Male animals typically show considerable plasticity in the behavioral tactics and signals that they use to obtain mates. For example, in many bird populations, some males breed in bright plumage while others breed in relatively dull plumage. It is generally thought that plastic expression of sexual traits depends on both intrinsic (body condition) and extrinsic cues (social interactions), allowing males to adjust their investment in signals according to their quality and relative likelihood of mating success, and consequently that such traits honestly signal male quality to conspecifics. However, the mechanisms that translate these cues to male sexual traits, and thereby allow for plastic expression of sexual traits, are poorly understood. This research will examine the mechanisms of flexible expression of male reproductive phenotypes in the red-backed fairy wren (Malurus melanocephalus). In particular, this project will determine experimentally the effects of physical condition, social environment and stress on the hormones that affect male reproductive type. This work will combine both functional and mechanistic analyses, and will push the study of phenotypic plasticity and sexual signals in new directions. In addition, the research will explore carry-over effects of early life environment on male condition and reproductive type, a cutting-edge field of research emerging from the recent acknowledgement that early development can have important effects on adult traits. These results will have major implications for theoretical models of the evolution of sexual signals. This research also will contribute directly to the training of two graduate students and numerous undergraduates. Undergraduate training will include a novel internship program that will pair students from American universities with Australian students to conduct collaborative research. Thus, this project will involve undergraduates in all aspects of the research experience, from project design through publication, as well as giving them an enriching international experience.
Animals typically show considerable variation across individuals in the behaviors and communication signals that they use to attract mates, such as plumage coloration and song in birds, yet the mechanisms underlying this variation, the ways that these mechanisms are shaped by evolutionary forces, and the broader consequences of this variation are poorly understood. This project has addressed these questions through research on the red-backed fairy-wren, an Australian bird. This species is an excellent model system for studying the evolution of sexual signals because (a) there is considerable variation in male plumage signals (some males breed in bright red/black plumage whereas others have cryptic brown, female-like, plumage), and (b) there is also considerable variation in plumage color across populations (in some populations bright males have red coloration, whereas in others they are orange). Accordingly, this study used a combination of field observations and experiments to examine the mechanisms underlying this variation and also the evolutionary consequences. Results show that male plumage coloration is regulated by the hormone testosterone. Bright males (with high levels of testosterone) were also found to differ from cryptic males (low testosterone) in a number of ways, including both behavioral (parental care, mating effort, sperm production) and morphological (testes size, bill color and tail length) traits. Moreover, experiments manipulating the social environment (e.g., social status of a male) have shown that testosterone levels are themselves regulated by social interactions. These results suggest that testosterone may affect a suite of traits to produce an integrated phenotype that is well matched to the social environment. Genetic analyses have revealed that bright males produce more offspring than do cryptic males, likely as a consequence of female mating preferences because the main advantage for bright males comes through matings with "extra-pair" females (i.e., females other than the males own mate). Finally, female reproductive behavior is also affected by the social environment, with female mating patterns being affected by how closely related she is to her mate and also by the composition of her breeding group (females in groups with non-breeding "helper" males are more likely to mate with extra-pair males, and also more likely to produce daughters rather than sons). These results indicate that individuals respond strongly to their social environment, and that multiple traits are integrated together, in part by the actions of hormones such as testosterone, to produce an individual that is well matched to its social environment. At the inter-population level, theory suggests that sexual signals (like plumage or song) may play a central role in preventing inter-breeding between populations, thereby leading to speciation and increased biodiversity. Investigating this possibility, this study has revealed that the "red" male plumage type is moving ("introgressing") into the genetic background of "orange" populations, and a plumage color manipulation experiment has revealed that this is being driven by female mating preferences ("red" males in "orange" populations are much more successful in siring young). Thus, in contrast to theoretical expectations, plumage signals seem to be increasing, rather than inhibiting, matings between birds from different populations. Surprisingly, though, song types differ between populations and do not seem to be introgressing from one populations to another. This is likely due to mode of transmission: plumage color is, at least in part, a genetic trait, whereas songs are learned rather than passed genetically from one generation to the next. This difference allows song and plumage type to become decoupled and have different evolutionary trajectories. Moreover, a playback experiment revealed that males respond more strongly to song than to plumage signals, indicating that plumage introgression is likely not inhibited by male aggression. These results show that sexual signals can indeed have pronounced effects on inter-breeding between populations, but that the patterns can be very complicated and asymmetric, and also may depend on signal type.
