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First published online December 26, 2008
Journal of Experimental Biology 212, 297-304 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.021212
Bioenergetics and inter-individual variation in physiological capacities in a relict mammal – the Monito del Monte (Dromiciops gliroides)
Instituto de Ecología y Evolución, Universidad Austral de Chile, Casilla 567, Valdivia, Chile
* Author for correspondence (e-mail: robertonespolo{at}uach.cl)
Accepted 10 November 2008
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) of bioenergetics for Monito del
Monte (Dromiciops gliroides), the sole living representative of an
otherwise extinct marsupial order (Microbiotheria). We measured resting
metabolic rate as CO2 production
(
CO2) and
O2 consumption
(O2)
simultaneously, together with minimum thermal conductance (C), evaporative
water loss (EWL) and respiratory quotient (RQ), in a sample of ca. 20
individuals. Our results suggest that D. gliroides exhibits poor
control of body temperature (Tb), with a thermal amplitude
of ca. 10°C in normothermia. As a consequence, repeatability of
Tb and metabolic rate (either as
CO2 or
O2) were
relatively low (Tb=0.25±0.04,
VCO2=0.14±0.03,
O2=0.24±0.02,
jackknife estimations of standard errors). Thermal conductance exhibited
near-zero or negative repeatability and was lower than expected for
marsupials. However, we found significant repeatability for RQ and EWL
(=0.32±0.03 and 0.49±0.09, respectively). In general, these
results suggest that Monito del Monte exhibits some `reptilian' physiological
characteristics. The relatively low repeatability of physiological variables,
which otherwise exhibit large inter-individual and genetic variance in
eutherian mammals, suggests that these capacities do not exhibit evolutionary
potential in the ancient order Microbiotheria.
Key words: whole-animal metabolism, respiratory quotient, Dromiciops, Australasian fauna, repeatability, evolution of endothermy
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) called
for more studies dealing with inter-individual variability. Since then, many
researchers have focused on characterizing the variation of physiological
capacities in natural populations (Berteaux
et al., 1996; Chappell,
1993; Chappell et al.,
1995; Friedman et al.,
1992; Garland and Bennett,
1990; Garland et al.,
1990; Garland and Else,
1987; Hayes et al.,
1998; Hayes and Chappell,
1990; Hayes et al.,
1992; Hayes and Jenkins,
1997; Huey and Dunham,
1987; Speakman et al.,
1994). In the case of mammalian physiology, it would be fair to
say that this new focus of research has culminated in a good understanding of
the genetic and environmental sources of variation of energy metabolism (see
below).
The literature suggests that energy metabolism is a repeatable trait, and
most of its consistency is due to additive genetic effects that vary depending
on the kind of variable being studied [e.g. locomotory, thermoregulatory,
maximum, basal (Dohm et al.,
2001; Hayes et al.,
1992; Konarzewski and Diamond,
1994; Ksiazek et al.,
2004; Labocha et al.,
2004; Nespolo et al.,
2003; Nespolo et al.,
2005; Nespolo and Franco,
2007; Sadowska et al.,
2005)]. These findings, however, were restricted to eutherian
mammals. As far as we are aware, there is not a single study of repeatability
in any aspect of physiology in other groups of mammals (i.e. monotremes and
marsupials) (Luo, 2007;
Warren et al., 2008). In
addition, inter-individual variation in several whole-animal physiological
capacities besides energy metabolism, such as respiratory quotient, minimum
thermal conductance and evaporative water loss, remain almost unexplored in
these groups.
One important individual capacity is the respiratory exchange ratio, or
respiratory quotient (RQ, the instantaneous ratio between CO2
production and O2 consumption). In animals, an RQ of near 1.0
indicates that most of the energy metabolism is utilizing carbohydrate
catabolism, and a RQ near 0.7 indicates that energy metabolism is occurring by
fat catabolism (Andrews, 2004;
Schmidt-Nielsen, 1995). Thus,
RQ might be an instantaneous indicator of the type of nutrients that are being
metabolized in a living animal. Not surprisingly, the use of RQ has proven to
be a valuable technique in, for instance, studies of human obesity
(Valtueña et al., 1997;
Wielinga et al., 2007), as an
indicator of metabolic switches in hibernating animals
(Buck and Barnes, 2000) and
hypoxia adaptation in invertebrates
(Nielsen and Christian, 2007).
However, whether RQ is a consistent property of individuals or depends totally
on a response to an environmental factor (i.e. fasting, nutrient type) is open
to question.
Another important variable derived from respirometry measures is `wet'
thermal conductance (sensu McNab,
1980) – the rate of heat loss from the body (the inverse of
insulation). Thermal conductance (C) is of key importance for survival in
small endotherms, especially those living in cold and/or seasonal
environments, as changes in the properties of fur or feathers can
significantly reduce heat loss (Bozinovic
and Merritt, 1992; Klaasen et
al., 2002; Luna-Jorquera et
al., 1997; McNab,
1980; Novoa et al.,
1994; Scholander,
1955). However, there have been few attempts to determine the
source of phenotypic variation for this trait in mammals, which has exhibited
significant heritability (Nespolo et al.,
2003).
Evaporative water loss (EWL) – the rate of water loss from the body
due to evaporation – is an important variable related to the resistance
to dehydration in vertebrates, which in small endotherms could be of crucial
relevance to survival (Anderson et al.,
1997; Hayes et al.,
1998; Maloney and Dawson,
1998; Munn and Dawson,
2001; Wang and Wang,
2000; Williams and Tieleman,
2000). The repeatability of this trait was studied by Hayes and
colleagues (Hayes et al.,
1998; see also Hayes and
Jenkins, 1997), who found up to 65% repeatable variation.
A response to natural selection needs genetic variation (or, in general
terms, high heritability) in a given trait within a population
(Roff, 2007). In the absence
of genetic-by-environmental interaction, and other confounding factors such as
non-additive genetic variation, when a trait exhibits high genetic variation,
it also exhibits high repeatability
(Falconer and Mackay, 1997;
Nespolo and Franco, 2007). In
such situations, the following assumptions can be made: (1)
mutation–selection balance maintains genetic variation in populations
[i.e. the increase in variation due to mutation/recombination is compensated
by its reduction due to directional/stabilizing selection (see
Roff, 2002;
Turelli, 1988)]; and (2) the
actual physiological features of a group have not changed much compared with
its ancestors [a basic assumption in studies of the evolution of endothermy
and the aerobic capacity model (see Bennett
et al., 2000; Crompton et al.,
1978; Dawson et al.,
1979; Hayes and Garland,
1995; Koteja,
2000; Sadowska et al.,
2005)]. With these assumptions, the existence of low repeatability
in an actual species of an ancient lineage would suggest that its ancestors
did exhibit low genetic variation (and hence the trait did not exhibit
potential to respond to selection). Obviously, low genetic variation could
also arise because of fixation of all genes related to the trait after strong
and persistent directional selection (i.e. disrupting the
mutation–selection balance). But in this case, further descendants of
this group (e.g. rodents, in the case of mammals) would also exhibit low
genetic and inter-individual variation, which is not supported by empirical
evidence in energy metabolism and related traits
(Bacigalupe et al., 2004;
Berteaux et al., 1996;
Dohm et al., 2001;
Hayes et al., 1998;
Hayes and Jenkins, 1997;
Hayes and O'Connor, 1999;
Konarzewski and Diamond, 1995;
Konarzewski et al., 2005;
Ksiazek et al., 2004;
Labocha et al., 2004;
Nespolo et al., 2003;
Nespolo et al., 2005;
Nespolo and Franco, 2007;
Sadowska et al., 2005). In
other words, what we are proposing is that repeatability studies performed on
living representatives of ancient groups could provide an insight into
questions regarding whether the trait had the potential to evolve in these
ancient lineages.
The study of mammalian evolution experienced a breakthrough after the
identification of the South American marsupial Monito del Monte
(Dromiciops gliroides) as the sole living representative of the
mammalian order (Microbiotheria), of Australasian origin, previously thought
to be extinct (Asher et al.,
2004; Palma and Spotorno,
1999; Spotorno et al.,
1997). A handful of studies have been conducted on this `living
fossil' (Amico and Aizen, 2000;
Asher et al., 2004;
Bozinovic et al., 2004;
Brugni and Flores, 2007;
Guglielmone et al., 2004;
Kirsch et al., 1991;
Lobos et al., 2005;
Marin-Vial et al., 2007;
Navone and Suriano, 1992;
Palma and Spotorno, 1999;
Pridmore, 1994;
Saavedra and Simonetti, 2001;
Silva, 2005;
Westerman and Edwards, 1991),
which, in addition to its phylogenetic relationships, describe a few basic
aspects of its biology. In fact, the sole study that addressed a physiological
feature of D. gliroides described it as a hibernator and reported
that its basal metabolic rate was below the expected value for marsupials
(Bozinovic et al., 2004).
In this study, our aims were: (1) to perform a wide screening of the bioenergetic traits of D. gliroides; (2) to determine the inter-individual variation in physiological capacities of D. gliroides; and (3) to use this information to provide insight into the ancestral physiological features of mammals.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Respirometry measurements
All measurements were performed with a respirometry system consisting of a
Li-Cor 6262 H2O/CO2 analyzer (LiCor, USA) and an Oxzilla
II (Sable Systems International, USA) dual oxygen analyzer, in a series
configuration. The H2O/CO2 analyzer was calibrated
periodically against a known gas sample of 291 p.p.m. for CO2 and
against air saturated with water vapor at 20°C for H2O. We used
cylindrical metabolic chambers of 200 ml, and a flow rate of 1000±1 ml
min–1 controlled by a Sierra mass-flow controller (Sierra
Instruments, USA), located upstream of the metabolic chamber and after two
columns with H2O and CO2 scrubbers (Drierite and
Baralyme, respectively). The metabolic chamber was located in an incubator,
and ambient temperature (Ta) was set to 20°C and
continuously recorded by a Cole Parmer (USA) thermocouple located inside the
incubator. Where small variations in Ta due to the
incubator inertia could inflate the residual error of further repeatability
analyses, then we included Ta as a covariable in all the
analyses, but it was never significant, and the results were unchanged when
not including it. As we used a test temperature (i.e. 20°C) below
thermoneutrality, technically what we obtained was resting metabolic rate
(RMR). This Ta was chosen in order to minimize the amount
of heat lost by evaporation (McNab,
1980), without increasing metabolism because of cold. Dry and
CO2-free air passed through the mass flowmeter, then to the
metabolic chamber and then through a Gast (Gast Manufacturing, USA) pump (i.e.
negative pressure). After that, the air was injected into the LiCor 6262 by a
subsampler (Intelligent Subsampler, Sable Systems, USA), at a flow rate of 200
ml min–1. Then, the air was passed again through the
scrubbers and finally it was injected into the Oxzilla II. With this system,
we recorded simultaneously: (1) carbon dioxide production
(CO2); (2)
oxygen consumption
(O2) and (3)
evaporative water loss (EWL).
Each record was corrected (1) for drift deviations, especially for the
O2 signal (the LiCor 6262 did not experience drift), (2) for
negative values in the O2 record (reciprocal transformation) and
(3) to align both
CO2 and
O2 record for a
ca. 10 s lag between them. Finally, to calculate
CO2 and
O2, we computed
(1) the average of the entire record; (2) the average of the minimum
steady-state 10 min of recording and (3) the average of the last 10 min of
recording. The basic statistics (coefficient of variation, normality and
correlation with body mass) indicated that the average of the last 10 min was
the parameter that gave by far the best statistical properties, probably
because animals were calmer having acclimatized to the conditions. We then
used this procedure for the general analyses. For EWL, we computed the overall
mean across the complete record.
|
):
CO2), as:
 | (1) |
CO2 is in
ml CO2 min–1; FiCO2 is the input
fractional concentration of CO2; FeCO2 is the excurrent
fractional concentration of CO2; FR is the flow rate (ml
min–1); FiO2 is the input fractional concentration
of O2; and FeO2 is the excurrent fractional
concentration of O2.
 | (2) |
 | (3) |
O2) as:
 | (4) |
O2 is in
ml O2 min–1. ):
 | (5) |
Physiological variables were measured three times in most individuals, with a three-week interval between measurements (i.e. a total period of nine weeks).
Statistics
All data were analyzed with Statistica 6.1 (StatSoft,
www.statsoft.com).
Repeatabilities were computed as the intraclass-correlation coefficient
(), which is the ratio between inter-individual variance and total
variance (inter-individual plus residual variance). Both variances were
computed from one-way ANOVAs and expected mean squares in a variance component
analysis, using body mass (Mb) as covariable when the
dependent variable was correlated with Mb. Standard errors
of were computed by jackknife, by deleting an individual each time and
computing the (N–1) (i.e. pseudovalue) and then by calculating the
standard deviation of this sample of pseudovalues
(Quinn and Keough, 2002;
Roff, 2006).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2 and
CO2 to 5% of the
common resting values. Furthermore, torpid D. gliroides exhibit
unambiguous behavioral characteristics in addition to low metabolism and
Tb (R.F.N., C. Verdugo and P.C., unpublished) (see also
Bozinovic et al., 2004).
Torpid individuals are characterized by their low respiratory frequency and
the position of ears and nose, which can be easily seen by eye during
metabolic trials.
|
The large variation in Tb was also reflected in the
physiological measures (Table
1, Fig. 1). There
was a significant increase in body mass (Mb) between
trials (F2,14=33.8; P<0.001; repeated-measures
ANOVA; Table 1), and a
reduction in Tb (F2,14=7.8;
P=0.005; repeated-measures ANOVA;
Table 1). This decrease in
Tb was observed as a negative correlation between
Mb and Tb (R=–0.59;
F1,18=9.51; P=0.006, data from the first
repetition), which suggests that larger individuals exhibited lower
Tb values. Thermal conductance increased across
repetitions as computed from
CO2
(F2,14=7.02; P=0.008; repeated-measures ANOVA;
Table 1) and from
O2
(F2,14=21.5; P<0.001; repeated-measures ANOVA;
Table 1). Although
O2 showed a
significant increase across repetitions (F2,14=5.7;
P=0.02; repeated-measures ANOVA;
Table 1),
CO2 did not
change significantly (F2,14=0.54; P=0.60;
repeated-measures ANOVA; Table
1).
The magnitude of the respiratory quotient (RQ) was reduced across
repetitions, but this trend was nonsignificant
(F2,14=1.41; P=0.28; repeated-measures ANOVA;
Table 1). Within records (in
each repetition), comparing the first, second and third hour of measurements,
there was a consistent increase in RQ (Fig.
2). Respiratory water loss (RWL) did not change across repetitions
(F2,12=3.16; P=0.08; repeated-measures ANOVA;
Table 1). Repeatability was
near zero and nonsignificant for thermal conductance, measured both from
CO2 and
O2, which
suggests that this variable does not exhibit inter-individual variation
(Table 2). However, with the
exception of EWL, we found moderate repeatability in the remainder of the
traits (Mb, Tb,
CO2,
O2 and RQ)
(Table 2).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Since
its proposition, the powerful tools of multivariate quantitative genetics have
been successfully applied to predict adaptive evolution in an enormous variety
of organisms and traits (Roff,
2007). This, together with advances in phenotypic selection
studies (Brodie et al., 1995;
Hoekstra et al., 2001;
Kingsolver et al., 2001), has
produced a considerable improvement in the knowledge of the processes and
mechanisms of adaptive evolution in the field. Most of these studies, however,
have been restricted to short-lived animals and plants and conducted on
morphological traits. The study of the sources of phenotypic variation in
mammalian bioenergetics has received some attention (see Introduction), but
mostly in rodents and other eutherians. It is surprising that marsupials and
monotremes, which have been studied in considerable detail by physiological
ecologists, are not known from this perspective. The first step in
characterizing inter-individual variation in a trait or a group of traits is
to determine its repeatability, which for energy metabolism appears to be high
(ca. 60%), irrespective of species
(Nespolo and Franco, 2007).
Repeatability, computed as the intraclass correlation coefficient, represents
the upper limit of heritability and hence could provide insight into whether a
trait would present heritable variation without the need to perform
pedigree-based analyses (Falconer and
Mackay, 1997; Lessells and
Boag, 1987). In this study, we performed a wide screening of the
repeatability of bioenergetics in a little-studied marsupial, D.
gliroides, and we found rather unexpected results, namely poor
thermoregulatory abilities and low inter-individual variation in most
bioenergetic traits. We will discuss each case separately.
Body temperature
In eutherians, body temperature (Tb) is one of the most
precisely controlled physiological variables, which usually has a circadian
amplitude of less than 2°C and is maintained over a wide range of ambient
temperatures (Arend and McNab,
2001; Haim, 1996;
Refinetti, 1999). Also (and
probably as a consequence), Tb appears in eutherians as a
repeatable trait that exhibits high heritability
(Gordon and Rezvani, 2001;
Nespolo et al., 2003;
Rhodes et al., 2000). By
contrast, non-hibernating marsupials and monotremes exhibit, in general,
larger short-term variations in Tb, whose daily range is
up to 6°C (Gemmell et al.,
1997). In fact, in several marsupial species,
Tb is correlated with metabolic rate
(Kinnear and Shield, 1975;
Opazo et al., 1999),
reflecting their somewhat imperfect control of Tb. Our
results suggest that awake (i.e. non-torpid) D. gliroides exhibits an
unusually large thermal variation in Tb (up to 10°C).
These results are supported by Tb measurements using
implanted data loggers (R.F.N., C. Verdugo and P.C., unpublished) and by the
negative correlation between body mass and Tb. This poor
control of Tb indicates high residual variation in this
trait, which is translated into low time-consistency, as its repeatability of
25% suggests.
Thermal conductance
According to McNab (McNab,
1980), minimum thermal conductance, as measured in this study and
below thermoneutrality, reflects the ease with which heat is exchanged between
the body and the environment. Thus, it is a measure of the ability of the
animal to maintain heat. The magnitudes of minimum thermal conductance
computed from oxygen consumption
(O2) and
CO2 production
(CO2) (i.e.
CO2 and
CCO2,
respectively) that we found are in agreement with what Bozinovic and
colleagues (Bozinovic et al.,
2004) found for this species and are lower than those expected for
marsupials. Both in small mammals (eutherians and marsupials) and birds
(Novoa et al., 1994), thermal
conductance can exhibit changes on a seasonal basis and also after thermal
acclimation (Bozinovic et al.,
1990; Dawson and Olson,
1988; Holloway and Geiser,
2001; Smith and Dawson,
1984). This phenotypic plasticity suggests an adaptive value for
thermal conductance. However, this contrasts with the almost absolute absence
of inter-individual variation in this trait in D. gliroides as only
negative repeatability estimations were found (i.e. the actual value of
repeatability was near zero). In other words, thermal conductance in D.
gliroides would not respond to selection.
Respiratory quotient
During a single trial, animals exhibited a consistent increase in
respiratory quotient, which could be interpreted as a shift from fat-based
metabolism to carbohydrate-based metabolism
(Buck and Barnes, 2000). This
finding appears contradictory to the 6 h fasting state that animals
experienced as they should gradually use fat reserves after a period of
fasting. However, it should be noted that, in carnivorous mammals, 6 h of
fasting could be enough for gut emptiness to occur but not for the complete
metabolizing of nutrients in circulating blood
(Hume et al., 1993). These
nutrients were the main fuel for individuals during the first hour of
metabolic recording, which explains the low RQ at the beginning of the trials.
Then, metabolism shifted into carbohydrate-based metabolism as the first line
of energy reserves are liver and muscle glycogen
(Willmer et al., 2005).
Similarly, Walsberg and Wolf (Walsberg and
Wolf, 1995) found in Verdins (insectivorous birds) fed with
mealworms (as our Dromiciops) that RQ increased during the first six
hours of fasting, from 0.71 to near 0.80, and showed that House Sparrows (a
granivorous bird) fed with grains actually reduced their RQ during the same
period, an exactly inverse result (from 0.81 to 0.70). In other words,
insectivorous animals appear to exhibit similar trends in the use of energy
reserves, irrespective of species.
Our repeatability estimation of RQ was a value of 30% and was significant.
This suggests that, to some extent, the capacity to metabolize different
nutrient types is not completely determined by the type of diet and the
physiological status of the animal. That is to say, some individuals would be
better suited to carbohydrate-based metabolism and others to fat-based
metabolism. Whether this inter-individual variation could be of adaptive
significance will depend on the pressures imposed by their environment. The
environment of D. gliroides is characterized by seasonal and
unpredictable food availability. In fact, in summer and autumn, this species
is frugivorous, shifting to insectivory during autumn and winter
(Amico and Aizen, 2000). In
this sense, inter-individual variation in RQ could benefit D.
gliroides as it would permit it to respond to changes in food
availability, both in type and magnitude.
Evaporative water loss
Our results suggest that evaporative water loss (EWL) exhibits high and
significant repeatability in D. gliroides. This is in accordance with
a previous determination of EWL repeatability in a rodent
(Hayes et al., 1998),
suggesting that inter-individual variation in this traits exists. The adaptive
value of EWL as a trait has been suggested several times as it exhibits
physiological flexibility after laboratory acclimation
(Williams and Tieleman, 2000)
and is reduced in marsupial species of desert environments
(Dawson et al., 2000;
Gibson and Hume, 2000). In
fact, Diaz and colleagues (Diaz et al.,
2001) reported a high capacity for urine concentration in a
didelphid, comparable to values in desert rodents. Thus, it is plausible that
the interspecific variation in EWL that we found could present evolutionary
potential.
Energy metabolism
According to Bozinovic and colleagues
(Bozinovic et al., 2004),
D. gliroides exhibits lower values of energy metabolism than what is
expected for a marsupial of its size. Our
O2 and
CO2 (corrected
by RQ) measurements at 20°C are in accordance with those reported by these
authors. However, metabolic rate appears to present low repeatability, which
could be explained by the poor thermoregulatory control that this species
exhibits. The repeatability of energy metabolism in D. gliroides is
not in accordance with what is known for mammals (see
Nespolo and Franco, 2007 and
references therein), although we do not know of another repeatability study
performed on marsupials. Furthermore, although marsupials in general are
considered to exhibit `mammalian' physiological features
(Crompton et al., 1978;
Hinds and MacMillen, 1984),
our results unambiguously suggest that D. gliroides (and hence
Microbiotheria) furnishes an exception. In terms of thermoregulatory
abilities, and with the exception of evaporative water loss, D.
gliroides exhibits `reptilian' features (e.g. large amplitude in
Tb, correlation between Tb and
Mb, low time-consistency of energy metabolism, low thermal
conductance).
Did microbiotherians have a reptile-like physiology?
The order Microbiotheria, with its seven described species, belongs to the
Australidelphia magnorder, of Australasian origin
(McKenna and Bell, 1997). The
oldest fossil is dated ca. 40 million years of age, when Australia,
South America and the Antarctic continent were merged into Gondwana. The
extinction of Microbiotheria coincided with the invasion of the North American
eutherian fauna, after the formation of the Panama isthmus (ca. 3.5
million years ago), with D. gliroides being the sole surviving
species (McKenna and Bell,
1997). According to Ruben
(Ruben, 1995) (see also
Warren et al., 2008), extant
mammals (monotrematas, marsupials and eutherians) probably shared a common
ancestor approximately 160 million years ago, and mammals probably evolved
from mammal-like reptiles (therapsids) 200 million years ago. Thus, the
evolution of endothermy could be a process that occurred during the past 100
million years, which includes the rise and supposed extinction of
Microbiotheria.
Several competing hypotheses have been proposed to explain the evolution of
endothermy in birds and mammals (see Hayes
and Garland, 1995). All of them propose that, at some point,
natural selection acted either directly or indirectly on body temperature,
energy metabolism and/or thermal conductance. Any response to selection would
have needed genetic variation in these traits. As repeatability represents the
upper limit of heritability, low repeatabilities would be indicative of low
genetic variation, and hence a low potential to respond to selection in a
given trait. Thus, our results suggesting low repeatability in bioenergetic
traits in the `relict mammal' D. gliroides support the idea of a low
potential to respond to selection on these traits in Microbiotheria. The low
thermoregulatory abilities of this species, together with the recent evidence
of the high repeatability and genetic variation in energy metabolism of
eutherian mammals (see Introduction), suggests that the adaptive shifts
towards controlled endothermy should have happened recently. This is of course
an ambitious conclusion that needs confirmation by further research on other
basal species such as insectivores and monotrematas. However, this would not
be the first time that an author has inferred past evolutionary processes from
experimental data obtained from an extant species (e.g.
Bennett et al., 2000;
Crompton et al., 1978;
Dohm et al., 2001;
Sadowska et al., 2005).
|
Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Amico, G. and Aizen, M. (2000). Mistletoe seed dispersal by a marsupial. Nature 408,929 -930.[Medline]
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Andrews, M. T. (2004). Genes controlling the metabolic switch in hibernating mammals. Biochem. Soc. Trans. 32,1021 -1024.[CrossRef][Medline]
Arend, A. and McNab, B. K. (2001). The comparative energetics of caviomorph rodents. Comp. Biochem. Physiol. 130A,105 -122.[CrossRef][Medline]
Asher, R. J., Horovitz, I. and Sánchez-Villagra, M. R. (2004). First combined cladistic analysis of marsupial mammal interrelationships. Mol. Phylogen. Evol. 33,240 -250.[CrossRef][Medline]
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