Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission

Abstract

The past 30 years of immunological research have revealed much about the proximate mechanisms of maternal antibody transmission and utilization, but have not adequately addressed how these issues are related to evolutionary and ecological theory. Much remains to be learned about individual differences within a species in maternal antibody transmission as well as differences among species in transmission or utilization of antibodies. Similarly, maternal-effects theory has generally neglected the mechanisms by which mothers influence offspring phenotype. Although the environmental cues that generate maternal effects and the consequent effects for offspring phenotype are often well characterized, the intermediary physiological and developmental steps through which the maternal effect is transmitted are generally unknown. Integration of the proximate mechanisms of maternal antibody transmission with evolutionary theory on maternal effects affords an important opportunity to unite mechanism and process by focusing on the links between genetics, environment and physiology, with the ultimate goal of explaining differences among individuals and species in the transfer of immune function from one generation to the next.

Heritable variation in maternally derived yolk androgens, thyroid hormones and immune factors

“…Yolk IgY concentration showed a tendency for low to moderate heritability but this was not statistically significant. Previous data from poultry and quail suggest a heritable basis for maternal IgY and lysozyme transfer (Grindstaff et al, 2003;Abdel-Moneim and Abdel-Gawad, 2006;Okuliarova et al, 2014). The lack of significant heritability for yolk IgY concentration may be due to lack of power (given the large s.e.s).…”

“…Indeed, high heritability of egg size in birds has been reported (reviewed in Williams, 2012). Additionally, other resources in the egg, such as antioxidants, immune factors and signals such as hormones, are now widely acknowledged as crucial for offspring fitness-related traits (McNabb and Wilson, 1997;von Engelhardt and Groothuis, 2011;Grindstaff et al, 2003). Estimating and verifying the genetic variation in the transfer of resources and developmental signals to the egg is important because it is often assumed that it is shaped by natural selection (Müller et al, 2007;Tschirren et al, 2014) and importantly, it could contribute to the evolution of multiple offspring traits.…”

“…These include immune factors, such as immunoglobulins (IgYs) (for example, Grindstaff et al, 2003) and albumen antimicrobial proteins (for example, lysozyme: Saino et al, 2002), which affect hatching success, growth and even survival in birds (reviewed in Grindstaff et al, 2003). Thus parent-offspring conflict and trade-offs between female survival and embryo survival may exist, and selection may be opposite for mothers and offspring.…”

“…Thus parent-offspring conflict and trade-offs between female survival and embryo survival may exist, and selection may be opposite for mothers and offspring. In poultry, artificial selection experiments on immune factors suggest a genetic basis of IgY and lysozyme transfer (Grindstaff et al, 2003;Abdel-Moneim and Abdel-Gawad, 2006;Okuliarova et al, 2014), but there are no studies on their heritability in non-domestic birds.…”

In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides

“…In mammals, antibodies are transferred across the placenta before birth and postnatally via breast milk (24). Birds, fish, and reptiles transmit passive immunity through the deposition of antibodies in eggs (25). Because of the diversity of microbes to which they and their offspring are exposed, animals that deposit their embryos in ponds and lakes, such as amphibians and fish, would be expected to have robust, reliable antimicrobial defenses.…”