Proposal Number: IOS-0718140
Project Title: Self-Referencing as a Universal Mechanism Promoting Polyandry in Insects
Female animals often mate with many different males, and this behavior has long puzzled evolutionary biologists. However, recent studies have revealed that by mating with more than one male, females secure good genes that enhance the health and survival of their offspring. That being the case, one might expect females to favor novel mating partners over previous mates, and indeed studies of several unrelated species have shown a clear female preference for novel males. But how do females distinguish between novel males and previous mating partners? Earlier work with crickets suggests that females do so by tagging males with their own odors during mating. When a female encounters a former mating partner later on, she need only compare her own scent with that of the male. If she finds that the male has been imbued with her own chemical signature, she can avoid mating with that male in favor of a novel mating partner. This simple form of self referencing could be a widespread mechanism by which females of diverse animal species maximize the diversity of their mating partners. The proposed research focuses on cuticular hydrocarbons (CHCs) as the basis of chemosensory self-referencing. CHCs are fat molecules abundant on the surface of the insect cuticle; they often play an integral role in insect communication. CHC profiles of females will be manipulated to see if females'' aversion to previous mates can be experimentally abolished. The reliance of females on chemical cues to identify previous mates will be examined by chemically disabling cricket contact chemoreceptors. Behavioral tests will be employed to determine how long self-referent chemosensory cues persist, and to what extent they are masked when males are imbued with odors of other females. Not only will these studies help establish a potentially universal mechanism of mate recognition in insects, they could also potentially lead to the identification of chemical compounds that inhibit female mating behavior, furnishing a relatively safe, but effective means of biological control of insect pest species. The proposed research will provide training to a postdoctoral fellow and several undergraduate and graduate students, and will help redress the current under-representation of women in science. Graduate students and the PIs will continue their participation in ongoing programs designed to enhance elementary school teachers'''' training in science and to mentor female high school students.
A major focus of recent work on the evolution of animal mating systems has been to understand why females typically mate with many different males (a pattern formally known as polyandry) when a single mating provides sufficient sperm to fertilize a female’s eggs. An emerging consensus is that females mate with different males to obtain direct material benefits or indirect genetic benefits for their young. If this is true, we might expect females to forego mating with previous partners in favor of novel males and, in fact, a female preference for novel mating partners has been demonstrated in a number of taxa. Recent experiments in our lab were the first to suggest a possible mechanism by which females recognize and discriminate against previous mates. The study, featured in both the New Scientist and Current Biology, revealed that female crickets appear to recognize previous mates by imbuing males with their own odors during mating. Studies supported by our recently completed, NSF-supported project collectively demonstrate that females utilize their own cuticular hydrocarbons (CHCs) as the underlying proximate basis for this type of chemosensory self-referencing, thereby maximizing their pool of prospective mates. The first study showed significant genetic variation (explaining in excess of 90% of total phenotypic variation) in the CHC profiles of females based on chemical analysis of nine highly inbred lines. Thus, CHCs offer the potential for the reliable, genetically unique chemical cues that are required for chemosensory self-referencing. In a second study, we used solvent-free, solid-phase microextraction (SPME) to directly analyze the CHC profiles of males before and after mating with a female. There were significant differences in the CHC profiles of males before and after mating, with the chemical profiles of mated males becoming more similar to those of their mates following mating. These results show clearly that the CHCs of females are transferred to males at the time of mating. Finally, we experimentally ‘perfumed’ males with CHC extracts derived from inbred female siblings of focal females or those derived from unrelated inbred females. Focal females showed a statistically significant aversion to males perfumed with the CHC extracts of their inbred female siblings, demonstrating that female mate choice decisions are profoundly influenced by self-referencing, leading females to favor novel males. The application of DNA profiling techniques to free-living animals in nature has revolutionized our understanding of animal systems, revealing that polyandry is pervasive across all major animal taxa. It is not surprising, therefore, that the pages of both Science and Nature are replete with accounts of the consequences of polyandry to female reproduction and offspring fitness. However, the proximate mechanisms by which cognitively simple animals, such as crickets, maximize their opportunities for polyandry remain virtually unknown. The results presented here demonstrate unequivocally that cuticular hydrocarbons provide the proximate basis for chemosensory self-referencing, mediating the female preference for novel mates demonstrated in crickets. Given the pervasiveness of CHCs as recognition cues among arthropods, chemosensory self-referencing via CHCs may be a ubiquitous mechanism by which females across a broad range of animal mating systems increase the diversity of their mating partners. Not only have these studies help establish a potentially universal mechanism of mate recognition in insects, they could also potentially lead to the identification of chemical compounds that inhibit female mating behavior, furnishing a relatively safe, but effective means of biological control of insect pest species. This NSF award has contributed directly to the training of three undergraduate students, ten M.S. students, one Ph.D. student, and three postdoctoral fellows.
