Doctor of Philosophy
MacDougall-Shackleton, Elizabeth A.
Avian chemical communication has been understudied due to the misconception that olfaction is unimportant or even lacking in birds. Early work focused on the olfactory foraging capabilities of seabirds because of their ecology (open ocean foraging) and large olfactory bulbs. In contrast, olfaction in passerine birds, comprising over half of all extant avian taxa, was long overlooked due to their relatively small olfactory bulbs. It is now well established that passerines can smell, and their olfactory acuity is comparable to that of macrosmatic mammals such as rats. Much of our theory on communication and mate choice has involved studying visual and acoustic signals in birds, especially passerines. However, there is mounting evidence that chemical cues are a previously overlooked but important element of avian communication and mate choice. I used gas chromatography to explore sources of variation in song sparrow (Melospiza melodia) preen oil. I then performed behavioural experiments to test whether song sparrows are capable of discriminating among preen oil odour cues. Finally, I explored the hypothesis that major histocompatibility complex (MHC) genotype underlies variation in preen gland microbiota and that this contributes to variation in preen oil chemical composition, providing a potential mechanism for MHC-based mate assessment. Preen oil differed between birds experimentally infected with haemosporidian malaria parasites (Plasmodium sp.) and sham-inoculated controls; between populations, ages, sexes, and breeding versus postbreeding seasons; and with MHC genotype. Song sparrows used preen oil odour to discriminate between the sexes, and to discriminate the MHC similarity and diversity of potential mates. Preen gland microbes differed between populations and sexes, and covaried with MHC genotype but not with preen oil composition. Collectively, my thesis establishes that preen oil is information-rich and that birds use preen oil odour cues in ecologically relevant contexts. I provide some of the first evidence that pathogen exposure alters chemical cues in birds, that birds use odour cues to discriminate the MHC genotype of potential mates, and that MHC genotype is positively correlated with both preen gland microbes and preen oil chemical composition.
Summary for Lay Audience
Most birds have a specialized preen gland that secretes preen oil, a waxy substance involved in both feather maintenance and chemical communication. I measured chemical differences in preen oil from different groups of birds and tested whether song sparrows use smell to detect such differences.
Avian malaria is a disease that affects over 70% of the world’s bird species, impacting their reproduction and survival. I compared preen oil from malaria-infected and uninfected birds, showing that preen oil changed with exposure to malaria parasites. I then tested whether birds avoid the preen oil of infected individuals, but found no evidence for this. Next, I showed that preen oil differs between species, populations, ages, sexes, and seasons. I tested song sparrows’ responses to preen oil from same versus opposite sexes and from brood parasites, species that rely on other species to raise their young. Both sexes spent more time with opposite-sex than same-sex preen oil, while males spent more time and females spent less time with brood parasite oil.
An essential part of immune defense in vertebrate animals is a set of genes called the major histocompatibility complex (MHC). High MHC allelic diversity can increase disease resistance, so animals should prefer mates with MHC genes different from their own. Offspring from MHC-dissimilar mates should have greater MHC diversity and disease resistance. Because this is so important, natural selection likely provides animals with ways to assess MHC. Fish and mammals use smell, but we do not know how birds assess MHC. Preen oil can reflect MHC genotype, so birds may use preen oil odour to choose MHC-dissimilar mates, thereby protecting their offspring from disease. Using behavioural trials, I showed that song sparrows spent more time with preen oil from MHC-dissimilar and MHC-diverse potential mates. Finally, I used genetic sequencing to identify the bacteria living in song sparrows’ preen gland, showing that bacteria differ between sexes and populations, and with MHC genotype. Birds with more similar MHC genotypes had more similar preen gland bacteria and oil. Overall, my thesis showed that scent-based communication in birds is more common and more complex than previously believed.
Grieves, Leanne A., "Chemical Communication in Songbirds" (2020). Electronic Thesis and Dissertation Repository. 6926.
Creative Commons License
This work is licensed under a Creative Commons Attribution-Noncommercial-No Derivative Works 4.0 License.