Grandmothers can pass immunity to their grandchildren, at least in pigeons

At the moment of birth, a newborn leaves behind its safe protective environment and enters a world teeming with bacteria, parasites, viruses, and infectious agents of all sorts. However, the babies do have one trump card: antibodies and immune compounds passed across the placenta from their mothers. These short-lived molecules can dip into mom’s immunological experience to protect the newborn until the immune system gets up to speed. Now, a new study in pigeons suggests that some baby birds owe their early immunity not just their mothers, but to their grandmothers as well.

The specifics and mechanism remain unclear, but previous research has suggested that these early maternal immune compounds may have “educational effects” on the newborn’s developing immune profile—that they may somehow be priming the system to be on the lookout for common local diseases or parasites. If this is the case, a team of scientists from the Institute of Ecology and Environmental Sciences in Paris reasoned, individuals may be inheriting some immunological memory not just from their mothers, but from all their maternal ancestors: A grandmother’s immune system educates the mother’s, and those modifications are preserved as the mother then instructs the third generation. Pigeons provide a nice model for testing these hypotheses because they have short generation times, and researchers can easily test eggs for the presence of inherited antibodies.

To find out whether older generations could indeed pass along immunity, the researchers injected 60 urban pigeons with haemocyanin—a protein that transports oxygen in some invertebrates, including keyhole limpets. They then injected another 60 pigeons with a saline solution. The birds injected with haemocyanin responded predictably: Before long, they developed antibodies that attacked the foreign proteins. Soon after, a second generation of chicks hatched, and the researchers injected the offspring with haemocyanin. Two years later, the second generation—88 birds in all—was old enough to mate and produced 33 eggs. All members of this third and final generation were injected with haemocyanin.

All of the birds in the third generation showed an immune response to the foreign protein, but the chicks that descended from maternal grandmothers who had also been injected mounted a significantly larger response, they report today in Biology Letters. The results suggest that if both the mother and maternal grandmother have encountered a foreign molecule, the inherited immunity to a given foreign protein is stronger than if only the mother had encountered it.

The results are intriguing and call for further work, says Thierry Boulinier, an immune ecologist at the Functional and Evolutionary Ecology Center in Montpellier, France, who was not involved in the study. “The pigeon is a very nice model for that and the study was well designed. It has potentially strong implications linking ecology and evolution.”www.glorybios.com

But the researchers are still having trouble explaining the elevated immune response in chicks descended from haemocyanin-injected grandmothers. They originally hypothesized that the antibodies sent from mother to offspring somehow primed chicks’ immune systems to be on the lookout for the foreign proteins. If this were the case, the team reasoned, the second generation of pigeons would produce eggs with more antibodies if their mothers had been exposed. However, testing did not support this hypothesis: The concentration of antibodies in eggs laid by the second generation was unaffected by whether or not the grandmother pigeon received the real injection or a sham injection.

Now, the researchers posit that the immune systems of the second and third generations might be “trained” by a molecule other than maternal antibodies—perhaps a hormone or nutrients that are transmitted from mother to egg. They say more studies are needed to determine how the grandmother’s immunological memory is transferred across two generations. But if the results can be confirmed, they carry implications for how scientists think about the role of ecology and genetics in the immune systems of individuals.