Journal of Insect Physiology 56 (2010) 271–276

Reduced female mating receptivity and activation of oviposition in twoCallosobruchus species due to injection of biogenic amines

Takashi Yamane *, Takahisa Miyatake

Laboratory of Evolutionary Ecology, Graduate School of Environmental Science, Okayama University, Tsushima-naka 1-1-1, Okayama 700-8530, Japan

A R T I C L E I N F O

Article history:

Received 4 June 2009

Received in revised form 26 October 2009

Accepted 26 October 2009

Keywords:

Biogenic amine

Tyramine

Receptivity

Oviposition

Callosobruchus

A B S T R A C T

Analyses of proximate mechanisms that control mating and oviposition behaviours in insects are

important because they link behavioural ecology and physiology. Recently, seed beetles have been used

as models to study evolution of female multiple mating and cost of reproduction including mating. In the

present study, we investigated the effects of biogenic amines into the abdomens of females of two

Callosobruchus species, Callosobruchus chinensis and Callosobruchus maculatus, on mating receptivity and

oviposition behaviour. In C. chinensis, injection of octopamine and tyramine reduced receptivity to

mating and tyramine and serotonin increased the number of eggs laid. Similarly, injection of tyramine

reduced the receptivity of females and increased the number of eggs laid by females of C. maculatus.

These results show the possibility that biogenic amines control mating receptivity and oviposition

behaviour in females of two Callosobruchus species.

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1. Introduction

Females usually lay eggs after receiving seminal fluids includingsperm during mating. Females of some insect species exhibitreduced receptivity after mating for a period of time, in extremecases until death (Chen, 1984; Gillott, 1988; Eberhard, 1996;Chapman et al., 1998). These changes in oviposition behaviour andreduction of receptivity of females are caused by components ofseminal fluids, the sperm itself, and mechanical stimulation(Eberhard, 1996; Chapman et al., 1998; Miyatake et al., 1999;Simmons, 2001; Wedell, 2005).

Biogenic amines are physiologically neuroactive substancesthat affect behavioural and physiological traits in vertebrate andinvertebrate animals, and they act as neurotransmitters andendocrine disruptors in the central and peripheral nervoussystems (Evans, 1980; Blenau and Baumann, 2001). Several rolesof monoamines in mating and oviposition in insects have beenreported: octopamine and tyramine regulate egg-laying inDrosophila melanogaster of Diptera (Monastrioti et al., 1996;Monastirioti, 2003; Cole et al., 2005), octopamine, tyramine andserotoinin regulate the muscle contractions in female reproduc-tive organs in Locusta migratoria (Clark and Lange, 2002, 2003;Donini and Lange, 2004; da Silva and Lange, 2008); and dopamineand tyramine accelerate ovarian development in reproductiveworkers in Hymenoptera (Dombroski et al., 2003; Sasaki and

* Corresponding author.

E-mail address: dev18205@s.okadai.jp (T. Yamane).

0022-1910/$ – see front matter � 2009 Elsevier Ltd. All rights reserved.

doi:10.1016/j.jinsphys.2009.10.011

Harano, 2007; Sasaki et al., 2009). Few studies, however, havereported the effects on female mating receptivity in insects,except for the report that the production of bombykol, the sexualhormone of Bombyx mori females, seemed to be regulated bytyramine (Hirashima, 2008).

In Coleoptera, reduction of female receptivity after mating isreported in some species of Bruchidae, including Callosobruchus

maculatus (Eady, 1995) and Callosobruchus chinensis (Miyatake andMatsumura, 2004). In these two Callosobruchus species, costs andbenefit of females in reproduction are complex, and the interests ofeach sex in mating are considered from the viewpoint of sexualconflict between sexes (Crudgington and Siva-Jothy, 2000; Eadyet al., 2004, 2007; Edvardsson and Tregenza, 2005; Ronn et al.,2006; Harano et al., 2006; Sakurai and Kasuya, 2008).

Unlike the above evolutionary ecological studies, in the presentstudy we investigated the possible effects of monoamines onfemale mating behaviour and oviposition in Callosobruchus, byinjecting them into the female abdomen and examining the effecton reductions in receptivity to mating and oviposition behaviour,from a physiological standpoint.

2. Materials and methods

2.1. Insects and culture

We used a strain of C. chinensis, referred to as the jC strain, thatwas established in 1936 and is maintained in our laboratories(Utida, 1941a,b, see also Harano and Miyatake, 2005) and the strainof C. maculatus, referred to as the hQ strain (Miyatake and

Fig. 1. Receptivity of Callosobruchus chinensis females to Milli-Q water as the control

(N = 30), or solution of dopamine (N = 29), octopamine (N = 30), tyramine (N = 30),

or serotonin (N = 30) at 3–4 h after injection. The same letters on each bar indicate

no significant difference by the sequential Bonferroni method (Rice, 1989) at 5%

significant level after x2-tests.

Table 1Repeated-measures one-way ANOVA of the eggs laid by Callosobruchus chinensis

females after amine injection.

Source df Mean squares F P

Between-subject

Amine 4 105.24 14.30 <0.001

Error 486 22.81

Within-subject

Day 1.19 10.21 10.21 0.001*

Day x amine 4.78 1.42 1.42 0.012*

Error 90.76 1.71

* Corrected P, Greenhouse-Geisser e= 0.2388.

T. Yamane, T. Miyatake / Journal of Insect Physiology 56 (2010) 271–276272

Matsumura, 2004). These cultures were maintained in a chamber(Sanyo, Tokyo, Japan) kept at 25 8C, 60% RH, and 16L8D conditionsat the density about 100 adults per plastic Petri dish (1.5 cm height,9.1 cm diameter). All beetles used for the experiments were rearedin adzuki beans (Vigna angularis ‘Dainagon’) from eggs laid byparents randomly collected from the stock culture. Mated femaleswere allowed to lay one egg per adzuki bean. If more than one eggwas laid on a bean, excess eggs were scraped off with forceps. Eachbean was transferred to a separate 48-well tissue culture plate(Greiner Bio-One, Frickenhausen, Germany) and kept in thechamber described above. Virgin males and females emergingfrom these beans were collected.

2.2. Injection of biogenic amines

Virgin females (body weight, C. chinensis: 5.87 � 0.10 mg(N = 30); C. maculatus: 5.95 � 0.12 mg (N = 25)) 1–4 days old werechilled on ice for a few minutes and fixed to agarose medium by usingfine forceps. A hole was made between the second and fifth segmentsof the ventral abdomen with forceps, and an amine solution wasinjected using a fine glass capillary whose tip was as thin as possibleconnected to an oil pressure injection machine (Nanoject Auto-nanoliter injector, Drummond Scientific Company, Broomall, PA, USA)under a microscope. Each amine, dopamine (Nacarai, Kyoto, Japan),octopamine (Nacalai Tesque, Kyoto, Japan), tyramine (Sigma–Aldrich,Tokyo, Japan), or serotonin (Sigma–Aldrich, Tokyo, Japan), wasdissolved in Milli-Q water, respectively, at a concentration of 10%(dopamine, octopamine: 0.53 M, tyramine: 0.58 M) except forserotonin (2%: 0.05 M). Serotonin dissolves with difficulty in waterand more than 2% serotonin solution could not be made. To examinethe dose-dependency of their effects, octopamine and tyraminesolutions were also injected at 10%, 5%, and 1%. An amine solution(0.05 ml) was injected into each female, and the same amount ofMilli-Q water was injected into females as control. Injection wasconducted in a laboratory kept at 25 8C. A few hours after theinjection, the female and a virgin male were placed in a small plasticPetri dish (1.5 cm height, 3.0 cm diameter) kept in the chamberdescribed above, and whether female mates or not for 1 h. Femaleshave mature eggs in their oviducts and bursa copulatrix when theyemerged from bean, and 3–6-day-old virgin females have enoughmature eggs in both C. maculatus (Wang and Horng, 2004) and C.

chinensis (Yamane, personal observation). Therefore, they shouldalready develop ovaries at mating. In addition, they lay immediatelyafter mating with males. So it is thought that they enhance egg-layingafter mating. To measure the number of eggs laid by females, virginfemale injected with biogenic amine and an adzuki bean wereimmediately transferred after injection to a separate 24-well tissueculture plate (Nalge Nunc International K.K., Tokyo, Japan), and thenumbers of eggs laid on a bean in each 24-h period was counted for 5days. If eggs were laid on a bean, the bean was replaced with a newone.

2.3. Statistics

To compare female mating receptivity among treatments, thesequential Bonferroni methods (Rice, 1989) were applied after thex2-test at the 5% significance level. StatView Version 5.0 (SASInstitute, 1998) was used for x2-tests.

Numbers of eggs were compared using repeated-measures one-way ANOVA with ‘‘amines’’ as the between-subject factor and‘‘days after injection’’ as the within-subject factor. BecauseMauchly’s test indicated a significant violation of the assumptionof sphericity (P < 0.001), significant levels for within-subjecteffects were calculated using a Greenhouse-Geisser test for thedegrees of freedom (Quinn and Keough, 2002). Separate one-wayANOVA tests were applied to the differences among amines. When

a significant interaction effect was encountered between-subjectand within-subject, separate one-way ANOVA tests were appliedto the differences among amines on each day. Tukey–Kramer testswith sequential Bonferroni corrections were performed to assessdifferences among amines when significant effects were detectedin the separate one-way ANOVA. The level of statistical significancewas set at P < 0.05. JMP Version 6.0.3 (SAS Institute, 2005) wasused for a series of analyses.

3. Results

Injection of octopamine or tyramine solutions significantlyreduced female receptivity compared to controls in C. chinensis,whereas no differences were found between injections of controland dopamine or serotonin solutions and the control (Fig. 1).Injection of 5% or 10% octopamine solution significantly reducedfemale receptivity compared to 1% solution or control, but nodifference in receptivity was found between the control and 1%solution or between 5% and 10% solutions (Fig. 2a). Injection of 5%or 10% tyramine solutions significantly reduced female receptivitycompared to the control or 1% solution, whereas no difference inreceptivity was found between the control or 1% solution orbetween 5% and 10% solutions (Fig. 2b). These results suggest thatthe effects of these amines on reduction of female receptivity aredose-dependent in C. chinensis.

Fig. 3 shows the total number of eggs laid by C. chinensis femalesinjected with Milli-Q water (control), dopamine, octopamine,tyramine, or serotonin solutions. A repeated-measures one-wayANOVA for the eggs laid by injected females revealed that ‘‘amines’’as between-subject, and ‘‘days after injection’’ and by ‘‘amineinteraction’’ effects were all significant factors affecting thenumber of eggs laid (Table 1). Therefore, separate one-wayANOVA tests were applied to the differences among amines in eachday. The number of eggs laid differed significantly among amine

Fig. 2. Receptivity of C. chinensis females to Milli-Q water as the control (N = 25), or

1% (N = 25), 5% (N = 25), or 10% (N = 26) octopamine solution at 3–4 h after injection

(a), receptivity of females to Milli-Q water as the control (N = 30), or 1% (N = 25), 5%

(N = 25), or 10% (N = 25) tyramine solution at 3–4 h after injection (b). The same

letters on each bar indicate no significant difference by the sequential Bonferroni

method (Rice, 1989) at 5% significant level after x2-tests.

Fig. 4. Receptivity of C. maculatus females injected with Milli-Q water as the control

(N = 25), or solution of dopamine (N = 25), octopamine (N = 25), tyramine (N = 24),

or serotonin (N = 25) at 3–4 h after injection. The same letters on each bar indicate

no significant difference by the sequential Bonferroni method (Rice, 1989) at 5%

significant level after x2-tests.

Fig. 5. Receptivity of C. maculatus females with Milli-Q water as the control (N = 22)

or 1% (N = 20), 5% (N = 18), or 10% (N = 22) tyramine solution at 3–4 h after injection.

The same letters on each bar indicate no significant difference by the sequential

Bonferroni method (Rice, 1989) at 5% significant level after x2-tests.

T. Yamane, T. Miyatake / Journal of Insect Physiology 56 (2010) 271–276 273

treatments for the first (one-way ANOVA, F4,171 = 3.55, P = 0.0083),second (F4,171 = 4.97, P = 0.0008), third (F4,171 = 5.89, P = 0.0002),fourth (F4,171 = 6.65, P < 0.0001) and fifth day (F4,171 = 7.65,P < 0.0001). Tyramine solution significantly increased the numberof eggs from day 1 and serotonin solution did so in 5 days afterinjection compared to the control (Tukey–Kramer test, P < 0.05).Injection of dopamine or octopamine did not change the number ofeggs laid by females.

Injection of tyramine solution significantly reduced femalereceptivity compared to the control in C. maculatus (Fig. 4). On

Fig. 3. Total number of eggs (mean � SE) laid by C. chinensis females injected with

Milli-Q water as the control (N = 18), or solution of dopamine (N = 15), octopamine

(N = 18), tyramine (N = 17), serotonin (N = 18) at 1–5 days after injection. The same

letters on each bar indicate no significant difference (P < 0.05, one-way ANOVA:

Tukey–Kramer test).

the other hand no differences were found in receptivity betweencontrol and dopamine, octopamine, and serotonin. Injection of 5%and 10% tyramine solutions significantly reduced female receptivitycompared to the control or 1% solution, whereas no difference inreceptivity was found between the control and 1% treatment orbetween 5% and 10% treatment in C. maculatus (Fig. 5).

Fig. 6 shows the total numbers of eggs laid by C. maculatus

females injected with Milli-Q water (control), dopamine, octopa-

Fig. 6. Total number of eggs (mean � SE) laid by C. maculatus females injected with

Milli-Q water as the control (N = 17), or solution of dopamine (N = 18), octopamine

(N = 19), tyramine (N = 18), serotonin (N = 18) at 1–5 days after injection. The same

letters among each amine indicate no significant difference (P < 0.05, one-way

ANOVA: Tukey–Kramer test).

Table 2Repeated-measures one-way ANOVA of the eggs laid by Callosobruchus maculatus

females after amine injection.

Source df Mean squares F P

Between-subject

Amine 4 19.92 11.43 <0.001

Error 480 1.74

Within-subject

Day 2.18 4.26 4.26 0.013*

Day�amine 8.72 1.42 1.42 0.184*

Error 170.12 0.88

* Corrected P, Greenhouse-Geisser e= 0.436.

T. Yamane, T. Miyatake / Journal of Insect Physiology 56 (2010) 271–276274

mine, tyramine or serotonin solution. A repeated-measures one-way ANOVA revealed that ‘‘amines’’ as between-subject, and ‘‘daysafter injection effects’’ were significant factors affecting thenumber of eggs laid, but ‘‘days after injection’’ by ‘‘amineinteraction effect’’ was not (Table 2). Therefore, separate one-way ANOVA tests were applied to the differences among amines.Separate one-way ANOVA tests revealed that tyramine solutionsignificantly increased the number of eggs compared to controls(Tukey–Kramer test, P < 0.05, Fig. 6), but dopamine, octopamineand serotonin did not significantly increase the number of eggs laidby females compared to controls in C. maculatus.

4. Discussion

Insect behaviours and physiology are regulated by biogenicamines (e.g. Libersat and Pfluger, 2004; Fahrbach and Mesce, 2005;Roeder, 2005). The present result is the first report suggesting thepossibility that biogenic amines have roles in reduction of femalemating receptivity and activation of oviposition in Coleopteraspecies. That is, injection of tyramine and octopamine solutionsdepended on concentration in reduction of female receptivity in C.

chinensis (Figs. 1 and 2a,b) and tyramine did so in C. maculatus

(Figs. 4 and 5). But, it may be due to low concentration that both C.

chinensis and C. maculatus females did not reduce their receptivityin case of serotonin injection. These results suggest thatconcentration of biogenic amines in a body is related to changesof female mating receptivity. However, these amines are known tobe neurotransmitters and neuromodulators functioning in thevicinity of releasing neurons. Injected substances might substituteor disrupt such functions.

In addition, other behavioural states such as starvation andstress may change in monoamine content, and may affect femalereceptivity. Starvation, an oxidative stress, and a mechanical stresschange monoamine, dopamine contents and these cause thechange of sexual receptivity and ovarian development in D.

melanogaster females (Neckameyer and Weinstein, 2005). There-fore, in this study, it is shown the possibility that the changes ofmonoamine content are capable of affecting females receptivityand egg-laying behaviour. These behavioural changes are affectedby stress such as starvation via changes of monoamine contents.

In Drosophila species, octopamine regulates ovulation inreproductive organs (Monastrioti et al., 1996; Monastirioti,2003), and tyramine, the precursor of octopamine, regulates eggretention in ovaries (Cole et al., 2005). Octopamine (Clark andLange, 2003) and tyramine (Donini and Lange, 2004; da Silva andLange, 2008) modulate muscle contraction in the spermatheca andoviduct, and serotonin (Clark and Lange, 2002) modulates musclecontraction in the spermatheca of female L. migratoria, suggestingtheir roles in egg-laying process. In addition, tyramine plays a rolein ovarian development in European honey bees (Sasaki andHarano, 2007; Thompson et al., 2007). In the present study,injection of tyramine increased the number of eggs laid by femalesfrom day 1 and injection of serotonin did so 5 days after injection in

C. chinensis. Similarly, injection of tyramine increased the numberof eggs laid by females in C. maculatus. Considering these results,tyramine and serotonin may play some roles in egg-laying processof females in C. chinensis, and tyramine may do in C. maculatus.Tyramine is an intermediate product required for octopaminesynthesis (Roeder, 2005) and an enzyme, tyramine-b-hydroxylase(TbH) converts tyramine to octopamine. Recently, the Tbh genewas characterized in D. melanogaster (Monastrioti et al., 1996;Monastirioti, 2003). Therefore, octopamine was synthesized frominjected tyramine by TbH and it may act on female’s receptivityand egg-laying in C. chinensis and C. maculatus.

Male seminal fluids consist of various components, and thesecomponents possess physiological functions that affect femalemating behaviour (Gillott, 1988, 2003). For example, accessory glandpeptides and/or proteins (Acps) reduce receptivity and stimulate eggproduction and laying in females of Drosophila species including D.

melanogaster (Chen et al., 1988; Aigaki et al., 1991; Wolfner, 1997;Kubli, 2003). Prostaglandin itself (B. mori: Yamaja Setty andRamaiah, 1980), and prostaglandin synthetase and arachidonic acidin the male spermatophore are transferred to females during matingand synthesize prostaglandin which activates egg-laying (Acheta

domesticus: Destephano and Brady, 1977; Teleogryllus commodus:Loher, 1979; Loher et al., 1981; Stanley-Samuelson and Loher, 1983;Stanley-Samuelson et al., 1986). In other cases, juvenile hormone isthought to influence female’s reproductive behaviour when it istransferred to females (Webster and Carde, 1984; Borovsky et al.,1994; Park et al., 1998) and/or when it is synthesized by Acpstransferred to females’ reproductive organs (Chen et al., 1988; Aigakiet al., 1991; Moshitzky et al., 1996; Wolfner, 1997; Fan et al., 2000;Kubli, 2003; Gillott, 2003).

In Coleoptera, there are chemical substances in male sperma-tophore that stimulate oogenesis of Acanthoscelides obtectus

(Huingnard, 1983) and Caryedon serratus (Boucher and Huingnard,1987). In A. obtectus, especially, two types of male secretionspassing into the female’s haemolymph after mating enhancefecundity (Huignard et al., 1977). Low-molecular-weight secre-tions increase ovarian activity during the first 24 h followingmating (Huignard, 1975), whereas high-molecular-weight sub-stances, which are considered to be proteins or mucopolysacchar-ides, appear in measurable quantities in the female haemolymphonly 16–24 h following mating (Huignard, 1974). In other species,the substances in the male ejaculate that increase egg productionand laying are included in Diabrotica virgifera (Sherwood andLevine, 1993), S. limbatus and C. maculatus (Savalli and Fox, 1998).

Previous studies using seed beetles revealed that male-derivedsubstances reduced female receptivity in C. chinensis and C.

maculatus (Yamane et al., 2008a,b). C. maculatus females laid moreeggs after remating (Savalli and Fox, 1999; Wilson et al., 1999;Eady et al., 2000; Tseng et al., 2007), and the same strain of C.

chinensis used in previous studies was used in the present one(Sakurai and Kasuya, 2008). These results suggest the existence ofsubstances that activate ovipositon behaviour in Callosobruchus

beetles. In the present study, biogenic amines reduced femalereceptivity and activated oviposition. As one of possibility, theseamines may be released from the nervous system accompanied byexpansion of bursa copulatrix due to the transfer of seminal fluids.In addition, components of seminal fluids may affect theconcentrations of biogenic amines inside the female body. It willbe interesting to clarify the mechanisms of nervous andphysiological functions involved in female mating and egg-layingbehaviour related to changes in the concentrations of biogenicamines inside the living female beetle.

Females of the C. chinensis strain used in this study hardly everremate (Harano and Miyatake, 2005), whereas, almost all C.

maculatus females do (Miyatake and Matsumura, 2004; Edvards-son and Tregenza, 2005). It was shown that the male-derived

T. Yamane, T. Miyatake / Journal of Insect Physiology 56 (2010) 271–276 275

substances that reduce female receptivity differed in the twoCallosobruchus species (Yamane et al., 2008a,b). Injection oftyramine or octopamine significantly reduced female receptivityin C. chinensis (Fig. 1), whereas females of C. maculatus did notrespond to octopamine (Fig. 4). These results may reflect thedifference of reduction in female receptivity between the twospecies. Females of the C. chinenesis strain used in the presentexperiment reduced receptivity immediately after mating andreduction of receptivity of females continue more than 10 days. Onthe other hand, females of C. maculatus reduced receptivityimmediately after mating but, reduction of receptivity of femalesdo not continue till 10 days (Miyatake and Matsumura, 2004). Sothere may be the possibility that the effect of tyramine on femalereceptivity act from immediately to a while after mating and theeffect of octopamine on female receptivity continue longer thantyramine. It seems likely that two mechanisms, one being reducedsensitivity, namely not to response, to courting males and the otherbeing activation of rejection of copulation with males by runningway from and kicking to them, act cooperatively in the reducedreceptivity.

C. chinensis females rarely dump eggs (Yanagi and Miyatake,2003), but egg-dumping behaviours by C. maculatus females arefrequently observed (Wang and Horng, 2004). And there is a strainin which females increased their number of eggs by remating(Harano et al., 2006; Sakurai and Kasuya, 2008). Injection oftyramine or serotonin increased number of eggs laid by C. chinensis

female (Fig. 3), but, C. maculatus female did not respond toserotonin (Fig. 6). These results suggest differences in theregulatory mechanisms of mating and oviposition between thetwo Callosobruchus species.

In conclusion, the present study suggests the possibility that theeffects of amines on reduction of receptivity and activation ofovipositon in females differ between closely related two Calloso-

bruchus species. Detailed analyses of the relationship between thelevel of biogenic amines in a female’s body and mating oroviposition behaviour will provide a good tool to understand theevolution of reproductive system and behaviour in insect speciesincluding these two Callosobruchus species.

Acknowledgements

We thank Dr. Ken Sasaki (Kanazawa Institute of Technology,Kanazawa, Japan) for reviewing the early manuscript and givinghelpful comments, Dr. Maki Katsuhara (Research Institute forBioresources, Okayama University, Kurasiki, Japan) for technicaladvices on injection, Dr. Shin-ya Ohba (Institute of TropicalMedicine of Nagasaki University, Nagasaki, Japan) and TomohiroHarano (Kyshu University, Fukuoka, Japan) for statistical advices.This work was supported by KAKENHI 19370011 and 19657026,Grant-in-Aid for Scientific Research, JSPS and MEXT to T.M., andResearch Fellowships for Young Scientists (JSPS 205869) to T.Y.

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