storage proteins in adult ants (camponotus festinatus): roles in colony founding by queens and in...

J. Insecr Physiol. Vol. 40, No. 8, 723-729, 1994 pp. Copyright 0 1994 Elsevier Science Ltd

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Storage Proteins in Adult Ants (Camponotus festinatus): Roles in Colony Founding by Queens and in Larval Rearing by Workers TERESA MARTINEZ,* DIANA E. WHEELER**?

Received 26 August 1993; revised 19 January 1994

Camponofusfisrinatus storage hexamers (Hex 1 and 2), first identilied in last instar larvae, constitute two major proteins in adult queens and broodless workers. We have examined the effects of colony founding by queens and larval rearing by workers on their storage protein content. Roth hexamerius accumulate in virgin queens, particularly Hex 2 in the fat body where it makes up about 70% of total soluble proteins. Colony founding causes a depletion of Hex 1 and 2 in queens. Levels of these proteins begin to decrease by the end of the claustral period when the first workers emerge, and they are depleted from fat body and hemolymph 1 month later. Larval rearing has an inhibitory effect on the accumulation of storage proteins in workers. Hex 1 occurs only in low concentrations in the hemolymph of 2- and Qweek-old workers kept with larvae, and disappears thereafter. Hex 2 does not accumulate in 2 to g-week-old workers kept with larvae. Our results with Camponotus queens support a role of the storage hexamers in egg development and/or nourishment of the brood. These data also suggest an important role of nutrition in the synthesis and accumulation of hexamerins in adult workers.

Storage protein Hexamerin Queen Colony founding Fat body

INTRODUCTION

Until recently, insect storage proteins have been con- sidered larval-specific proteins. Their presence in the adult stage of different species has only been recognized in the last few years. Storage proteins have been identified in adults of Drosophila melanogaster (Benes et al., 1990), Locusta migratoria (Wyatt, 1990; Wyatt et al., 1992), males of Triatoma infestans (Gonzalez et al., 1991), and diapausing adults of the bean bug, Riptortus clavatus (Miura et al., 1991) and Leptinotarsa decemlin- eata (Koopmanschap et al., 1992).

Sexual differences in the amounts of storage proteins have been reported in larvae of Lepidoptera, with the females containing larger quantities (reviewed in Wyatt, 1991). In R. cluvatus, a storage protein (cyanoprotein-1) has been found in egg extracts (Chinzei et al., 1992). These findings have suggested a role of storage proteins in reproduction. Their presence in adult males of some species, however, suggests additional functions in the adult.

We have isolated and characterized two storage hexamers (Hex 1 and 2) from larvae and adult workers of Cumponotus j&tin&us (Martinez and Wheeler, 1993).

*Department of Entomology, University of Arizona, Tucson,

AZ 85721, U.S.A.

tTo whom correspondence should be addressed.

Here we report an accumulation of these hexamers in founding queens and their decline during the claustral founding period. C. festinatus queens are claustral foundresses, that is they begin a new colony by seques- tering themselves in a chamber and rearing the first set of workers without seeking or obtaining additional food (Hiilldobler and Wilson, 1990).

We have previously reported an influence of larvae on the concentration of vitellogenin in the hemolymph of workers (Martinez and Wheeler, 1991a). In ant colonies, young workers take care of the brood and transfer nutrients, in particular amino acids, to developing larvae (Howard and Tschinkel, 1981; Sorenson and Vinson, 1981). In the present study, we analyze the influence of larval rearing on workers isolated from the colony, to examine a possible effect of nutrition on the accumulation of storage hexamers in Cumponotus adults.

MATERIALS AND MRTHODS

Insects

General. Camponotus festinatus colonies were maintained in plastic boxes at 30°C and fed a diet consisting of fresh-frozen cockroaches (Nuuphoeta cinerea) and a solution of honey, vitamins and minerals. Test tubes half-filled with water and plugged with cotton provided a humid nest environment.

723

124 TERESA MARTINEZ and DIANA E. WHEELER

Founding queens. Queens were captured on their mating flight during the summer, placed in test tubes plugged with damp cotton, and maintained under the same conditions as larger colonies. A sample of foundresses (n = 79) was weighed the day after capture and again after the first workers emerged. No food was provided prior to eclosion of the first brood. Samples of hemolymph and fat body were collected from mated queens at the time the first eggs were laid, and 1, 2, 3, and 4 weeks later. The first eggs were laid within 48 h after mating, and the first workers emerged 4 weeks later. Queens that were collected at the same time as the mated individuals but did not lay eggs were used as virgin controls. Hemolymph and fat body samples were taken at the same time points as for mated queens, and lack of sperm in their spermathecae was confirmed. Food was provided to some virgin and mated queens 1 week after the first workers emerged. Hemolymph and fat body from those queens were collected 2 and 4 weeks later, at 7 and 9 weeks after mating. Four virgin and mated queens were analyzed for each time period.

Queenless workers. Newly emerged adults were re- moved from the parent colony and placed in two petri dishes (140 mm dia) with 40 individuals each. Larvae (4th-5th instars) were added to one group while the other was made up only of workers. Larvae were replaced before pupation.

Hemolymph and fat body samples were collected from these queenless workers at 2, 4, 6, and 8 weeks after eclosion. Four individuals of each experimental group were sampled each time period.

Sample preparation

Hemolymph was collected in glass capillary tubes through a dorsal incision in the thorax. The perivisceral fat body was dissected from the abdomen in Grace’s medium. All samples were stored immediately at - 70°C and maintained at this temperature until use. Individual fat bodies were homogenized in Tris-buffered saline (20mM Tris, 150mM NaCl, 5 mM EDTA, pH 7.5) containing the following protease inhibitors: 1 mM phenylmethylsulfonyl fluoride (PMSF), 5 mM benza- midine, 0.7 PM pepstatin A, 8 ,uM chymostatin, 10 PM leupeptin, 8 PM antipain, and 0.8 PM aprotinin (Tsuchida and Wells, 1990). Fat body homogenates were centrifuged at 12,OOOg for 20 min at 4°C. The super- natant or an aliquot was used for polyacrylamide gel electrophoresis and immunochemical analysis.

Polyacrylamide gel electrophoresis

SDS-PAGE was performed according to Laemmli (1970) in 615% gradient or 7.5% acrylamide gels. The 7.5% gels produced good separation of the two hexamers when sample load was moderate. Electrophoresis was conducted at 20mA constant current. Gels were stained with 0.1% Coomassie Brilliant Blue R 250 in 50% methanol and 10% acetic acid. In order to get an estimation of the concentration of storage hexamers in the hemolymph and fat body, 7.5% acrylamide gels were

scanned with a laser densitometer (LKB 2222-020, Ultrascan XL).

Immunology

Rabbit antisera against C. festinatus storage hexamers (Hex 1 and 2) were obtained as described previously (Martinez and Wheeler, 1993). Samples of hemolymph and fat body from queens and workers were subjected to SDS-PAGE, and the proteins electrophoretically trans- ferred to nitrocellulose (Polyblot, American Bionetics, Emeryville, CA). The membrane was incubated with the specific antiserum, and goat anti-rabbit IgG-conjugated alkaline phosphatase was used as the detection agent.

RESULTS

Eflect of colony founding on the storage proteins of queens

Camponotus storage hexamers (Hex 1 and 2), first identified in last instar larvae (Martinez and Wheeler, 1993), were also present in adult queens. The immuno- logical relationship with the larval hexamers was confirmed with antibodies raised against the larval proteins (Fig. 1). Hex 1 constituted a major hemolymph protein of unmated queens, together with vitellogenin and lipophorin (Fig. 2). Hex 2 particularly accumulated in large quantities in the queen fat body, making up about 70% of total soluble proteins (Figs 1 and 2).

In mated queens, the concentration of Hex 1 in the hemolymph began to decrease about 3 weeks after mating. Hex 1 was either absent or barely detectable in these queens after 7 weeks (Fig. 3) and absent by 9 weeks. Hex 2 remained in large amounts in the fat body of queens for several weeks after mating. However, 3 to 5 weeks after the first workers had emerged (7-9 weeks after mating) Hex 2 was found in concentrations 10 to 25-fold lower than those found in virgin queens. In some mated females, the fat body was depleted of Hex 2 9 weeks after they laid their first eggs (Fig. 4). In this latter

anti-Hex 1 anti-Hex 2

FIGURE 1. Immunoblot of Cumponorus storage hexamers (Hex 1 and 2) from a virgin queen. H, hemolymph, FB, fat body. Antibodies raised against larval Hex 1 and 2 were diluted to I: 10,000 and 1: 5000,

respectively.

Hexlw

STORAGE PROTEINS IN ADULT ANTS 12

day 1

NIV MV

<Hex2

FIGURE 2. Electrophoretic pattern of hemolymph (H) and fat body

soluble proteins (FB) from C. festinatus queens showing the two

storage hexamers (Hex 1 and 2). Samples were prepared on the day the

mated queens laid their first eggs (day 1). 0.25 ~1 hemolymph was used

per sample. The perivisceral fat body was dissected out from the

abdomen and homogenized in 100 ~1 buffer (see text for details). 10 ~1

of the supematant were used per sample. M, mated queen; V, virgin

queen; Vg, vitellogenin.

case, whole fat body extracts were analyzed to confirm the absence of Hex 2. It is important to note that depletion continued even though queens received regular feedings after the first workers had emerged. In virgin queens, the concentration of the two storage proteins remained high during the entire period studied, in particular that of Hex 2 in the fat body.

During colony founding, queens lost a large pro- portion of their body weight. Queens weighed an average of 40.0 mg (f3.8) just after their mating flight and 28.4 mg (k4.1) after workers emerged. They lost an average of 27.3% (k7.9) of their initial wet weight (range: 9.5550.7%). A portion of this loss may be attributed to depletion of the two storage hexamers.

Effect of larvae on the accumulation of storage proteins in workers

Camponotus hexamerins were found to accumulate in the hemolymph and fat body of workers maintained in isolation from the colony (queen and brood). Rearing of larvae had an inhibitory effect on the accumulation of storage proteins in queenless workers. Immunoblots of fat body from workers maintained with larvae showed no accumulation of Hex 2 through- out the 2- to g-week period after eclosion (Fig. 5). Hex 1 was found only in low concentrations in the hemolymph of 2- and 4-week-old workers, com- parable to those of newly emerged adults (Fig. 6). No Hex 1 accumulated in 6- or 8-week-old individuals (Fig. 5). In contrast, in queenless workers isolated from larvae, storage proteins reached concentrations about IO-fold higher in the hemolymph (Hex 1) and about 50-fold higher in the fat body (Hex 2), compared to those characteristic of newly emerged adults (Fig. 6).

DISCUSSION

The accumulation of storage proteins has been best documented in the last larval stage of holometabolous species (Telfer and Kunkel, 1991). The imbalance be- tween resources required and accessibility of food is extreme during metamorphosis since the pupal stage cannot feed during a time when massive restructuring of the body takes place. In a general sense, storage proteins are synthesized and accumulated during periods when the intake of nutrients exceeds their use, and they are subsequently depleted during periods when demand exceeds intake. In addition to metamorphosis, there are other circumstances in which this capacity for storage and use can be advantageous to insects. Two such cases of storage protein accumulation and use in adult insects are reported here for the ant Camponotus festinatus.

day 1 lwk 2wk 4wk 7wk 9 wk

Hex1 w

FIGURE 3. Immunoblot of C. festinatus Hex 1 from queen hemolymph. M, mated queen; V, virgin queen. Day 1 corresponds

to the day mated queens laid their first eggs. The number of weeks after that date is indicated on top. 0.25 ~1 hemolymph

was used per sample. Anti-Hex 1 was diluted to 1: 10,000.


day1 1 wk 2 wk 4wk 7wk 9wk t I

FIGURE 4. Immunoblot of C. festinatus Hex 2 from queen fat body. M, mated queen; V, virgin queen. Day I corresponds to the day mated queens laid their first eggs. The number of weeks after that date is indicated on top. The abdominal fat body from individual queens was homogenized in 100 ~1 buffer and 5 ~1 of the supematant were used per sample. Anti-Hex 2 was

diluted to 1: 5000.

Founding queens

In claustral founding, the predominant mode of start- ing new colonies in ants (Holldobler and Wilson, 1990) queens seal themselves in a chamber, lay eggs, and rear the first set of workers entirely from their internal reserves. Claustral colony founding rivals metamorphosis in the level of protein demand combined with the absence of supplementary nourishment.

Weight loss during colony founding is an indication of depletion of body reserves. In ants with queens that found singly, wet weight loss ranges from an average of 16% in Camponotus lignaperda to over 50% in Solenop- sis invicta (Toom et al., 1976; Keller and Passera, 1990). In comparison, Camponotus festinatus queens lose a moderate amount of weight (27%). In ants, protein for rearing the first brood is believed to be captured from the amino acids released by histolysis of the flight muscles. After the mating flight, queens break off their wings and their flight muscles quickly degenerate (Janet, 1907; Jones, 1979; Holldobler and Wilson, 1990). The two storage proteins identified in queens of Camponotus festinatus, which are present prior to and depleted during colony founding, represent a previously unrecognized resource for foundresses.

Both the storage proteins and the flight muscle prob- ably contribute amino acids for the production of the first group of workers. The demand for protein should increase as larvae grow larger and approach metamorphosis. Our data, together with evidence from other ant species (Jones, 1979; Cannon, 1990), suggest that flight muscle tends to be used first and then the storage proteins. In Solenopsis invicta, muscle breakdown begins within a few hours of insemination, and peripheral fibers have completely broken down by 36 h. After 20 days, no structural trace of flight muscle remains (Jones, 1979). Data from Camponotus pennsylvanicus indicate that, during colony founding, weight is first lost from the thorax and then from the gaster (Cannon, 1990). In C.

festinatus, levels of Hex 1 and 2 appear to be maintained during the first 2-3 weeks of the 4 week claustral period. Both storage proteins begin to be depleted during the latter part of this period, and the levels continue to drop during the first weeks following worker emergence.

Workers

Ant colonies are generally long-lived, with l&20 years being typical (Porter and Jorgensen, 1988; Holldobler and Wilson, 1990; Pamilo, 1991), and species in which queens are replaced can have colonies that are perpetual. Seasonal variation in food availability in the environment provides an appropriate background for selection of annual cycles of storage and use. One type of storage is internal, in fat body, which can accumulate fat, protein and glycogen. The phenomenon of adipogastry (fat body hypertrophy) has been noted previously in Formica japonica (Kondoh, 1968), two species of nocturnal Cam- ponotus from the Caucasus and North Africa (Emery, 1898), Camponotus sp. from the Namib Desert (Tschinkel, personal communication), and Prenolepis imparis (Tschinkel, 1987). Interestingly, all three of these genera belong to the subfamily Formicinae. In the case of Camponotus festinatus, a North American nocturnal, desert-dwelling species, the fat body of adult ants can store protein (Martinez and Wheeler, 1991 b), as well as lipid and carbohydrate (Rose11 and Wheeler, unpublished results), in large quantities. We have focused on protein storage, which has been consistently overlooked in studies of nutrient reserves in queens and workers (e.g. Keller and Passera, 1989; Martin, 1991; Lauchaud et al., 1992).

Our laboratory colonies of Camponotus festinatus undergo a period of reduced brood production during the winter, even though they are maintained at a constant temperature, food is supplied in a constant pattern, and light cycles are not programmed to track seasonal trends. During this period of quiescence, the fat body of


workers, especially soldiers, tends to hypertrophy. Although the cause of reduced brood production is unknown, the results reported here suggest a mechanism for an annual cycle of alternating brood production and fat body hypertrophy in workers. In the presence of larvae, adult workers store neither hexamerin. Without larvae to feed, however, workers accumulate both proteins (Figs 5 and 6). Studies on food flow within colonies of other ant species indicate that dietary protein moves preferentially towards the larvae and the queen while carbohydrates and fats move preferentially into the workers (Eisner and Wilson, 1958; Markin, 1970; Soren- son et al., 1981, 1983). Without larvae, as in the case of Camponotus, dietary protein appears to be converted to and stored in the form of hexameric proteins.

A similar but more pronounced example of alternating periods of fat body hypertrophy and brood production is found in Prenolepis imparis, a formicine ant in which the fat body of many workers becomes enlarged in the spring, when the colony is foraging but no brood

205 -

116-

80-

2 wk 4 wk

is present. After a period of quiescence in the summer, brood appears before winter foraging begins and their presence is correlated with the depletion of the workers’ fat body reserves (Tschinkel, 1987).

The potential importance of storage proteins in the adult stage of insects has only recently been pointed out (Telfer and Kunkel, 1991; Wyatt, 1991, Chinzei et al., 1992). Camponotus festinatus presents two situations during colony development and maturation in which adult insects store and use hexameric proteins. First, virgin queens in this claustrally founding species store large quantities of protein, particularly in the fat body. This protein supply is partially depleted during the claustral period, when the first set of worker ants is produced from stored reserves, and the period immediately following worker emergence when new food is just beginning to be brought into the colony. A preliminary survey of other ant species indicates that protein storage by virgin queens is common (unpublished data). Second, workers in C. festimztus store two hexameric proteins,

6 wk 8 wk

N Hex 1

*Hex 2

FIGURE 5. lmmunoblot of C. festinarus storage hexamers (Hex I and 2) from adult queenless workers. +L, workers

maintained with larvae; H, hemolymph; FB, fat body. Numbers at the top indicate the adult age in weeks. 0.25 ~1 hemolymph

used per sample. Fat body samples correspond to whole individual fat bodies. Molecular weight markers are shown on the

left (kDa).


FIGURE 6. Electrophoretic pattern of hemolymph (H) and fat bo dy (FB) of a newly emerged worker (day 1) and an g-week-old queenless worker (8 wk). 0.5 ~1 hemolymph was used per sample. Fat body

samples correspond to whole individual fat bodies.

day 1 8wk

FB H

when larvae are absent or present only in low numbers. Protein does not accumulate when larvae are present. Such seasonal storage of protein by workers could sustain colonies during inclement seasons and enhance the production of eggs and larvae, without the require- ment of newly foraged food.

In summary, our results with founding queens of Cumponotus support a role of storage hexamers in egg development and/or nourishment of the brood. In addition, the inhibitory effect of larvae on the storage proteins of workers suggests an important role of nutrition in the synthesis and accumulation of this class of proteins in the adults. Deprivation of nutrients is associ- ated with the inhibition of storage protein synthesis in larvae of other insects, such as Bombyx mori (Tojo et al., 1981) and Munduca sextu (Webb and Riddiford, 1988).

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storage proteins in adult ants (camponotus festinatus): roles in colony founding by queens and in...

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