naked and without the ability to produce
body heat; that is they are ectothermic (Rose et al.,
1998). Endothermic prowess develops slowly and in
tandem with the development of the thyroid gland (Rose
et al., 1998). Many eutherian neonates use brown adipose tissue to produce body heat; however, the vast
majority of marsupials have neither brown adipose tissue (BAT) nor uncoupling protein one (UCP1) and must
use other means to produce body heat (Kabat et al.,
2003a; Rose et al., 2000). How they do this is of intense
interest: most likely it involves changes in membrane
*
Corresponding author. Fax: +613-6226-2745.
E-mail address: [email protected] (R.W. Rose).
1
Present address: Biologi, FPMIPA, IKIP JI, Ketintang Surabaya
60321, Indonesia.
0016-6480/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved.
doi:10.1016/j.ygcen.2003.11.007
physiology (Hulbert, 2000) with the likely involvement
of the thyroid gland (Rose et al., 2000). Previously,
Hulbert (1987) had postulated that the evolutionary
changes leading to the characteristics of endothermic
mammals were due, in part, to an increase in thyroid
gland activity.
The mode of action of thyroid hormone is generally
unclear (Hulbert, 2000). It does result in thermoregulatory ability and an increase in oxygen consumption in
young mammals including those marsupials in which it
has been examined (Gemmell and Buaboocha, 1998;
Gemmell and Sernia, 1992; Hulbert and Augee, 1982;
Janssens et al., 1990, 1997; Setchell, 1974).
Bauman and Turner (1966) determined that in the
American marsupial (Didelphis marsupialis) thyroid secretion rates were higher in winter than in summer. The
values in young were even higher than adult rates.
Subsequently, work by Setchell (1974) on the tammar
wallaby (Macropus eugenii) demonstrated an increase in
thyroid hormone during pouch life and that inhibition
of the thyroid gland resulted in a failure of thermoregulation. Moreover, he found that pouch young
18
R.W. Rose, N. Kuswanti / General and Comparative Endocrinology 136 (2004) 17–22
thyroidectomized before 140 days failed to grow at the
normal rate, to differentiate or grow a full coat of hair.
They were also unable to respond to low temperature by
increasing oxygen consumption. Hulbert and Augee
(1982) demonstrated that thyroid function in the bandicoot (a marsupial) was similar to that in eutherian
mammals and did not account for the phylogenetic
differences in metabolic rate between these two major
mammalian groups. They showed that removal of the
thyroid gland resulted in a 30% drop in metabolic rate in
the bandicoot. Subsequently several authors have demonstrated that thyroid hormones (T4 and/or T3) increase to a peak during pouch life and then decrease to
adult levels. The peak in T4 levels correlate with the
attainment of thermoregulation and endothermy, including the ability to increase heat production in response to cold (Gemmell and Sernia, 1992; Hulbert,
1987; Janssens et al., 1990, 1997).
Although some previous work on the kangaroo
(Macropodidae) group has been published, there has
been very little study of the related group the rat-kangaroos (Potoroidae). Nicol (1977) showed that although
the total plasma thyroxine in the adult rat-kangaroo
(Potorous tridactylus), was low, the free levels were
similar to those in adult eutherian mammals (free T4
11.86 0.3 pM ml1 ). Gemmell and Rose (1989) showed
that the thyroid gland in two rat-kangaroos was not
functional at birth. In a pilot study of another ratkangaroo, the Tasmanian bettong (Bettongia gaimardi),
Rose et al. (1998) demonstrated that T4 levels peaked in
week 12 of the 15 week pouch life; also found in week 12
were peak levels of oxygen consumption at 35 °C (pouch
temperature), after exposure to cold (22 °C) and norepinephrine injection.
The Tasmanian bettong is a small rat-kangaroo (1–
2 kg) found only on the island of Tasmania, Australia; it
has a pouch life of 15 weeks and young become adult by
12 months.
Thermoregulation of the adult (Rose, 1997; Rose
et al., 1990) and young (Rose, 1987b, 1997) has been
documented. In the young bettong, thermoregulation
and endothermy develops slowly (Rose, 1987a,b; Rose
et al., 1998). Born ectothermic, the young are first able
to increase their metabolic heat production (endothermy) from week 10 of the 15 week pouch life.
Young are homoeothermic by week 12 (corresponding
with fur development). Unlike some marsupials this
species exhibits non-shivering thermogenesis, in that
older young and adults are able to increase their metabolic rate significantly in response to cold and/or
noradrenaline injection (Rose et al., 2000; Ye et al.,
1996). In addition, Rose et al. (2000) determined that
cold-acclimation enhances the response to nor-adrenaline. This paper sets out to examine the role of thyroid
hormone in the development of endothermy in this
species.
2. Material and methods
2.1. Animals
The bettongs used in this project came from a longestablished breeding colony at the University of Tasmania in Hobart. Five young were monitored over time
in all experiments, although not all young were sampled
every week.
2.2. Blood sampling
Blood samples were taken from the tail vein of each
animal. Two methods were used depending on the age of
the bettong. In early pouch young, the blood was obtained by puncturing the tail vein. It was then collected
into heparinized microtubes, and centrifuged for 10 min.
The plasma was kept in the refrigerator for further
analyses. With larger veins, blood collection was
carried out by heparinized syringe and needle. The
plasma separated was kept in tubes for storage in the
refrigerator.
2.3. Free thyroxine concentrations
Forty-two plasma samples were collected from five,
6–20-week-old bettongs. These were then analysed with
an Amerlex-Mab FT4 Kit. Only one tube was used for
each plasma sample, as there was insufficient solution
for duplicates. The amount of labelled T4 in each tube
was counted in a gamma counter (MR252, Roche,
Switzerland). A standard curve was produced and the
percentage of the hormones labelled from each sample
could then be calculated to assess the level of free T4.
2.4. Oxygen consumption
Oxygen consumption was measured by indirect calorimetry as in Rose et al. (1998). Metabolic rates were
measured in perspex chambers of various sizes (to accommodate the growing young), totally enclosed within
a water bath. The air pumped into the chamber was
varied with a flowmeter that had been obtained and
calibrated prior to the start of the experiments by Halu
Glass, Tasmania. The air passed through a one metre
long copper pipe that was coiled within the water bath
so that the air entering the chamber was at a similar
temperature to the water bath. A sample of air leaving
the chamber passed through drying tubes containing
indicating soda lime and then silica gel before entering
the oxygen analyser (AMETEK S-3A/11, 2-channels).
Similarly, a sub-sample of air entering the chamber was
passed though the drying tubes and soda-lime into a
separate channel of the oxygen analyser. The difference
between the % oxygen of the air entering and leaving the
chamber could be read directly on the analyser. The flow
R.W. Rose, N. Kuswanti / General and Comparative Endocrinology 136 (2004) 17–22
rate varied with the size and age of the young from 150
to 1000 ml/min. The measurements and calculation of
metabolic rates were made using equations in Rose
(1997) and Rose et al. (1998).
At least, 10 min elapsed before any readings were
obtained; we have shown that this period is sufficient for
animals to recover from the ÔstressÕ of an injection of
saline (Rose et al., 1998).
2.5. Oxygen consumption after thyroxine injection
Sodium thyroxine was dissolved in 0.02 N NaOH and
0.9% NaCl to produce a T4 concentration of 400 ng/L.
A preliminary experiment was performed with injections
of 100 pg T4/100 g body weight being administered to
the fully furred young. Oxygen consumption was measured for 48 h. Because there was no change in the degree of oxygen consumption before and after
administration, the amount of T4 injected was then
doubled to 200 pg/100 g body weight. This produced an
increase in oxygen consumption after 3–5 h. Accordingly, this concentration was used in the subsequent
experiments.
Injections were administered weekly on young at an
ambient temperature of 20 °C. Young of known age were
placed in the metabolic chamber of the oxygen measurement system until the reading became stable.
Meanwhile, the T4 solution was prepared in doses proportional to the weight of the young. After stabilisation,
the oxygen consumption of the young was read two to
three times in half-hour intervals, and the average was
taken as the control reading. The animals were removed
from the container and injected intra-peritoneally with
the T4 solution. As before, oxygen consumption was
measured after stabilisation, at half hourly intervals from
3 to 6 h. The average measurement was used as the level
of oxygen consumption after a T4 injection.
19
3. Results
3.1. Growth
Analysis of the growth of the two groups of bettongs
showed them to be not statistically different ðF1;112
0:634; p ¼ 0:428Þ: the slopes of the two regressions were
3.186 and 3.338 for the control and thyroid treated
groups, respectively. Therefore regular injections of
small amounts of T4 have had little apparent effect on
growth.
3.2. Free T4
The data on free T4 are presented in Fig. 1. The mean
concentration was 6.2 1.9 pmol L1 in week 7, increased and peaked to 19.2 4.3 pmol L1 in week 12,
and declined to 5.6 0.4 pmol L1 by week 20. This was
similar to adult levels (3.2 3.8 pmol L1 ). These concentrations showed significant differencesðF14;42 2:815;
p < 0:014Þ.
3.3. Oxygen consumption and T4 injection
Figs. 2 and 3 show the change in VO2 before and after
the injection of T4 from weeks 6 to 21. During development, oxygen consumption per unit mass prior to
injection of T4 followed a sigmoidal pattern. At week 6
VO2 was 0.46 0.28 ml O2 g1 h1 increasing to
1.99 0.21 at week 12 and dropping to near adult levels
(0.65 0.08) after pouch vacation at week 16. Prior to
and including week 11, oxygen consumption after injection changed little or even dropped. From week 12,
T4 injection raised oxygen consumption, while the level
of control VO2 decreased. Maximum levels of VO2 after
2.6. Thyroxine effects on development
Although injections of thyroxine were given at most
once a week, there was the possibility that this may have
effected changes in development and thereby produced
results that differed from normal development. To test
whether this occurred, the results for growth were
compared with data obtained from a group of growing
bettongs that had not been subjected to T4 injection
(Rose, 1989; Rose et al., 1998).
2.7. Statistical analyses
The statistical package (SPSS 10) was used for all
tests. Repeated measure ANOVAs were used with independent variable of age and treatment (control or
thyroxine injection). Dependant variables were oxygen
consumption or weight.
Fig. 1. Mean free T4 concentrations ( SEM) in the Tasmanian
bettong over weeks 7–20.
20
R.W. Rose, N. Kuswanti / General and Comparative Endocrinology 136 (2004) 17–22
4. Discussion
4.1. Thyroxine in maternal milk
Fig. 2. Oxygen consumption before (open circles) and after (closed
circles) thyroxine injection at 20 °C in Bettongia gaimardi.
Gemmell and Sernia (1992) demonstrated that maternal thyroxine could be transferred via milk to pouch
young marsupials. Subsequently they also showed
(Sernia et al., 1997) that T4 receptors are present in
pouch young before their own thyroid gland was functional. However, Gemmell and Buaboocha (1998) were
able to show little effect of this transferred hormone, as
inhibition of maternal thyroid had no discernible effect
on the growth of the young. Only very small amounts of
milk are drunk in early lactation (Smolenski and Rose,
1988) before the thyroid becomes functional and hence
maternal T4 probably plays little role (if any) in early
development of marsupials. When greater amounts of
milk are consumed later in lactation it seems likely that
the production of T4 by the youngÕs thyroid gland
would ÔswampÕ any maternally transferred hormone.
4.2. Thyroxine effects on development
Fig. 3. Percentage change in oxygen consumption after thyroxine injection in Bettongia gaimardi.
T4 injection occurred at weeks 14–15. Although adult
levels were lower if measured as a percentage increase,
the change in adult consumption is still about 50%.
A repeated measures ANOVA was used to analyse
the results. The control oxygen consumption of young
bettongs at various ages was significantly different
ðp ¼ 0:002Þ. Although the overall effect of T4 injection
on the animalsÕ oxygen consumption was not significant
ðp ¼ 0:447Þ, the interaction between age and treatment
was significant ðp ¼ 0:023Þ.
From week 12, the level of control oxygen consumption decreased significantly with age, while T4 injection increased it significantly ðp ¼ 0:008Þ. Due to the
large standard errors about the oxygen consumption
after T4 injections in weeks 14–16, it may be that the
apparent increase is solely due to the decrease in the
controls.
Setchell (1974) and Gemmell and Buaboocha (1998)
found that the thyroid of the young marsupial controlled weight increase. In our experiments the injection
of T4 into developing bettong pouch young might have
resulted in enhanced growth and development and thus
compromised the results obtained on metabolic rate/
oxygen consumption to some extent. However two sets
of results suggest this to not be the case. First, there was
no increase in weight in the T4-injected group compared
with the control group. Second, the increase in O2
consumption that occurred in the group injected with T4
occurred in the same week as that found by Rose et al.
(1998) in bettongs not being regularly injected with T4.
These suggest that there has been no increased development. Subsequently we can assume that the results
obtained are representative of bettongs developing
normally.
4.3. Free thyroxine variations
The concentration of free thyroxine increased from
minimal levels to a peak near week 12, they subsequently decreased to values similar to that of adults.
This pattern is similar to that found in the tammar
wallaby (Janssens et al., 1990), brushtail possum (Buaboocha and Gemmell, 1995), and bandicoot (Saunders
et al., 2000). The peak values of 19 pM compare to
44 pM for free T4 in the developing tammar (Janssens
et al., 1990). In the tammar wallaby pouch young, the
changes in free T4 followed a similar pattern to the
changes in total T4 but at much lower concentration
(Janssens et al., 1990). Total T4 values generally are
much higher in adult marsupials than free values, e.g.,
R.W. Rose, N. Kuswanti / General and Comparative Endocrinology 136 (2004) 17–22
58 ng (75 pM) ml1 in the tammar, 45 ng (58 pM) ml1 in
the brushtail possum (Buaboocha and Gemmell, 1995),
and 9.2 ng (11.9 pM) ml1 in the bandicoot (Saunders
et al., 2000). Adult values of free T4 in the bettong were
approximately 10–12 pM similar to that in the potoroo
(11.8 pM, Nicol, 1977) and tammar (8.1 pM, Janssens
et al., 1990) but higher than in the koala (3.3 pM, Lawson
et al., 1996). The values found in adult marsupials are
similar to those in eutherian mammals (Hulbert, 2000).
4.4. Thyroxine and metabolic rate
In the present work oxygen consumption in controls
increased to a peak in weeks 10–12 as found previously
for this species (Rose et al., 1998). Subsequently, oxygen
consumption decreased as did thyroxine concentrations.
Thyroxine has no obvious metabolic effect in the bettong before week 14. The effect of T4 injection on oxygen consumption first appeared in week 14 when it
caused an 100% increase; this coincides with the stage
when bettongs first venture out of the pouch (Rose,
1986) and could be exposed to cold ambient temperatures. Under normal conditions young marsupials
would never be exposed to cool temperatures in the
pouch. The ability to respond to T4 was maintained
subsequently during development and into adulthood.
The ability to respond to T4 was approximately two
weeks later than peak T4 values and the bettongÕs first
ability to respond to noradrenalin. Thyroid hormones
enhance the effect of catecholamines (Clement et al.,
2002) and it is possible that they have assisted in the
maturation of adrenergic receptors in the bettong as
found by Whitsett et al. (1980) and Feng et al. (2000) in
the rat and by Viguerie et al. (2002) in humans.
Rose et al. (1998) noted the changing relationship of
both thermal conductance and hair length with the development of endothermy in the bettong. Fig. 4 illustrates the replotting of that data, averaged and grouped
with age.
21
Table 1
Development of endothermy in the Tasmanian Bettong
Age (weeks)
0
6
8
10
12
14
15 (Final pouch
vacation)
Parameter
Birth (0.3 g)
Peripheral vasoconstriction and
behavioral regulation
Shivering first appears
Increased MR to cold and NE. Fur,
UCP 2 first appears
Homeothermic; peak MR and T4 levels;
peak response to cold and NE
Increased MR to T4
Peak in milk energy due to high lipid
levels. Body temperature increase in
mother due to imminent oestrus
MR, metabolic rate; NE, noradrenalin; T4, free thyroxine; UCP2,
uncoupling protein 2. Data from Rose (1987a,b), Smolenski and Rose
(1988), Rose (1997), Rose et al. (1998), and Kabat et al. (2003b) and
this paper.
It can be seen that the data group pre- and post-development of thyroid function with an intermediate
group of data points around the time the young is able
to enter and leave the pouch This is just after maximal
concentrations of plasma T4 and coincides also with the
period when a metabolic response to T4 is first demonstrated.
The data presented in the paper further attest to the
likely important role of the thyroid gland in the development of endothermy in marsupial pouch young and fills
in more of the Ôjig-sawÕ of development of the Tasmanian
bettong as illustrated in Table 1. Initially, the bettong is
only able to restrict peripheral blood flow as evidenced by
ÔblanchingÕ and reduce its surface area by curling-up until
week 8 when it is first able to shiver for short periods. By
week 10 the young is able to respond to cold and noradrenaline by increasing its oxygen consumption/heat
production. At week 12 it is furred, able to maintain its
body temperature; this coincides with peak levels of T4. It
leaves the pouch permanently at week 15 at which time it
is already able to respond to T4.
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