The evolution of recovery from desiccation stress in laboratory-selected populations of Drosophila melanogaster
Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA 92697-2525, USA
* Author for correspondence (e-mail: dfolk{at}adelphia.net)
Accepted 26 April 2004
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: Drosophila melanogaster, desiccation resistance, evolution, water restoration, sodium content, dry mass
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
As a consequence of small body size and high mass specific metabolic rate,
insects face unique challenges to water conservation, particularly during
flight (for reviews, see Edney,
1977; Hadley,
1994
). Yet insects are among the most speciose and widely
distributed terrestrial animals (Gillott,
1995
). The ability of insects to live successfully on land can be
attributed to various behavioral, structural and physiological features (e.g.
Wigglesworth, 1972
;
Edney, 1977
;
Hadley, 1994
;
Chapman, 1998
). We have
investigated the evolution of physiological traits related to water
conservation in very small insects, specifically fruit flies, by placing
populations of Drosophila melanogaster under laboratory selection for
enhanced desiccation resistance (D populations). Control (C) populations that
have not been selected for improved desiccation resistance are maintained
concurrently with the D populations. The evolved responses of the D
populations to selection have led to an increased ability to survive when
desiccated (Rose et al., 1992
;
Graves et al., 1992
;
Gibbs et al., 1997
;
Chippindale et al., 1998
;
Djawdan et al., 1998
;
Williams et al., 1998
;
Folk et al., 2001
;
Folk and Bradley, 2003
).
Phenotypic traits associated with desiccation resistance in the D populations
include a large hemolymph pool (>300 nl,
sixfold increase in hemolymph
volume relative to the C populations), which buffers the tissues against water
loss for an extended period during desiccation
(Folk et al., 2001
;
Folk and Bradley, 2003
); an
elevated carbohydrate content, comprising
30% of total dry mass
(Graves et al., 1992
;
Djawdan et al., 1998
;
Folk et al., 2001
); and a
reduced rate of water loss during periods of extreme water stress
(Gibbs et al., 1997
;
Williams and Bradley, 1998
;
Folk and Bradley, 2003
). In
contrast, the C populations have a small hemolymph pool (
50 nl), which
appears to afford the tissues only minimal protection from water loss during
desiccation; a lower carbohydrate content, comprising
15% of total dry
mass; and a relatively high water loss rate.
Drosophilids lose significant quantities of water and dry mass during
desiccation (Arlian and Eckstrand,
1975; Graves et al.,
1992
; Hoffmann and Parsons, 1993;
Gibbs et al., 1997
;
Lehmann et al., 2000
;
Marron et al., 2003
). In
addition, inorganic ions, such as Na+, Cl and
K+, are permanently excreted during desiccation as a consequence of
osmoregulatory strategies (Folk and
Bradley, 2003
). In previous studies, we examined the loss of water
and Na+ from the hemolymph and the tissues in the C and D flies
during desiccation. In 24 h, the D flies lost
60% and
70% of
hemolymph volume and Na+ content, respectively, while tissue water
and Na+ content were not significantly reduced. Comparable losses
from the hemolymph of the C flies during desiccation occurred within only 8 h:
60% of volume and
80% of Na+ content were lost.
Furthermore, the C flies lost significant water and sodium content from the
tissues within 8 h.
Following desiccation, many adult insects are capable of restoring water
content by drinking (Djajakusumah and
Miles, 1966; Wall,
1970
; Broza et al.,
1976
; Loveridge,
1975
; Hamilton and Seely, 1976;
Tucker, 1977
;
Nicolson, 1980
;
Naidu and Hattingh, 1988
;
Naidu,
2001a
,b
).
Some insects will drink saline and/or sugar (e.g. sucrose) solutions to
restore water and, presumably, ionic and energy content as well
(Evans, 1961
;
Dethier and Evans, 1961
;
Browne et al., 1976
). Although
the ability to restore water content by drinking has been ascertained in
various insects, relatively little is known about the ability to restore
depleted somatic components, such as inorganic ions and metabolic fuel
stores.
We present here the first study of the capacity of populations of Drosophila melanogaster selected for enhanced desiccation resistance to recover whole-body water, dry mass and sodium content following a sublethal bout of desiccation. We ascertain and compare the capacities of the D and C flies to restore these somatic components when allowed to recover on one of three fluids: water, saline solution or saline+sucrose solution. We propose that the future physiological health, and thus future stress resistance, of desiccated flies may be contingent upon their ability to restore somatic resources that are expended during periods of desiccation stress.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Details of the fly maintenance protocol and selection regime are provided
in Folk et al. (2001).
Briefly, multiple batches of eggs (6080 eggs per batch) were collected
from all C and D populations for the propagation of the subsequent generation.
Following egg collection, the flies were allowed to develop and mature for 14
days (i.e. approximately 4 days into adulthood), at which time the D
populations were subjected to selection for enhanced desiccation resistance
until 80% mortality was reached. During selection, the D populations were
deprived of food and water, while the C populations were deprived only of
food. When selection was terminated, all surviving flies were allowed to
recover on moist food supplemented with yeast paste for 3 days. Eggs were then
collected for rearing of the next generation. Selection for enhanced
desiccation has been imposed every generation for more than 250
generations.
Prior to all experiments, subsets of flies from the five D populations were maintained for two generations without undergoing selection. Subsets of flies from the five C populations were supplied a normal diet throughout development and maturation during the same two-generation period. By withholding the flies from the pressures of selection prior to experiments, we eliminated grandparental and parental phenotypic effects that derived from the selection regime. To eliminate the effects of gender, only females were used in the experimental assays. All experiments were performed on mated females that were approximately 4 days old.
Desiccation protocol
Experimental flies from the C and D populations were subjected to an
initial, sublethal bout of desiccation. Flies were briefly anesthetized with
CO2 and then placed into 30 ml glass vials. A foam stopper was
placed 3 cm down into the vial and
4.5 g of DrieriteTM, a
calcium sulfate desiccant (W. A. Hammond Drierite Company, Ltd., Xenia, OH,
USA), was placed on top of the foam stopper. The open end of the vial was then
sealed with ParafilmTM (Pechiney Plastic Packaging, Chicago, IL, USA).
During the initial bout of desiccation, 200 flies (40 vials, 5 flies per vial)
from each C and D population were desiccated for 8 h (C flies) or 24 h (D
flies). Previous studies have shown that water content, dry mass and sodium
levels are significantly reduced during 8 h and 24 h ofdesiccation in the C
and D flies, respectively (Folk et al., 2003).
Following this initial bout of desiccation, flies from each population were divided into three groups, each comprising 65 flies (13 vials, 5 flies per vial). Each group was allowed access for 24 h to only one of three fluids: doubly distilled water, saline solution, or sucrose+saline solution (see below for details of the fluid treatments). Immediately following recovery on the fluids, the flies were desiccated again as described above. During this second desiccation period, flies were desiccated to death. The capacity to resist desiccation was estimated as the time (h) that the flies were able to survive. In summary, the differences between the two desiccation periods were: (1) during the initial bout of desiccation, the C and D flies were desiccated for 8 h and 24 h, respectively; and (2) during the latter bout of desiccation, the flies were desiccated until death in order to estimate recovery of desiccation resistance.
Fluid treatments
Immediately following the initial bout of desiccation, C and D flies were
provided one of three fluids: doubly distilled water (ddH2O),
isotonic saline solution (20 mmol l1 KCl + 135 mmol
l1 NaCl), or saline+sucrose solution [the isotonic saline
solution + 5% (146 mmol l1) sucrose]. (Refer to the previous
paragraph for details on the experimental design.) During the fluid treatment
period, flies were held in 30 ml glass vials for 24 h. Prior to placing the
flies into the vials, a single KimwipeTM (laboratory-grade tissue paper,
Kimberly-Clark Corporation, Denver, CO, USA) was evenly packed into the bottom
of each vial, and either 1.5 ml of ddH2O, saline solution, or
saline+sucrose solution was added. The Kimwipe absorbed the fluid and provided
a moist substrate from which it could be extracted and consumed by the flies
without danger of drowning.
Gravimetric estimation of wet mass, water content and dry mass
Mature females from each C and D population were anesthetized with
CO2 and immediately weighed using a Cahn 29 automatic
electrobalance (Cerritos, CA, USA). The flies were then dried overnight at
6065°C and reweighed to obtain dry mass. Water content of whole
flies was estimated by subtracting the dry mass from the wet mass. Wet mass,
dry mass and water content of 10 flies from each C and D population were
measured prior to and after the initial desiccation bout, and following the
fluid treatments.
Sodium measurements
Ten samples were prepared from each C and D population prior to desiccation
and following each of the fluid treatments. Each sample comprised two flies
that had been liquefied overnight in 100 µl of concentrated HNO3
(containing 0.02 p.p.m. sodium) at room temperature (2123°C).
Following solubilization of the flies, 2.9 ml of doubly distilled water was
added to each sample. The Na+ concentration of each sample was
determined using atomic absorption spectrophotometry (AA-125 series, Varian
Analytical Instruments, Springvale, Australia). The mean whole-body
Na+ content (nmol fly1) was then calculated from
the Na+ concentration of each sample.
Statistical analyses
We investigate the ability of desiccated C and D flies to restore water,
dry mass and Na+ content to their respective pre-desiccation values
when offered one of three different fluids during a period of recovery. We
also examine the desiccation resistance of C and D flies following recovery on
the different fluids. Previous work has shown that non-desiccated, hydrated D
flies have a greater water and Na+ content than the C flies
(Gibbs et al., 1997;
Folk and Bradley, 2003
). In
addition, during desiccation the rates of water loss and Na+
excretion have diverged significantly between the C and D flies. Within only 8
h of desiccation, the C flies experience significant losses of both water and
Na+ from the hemolymph and the tissues
(Folk and Bradley, 2003
). The
D flies must be desiccated for a longer period of time for comparable losses
to occur. For these reasons, we do not compare the recovery of water,
Na+, dry mass and desiccation resistance between the C and D groups
in the ANOVA (recovery of water was analyzed using t-test, see
below); but rather, we examine recovery of these components within the C or D
group. Data were analyzed using Model I ANOVA, in which the C or D populations
and the fluid treatments were treated as fixed effects. Bonferroni post
hoc pairwise comparisons of means within the C or D group were used to
determine if: (1) water, Na+ and dry mass were significantly
reduced following the initial bout of desiccation; (2) the somatic components
were restored, depending upon the type of fluid provided during recovery; and
(3) if desiccation resistant following recovery was affected by the fluid
provided during recovery. Student's t-test was used to compare
restoration of whole-body water in the C and D flies that were provided
saline+sucrose. We tested for differences in (1) rate of volume restoration,
(2) total volume restored, and (3) proportion of total lost volume that was
restored. An arcsine transformation was applied to the proportions prior to
statistical analysis.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
During 24 h of desiccation, the desiccation-resistant flies lost 0.523
µl of whole-body water content, which is a 33% reduction
(P<0.0001, Fig.
1B). Those D flies that had access to water or saline solution
during recovery did not increase body water content above the post-desiccation
level. A net gain of water was observed only in that group that recovered on
saline+sucrose solution. This group did not fully restore body water to the
level of the non-desiccated, hydrated flies: 55% of the total water lost
during desiccation (i.e. 0.287 µl) was recovered. The D flies that
recovered on saline+sucrose restored water at a significantly higher rate
(0.012 µl h1) during recovery than the C flies (0.003
µl h1, P=0.04). The proportion of the total lost
volume that was restored did not appear to differ between the two groups
(P=0.21).
Restoration of dry mass
The C flies experienced a reduction (7.5%) in dry mass during 8 h of
desiccation (P<0.0001, Fig.
2A). The mean rate of dry mass loss was 5 µg
h1. Dry mass continued to be lost at a mean rate of
3
µg h1 during recovery, when flies were provided either
water or the saline solution. When flies were offered the saline+sucrose
solution, dry mass was maintained at the post-desiccation level.
|
The D flies lost 15% of their dry mass at a mean rate of 4 µg
h1 during 24 h of desiccation (P<0.0001,
Fig. 2B). Dry mass continued to
be lost at the same rate (
4 µg h1) during recovery
when flies were provided either water or saline solution. In contrast to the C
flies, dry mass in the D flies was fully restored to levels observed in
non-desiccated, hydrated flies when the saline+sucrose solution was supplied
during recovery.
Restoration of whole-body sodium
The mean whole-body Na+ content in the non-desiccated, hydrated
C flies was 43 nmol fly1
(Fig. 3A). A previous study
indicated that whole-body Na+ in the C flies is reduced by 15%
during 8 h of desiccation (Folk and
Bradley, 2003
); therefore, we estimated that the Na+
content dropped to
36 nmol fly1 during the 8 h
desiccation period in this study. The Na+ content following
recovery on water was 37 nmol fly1, which was significantly
lower than that in non-desiccated, hydrated flies (P<0.0001,
Fig. 3A). These data suggest
that the Na+ content in the C flies was maintained at
post-desiccation levels when only water was provided. The Na+ level
was fully restored to that observed in non-desiccated, hydrated flies when
saline was offered, but it surpassed that of the non-desiccated, hydrated
flies by 44% when saline+sucrose was provided (P<0.0001).
|
The mean whole-body Na+ content in non-desiccated, hydrated D
flies was 85 nmol fly1
(Fig. 3B), approximately
twofold higher than that of the C flies. The D flies lose
30% of
Na+ content during 24 h of desiccation
(Folk and Bradley, 2003
);
thus, we estimated that the Na+ content fell to
60 nmol
fly1. The Na+ content of the D flies following
recovery on water or saline (i.e.
50 and
60 nmol
fly1, respectively), was significantly lower than that of
the non-desiccated, hydrated flies (P<0.0001) and was at
approximately the same level observed in the desiccated flies. Whole-body
Na+ in the D flies was fully restored to the level observed in the
non-desiccated, hydrated flies only when the saline+sucrose solution was
provided.
Restoration of desiccation resistance
Desiccation resistance in the C populations following recovery on water or
saline solution was the same (21 h), but increased significantly (24.5 h)
following recovery on the saline+sucrose solution (P<0.0001,
Fig. 4). A similar trend was
observed in the desiccation resistant populations
(Fig. 4). Desiccation
resistance did not differ significantly (50 h) following recovery on
water or saline solution in the D flies, but increased to 75 h when the flies
were allowed to recover on the saline+sucrose solution
(P<0.0001).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A previous study indicated that during 24 h of desiccation, the D flies
lose significant water volume, principally from the hemolymph; and after 8 h
the C flies lose significant volume from both hemolymph and tissues
(Folk and Bradley, 2003).
Others (M. A. Albers and T. J. Bradley, unpublished data) examined the
restoration of hemolymph volume in the C and D populations using the same
experimental design and recovery fluids described in this paper. Their
findings indicate that D flies provided saline+sucrose during recovery
replenished
75% of lost hemolymph volume. We estimate that of the total
water volume restored,
50% appears to be allocated to the hemolymph and
50% to some other compartment. The portion of restored water not
allocated to the hemolymph may possibly be water of hydration bound to
glycogen, presuming that restoration of dry mass signified replenishment of
glycogen stores (see Dry mass below).
The recovered C flies appeared to have restored hemolymph volume to levels above those of the non-desiccated, hydrated flies, regardless of recovery fluid (M. A. Albers and T. J. Bradley, unpublished observations). The average hemolymph volume restored was 0.070 µl, or >90% of the total water restored. Although hemolymph volume was restored, total body water content in the C flies remained significantly lower than that of non-desiccated, hydrated flies, suggesting that tissue-associated water was not replenished.
Restoration of lost water volume following desiccation has been examined in
various species of desert tenebrionid beetles
(Broza et al., 1976;
Nicolson, 1980
; Haidu,
2001a,b). During desiccation the beetles lost significant hemolymph volume,
which they were able to quickly replenish when allowed to rehydrate on water.
Despite complete restoration of hemolymph volume in some of the beetles, the
original body mass was not fully restored, suggesting that tissue-associated
water was not restored and/or that dry mass had been significantly reduced
(Naidu and Hattingh, 1988
;
Naidu, 2001b
). This pattern of
rehydration was also observed in cockroaches
(Tucker, 1977
).
Dry mass
Glycogen appears to be the principal fuel metabolized during desiccation in
Drosophila (D. G. Folk and T. J. Bradley, unpublished;
Marron et al., 2003). Various
other insect species preferentially metabolize lipids during desiccation,
presumably because metabolic water production is highest (on a `per gram'
basis) when lipids are oxidized (e.g.
Tucker, 1977
;
Nicolson, 1980
;
Naidu, 2001a
). The
significance of glycogen to desiccation resistance may be related to the
ability of this polymer to bind water, which is released during glycogenolysis
(Gibbs et al., 1997
;
Chippindale et al., 1998
).
Mammal glycogen has the ability to bind 35 times its mass in water
(Schmidt-Nielsen, 1997
).
Whether insect glycogen is similar to that isolated from mammals remains
unclear (Friedman, 1985
).
When desiccated for 24 h, the D flies lost dry mass (presumed to be
primarily glycogen) at an average rate of 4 µg h1.
Provided the flies were using glycogen-derived glucose to fuel metabolism, the
water of hydration that would be released in 24 h is estimated to range from
0.290 to
0.480 µl, while the volume of metabolic water produced
is
0.050 µl. Hence, the volume of water derived from catabolized
glycogen would total
0.3400.530 µl. If we add the volume of
glycogen-associated water produced and potentially lost in 24 h (e.g. 0.340
µl) and the volume of hemolymph lost (
0.200 µl;
Folk and Bradley, 2003
), we
are able to fully account for the 0.523 µl reduction in whole-body water.
These data support our previous findings that during 24 h of desiccation, the
drought-sensitive tissues of the D flies appear to be protected from loss of
water.
When desiccated for 8 h, the C flies lost dry mass (presumed to be
primarily glycogen) at an average rate of 5 µg h1.
If we apply the same calculations used for the D flies, the catabolism of
glycogen would contribute an estimated total volume of
0.1400.220
µl of water in 8 h. If we add the lower estimated volume of
glycogen-associated water produced and potentially lost (i.e. 0.140 µl) and
the hemolymph volume lost (
0.011 µl;
Folk and Bradley, 2003
), only
60% of the reduction in whole-body water volume is accounted for. These
data are consistent with our previous findings that, in contrast to the D
flies, tissue water in the C flies is reduced significantly in 8 h
ofdesiccation. (If we used the upper estimated volume of glycogen-associated
water in these calculations, we could then account for >90% of the lost
water in the C flies; but we chose the lower limit to maintain consistency in
calculating water balance within both groups.)
The C and D flies have an average carbohydrate content of 94 µg and 168
µg, respectively, which is presumed to be principally glycogen
(Graves et al., 1992;
Gibbs et al., 1997
;
Chippindale et al., 1998
;
Djawdan et al., 1998
;
Folk et al., 2001
). Our data
suggest that glycogen may be a major contributor of water during desiccation
until the estimated time of glycogen depletion:
19 h in the C flies and
42 h in the D flies, assuming that the rates of glycogen depletion remain
constant.
Dry mass continued to decline during the 24 h recovery phase in C and D
flies provided only water or saline (Fig.
2A,B). Despite the provision of an energy source, namely sucrose,
the C flies only maintained dry mass at the post-desiccation level. The
inability of the C flies to recover dry mass fully on the saline+sucrose
solution may be related to an excessive accumulation of Na+
(Fig. 3A). Dethier and Evans
(1961) demonstrated that the
drinking response in blowflies is lowered when the osmotic concentration of
the hemolymph increases. If hemolymph osmolality increased in the C flies
(even transiently) because of excessive accumulation of Na+, then
drinking rates, and thus consumption of sucrose, may have been negatively
affected. This chain of events may have prohibited full recovery of dry mass
in the C flies when provided saline+sucrose. The D flies were capable of fully
restoring dry mass to the level of the non-desiccated, hydrated flies when
provided saline+sucrose (Fig.
2B). In contrast to the C flies, the D flies appear to have the
capacity to regulate Na+ levels and replenish dry mass while
consuming this solution.
Restoration of sodium content
Sodium is the major inorganic ion in the hemolymph of drosophilids
(Sutcliffe, 1963). A
consequence of the voluminous hemolymph pool in hydrated D flies is a
significant increase in hemolymph Na+ content
(Folk and Bradley, 2003
).
During 24 h of desiccation, the hemolymph Na+ content in the D
flies is dramatically reduced, while Na+ level remains unaltered in
the tissues. In contrast, during 8 h of desiccation in the C flies, the
Na+ content of both the hemolymph and tissues are significantly
reduced.
In C flies provided water during recovery, whole-body Na+
content was maintained only at the reduced, post-desiccation level
(Fig. 3A). Although whole-body
water was only partially restored in these C flies, hemolymph volume was fully
replenished. In many insect species, hemolymph Na+ is
well-regulated during desiccation (Hadley,
1994); and in those that rehydrate only on water, hemolymph
Na+ concentration may be reduced relative to non-desiccated flies
(Tucker, 1977
;
Nicolson, 1980
;
Naidu and Hattingh, 1988
;
Naidu, 2001a
) or restored to
original concentrations (Naidu,
2001b
). It remains unclear which strategy is employed by these
fruit fly populations.
The C flies provided the saline solution were able to fully restore whole-body Na+ content, even though water volume was only partially restored. These results suggest that during recovery on saline, the osmotic concentration of some compartment in the body may have increased, or that osmotic concentration was regulated and the restored Na+ replaced some other osmolyte. When provided saline+sucrose during recovery, the C flies experienced an increase in whole-body Na+ to a level significantly greater than that of the non-desiccated, hydrated flies, possibly leading to the same consequences discussed above. The apparent Na+ overload may have resulted from the attempt to restore water and/or energy stores, perhaps leading to extensive drinking initially. As a consequence, the Na+ load may have increased to such an extent that the regulatory capacity of the excretory system of the C flies was surpassed, resulting in an elevated Na+ content.
Whole-body Na+ content in the D flies was sustained only at the
post-desiccation level when either water or saline were provided
(Fig. 3B). The D flies restored
Na+ content only when provided saline+sucrose. Although
Na+ content was fully restored on this solution, the hemolymph
volume was only partially restored. The disparate capacities for restoring
Na+ (full restoration) and water content (partial restoration) lead
to interesting questions: Was hemolymph Na+ concentration regulated
during recovery? Did the Na+ concentration increase in some
compartment(s)? Did the restored Na+ replace other cations within
the hemolymph? [Some insects osmoregulate the hemolymph by adjusting the amino
acid content (Djajakusumah and Miles,
1966; Broza et al.,
1976
; Coutchie and Crowe,
1979
). The replacement of some cations, such as free amino acids,
with Na+ may be a means by which the recovering D flies maintain
hemolymph osmolality, despite full recovery of Na+ and only partial
recovery of hemolymph.] Although these questions cannot be answered within the
scope of this study, they would be interesting to address in future
studies.
Desiccation resistance
Relative to recovery on water or saline, the C flies had a small, but
significant, increase (14%) in desiccation resistance when provided
saline+sucrose during recovery (Fig.
4); yet water was only partially restored, dry mass was maintained
at post-desiccation levels, and Na+ content had exceeded that of
hydrated flies. Relative to recovery on water or saline, the D flies increased
post-recovery desiccation resistance by 50% when allowed to recover on
saline+sucrose (Fig. 4). When
provided this fluid, the D flies were capable of full replenishment of dry
mass (glycogen stores?) and partial replenishment of water content. Previous
results suggest that desiccation resistance in the D flies is positively
correlated with glycogen content and hemolymph volume
(Folk et al., 2001). Our
current results suggest that the capacity to replenish these somatic
components, leads to the highest recovered desiccation resistance. The D flies
were also able to recover whole-body Na+ content fully when
provided the saline+sucrose solution. Sodium may play an important role in
water conservation during desiccation. Antidiurectic hormone (ADH) stimulates
the uptake of water from the rectal lumen in some insect species, including
the cockroach (Wall, 1967
;
Phillips et al., 1986
). The
rectal epithelia in the cockroach are rich in Na+-K+
ATPase and Na+ is required during ADH-stimulated water uptake
across the rectum, suggesting that the process requires energy
(Tolman and Steele, 1976
;
Steele and Tolman, 1980
).
Further investigation suggests that glycogen is the principal energy source
used to fuel the energy-requiring transport of water across the cockroach
rectum (Tolman and Steele,
1980
). Although the importance of Na+ to water
conservation during desiccation in our flies remains unclear, these findings
suggest that Na+, as well as glycogen, may play crucial roles in
the reabsorption of water from the rectal lumen during desiccation stress.
Conclusion
Selection for enhanced desiccation resistance in Drosophila
melanogaster leads not only to an improvement in the capacity to resist
the stresses of desiccation, but also to a greater ability to recover
physiological robustness following desiccation. The desiccation-resistant
populations, when compared to the control populations, were able to restore a
greater amount of body water and dry mass. Furthermore, the restoration of
water, dry mass, Na+ content and desiccation resistance was greatly
improved in D flies that consumed fluid supplemented with sucrose. We propose
that energy consumption appears to be an important aspect of recovery from
desiccation in these fruit fly populations.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Arlian, L. G. and Eckstrand, I. A. (1975). Water balance in Drosophila pseudoobscura, and its ecological implications. Ann. Entomol. Soc. Am. 68,827 -832.
Browne, L. B., Moorhouse, J. E. and van Gerwen, A. C. M. (1976). A relationship between weight loss during food deprivation and subsequent meal size in the locust Chortoicetes terminifera. J. Insect. Physiol. 22, 89-94.[CrossRef]
Broza, M., Borut, A. and Pener, M. (1976). Osmoregulation in the desert tenebrionid beetle Trachyderma philistine Reiche during dehydration and subsequent rehydration. Isr. Med. J. 12,868 -871.
Chapman, R. F. (1998). The Insects: Structure and Function. 4th edition. Cambridge, UK: Cambridge University Press.
Chippindale, A. K., Gibbs, A. G., Sheik, M., Yee, K. J., Djawdan, M., Bradley, T. J. and Rose, M. R. (1998). Resource acquisition and the evolution of stress resistance in Drosophila melanogaster. Evol. 52,1342 -1352.
Coutchie, P. A. and Crowe, J. H. (1979). Transport of water vapor by tenebrionid beetles. II. Regulation of the osmolarity and composition of the hemolymph. Physiol. Zool. 52,88 -100.
Dethier, V. G. and Evans, D. R. (1961). Physiological control of water ingestion in the blowfly. Biol. Bull. 121,108 -116.
Djajakusumah, T. and Miles, P. W. (1966). Changes in the relative amounts of soluble protein and amino acid in the haemolymph of the locust, Chortoicetes terminifera Walker (Orthoptera: Acrididae), in relation to dehydration and subsequent rehydration. Aust. J. Biol. Sci. 19,1081 -1094.
Djawdan, M., Chippindale, A. K., Rose, M. R. and Bradley, T. J. (1998). Metabolic reserves and evolved stress resistance in Drosophila melanogaster. Physiol. Zool. 71,584 -594.[Medline]
Edney, E. B. (1977). Zoophysiology and Ecology 9: Water Balance in Land Arthropods. New York: Springer-Verlag.
Evans, D. R. (1961). Control of the responsiveness of the blowfly to water. Nature 190,1132 -1133.
Folk, D. G. and Bradley, T. J. (2003). Evolved
patterns and rates of water loss and ion regulation in laboratory-selected
populations of Drosophila melanogaster. J. Exp. Biol.
206,2779
-2786.
Folk, D. G., Han, C. and Bradley, T. J. (2001).
Water acquisition and partitioning in Drosophila melanogaster:
effects of selection for desiccation-resistance. J. Exp.
Biol. 204,3323
-3331.
Friedman, S. (1985). Carbohydrate metabolism. In Comprehensive Insect Physiology, Biochemistry and Pharmacology. Vol. 10, Biochemistry (ed. G. A. Kerkut and L. I. Gilbert), pp. 43-76. New York: Pergamon Press Inc.
Gibbs, A. G., Chippindale, A. K. and Rose, M. R.
(1997). Physiological mechanisms of evolved desiccation
resistance in Drosophila melanogaster. J. Exp. Biol.
200,1821
-1832.
Gillott, C. (1995). Entomology. 2nd edition. New York: Plenum Press.
Graves, J. L., Toolson, E. C., Jeong, C., Vu, L. N. and Rose, M. R. (1992). Desiccation, flight, glycogen, and postponed senescence in Drosophila melanogaster. Physiol. Zool. 65,268 -286.
Hadley, N. F. (1994). Water Relations of Terrestrial Arthropods. San Diego, CA: Academic Press.
Hamilton, W. J., III and Seeley, M. K. (1976). Fog basking by the Namib Desert beetle, Onymacris unguicularis.Nature . 262,284 -285.
Hoffman, A. A. and Parsons, P. A. (1993). Direct and correlated responses to selection for desiccation resistance: a comparison of Drosophila melanogaster and D. simulans. J. Evol. Biol. 6,643 -657.
Lehmann, F.-O., Dickinson, M. H. and Staunton, J.
(2000). The scaling of carbon dioxide release and respiratory
water loss in flying fruit flies (Drosophila sp.). J. Exp.
Biol. 203,1613
-1624.
Loveridge, J. P. (1975). Studies on the water balance of adult locusts. III. The water balance of non-flying locusts. Zool. Afr. 10,1 -28.
Marron. M. T., Markow, T. A., Kain, K. J. and Gibbs, A. G. (2003). Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila. J. Insect Physiol. 49,261 -270.[CrossRef][Medline]
Naidu, S. G. (2001a). Water balance and osmoregulation in Stenocara gracilipes, a wax-blooming tenebrionid beetle from the Namib Desert. J. Insect Physiol. 47,1429 -1440.[CrossRef][Medline]
Naidu, S. G. (2001b). Osmoregulation in Onymacris rugatipennis, a free-ranging tenebrionid beetle from the Namib Desert. Comp. Biochem. Physiol. 129A,873 -885.
Naidu, S. G. and Hattingh, J. (1988). Water balance and osmoregulation in Physadesmia globosa, a diurnal tenebrionid beetle for the Namib Desert. J. Insect Physiol. 34,911 -917.[CrossRef]
Nicolson, S. W. (1980). Water balance and osmoregulation in Onymacris plana, a tenebrionid beetle from the Namib Desert. J. Insect Physiol. 26,315 -320.
Phillips, J. E., Hanrahan, J., Chamberlin, M. and Thomson, B. (1986). Mechanisms and control of reabsorption in insect hindgut. Adv. Insect Physiol. 19,329 -422.
Rose, M. R. (1984). Laboratory evolution of postponed senescence in Drosophila melanogaster. Evol. 38,1004 -1010.
Rose, M. R., Graves, J. L. and Hutchison, E. W. (1990). The use of selection to probe patterns of pleiotropy in fitness characters. In Insect Life Cycles (ed. F. Gilbert), pp. 29-42. New York: Springer-Verlag.
Rose, M. R., Vu, L., Park, S. U. and Graves, J. L. (1992). Selection on stress resistance increases longevity in Drosophila melanogaster. Exp Gerontol. 27,241 -250.[CrossRef][Medline]
Schmidt-Nielsen, K. (1997). Animal Physiology: Adaptation and Environment. 5th edition. Cambridge, UK: Cambridge University Press.
Steele, J. E. and Tolman, J. H. (1980). Regulation of water transport in the cockroach rectum by the corpora cardiacacorpora allata system: The requirement of Na+. J. Comp. Physiol. 13,357 -366.
Sutcliffe, D. W. (1963). The chemical composition of haemolymph in insects and some other arthropods in relation to their phylogeny. Comp. Biochem. Physiol. 9, 121-135.[CrossRef]
Tolman, J. H. and Steele, J. E. (1976). A ouabain sensitive (Na+K+)-activated ATPase in the rectal epithelium of the American cockroach, Periplaneta americana.Insect Biochem. 6,513 -517.[CrossRef]
Tolman, J. H. and Steele, J. E. (1980). The effect of the corpora cardiaca-corpora allata system on oxygen consumption in the cockroach rectum. The role of Na+ and K+. J. Comp. Physiol. 66B,59 -67.
Tucker, L. E. (1977). Effect of dehydration and rehydration on the water content and Na+ and K+ balance in adult male Periplaneta americana. J. Exp. Biol. 71, 49-66.
Wall, B. J. (1967). Evidence for antidiuretic control of rectal water absorption in the cockroach, Periplaneta americana L. J. Insect Physiol. 13,565 -578.[CrossRef][Medline]
Wall, B. J. (1970). Effects of dehydration and rehydration on Periplaneta americana. J. Insect Physiol. 16,1027 -1042.[CrossRef][Medline]
Wigglesworth, V. B. (1972). The Principles of Insect Physiology. London: Chapman and Hall.
Williams, A. E. and Bradley, T. J. (1998). The
effect of respiratory pattern on water loss in desiccation-resistant
Drosophila. J. Exp. Biol.
201,2953
-2959.
Williams, A. E., Rose, M. R. and Bradley, T. J.
(1998). Using laboratory selection for desiccation resistance to
examine the relationship between respiratory pattern and water loss in
insects. J. Exp. Biol.
201,2945
-2952.