A project undertaken at Macquarie University, and supervised by Vivian Mendez
Compounds on the cuticle of Queensland fruit fly (Bactrocera tryoni) provide conspecifics a source of information about sexual maturity, sex, recent nutrition and physical injury. The cuticular compounds found on the body of the flies are deposited on substrates as the flies walk, and these ‘footprints’ match the cuticular profile of the individual fly. We found that flies are attracted to the footprint left by consecifics of the opposite sex and that the footprints are persistent, a key feature if the footprints are used to gather information by other flies in nature. Footprints of mated flies were repellent to other mated females, and in oviposition assays the footprints of mated females acted as oviposition deterrents for other mated females. In Y-maze bioassays, we found that males can distinguish the volatiles coming from the cuticular compounds of mature females and when given a choice between volatiles from mature and immature females, the males choose the mature volatiles from mature ones. Being able to identify mature females is potentially critical for males, as attempts to mate with females that are not fully sexually developed are likely to be detrimental to the male reproductive success.
We also investigated the cuticular chemistry of Jarvis’ fruit flies (Bactrocera jarvisi) collected in the field. We collected cocky apples, the natural host of B. jarvisi, from the Northern Territory and reared the flies in the laboratory. Immature and mature flies of both sexes were collected and the cuticular chemistry was extracted. We also dissected and measured the reproductive organs of the flies to see if the sexual development matched the cuticular profile of the flies.
Some immature males of B. jarvisi are attracted to zingerone, a phytochemical found in orchids of the genus Bulbophyllum and Passiflora flowers. Through dissection of reproductive organs, we found that males attracted to zingerone as immatures are more sexually developed than non-attracted males, and the cuticular chemistry of males attracted to zingerone is more similar to that of older mature males. We also fed the males zingerone and found, by dissecting and measuring the reproductive organs, that zingerone feeding accelerates sexual development, and the sexual development is also reflected in the males’ cuticular chemistry. Zingerone accumulated in the rectal glands of the males, but no zingerone was found in the cuticular chemistry of the male flies. Zingerone storage in the rectal gland might be a way of maintaining constant access to the compounds and will explain the long-term effects of zingerone that have been observed in lab-reared flies, with males having higher mating rates days after zingerone ingestion.
Our results also showed that, compared to non-fed males, zingerone-fed males had higher mating rates throughout their lives and were more attractive to females in Y-mazes, which in conjunction with male sexual acceleration, allows the males to mate earlier in life and obtain more matings throughout their life compared to non-fed males. Zingerone-fed males have a reduced lifespan compared to non-fed males, suggesting a physiological cost for the zingerone-fed males, possibly due to higher metabolic demands induced by the ingestion of the compound.
The analysis of the cuticular chemistry showed that in B. jarvisi, sexual dimorphism of the cuticular chemistry is evident not only in the mature flies, as we previously found in B. tryoni, but also in the immature flies. The sexual development of females also matched their cuticular profile. Compared to mature females, immature females have lower concentrations of esters, spiroacetals and amides, which the immature males completely lack. The concentration of compounds on both sexes increases as the flies mature, as was also observed in B. tryoni. By investigating sexual development through dissections of the genitalia and analysis of the cuticular chemistry, we have been able to establish that sexual development and cuticular profiles of both sexes are closely linked, for both species, B. tryoni and B. jarvisi. Previous research on the cuticular chemistry of tephritid flies have primarily focused on taxonomy, serving as a tool for species identification. This work represents the stepping-off point for what promises to be a rich line of research focused on understanding the biological importance of cuticular chemistry of tephritid fruit flies, and the role of the cuticular compounds in communication, reproduction and social interactions.