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First published online August 9, 2007
Journal of Experimental Biology 210, 2897-2904 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007591
Life history consequences of temperature transients in Drosophila melanogaster
1 Department of Biology, Box 351800, University of Washington, Seattle, WA
98195-1800, USA
2 Department of Biology, Whitman College, Walla Walla, WA 99362,
USA
* Author for correspondence (e-mail: dillonm{at}u.washington.edu)
Accepted 29 May 2007
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Summary |
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Key words: fitness, fecundity, intrinsic rate of increase, net reproductive rate, weather front
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; Cossins and Bowler,
1987). Temperature effects are typically studied by maintaining
organisms in the laboratory either at different constant temperatures or on
different fixed temperature cycles. Nevertheless, ectotherms in nature
experience transient weather fronts that may alter their body temperatures for
short periods (e.g. Kingsolver,
2000). Weather fronts may not only alter an organism's performance
during the front itself, but also induce carry-over effects that persist even
after weather returns to normal. Surprisingly little is known about the impact
of such thermal transients on the physiology and life history of ectotherms,
except in regards to short-term exposure to extreme temperatures
(Bubliy and Loeschcke, 2001;
David et al., 2003;
Gibert et al., 2001;
Hercus et al., 2003;
Krebs and Loeschcke, 1994a;
Krebs and Loeschcke, 1994b;
Lee et al., 1987;
Maynard Smith, 1958;
Rohmer et al., 2004;
Sisodia and Singh, 2006;
Zani et al., 2005a;
Zani et al., 2005b).
Drosophila melanogaster is suitable for an examination of the
physiological and fitness impacts of non-stressful thermal transients. These
flies are widely distributed in temperate zones
(Mueller, 1985) where weather
fronts are common: thus studies of thermal transients are ecologically
relevant to this species. Moreover, a wealth of information is known about the
effects of chronic temperature exposure on performance and life history traits
in D. melanogaster (David et al.,
1983; Hoffmann et al.,
2003). For example, fecundity increases gradually with temperature
to 
25°C and then decreases rapidly at temperatures above 28° to
30°C (David and Clavel,
1969; Huey et al.,
1995; McKenzie,
1975; Schnebel and Grossfield,
1986; Siddiqui and Barlow,
1972).
We studied the impact of thermal transients on fecundity (eggs) and progeny
production of Drosophila melanogaster. Initially we measured daily
fecundity and progeny production of flies living at 25°C for 3 days and
then transferred flies to one of three transient treatments (1 day at
18°C, 3 days at 18°C, or 1 day at 29°C) before returning them to
25°C for 3–5 days. The 1- or 3-day transient exposures are
equivalent to typical weather front durations
(Allen et al., 1996;
Bosart et al., 1973;
Robb and Forbes, 2006). We
selected transient temperatures of 18°C and 29°C because these are
displaced from the optimal temperature (25°C) of these flies
(Cohet and David, 1978;
Huey et al., 1995;
Siddiqui and Barlow, 1972),
but are not extreme (David et al.,
2005). We also maintained some flies at constant temperatures
(18°C, 25°C or 29°C) so we could compare the effects of chronic
versus transient temperature exposures.
To determine whether transient exposures affected progeny of exposed females, we estimated development time of offspring produced during the experiment. From these data we computed generation time of offspring of experimental flies, net reproductive rate (R0, that is, total female progeny produced during the experiment) and intrinsic rate of population growth (r). Thus our experimental design enabled us to determine how key life history traits changed during, as well as after, a thermal transient. Although we expected that temperature transients would depress egg production during the exposure, we were uncertain as to whether and how transient exposure would induce carry-over effects once flies were returned to 25°C. Consequently, we considered four competing hypotheses (Fig. 1):
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), their fecundity may not return to normal levels for some
time, if ever. Because the transient temperatures we selected were
intentionally non-extreme (David et al.,
1983), this outcome is unlikely in our experiments, but would be
likely following more extreme treatments. ) that unfavorable weather will persist for some time, they
might reallocate resources from reproduction to survival. If so, their
fecundity might remain low for some time even following a return to normal
temperatures (Mitrovski and Hoffmann,
2001; Schmidt and Conde,
2006). Note that the resulting pattern of fecundity parallels that
for the `induced damage hypothesis' but has a different causal basis. We find little effect of thermal transients on flies once they return to 25°C. This result strongly supports the `no carry-over hypothesis'. Consequently, D. melanogaster seems well buffered against short-term exposure to non-optimal (but non-extreme) temperatures. Parallel studies with exposure to more extreme temperatures (or perhaps with longer durations) will be necessary to set boundaries on the range of permissive temperatures.
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Materials and methods |
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),
we chose to work with a relatively fresh stock. Accordingly, we collected 100
isofemale lines of D. melanogaster from an apple orchard near
Wenatchee, WA, USA (47°30'N, 120°17'W) in June 2005, and
established a base stock by pooling about 25 males and 25 females from each
isofemale line. This stock was maintained at 25°C (12 h:12 h L:D) until
July and early August 2006, when these experiments were run. Thus the flies
had been in the laboratory for just over 1 year. To maintain the colony at
1000–3000 flies, eggs were collected approximately every 10 days and
reared in controlled conditions (50–100 eggs/vial; 25°C and 12 h:12
h L:D; diet of cornmeal, molasses, yeast, agar, tegosept) before newly emerged
adult flies were transferred into the colony. Colony food bottles (150 ml)
were replaced every 3–5 days to ensure that all colony flies developed
in controlled conditions.
Experimental conditions
Eggs collected from the base stock on July 12, 2006 were reared at low
densities of 50–70 eggs/vial (25°C, 12:12 L:D; 2.5x9.5 cm
glass vials containing 10 ml food). Within 12 h after flies emerged (7/21
and 7/22), adults were briefly anesthetized (CO2) and triads of
flies (one female, two males) were placed into individual vials seeded with
live yeast. Egg production increases until females are about 3 days of age
(Huey et al., 1995), so fly
triads were maintained at 25°C until females were 3 to 4 days of age
before assigning them to treatment groups. Flies that did not lay eggs during
this initial period were eliminated from the experiment. Fly triads were then
transferred (without anesthesia) into fresh vials without supplemental yeast
(to facilitate egg counting) and then randomly assigned to one of six
treatment groups, with about 18 triads per group. One transient group was kept
for 3 days at 25°C, 1 day at 18°C and then 5 days back at 25°C. A
second was kept for 3 days at 25°C, 3 days at 18°C, and 3 days back at
25°C. The third was kept for 3 days at 25°C, 1 day at 29°C, and 5
days back at 25°C. Three additional sets of fly triads were maintained at
constant temperatures of 18°C, 25°C or 29°C for 9 days. Flies were
housed in environmental chambers (Percival Scientific, Perry, IA, USA; 12:12
L:D cycle starting at 07:00 h). Chamber temperatures were monitored daily and
vials within a chamber were rotated daily to minimize effects of
within-chamber temperature variation. Each triad was transferred without
anesthesia into a new vial every day at 09:30–10:00 h so as not to
interfere with peak oviposition, which occurs in late afternoon in these
flies. Flies were briefly at room temperature (23°C) during
transfers.
After returning triads to environmental chambers, we counted `transient' eggs laid during the previous 24 h period and then immediately transferred them to 25°C for development. We maintained `constant' eggs at their respective temperatures. Subsequently, we counted newly emerged flies in late morning every day until no more emerged. Because eggs collected during transient exposure completed most of their development at 25°C, any between-groups difference in progeny viability should be due to effects of the transient on the female or on the eggs themselves.
We estimated egg-to-adult viability as the proportion of eggs that produced adults. Egg counts in vials are often in error, because some eggs either might have hatched by scoring time or might simply have been overlooked. Indeed, 156 of 834 vials had a few more flies emerged than eggs counted (treatment had no effect on the number or magnitude of miscounts). For these vials, viability was taken as the number of emerged flies instead of the number of eggs (thus these females were assumed to have 100% viability). Two vials were excluded from the analysis because they had many fewer eggs than emerged adults. However, the statistical results presented below are robust, even if these vials are included.
Development time and fitness estimates
To determine fitness consequences of the various temperature treatments, we
used a life-table analysis (Birch,
1948) and estimated generation time (Tg), net
reproductive rate (R0, the total number of female eggs
laid during the experiment), and intrinsic rate of increase (r,
computed using an iterative technique; see Appendix A) for each female.
Estimates of r require development time, which was not measured for
experimental females themselves (because all were reared at 25°C, see
above). Instead, the average development times of the females' progeny were
used as estimates of their development times. (Thus, our estimate of
r is based on fecundity patterns of female parents and development
times of their progeny, rather than on data collected within a single
generation.) For these calculations we assumed a 50:50 sex ratio of
progeny.
Statistical analyses
During the experiment 6 females died (2 at 18°C, 3 at 25°C and 1 at
29°C), 6 escaped during transfers (2 at 18°C and 4 at 25°C), and
12 did not lay any eggs (3 at constant 18°C, 2 at constant 25°C, 1 at
constant 29°C, 2 at short 18°C, and 1 at short 29°C). These were
excluded from further analysis. Females for which one male escaped or died
were included in the analysis. To correct for non-independence of daily
measurements within females, we used a repeated-measures MANOVA with daily
fecundity, viability (arcsine square root-transformed), or development time as
the dependent variable, temperature treatment as the between-subjects effect,
and day and treatmentxday within-subjects effects. This technique is
robust to violations of normality and sphericity
(Obrien and Kaiser, 1985). For
these analyses, we report several statistics (Pillai's Trace, Hotelling's
Trace, Wilks's lambda, and Roy's statistic) because these did not always give
similar results. For data not requiring repeated measures, we used
multivariate ANOVA analyses with Tukey-HSD post-hoc tests when the
data were normally distributed. For non-normal data, we used
Kruskal–Wallis rank sum tests with non-parametric Behrens–Fisher
post-hoc multiple comparisons tests. All statistics were done in R
(R Development Core Team,
2006), with packages multcomp
(Bretz et al., 2004) and npmc
(Helms and Munzel, 2006) for
parametric and non-parametric post-hoc tests, respectively, nlme
(Pinheiro et al., 2006) for
linear mixed effects modeling, and gregmisc
(Warnes, 2006), Hmisc
(Harrell, 2006), IDPmisc
(Ruckstuhl et al., 2006), and
gridBase (Murrell, 2006) for
advanced plotting features.
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32=2.18, 1.42, 1.42 on days 1, 2 and 3,
respectively, all P>0.536; see
Fig. 2B). Differences in
fecundity among treatment groups on days 4–6 could therefore be
attributed to the transient temperature exposure. A 1-day `hot' temperature transient had no immediate or carry-over effects on female fecundity. Females at 29°C for 1 day had fecundities similar to those of females kept at 25°C on the transient day (Fig. 2B; day 4 post-hoc Behrens–Fisher P=0.700) and on each subsequent day at 25°C (days 5 to 9, Behrens–Fisher, all P>0.52).
Both 1- and 3-day `cold' temperature transients strongly reduced female
fecundity, but these effects disappeared immediately when flies were returned
to 25°C. While at 18°C for 1 or 3 days, females laid significantly
fewer eggs on those days than did the constant 25°C females
(Fig. 2B; Behrens–Fisher,
all P<0.001). When returned to 25°C transient cold females had
similar fecundities to constant 25°C females
(Fig. 2B; Behrens–Fisher
P=0.960 for post-hoc comparison of 1-day 18°C with
constant 25°C on day 5; Kruskal–Wallis
32=2.44, P=0.486 for day 7). These results
strongly support the `no carry-over hypothesis'
(Fig. 1).
Effects of temperature on egg-to-adult viability
Constant low temperatures strongly reduced egg-to-adult viability. Progeny
developing at 25°C and 29°C had similar viabilities that were much
higher than viabilities of those developing at 18°C (MANOVA,
between-subject Temperature effect, P=0.005;
Table 1;
Fig. 3A).
Egg-to-adult viability did not differ among the three transient treatment
groups and the 25°C control on days 1 to 3, indicating that these groups
were homogeneous prior to temperature transients
(Fig. 3B; Kruskal–Wallis
32=6.01, 1.88, 2.55; and all P>0.46). A
1-day exposure of flies to 29°C did not affect egg-to-adult viability of
their progeny (Fig. 3B;
Behrens–Fisher P=0.904 for comparison of 1-day 29°C group
with 25°C group on day 4). A 1-day exposure of flies to 18°C reduced
egg-to-adult viability of their progeny
(Fig. 3B, broken line), but not
significantly so (Behrens–Fisher P=0.110). However, a 3-day
exposure of flies to 18°C significantly reduced egg-to-adult viability of
their progeny on the first 2 days (Fig.
3B, broken line; Behrens–Fisher P=0.002, 0.036 for
days 4 and 5, respectively), and marginally so on day 3 (Behrens–Fisher
P=0.087 for comparison of 3-day 18°C group and 25°C group on
day 6). In no case did temperature transients have carry-over effects on
egg-to-adult viability (Fig.
3B; Behrens–Fisher, all P>0.800).
Effects of temperature on development time
Development time decreased significantly with increasing constant
temperature (Fig. 4A;
Table 1, between-subjects
Temperature effect, P<0.0001). Flies eclosed in 21.8±1.3
days at 18°C, in 9.8±0.8 days at 25°C, and in 8.3±0.7
days at 29°C. Progeny development time did not change significantly with
female's age (Fig. 4A;
Table 1, within-subjects Day
effect, P=0.480). Therefore we compared development time of transient
treatment groups directly to the 25°C control.
Transient temperature exposure did not affect development time. Progeny of
females moved to 18°C or 29°C for 1 day developed in the same time as
progeny of females held at constant 25°C
(Fig. 4B, day 4, Kruskal-Wallis
32=4.95, P=0.175). Development times of
progeny from eggs laid by females during their third day at 18°C were
slightly but not significantly longer than eggs laid at 25°C on the same
day (Fig. 4B, day 6;
Behrens–Fisher P=0.085).
Effects of temperature on fitness
Low constant temperatures significantly reduced fitness. Mean generation
time decreased significantly, and both net reproductive rate
(R0) and intrinsic rate of increase (r) increased
significantly with temperature (Table
2; ANOVA, all P<0.002). Both R0
and r were significantly lower for 18°C flies than for 25°C
and 29°C flies (Tukey HSD P<0.05), but these traits were not
significantly different for 25°C versus 29°C flies.
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Surprisingly, exposure to transient temperatures did not decrease female fitness. Despite major depression effects of transient exposure to 18°C on fecundity and on egg-to-adult viability (Fig. 2B, Fig. 3B), transient exposure to 18°C or to 29°C temperatures did not affect Tg, R0, or r relative to the constant 25°C treatment (Table 3; ANOVA all P>0.257).
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; McCabe and Partridge,
1997; Gilchrist and Huey,
2001). Many ectotherms use behaviors to avoid – or at least
reduce – the impact of fluctuations in operative temperatures
(Cowles and Bogert, 1944;
Stevenson, 1985;
Huey et al., 2003).
Nevertheless, ectotherms will likely be forced to experience non-optimal
temperatures during weather fronts. Two issues are germane. First, how much
are performance and fitness depressed during a weather front? Second, are
there carry-over effects that persist once temperatures return to normal? Our
results suggest that female flies experiencing even minor cold fronts (though
not minor warming) will have reduced fecundity and egg-to-adult viability
during those fronts. Nevertheless, they recover quickly when temperatures
return to normal, supporting the `no carry-over hypothesis'.
The constant temperature treatments provide a necessary baseline for
comparison of our fly population with other stocks. Overall, the flies used in
this study responded to chronic temperatures as expected from previous work.
Chronic exposure to 18°C reduced fecundity and viability in our flies, and
increasing chronic temperatures reduced development time and changed the
pattern of egg production over time. All of these findings qualitatively match
previous work in Drosophila
(Bochdanovits and de Jong,
2003; Bouletreau-Merle et al.,
2003; David and Clavel,
1969; David and Clavel,
1967; Fernandez and
Lopez-Fanjul, 1997; Gilchrist
and Huey, 2001; Huey et al.,
1995; Schnebel and Grossfield,
1986; Siddiqui and Barlow,
1972; Trotta et al.,
2006). However, chronic exposure to 29°C did not reduce
fecundity, viability or fitness of our flies even though this temperature is
stressful for many fly stocks (David and
Clavel, 1967; Fernandez and
Lopez-Fanjul, 1997; Gilchrist
and Huey, 2001; Huey et al.,
1995; Schnebel and Grossfield,
1986; Siddiqui and Barlow,
1972; Trotta et al.,
2006). Thus our stocks appear heat tolerant relative to previously
studied ones. This might reflect geographic variation
(Schmidt and Conde, 2006;
Hoffmann et al., 2003), or the
fact that our flies had been in the laboratory for only a year, whereas prior
studies often used lab-adapted stocks; heat tolerance in D.
subobscura decays quickly in the laboratory
(Quintana and Prevosti,
1990).
Immediate impact of thermal transients
We first review changes in life history parameters during transient
exposure. Transient exposure to 18°C negatively affected both fecundity
and viability. The reduction in fecundity is not surprising, as chronic
exposure to 18°C is known to reduce fecundity in many Drosophila
stocks (Bochdanovits and de Jong,
2003; Bouletreau-Merle et al.,
2003; David and Clavel,
1969; David and Clavel,
1967; Fernandez and
Lopez-Fanjul, 1997; Gilchrist
and Huey, 2001; Huey et al.,
1995; Schnebel and Grossfield,
1986; Siddiqui and Barlow,
1972; Trotta et al.,
2006), and in our flies (Fig.
2A). However, our finding that viability of progeny is reduced by
a 1-day (or less) exposure to 18°C is novel and exacerbates the ecological
impact of a weather transient. Eggs were exposed to only 1 day (or less) at
18°C and were at 25°C for the remainder of development (10 days),
suggesting that fly embryos are very sensitive to even brief exposure to
moderately cool temperatures. Whether later stages of development are also
sensitive will require additional experiments.
Flies experiencing a 1- or 3-day 18°C transient had a larger decline in
fecundity during that transient (70–80% decline relative to constant
25°C females, see Fig. 2B)
than did same-age females maintained at constant 18°C (32–65%
decline on days 4–6; Fig.
2A). Egg viabilities were similar for the two groups (30–50%
for 18°C transients, 20–50% for constant 18°C flies). Thus,
transient exposure to 18°C depressed fecundity more than did chronic
exposure to 18°C; perhaps chronic exposure to 18°C post-eclosion
induces a `beneficial acclimation' effect
(Ayrinhac et al., 2004;
Nunney and Cheung, 1997).
Transient exposure to 29°C did not significantly affect fecundity or
viability relative to flies maintained at 25°C. We were surprised by this
result because chronic exposure to 29°C typically reduces the performance
and fitness of D. melanogaster
(David and Clavel, 1967;
Fernandez and Lopez-Fanjul,
1997; David et al.,
2005; Schnebel and Grossfield,
1986; Siddiqui and Barlow,
1972). However, in our flies, chronic exposure to 29°C did not
depress fitness; thus 29°C appears not to be particularly `hot' for this
stock.
Recovery from thermal transients
Although fecundity and progeny viability were markedly reduced during a 1-
or 3-day exposure to 18°C, these traits returned to baseline levels
immediately after return of females to 25°C
(Fig. 2B,
Fig. 3B, days 5–9). This
pattern strongly supports the `no carry-over hypothesis' and contradicts
alternative hypotheses (Fig.
1).
For our flies, neither fecundity nor progeny viability changed during
exposure to 29°C (Figs 2,
3), either chronically or
transiently, so it is not surprising that these traits were unchanged
(relative to constant 25°C flies) after return to 25°C. Our data
document that transient exposures to temperatures as low as 18°C or as
high as 29°C have no sustained effects on fecundity or viability. Thus
these flies are buffered against temperature fluctuations of more than
10°C. Brief exposures to more extreme temperatures do have sustained
negative effects on fitness traits of flies
(Krebs and Loeschcke, 1994a;
Sisodia and Singh, 2006). In
any case, additional experiments will be required to demarcate the range and
duration of transient temperatures that inflict sustained damage on flies.
Fitness consequences of thermal transients
Because transient exposure to 29°C did not alter fecundity or progeny
viability relative to control flies, we focus only on the fitness consequences
of transient exposure to 18°C. Although these transients reduced fecundity
and viability, they did not significantly reduce lifetime fitness relative to
constant 25°C flies (R0, r,
Table 3). Initially, this
seemed paradoxical to us, but on reflection we believe two factors are
responsible:
). Very likely,
exposure of younger flies to a temperature transient would have significantly
reduced fitness. In conclusion, our experiments demonstrate that non-extreme thermal transients can reduce fecundity and progeny viability, but that these transients have no sustained effects on flies. Thus these flies seem relatively well buffered against moderate weather fronts. Future studies should attempt to delimit the range of transients that are tolerable by flies, as well as whether sensitivity to transients varies with age. Our egg viability data suggest that early embryos are very sensitive to brief exposure to temperatures as mild as 18°C.
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Acknowledgments |
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