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.
This project had the goal of discovering genetic and behavioral mechanisms by which birds choose mates and the genetic factors that influence the number and quality of offspring of mated pairs and the growth and survival of their offspring. Determining the genetic factors that influences these key aspects of life history has been a long-term goal of ecology and evolutionary biology, with clear relevance for humans and human behavior. It has been hypothesized that genes of the major histocompatibility complex (MHC), a cluster of genes in vertebrates with primary functions in disease resistance and immune response, have a strong influence on the process of choosing a mate for reproduction. The primary function of MHC genes is to bind fragments of bacteria and viruses that invade our bodies, and to present these fragments to key molecular players in the immune response so that our immune system can clear these infections. Because MHC genes are different in almost every individual, and because their structure allows them to bind different and sometimes-volatile fragments in an individual-specific manner, it is thought that MHC genes play a role behaviors that involve chemosensation, such as smell (olfaction). Thus both the MHC and the sense of smell have been thought to play an important role in the process of mate choice and it is important to understand the rules by which vertebrates use the MHC to individually choose mates. Studies demonstrating an affect of MHC on the mating process have been conducted in mice, humans and other mammals, but there are few such studies in birds, so it is unclear how general and widespread the effects of MHC genes are. We chose to study MHC in the context of mate choice and chick growth in a small seabird called a storm-petrel, because storm-petrels exhibit several key traits that make them likely candidates for a role of MHC genes in the mating process. The species we studied was the Leach’s Storm Petrel (Oceanodroma leucorhoa), a ~380 gram seabird with colonies all over the Atlantic and Pacific seaboards of the United States and Canada. We studied a colony on Bon Portage Island (BPI) on the southern tip of Nova Scotia. Unlike many birds they have an excellent olfactory system with large olfactory lobes in the brain. They nest in burrows underground, often mate for life, and their chicks have an intriguing life history pattern that takes them 45 days to incubate in the egg and hatch – a long time for a bird of its size. They are easily studied by reaching into their burrows and extracting chicks or adults. Once a bird is extracted, it was weighed, measured and a blood sample and a chemical swab were taken to characterize volatile compounds of both the bird and the burrow. Back in the lab at Harvard we characterized the MHC genes from the blood samples using molecular biology techniques. We found that Leach’s Storm Petrels have two MHC genes in the particular class we studied (class II) and that they are both polymorphic. We produced sequences of these genes at both the nucleotide and amino acid levels, evolutionary comparisons of storm-petrel alleles to those of other birds, and distributions of the alleles in the population at BPI. (An allele [pronounced ‘ah-LEEL’] is a particular form or sequence of a given gene in an individual). We also showed 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 are currently studying two of the most common alleles (01 and 02), since we have found that chicks with these two alleles seem to grow faster than chicks with other alleles. Overall our studies have allowed us to characterize MHC class II genes in petrels and to set the stage for detailed studies of MHC genotypes in mated pairs (adult birds found in single burrows) and the effect of MHC on chick growth. In the future we will correlate MHC patterns yet further with detailed chemical profiles of each bird to discern the effect of particular alleles. We now have hundreds of blood samples and chemical swabs from petrels from BPI and which will allow us to examine the interrelationships of genes, chemistry and behavior in detail. Although the study is not yet completed, the results will be of significance to a wide variety of questions in ecology, behavior, genetics and human biology. In the process of this project we trained several undergraduates in biological research; these students have now gone on to begin their careers in areas such as field biology and neurobiology. We have also supported a postdoctoral fellow who received valuable training in molecular biology techniques.
