Pheromone production and mating behaviour by allatectomized males of the cockroach, Nauphoeta cinerea

Males of Nauphoeta cinerea produce a volatile pheromone which attracts the female for mating. Allatectomy of males either 5 days prior to or within 12 hr following the imaginal ecdysis does not impair pheromone production, pheromone release, nor any observable aspect of mating behaviour. It is proposed that in N. cinerea, and in other cockroach species where the male releases a volatile pheromone to attract the female, pheromone production is not controlled by the corpora allata, and pheromone release is under direct motor control.     

Does the scent of a potential mate prevent the resorption of oocytes by apoptosis in Nauphoeta cinerea?

Abstract  We expect organisms to have evolved mechanisms to gather and use the information available within their environments, to steer resource investment decisions toward the traits that will give the greatest fitness returns. Pheromones are social signals, a common purpose of which is to act as indicators of mate presence. Consequently, pheromones have the potential to act as signals to increase or maintain reproductive investment over that of competing life-history traits. In the cockroach, Nauphoeta cinerea (Oliver), females pay costs of maintaining investment in reproduction when there are no males, and males produce pheromones that are known to effect female reproductive outcomes. Whether the pheromones have an influence on resource physiology is unknown. We subjected newly eclosed females to either a synthetic blend of male pheromones or control. We dissected females at 7, 12, 17 or 22 days. We measured apoptosis levels and size of all oocytes within the vitellerium, and measured dry fat body mass. Synthetic male pheromone blend did not have an effect on any measure of female reproductive or somatic resource physiology. Although negative results are always problematic, the success of the synthetic pheromone method in the past suggests that females may be insensitive to male pheromones in the pre-oviposition period, and may rely on mating stimulus rather than pheromone as the cue for oocyte maintenance and growth. Previous studies reporting effects of male pheromones on female reproduction suggest that the period of pheromone sensitivity may be between mating and birth.     

Sexual conflict and the evolution of female mate choice and male social dominance

Conflicts between the sexes over control of reproduction are thought to lead to a cost of sexual selection through the evolution of male traits that manipulate female reproductive physiology and behaviour, and female traits that resist this manipulation. Although studies have begun to document negative fitness effects of sexual conflict, studies showing the expected association between sexual conflict and the specific behavioural mechanisms of sexual selection are lacking. Here we experimentally manipulated the opportunity for sexual conflict in the cockroach. Nauphoeta cinerea and showed that, for this species, odour cues in the social environment influence the behavioural strategies and fitness of males and females during sexual selection. Females provided with the opportunity for discriminating between males but not necessarily mating with preferred males produced fewer male offspring than females mated at random. The number of female offspring produced was not affected, nor was the viability of the offspring. Experimental modification of the composition of the males' pheromone showed that the fecundity effects were caused by exposure to the pheromone component that makes males attractive to females but also makes males less likely to be dominant. Female mate choice therefore carries a demographic cost but functions to avoid male manipulation and aggression. Male-male competition appears to function to circumvent mate choice rather than directly manipulating females, as the mate choice can be cryptic. The dynamic struggle between the sexes for control of mating opportunities and outcomes in N. cinerea therefore reveals a unique role for sexual conflict in the evolution of the behavioural components of sexual selection.     

Male cockroaches prefer a high carbohydrate diet that makes them more attractive to females: implications for the study of condition dependence

Sexual selection is a major force driving the evolution of elaborate male sexual traits. Handicap models of sexual selection predict that male sexual traits should covary positively with condition, making them reliable indicators of male quality. However, most studies have either manipulated condition through varying diet quantity and/or caloric content without knowledge of specific nutrient effects or have correlated proxies of condition with sexual trait expression. We used nutritional geometry to quantify protein and carbohydrate intake by male cockroaches, Nauphoeta cinerea, and related this to sex pheromone expression, attractiveness, and dominance status. We found that carbohydrate, but not protein, intake is related to male sex pheromone expression and attractiveness but not dominance status. Additionally, we related two condition proxies (weight gain and lipid reserves) to protein and carbohydrate acquisition. Weight gain increased with the intake of both nutrients, whereas lipid reserves only increased with carbohydrate intake. Importantly, lipid accumulation was not as responsive to carbohydrate intake as attractiveness and thus was a less-accurate condition proxy. Moreover, males preferentially consumed high carbohydrate diets with little regard for protein content suggesting that they actively increase their carbohydrate intake thereby maximizing their reproductive fitness by being attractive.     

THE EVOLUTION OF SOCIAL SIGNALS: MORPHOLOGICAL,FUNCTIONAL, AND GENETIC INTEGRATION OF THE SEX PHEROMONE IN NAUPHOETA CINEREA

Social signals that mediate intraspecific interactions can be complex, conveying considerable information concerning the probable behavior of individuals and minimizing overt aggression and wasted energy. In the cockroach Nauphoeta cinerea, male-male competition and female mate choice are mediated by a multicomponent male-produced sex pheromone. In this study, I examine variation in this pheromone. First I measure differences among males in both individual pheromone compounds and the overall composition of the pheromone. Principal component analysis is used to quantify and describe pheromone composition. Next, I explore some of the causes and consequences of this variation by examining the pheromone of males with different social experiences. Compared to subordinate males, dominant males have significantly less variable quantities of the individual pheromone compounds and are significantly less variable in the composition of their pheromone. Because of an association between status and mating success, male-male competition can result in stabilizing sexual selection on the sex pheromone. Finally, I test the hypothesis that the pheromone compounds evolve in a manner consistent with their function. As predicted for morphologically integrated characters, the patterns of phenotypic, genetic, and environmental correlations among my measures of pheromone compounds and composition match functional patterns suggested by this study and the developmental patterns demonstrated in my previous studies. Based on these studies of the N. cinerea sex pheromone, I argue that stabilizing sexual selection shapes the evolution of pheromonal communication involved in social interactions among male N. cinerea. Further, I argue that coordinated evolution of social signals may be possible due to the morphological integration of their multiple compounds.     

Morphology of the sternal and tergal glands producing the sexual pheromones and the aphrodisiacs among the cockroaches of the subfamily oxyhaloinae

Among cockroaches in the subfamily of Oxyhaloinae, the adult males produce two essential and successively active chemical signals: the sex pheromone attracting females from a distance secreted by the sternal glands, and the aphrodisiac required for mating which is secreted by the tergal glands. The adult males of the seven species studied, Nauphoeta cinerea, Henschoutedenia flexivitta, Leucophaea maderae, Jagrehnia madecassa, Gromphadorhina portentosa, G. laevigata, and G. chopardi, possess well-developed sternal and tergal glands whose number varies according to the species and methods of mating (three to six sternal glands and four to seven tergal glands). These glands are basically composed of type three glandular units (glandular cell + duct cell) and type 2 cells (modified oenocytes) which exhibit no significant external cuticular modification except for tergite 2 of L. maderae. The extreme variance in development of these glands can be linked to sexual behavior. The hypothesis put forward here is that of a regressive evolution of the tergal glands, related to a modification of the role played by the aphrodisiacs which they secrete.     

Behavioural changes induced by irradiating Dacus cucumis with gamma rays

Locomotor activity, measured in a circular runway apparatus, declined progressively at doses of 40, 60, and 80 krad. There was no detectable difference between normal and 10 krad flies.Females tended to lose their mating inhibition with increasing dose, whereas 40 krad males in non-competitive trials tended to mate less frequently than normal or 10 krad males.A diurnal rhythm of ecdysis was not changed by exposure to chronic low doses 12 hr out of phase with the rhythm. However, a single, large dose 12 hr out of phase resulted in a bimodal emergence rhythm, with the abnormal peak shifted towards the time of exposure to radiation.     

Regulation of sex pheromone production in the male Nauphoeta cinerea cockroach: Role of brain extracts,corpora allata�(CA), and juvenile hormone (JH)

The neuroendocrine mechanisms underlying pheromone regulation in cockroaches are unclear because of a lack of physiological and chemical data. The present report describes experiments designed to determine the role of the brain, corpora allata, and juvenile hormone III in the production of sex pheromone by male Nauphoeta cinerea cockroaches. The levels of two sex pheromone components, i.e., acetoin and 2‐methylthiazolidine, were measured by gas chromatographic analysis of sternal gland extracts obtained from individual males. Allatectomy or decapitation performed up to 2 to 3 days after imaginal molt caused a decrease in sex phermone levels. Conversely decapitation or allatectomy performed after 3 to 4 days post‐eclosion had almost no effect on sex pheromone levels. Injection of JHIII into allatectomized and decapitated males stimulated pheromone production while injection of brain extract had no effect. These results indicate that JHIII is involved in the differentiation of sternal glands and that regulation via pheromone biosynthesis activating neuropeptide (PBAN) does not occur in N. Cinerea cockroaches. Arch. Insect Biochem. Physiol. 40:165–172, 1999. © 1999 Wiley‐Liss, Inc.     

Directional cues in tactile stimuli involved in agonistic encounters in cockroaches

ABSTRACT. The ability of male cockroaches, Nauphoeta cinerea and Periplaneta americana , to respond directionally to tactile agonistic acts was tested using stimulation by artificially manipulated appendages. Responses by Nauphoeta included turning towards the stimulus at preferred angles of c. 40°, 90° and 180°, apparently relying on internally-stored directional sensory information. This turning responsiveness depended in part on the social status of the receiving individual, since subordinate individuals often retreated or failed to respond. Periplaneta males reacted to tactile stimuli by quick movements away from the stimulus or by kicking towards it. The leg used in kicking was that nearest to the part of the body which was stimulated.     

Sexual conflict and cooperation under naturally occurring male enforced monogamy

An evolutionary conflict often exists between the sexes in regard to female mating patterns. Females can benefit from polyandry, whereas males mating with polyandrous females lose reproductive opportunities because of sperm competition. Where this conflict occurs, the evolution of mechanisms whereby males can control female remating, often at a fitness cost to the female, are expected to evolve. The fitness cost to the female will be increased in systems where a few high status males monopolise mating opportunities and thus have limited sperm supplies. Here we show that in the cockroach Nauphoeta cinerea, a species where males enforce female monogamy in the first reproductive cycle, males that have become sperm depleted continue to be able to manipulate female remating behaviour. Although the manipulation severely decreases fecundity in females mated to sperm-depleted males, males benefit, increasing their relative fitness by preventing other males from reproducing. Our results suggest that there is selection on maintaining the mechanism of manipulation rather than maintaining sperm numbers. Taken with previous research on sexual conflict in N. cinerea, this study suggests that the causes and consequences of sexual conflict are complex and can change across the life history of an individual.     

Olfactory cues in discrimination among individuals in dominance hierarchies in the cockroach, Nauphoeta cinerea

ABSTRACT. The purpose of this study was to explore the olfactory recognition mechanisms used by individual subordinate male cockroaches, Nauphoeta cinerea (Olivier), in a dominance hierarchy. Results of two independent sets of experiments, one using an olfactometer and the other using an arena, suggest that olfactory cues are important to males. Subordinate males did not avoid dominant male odour in an olfactometer but could discriminate between the odours of familiar and unfamiliar individual dominant males, preferring the odour of the dominant male with which they had previous social contact. Since test subordinates did not avoid dominant male odours in the olfactometer, it is possible that the distance an individual remains from a dominant is important. To test this, individual dominant and subordinate males were tethered in the centre of an arena. Subordinate males were introduced into the arena and allowed to approach the tethered male. They approached tethered dominants and subordinates differently, and tended to keep away from the dominants. Tethered males unfamiliar to the test animals were avoided as well.     

Balancing sexual selection through opposing mate choice and male competition

Male–male competition and female mate choice act contemporaneously in the cockroach Nauphoeta cinerea and the social pheromone of males influences the outcome of both forms of sexual selection. We therefore examined the joint and separate effects of male–male competition and female mate choice to determine if the selective optima for the pheromone were the same or different. Dominant males in a newly established hierarchy mated more frequently, but not exclusively. Manipulations of the multi-component social pheromone produced by males of N. cinerea showed that both long- and close-range attraction of females by males were influenced by the quantity and composition of the pheromone. The most attractive composition, however, differed from that which was most likely to confer high status to males. Since the outcome of male–male competition can conflict with mating preferences exhibited by females, there is balancing sexual selection on the social pheromone of N. cinerea. Such balancing selection might act to maintain genetic variation in sexually selected traits. We suggest that the different forms of sexual selection conflict in N. cinerea because females prefer a blend different to that which is most effective in male–male competition in order to avoid mating with overly aggressive males.     

Effects of gamma radiation on spermatogenesis and fertility of male Amblyomma americanum (Acari: Ixodidae)

Amblyomma americanum males were treated with 0.5, 1, 2, 3, 4, 8, and 16 krad of gamma radiation. Testes of ticks treated with 2, 3, 4, 8, and 16 krad were smaller than those of ticks irradiated at lower levels and controls. No recognizable alteration in timing of spermatogenesis was noted among the different radiation groups, but severe breakdown and depletion of germinal cells was noted at 4, 8, and 16 krad. Percent hatch of larvae from crosses of irradiated males and untreated females decreased with increasing radiation level. No hatch was observed from eggs of females mated to males treated at 2 krad or higher.     

Changes of species specific cuticular hydrocarbon profiles in the cockroaches Nauphoeta cinerea and Leucophaea maderae reared in heterospecific groups

The cuticular hydrocarbon profiles of the cockroaches Nauphoeta cinerea and Leucophaea maderae are species-specific when maintained in homospecific rearings. When individuals were reared in mixed species colonies, they initially remained in homospecific groups under different shelters. However, after 14 days they formed one heterospecific group with cuticular profiles showing characteristics of both species. When individuals were returned in monospecific rearings, their cuticular hydrocarbon profiles returned to species-specific ones within 3 weeks.     

Effects of gamma radiation on spermatophore production and reception and subsequent fecundity and egg viability inAcarus siro L. (Acari: Acaridae)

Gamma radiation at doses higher than 10 krad significantly lowered the fecundity of the grain mite,Acarus siro. The fecundity of irradiated females was inversely correlated with dose, both when control or irradiated males were used in the pairing.Irradiation with ionizing radiation affected sexual activity of males. At doses above 10 krad the number of formed or observed spermatophores was lowered significantly.Sexual attractiveness of irradiated and control females to irradiated males was similar. However, non-irradiated males were observed mating more often with non-irradiated than with irradiated females.No correlation was found between the numbers of spermatophores present in the spermathecae of the female and the fecundity of the female. Irradiation had a greater effect on fecundity of the female than on sexual activity of the male; it did not affect the shape or behavior of spermatophores in the spermathecae of the female.Viability of eggs laid by females decreased by at least 50% when females or males were irradiated with doses above 20 krad. Irradiation also affected the survival of adults, but females were more sensitive than males. Net sterility index indicates that doses higher than 20 krad induce more than 90% sterility.     

The influence of social experience on the behavior of male cockroaches,Nauphoeta cinerea

The influence of social experience on rates of agonistic behavior was investigated in a cockroach, Nauphoeta cinerea. Social experience was manipulated by establishing three types of groups of four identically aged males: (1) ran-domly chosen, socially naive males (control); (2) males of similar status and activity level (from treatment 1); and (3) males returned to their original hierarchy after experiencing treatment 2. In the control groups, we found stable hierarchies, significant differences in the rate of agonistic behaviors exhibited among different status males, and a significant relationship between social status and level of agonism. We also compare activity levels within and among groups after males had novel social experiences. Among similar status individuals, we found less activity than when they wereintheir original groups. When males were returned to their original groups, the level of activity increased compared to the level of activity before treatment. The social status of males was unstable after these treatments. Losing tended to result in relatively more subordinate behavior, and winning in relatively more dominant behavior by a male. Within groups, the rate of agonism also increased over 5 days in groups of males that had no previous interactions with each other, while the rate of agonism remained the same in groups of familiar males. We interpret these results in light of male-male assessment and the maintenance of social status in this species.     

Females avoid manipulative males and live longer

Abstract Female mate choice has been demonstrated in a wide variety of species and is now accepted as an important factor in sexual selection. One of the remaining questions, however, is why females prefer specific males. Do females or their offspring benefit from their choice? Or do females choose mates to minimize costs of mating? Here we show that, in the ovoviviparous cockroach Nauphoeta cinerea, where sexual selection has been well documented, females chose mates to avoid costly male manipulation. Females were partnered with preferred or nonpreferred mates, and fitness of the females measured. We found that females lived longer when they mated with preferred males. Female lifespan depended on the rate at which offspring developed from egg to parturition: slower development led to longer life. We manipulated the male pheromone and showed that the component of the pheromone blend that makes males attractive to females also delayed parturition. Thus, like other aspects of sexual conflict in this species, offspring development and thereby the mother's lifespan depended on exposure of females to specific components of the male pheromone. Males benefit from manipulating offspring development because females with accelerated parturition remained unreceptive whereas females with slower developing offspring readily remated after giving birth to their offspring. Our results suggest a hormone‐like role for the male pheromone in N. cinerea and provide the first direct evidence of mate choice to avoid male manipulation. This study shows that dominant males may not be preferred males if they are manipulating females, why multiple components with contrasting effects can exist in a sexual signal, and emphasizes the complex fitness relationships that can arise in species with sexual conflict.     

Effects of gamma radiation on development, sterility, fecundity, and sex ratio of Dermanyssus gallinae (DeGeer) (Acari: Dermanyssidae)

Protonymphal Dermanyssus gallinae were irradiated with 0.50, 0.75, 1.0, 3.0, and 6.0 krad of gamma radiation and subsequently monitored regarding their developmental, feeding, and mating success. Also, sex ratios of adults treated as protonymphs were recorded as were sex ratios of embryos and F1 adults produced by these adults. Doses up to 1.0 krad did not prevent development of treated protonymphs to the adult stage or stop mating. Three krad reduced the number of treated protonymphs attaining adulthood and 6.0-krad treatment prevented all mites from developing to the adult stage. Egg (embryo) production was normal for mites treated with 0.50 krad, but significantly curtailed by doses of 0.75 krad and greater. Radiation doses used in this study did not appear to affect the normal variable sex ratios observed in untreated mites.     

Sperm competition and male ejaculate investment in Nauphoeta cinerea: effects of social environment during development

Selective pressure arising from sperm competition has been predicted to influence evolutionary and behavioural adjustment of ejaculate investment, but also may influence developmental adjustment of ejaculate investment. Immature males able to target resources strategically based on the competitive environment they will experience when they become sexually mature should be at a selective advantage. In our study we investigated how the presence of potential competitors or mates affects ejaculate and testes investment during development in the cockroach Nauphoeta cinerea, a species where males control female remating via their ejaculate size (large spermatophores prevent females from remating and therefore function to avoid sperm competition for males) and females store sperm. Our aim was to determine whether the social environment influences developmental adjustment of ejaculate investment and the relative importance of ejaculate components with different functions; avoidance of or engagement in sperm competition. We conclude that the social environment can influence developmental and behavioural flexibility in specific ejaculate components that may function to avoid or engage in sperm competition.     

The effects of gamma-irradiation on migration and survival of Schistosoma mansoni schistosomula in mice

Infections with irradiated Schistosoma mansoni were established by intramuscular (i.m.) injection of mechanically transformed schistosomula. A dose of 2.3 krad. allowed persistence of a small proportion of worms to adulthood, and of these survivors the majority of the female worms were sexually sterile. However, a small proportion of 2.3 krad.-irradiated females and a larger proportion of similarly irradiated males were capable of pairing successfully with non-irradiated partners. Radiation in the range 2.3 to 10 krad. resulted in slightly reduced peak recoveries from the lungs while 20 krad. resulted in a much reduced and 40 krad. a virtual absence of survival to the lung stage. Increasing doses of radiation in the range 2.3 to 10 krad. resulted in successively fewer parasites reaching the liver. Thus, the major sites of the radiation-induced mortality appeared to be as follows: 2.3 krad., mainly in the liver; 4 krad., in the lungs and liver; 10 krad., mainly in the lungs; 20 krad., at the injection site and in the lungs and 40 krad., mainly at the injection site. The infections studied here showed reduced survival following exposure to high doses of radiation compared with the infections, established as percutaneously applied cercariae, which have been reported by other workers. Possible reasons for the disparity are discussed.