Personal odors can be influenced by genes of the major histocompatibility complex (Mhc), which is a cluster of genes essential for immune function. These odors impact recognition and preference in mammals, lizards and fish, but whether Mhc-associated odors could play a similar role in birds is currently not known. The tube-nosed seabirds (Order: Procellariiformes: petrels and albatrosses) are an ideal group for investigating this possibility. These birds mate for life. They also have a remarkable sense of smell, and some species can tell each other apart using only odors. This latest finding suggests that personal scent may play a role in social behaviors, which, until now, has not been seriously considered in birds.
To investigate this possibility further, Professor Gabrielle Nevitt, a sensory ecologist specializing in bird olfaction, has teamed up with Professor Scott Edwards, an evolutionary biologist and expert in the field of Mhc in birds. They will investigate this problem using the Leach's storm-petrel (Oceanodroma leucorhoa) as a model system. The primary objectives of this project are: 1) To perform the first multigene characterization of Mhc class II genes, and other genes related to olfactory and immune function, in a procellariiform seabird; 2) To investigate the role of Mhc in individual scent recognition; and 3) To investigate whether Mhc is involved in life-long partner choice.
Results showing that birds can either detect Mhc odors or use them to choose mates would represent a paradigm shift in how biologists typically view mate choice decisions in birds. Just as importantly, many species of petrels and albatrosses are facing extinction, and understanding the factors driving mate choice will make a valuable contribution to comprehensive management plans for endangered species. Finally, the project will provide interdisciplinary training at the undergraduate, graduate and postdoctoral levels, particularly for minorities and women, who will be targeted for these positions.
Our overarching aim was to investigate the genetic and behavioral mechanisms by which birds choose mates, and this is a fundamental problem in Behavioral Ecology. This collaborative study focused specifically on the interaction of genes involved in immune function, and how these genes may impact the individual odor quality of birds. Since birds are important vectors of disease, our research has clear implications for human health by providing more detailed information about how birds might advertise their own health status, or ‘quality’ to each other using scent, for the purposes of attracting a mate. In an era where birds carry diseases that are transmissible to humans, understanding these signal is increasingly important. Our research plan centered on characterizing the major histocompatibility complex (MHC), and how this relates to odor recognition in a carefully chosen species, the Leach’s storm-petrel (Oceanodroma leucorhoa). Storm-petrels are somewhat unique among birds because they have large olfactory bulbs and, unlike most other birds, they can smell about as well as a bloodhound. They are long-lived (~45 years), and they tend to mate for life. They dig a nest in a ~1-meter long underground burrow to which they return year after year. They can relocate this burrow at night by its unique scent, which smells musky to the human nose. Adults rear only one offspring each year, and incubation (~45 days) and chick-rearing (~50 days) is a lengthy process compared to other birds. Since these birds tend to nest on remote islands, a major goal for us was first to establish a robust study population of banded (identified) individuals that could be monitored for reproductive success and other demographic data over multiple years. For this investigation, we established study colonies on Bon Portage Island in Nova Scotia. We were able to locate, mark and map over 500 occupied burrows, which now comprise our long-term study population. In terms of genetic information, we have been specifically focused on characterizing the MHC in these birds, because these genes are also thought to influence mate choice in a number of vertebrate species, including humans. The MHC is a cluster of genes with primary functions in disease resistance and immune response. MHC genes bind fragments of bacteria and viruses that invade the body, and present these fragments to key molecular players in the immune response so that the immune system can clear these infections. MHC genes are different in almost every individual, and individuals with different MHC profiles can be discriminated by members of the opposite sex of the same species. The mechanisms by which MHC is linked to a unique scent profile is not well understood, but the structure of MHC molecules allows them to bind different and sometimes-volatile fragments in an individual-specific manner. It has been suggested, therefore, that this interaction may be part of the mechanism leading to individual scent recognition. Co-PI Edwards (Harvard) characterized the MHC genes from the blood samples we collected using molecular biology techniques. We found that petrel MHC genes are showing evidence of natural selection in the way we expect them to if they play a role in mate choice and disease resistance. We also found that about half the birds in our study population share two of the most common alleles (01 and 02) and we are currently investigating whether chick quality (as defined by both hatch date and growth over time) is linked to specific aspects of MHC genotype. We have found that petrel feathers contain hundreds of scented compounds, and this has encouraged us to develop and exploit novel tools to analytically discriminate odor profiles of individuals. We have also identified several compounds in feathers that may be linked to MHC genotype and mating preference, and this is the subject of ongoing collaboration and research. Overall our studies have allowed us to characterize MHC class II genes in petrels and to set the stage for detailed studies of mate choice, chick growth and survival. Our ongoing research will further examine MHC patterns with subsets of chemical compounds found in feathers and we hope to tease apart whether particular genetic profiles yield identifiable variation in odor profile. This is one of the only studies to investigate the interrelationships of genes, volatile chemistry and behavior in detail in any vertebrate, let alone a bird. The study is not yet completed, and there is every indication that the results will be of significance to a wide variety of questions in ecology, behavior, genetics and human biology. This research program has been instrumental in training several undergraduate and graduate students (including a Hispanic student) in field ecology, molecular biology and sensory neuroscience, and has offered numerous opportunities for sharing techniques and resources between Harvard and UC Davis.
