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First published online December 14, 2007
Journal of Experimental Biology 211, 79-85 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.009530
A cumulative feeding threshold required for vitellogenesis can be obviated with juvenile hormone treatment in lubber grasshoppers
University of North Florida, Department of Biology, 1 UNF Drive, Jacksonville, FL 32224, USA
* Author for correspondence (e-mail: jhatle{at}unf.edu)
Accepted 16 October 2007
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: developmental threshold, life history, physiology, phenotypic plasticity, reproduction, terminal investment hypothesis, trade-off
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Morey and Reznick, 2000;
Schoech et al., 2004;
Davidowitz et al., 2005); this
plasticity can have important effects on fitness
(Denver et al., 1998). Prior to
a developmental transition, a threshold describes the status needed and
ensures that an adequate condition has been attained to proceed through the
transition (Wilbur and Collins,
1973; Frisch,
2002; Reynolds et al.,
2003; Moczek and Nijhout,
2003; Nijhout,
2003; Davidowitz et al.,
2005; Nijhout et al.,
2006).
Thresholds can be described: (1) morphologically as a critical body or
organ size (e.g. Nijhout and Williams,
1974a; Nijhout and Williams,
1974b; Davidowitz et al.,
2005; Mirth et al.,
2005); (2) physiologically as a level of storage
(Frisch, 2002) or (3)
nutritionally as an amount ingested
(Nijhout, 1994;
Klowden, 1987;
Juliano et al., 2004).
Clearly, nutrition is vital to attaining all of these thresholds, because it
is needed for both growth and storage. However, these thresholds must be
translated to endocrine signals that mediate the life history transition
(Nijhout and Williams, 1974a;
Nijhout and Williams, 1974b;
Day and Rowe, 2002;
Moczek and Nijhout, 2003;
Juliano et al., 2004;
Davidowitz et al., 2005;
Nijhout et al., 2006). The
relationships between developmental thresholds and these endocrine signals are
poorly understood, yet they are a critical link in how environmental
conditions produce variation in life histories
(Emlen and Nijhout, 1999;
Zera and Harshman, 2001;
Davidowitz et al., 2005;
Shingleton et al., 2007).
In lubber grasshoppers (Romalea microptera), a cumulative feeding
threshold of 4.0 g dry mass of Romaine lettuce is required to initiate the
transition from somatic growth to vitellogenesis and ultimately oviposition
(Juliano et al., 2004)
(Fig. 1). Diet prior to adult
molt has little effect on the timing of reproduction
(Moehrlin and Juliano, 1998).
Hence, a single developmental program produces different phenotypes simply due
to its expression in different environments (e.g. nutritional levels)
(Reznick, 1990). Plasticity of
reproductive timing is thus dependent only on the time to attain that
threshold.
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35 days after the adult
molt. By contrast, in low-fed animals (0.12 g dry mass
day–1), first oviposition occurs 65 days after the adult
molt (Hatle et al., 2000;
Hatle et al., 2003a). Mature
females generally lay 2–3 clutches during their life
(Hatle et al., 2006b). Lubber
grasshoppers are univoltine and overwinter as eggs; therefore, reproduction is
potentially time-constrained with the onset of winter
(Rowe et al., 1994;
Luker et al., 2002).
Nutrition is needed to stimulate the production of the major gonadotropin
juvenile hormone (JH) in lubber grasshoppers. But whether nutrition is needed
to attain the status needed for JH response (i.e. competence) is unknown.
During the oviposition cycle, JH levels start at zero, first rise to low
levels (which corresponds to the initiation of vitellogenin production), then
rise to a maximum around mid-vitellogenesis (which corresponds to oocyte
growth and patency) and finally fall before oviposition. The maximum titer of
JH is the point at which JH degradation becomes favored over JH synthesis; the
maximum always occurs about 12 days before oviposition
(Hatle et al., 2000;
Hatle et al., 2003a). These
studies on the effects of nutrition on JH levels suggest that threshold
feeding (see Juliano et al.,
2004) (Fig. 1) is
only needed to allow production of JH, and the female is competent to respond
to JH prior to attaining the threshold.
By contrast, studies on vitellogenesis suggest that feeding to the
threshold is required in addition to JH. Production of vitellogenin mRNA
requires JH (Fei et al.,
2005). In starved grasshoppers, the infusion of JH increases
vitellogenin mRNA, but feeding is required for synthesis of vitellogenin
protein by the fat body (Fei et al.,
2005). These results suggest that JH may not be the only factor
involved in the regulation of vitellogenin production, but instead some other
nutrition-dependent change is needed. Similarly, Hatle et al. found that total
vitellogenin production relies more on total fat body mass than on
mass-specific tissue stimulation (typically by JH)
(Hatle et al., 2006a). This
suggests that growth factors affecting the fat body, which are likely
nutrition dependent, might be a co-requirement with JH for vitellogenesis
(Hatle et al., 2006a). Hence,
studies on vitellogenin production suggest threshold feeding is needed both to
initiate production of JH and to bring about competence to JH.
We manipulated both feeding and the timing of initial JH treatment to test
whether JH is solely responsible for vitellogenesis or if the feeding
threshold must also be met for competence to JH. We predict that the feeding
threshold must be met (see Fei et al.,
2005; Hatle et al.,
2006a). Specifically, individuals that are sub-threshold at the
start of JH analog treatment will delay vitellogenesis, and ultimately
oviposition, in comparison with individuals that are supra-threshold at the
start of JH analog treatment. In other words, we predict a statistically
significant interaction of diet and timing of JH initiation on the onset of
vitellogenesis and timing of oviposition. Alternatively, if attainment of the
feeding threshold is not required along with JH, sub-threshold females treated
with JH should undergo vitellogenesis in concert with supra-threshold females
treated with JH.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The timing of early JHAi was chosen to ensure that, when fed ad
libitum, the high food/early JHAi group had consumed a supra-threshold
quantity of lettuce at JHAi [i.e. greater than 4.0 g dry mass as determined by
Juliano et al. (Juliano et al.,
2004)]. The timing of late JHAi was chosen to ensure that the low
food/late JHAi group also had consumed a supra-threshold quantity of lettuce
at JHAi when fed at the same rate as the low food/early JHAi group. The low
food/early JHAi group was the only sub-threshold feeding group at the start of
hormone treatments (Table
1).
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Animal rearing
Lubber grasshoppers Romalea microptera (Beavois) (=R.
guttata Houttuyn) were shipped from a lab colony at Illinois State
University in Normal, IL, USA (gift of D. W. Whitman). The colony was founded
with grasshoppers from Copeland, FL, USA. Juveniles were reared en
masse in screen cages with a 14 h:10 h L:D photoperiod at 32°C and
fed Romaine lettuce and oatmeal ad libitum. Newly molted females were
isolated and reared individually in 500 ml ventilated containers at a 14 h:10
h L:D photoperiod and a corresponding 32:24°C thermocycle.
Allatectomy procedure
The corpora allata (the sole source of adult JH; T. O. Barry, J.D.H. and D.
W. Borst, unpublished data) of all individuals were surgically removed
4–6 days after adult molt. The day before surgery, food was withheld.
Grasshoppers were cold anesthetized for 
1 h, fastened to the dissecting
dish with modeling clay, and the intersegmental neck membrane was opened with
a U-shaped incision. Two air sacs were removed, both corpora allata were
excised, a 25 µg dose of gentamicin sulfate (ICN Biomedicals, Irvine, CA,
USA) was placed in the open wound, and the neck membrane was folded back into
place.
Diet treatments and timing of juvenile hormone analog initiation
Our experimental goal was to test whether each group was competent to
respond to JH at the initiation of hormone treatment. Using this design, we
predict that individuals that were not competent to respond to JH at the
moment of JHAi should have later times of vitellogenin onset (Vg onset; the
first sampling date with detectable Vg) or oviposition.
Daily food rations were weighed fresh and all grasshoppers were always fed
fresh lettuce. The previously determined threshold was described as dry mass
(Juliano et al., 2004), so the
dry mass ingested at each meal was determined. Daily, each individual was
offered a specific amount of fresh lettuce. Several 5.0 g wet mass controls
were dried at 55°C and weighed to obtain a fresh-to-dry conversion factor.
Using this conversion factor, the dry mass offered was calculated. The next
day, each individual's uneaten food was collected, dried and weighed. The dry
mass uneaten was subtracted from the dry mass offered to determine the dry
mass eaten.
Juliano et al. found cumulative feeding, and not the feeding rate, to be
critical for commitment to oviposition
(Juliano et al., 2004).
Therefore, the important feeding variable to manipulate is the amount that has
been ingested when JH is restored. From adult eclosion to the day before
surgery, all individuals were fed 0.15 g dry mass of lettuce and 3–5
oatmeal flakes daily. Immediately following surgery, the grasshoppers began
their assigned diets. Allatectomized females ate low amounts of food (about
one-third that of unmanipulated females) and therefore took a longer time to
reach the feeding threshold. The feeding schedules were designed to produce a
sub-threshold feeding group (low food/early JHAi) and three supra-threshold
feeding groups at JHAi.
Hormone analog treatments and hemolymph sampling
Hormone replacement was achieved by applying methoprene (Sigma Chemical, St
Louis, MO, USA), an analog of JH (Nijhout,
1994; Flatt and Kawecki,
2007). Once the designated age was reached, a 5 µl hemolymph
sample was collected from each grasshopper and a topical application of 500
µg of methoprene in 10 µl of 95% ethanol was applied to the neck
membrane [as per Chinzei and Wyatt (Chinzei
and Wyatt, 1985) for locusts]. Hemolymph samples were acquired
once a day for the first 5 days after methoprene treatment initiation and
twice a week thereafter. All hemolymph samples were placed in 250 µl of
hemolymph buffer (Hatle et al.,
2001) and stored at –20°C for later analysis of Vg and
total protein. Twice a week until oviposition, methoprene was applied
immediately before hemolymph sampling. We repeatedly dosed grasshoppers with
500 µg methoprene to force all individuals into the same hormonal status
once hormone replacement was begun. This design has low power to separate the
requirements of JH for vitellogenesis from the requirements for oviposition.
However, it is excellent for testing our primary experimental goal, namely
determining the ability of the animals to respond to restored JH. By
artificially maintaining high levels of JH in all groups regardless of past or
current diet, effects from the individual's status at the time of JHAi (i.e.
sub- or supra-threshold) could be identified.
Oviposition
Females were allowed to oviposit in their cages as virgins. Lubber
grasshoppers will lay eggs without mating; if oviposition substrate is not
available, egg laying is delayed by 7 days but still occurs
(Mefferd et al., 2005). At
oviposition, the individual's age was recorded and it was removed from the
study. Laid eggs were counted; because egg size is largely fixed, number of
laid eggs is a good estimate of clutch mass (Moerhlin and Juliano, 1998;
Hatle et al., 2000).
Grasshoppers were dissected to measure the number of retained eggs, the number
of secondary oocytes and the size of secondary oocytes. Secondary oocytes
represent the current commitment to the second clutch. Lubber grasshoppers can
alter the number of eggs per clutch by resorbing oocytes, which would then not
contribute to clutch size. Laid eggs and fully developed retained eggs were
combined as the total number of developed eggs.
Together, secondary oocyte size and number indicate the investment in future reproduction. The number of secondary oocytes implies the potential for the mass of the ensuing clutch. The size of secondary oocytes implies the probable timing of the ensuing clutch, because oocytes need to grow to 1.0 cm to be ready for oviposition.
Hemolymph vitellogenin
Vitellogenin was measured by ELISA [modified from Borst et al.
(Borst et al., 2000)]. All
samples from an individual were analyzed concurrently, and groups were
analyzed alternately. The time of Vg onset for each individual was determined
by identifying the age at the first sample in which Vg was detectable. The
time of maximum Vg titer was determined by identifying the age at the sample
with the highest amount of Vg for each individual, throughout the oviposition
cycle. The maximum Vg titer is the point at which sequestering Vg into the
oocytes becomes favored over synthesizing Vg and exporting it into the
hemolymph (Hatle et al.,
2001). Individuals that showed detectable Vg prior to JHAi (likely
due to failed allatectomy) were removed from the study (N=5).
Hemolymph storage proteins
Total hemolymph protein was measured using the Bradford assay
(Bradford, 1976) with bovine
serum albumin standards. The amount of Vg in the same sample was subtracted
from this measure of total protein. Total non-Vg hemolymph protein is an
estimate of storage proteins, because 80% of non-Vg hemolymph protein
exists as three hexamerin storage proteins throughout the first oviposition
cycle (Hatle et al., 2001).
Hexamerins are a conserved family of storage proteins in insects
(Haunerland, 1996). The time
to storage protein maximum and the storage protein maximum were calculated in
the same way as in the Vg analysis.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Oviposition
The time from JHAi to oviposition was significantly affected by timing of
JHAi (ANOVA; F1=7.184; P=0.013) but not by diet
(F1=2.311; P=0.141) or the interaction of JHAi
and diet (F1=2.468; P=0.129). Early JHAi groups
had a longer period from JHAi to oviposition than did late JHAi groups
(Fig. 3). Notably, the low
food/early JHAi (sub-threshold) group did not have a longer period from JHAi
to oviposition than all three other groups.
Egg and oocyte production
The number of eggs was significantly affected by the timing of JHAi (ANOVA;
F1=5.488; P=0.027) but not by diet
(F1=1.081; P=0.308) or interaction
(F1=0.064; P=0.802). Early JHAi groups produced
fewer eggs than the late JHAi groups (Fig.
4).
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Upon dissection immediately following oviposition, the low food groups had fewer secondary oocytes than the high food groups (Fig. 5) (P=0.001). This was the only significant effect of diet in the entire experiment. The number of secondary oocytes was not affected by the timing of JHAi (P=0.732) or the interaction of diet and JHAi timing (P=0.173).
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Analysis of vitellogenin
Vitellogenin profile characteristics were significantly affected by the
timing of JHAi (MANOVA; Pillai's trace F4,21=6.918;
P=0.001) but not by diet (F4,21=2.754;
P=0.055) or interaction (F4,21=0.541;
P=0.708). For diet, all univariate P>0.10. Because diet
did not have a significant effect on Vg parameters, we combined the Vg
parameter data by diet groups for clearer graphical presentation
(Fig. 6).
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Our primary prediction (see last paragraph of Introduction) was that vitellogenesis would be delayed in females with sub-threshold food intake that were treated with JH (i.e. low food/early JHAi). Hence, the Vg onset data are particularly relevant to our hypothesis. The time from JHAi to Vg onset was not significantly affected by JHAi (P=0.051), diet (P=0.130) or interaction (P=0.493). The mean (± s.e.m.) times of Vg onset were: low food/early JHAi=15.5±2.1 days; low food/late JHAi=7.2±1.8 days; high food/early JHAi=16.0±3.9 days; and high food/late JHAi=10.2±2.9 days. The non-significant trend was for Vg onset to be delayed in all early JHAi groups, not only the low food/early JHAi group.
Storage proteins
Storage protein profiles were not significantly affected by the timing of
JHAi (Fig. 7) (MANOVA; Pillai's
trace F2,26=1.144; P=0.334), diet
(F2,26=0.175; P=0.841) or the interaction
(F2,26=0.202; P=0.819).
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|
DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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JH was sufficient for vitellogenesis, even with sub-threshold feeding
Due to differences in the timing of JHAi, the low food/late JHAi group
consumed 137% more food before JHAi than the low food/early JHAi group.
Similarly, the high food/late JHAi group consumed 59% more food before JHAi
than the high food/early JHAi group. Despite these large differences in
cumulative consumption, when JH was controlled, the only variable affected by
diet was the number of secondary oocytes. Previous work has repeatedly found
strong effects of diet on the timing of first oviposition, age at Vg maximum
and the number of eggs (Moehrlin and
Juliano, 1998; Hatle et al.,
2000; Hatle et al.,
2001; Hatle et al.,
2003a; Hatle et al.,
2003b; Hatle et al.,
2004; Juliano et al.,
2004). By controlling JH levels, the present paper suggests that
feeding for vitellogenesis is required only to produce adequate JH.
Our results suggest that attaining the threshold causes the release of JH.
In lubber grasshoppers, JH production is positively controlled by
allatotropins (Li et al.,
2005). The regulation of allatotropins is somewhat unclear. It may
be that attaining feeding thresholds are important in stimulating production
of allatotropins.
This demonstration of the dominance of JH over diet in vitellogenesis has
been conducted in a species for which a feeding threshold has been explicitly
established by two distinct approaches. Juliano et al. used constant feeding
rates and mathematical modeling to estimate the threshold as 4.0 g dry mass
cumulative feeding (Juliano et al.,
2004). Further, Moehrlin and Juliano used abrupt switches in food
availability to show that the timing of oviposition is unaffected by diet
level (short of starvation) after 14 days of full feeding
(Moehrlin and Juliano, 1998).
Further, lubber grasshoppers are appropriate for this experiment because JH
titers have been directly measured (Borst
et al., 2000; Hatle et al.,
2000), and the requirement of JH in Vg mRNA production is clear
(Hatle et al., 2000;
Fei et al., 2005). Hence, it
is appropriate to use an analog of JH in experiments with lubbers
(Zera, 2006).
Our experiment focused on the ability to commit to vitellogenesis, and
perhaps ultimately oviposition, after certain levels of feeding. Once we
restored gonadotropin (i.e. JH), we continued hormone treatments until
oviposition. A weakness of this design is the low probability of identifying
developmental plasticity between the initiation of vitellogenesis and
oviposition. Indeed, we failed to find effects of post-JHAi diets on
reproductive tactics, as could be expected with repeated methoprene
applications. At least a low level of developmental plasticity between the
initiation of vitellogenesis and oviposition seems likely. Indeed, complete
starvation starting at 20 days (i.e. after Vg onset but 2 weeks before
oviposition in well-fed grasshoppers) halts oocyte growth
(Fei et al., 2005).
Nonetheless, our experiment demonstrates that even sub-threshold females,
maintained on a low diet throughout adulthood, have the hormonal competence
and resources needed to initiate vitellogenesis and commit to oviposition if
JH is provided and maintained.
Undergoing vitellogenesis in the absence of adequate nutrition (as done by
the low food/early JHAi females in this experiment) implies that some cost
would be incurred. In grasshoppers, the investment presently allocated for
future reproduction can be observed at any point by measuring the size and
number of secondary oocytes (Sundberg et
al., 2001). However, both low food/early JHAi and low food/late
JHAi had fewer secondary oocytes, and low food/late JHAi grasshoppers had
supra-threshold feeding. Hence, the reduced number of secondary oocytes in low
food/early JHAi females likely does not represent a cost of reproduction in
response to insufficient nutrition.
The time from JHAi to Vg onset was statistically indistinguishable across groups; however, the low probability (P=0.051) suggests that a trend might exist. This trend was for Vg onset to occur later in both early JHAi groups, not only in the low food/early JHAi group as we predicted. These data on Vg onset are inconsistent with the notion that threshold feeding is needed for competence to JH.
Current reproduction was favored by late JHAi groups
The terminal investment hypothesis suggests that as life expectancy
decreases, favoring of current reproductive investment increases at the cost
of future reproduction (Williams,
1966; Hirshfield and Tinkle,
1975; Clutton-Brock,
1984). Our results are consistent with the terminal investment
hypothesis. We observed a trade-off between the timing of the first clutch and
the timing of the second clutch (as estimated by the length of secondary
oocytes). At the expense of delaying the production of their second clutch,
late JHAi individuals allocated more resources in less time to their first
clutch. By manipulating JH, we have demonstrated a developmental shift that
was previously undetected in experiments manipulating only diet (e.g.
Juliano et al., 2004;
Hatle et al., 2006a).
Vitellogenin profiles also tended to fit the predictions of the terminal
investment hypothesis. Taken together, our results suggest that lubber
grasshoppers can adjust reproductive tactics depending on their age, but this
control is secondary to JH, which is in turn subject to nutrition.
It was previously hypothesized that a threshold level of hemolymph storage
protein would serve as a physiological manifestation of the feeding threshold
(Hatle et al., 2003b;
Juliano et al., 2004).
Inconsistent with this hypothesis, sub-threshold feeding did not affect
initial storage protein titers [similar to Hatle et al.
(Hatle et al., 2006b)] or
response to JH. In fact, Hatle et al.
(Hatle et al., 2006a) found
that reproductive plasticity was affected more by the mass of the fat body
(which produces storage proteins and Vg) than by changes in storage protein
titers. In Drosophila, the fat body serves as a nutrient sensor,
regulating body growth (Colombani et al.,
2003). The fat body of grasshoppers may be playing a nutrient
sensing role in reproduction. We hypothesize that the fat body is more
critical to pre-reproductive development than are hemolymph storage
proteins.
Hormonal cue exceeded nutritional threshold
In other animals that exhibit growth-dependent thresholds for development,
the nutritional state or critical size induces development via
endocrine cues (e.g. Emlen and Nijhout,
1999; Davidowitz et al.,
2005; Truman et al.,
2006). This suggests that endocrine-producing tissues would
respond to some signal to make the hormonal signal and stimulate the
commitment to the next developmental stage (e.g.
Mirth et al., 2005). However,
it does not yield insight into whether or not the subsequent events will be
followed through without the actual nutritional state or critical size. The
present experiment suggests that hormones are more important than growth or
size thresholds, and individuals early in development are competent to respond
to developmental hormones, but simply have not yet attained sufficient levels
of these hormones. Further studies on other experimental systems are needed to
test the generality of this conclusion.
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Acknowledgments |
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