Ecological and life-history factors influencing the evolution of maternal antibody allocation: a phylogenetic comparison

Abstract

Maternally derived yolk antibodies provide neonates with immune protection in early life at negligible cost to mothers. However, developmental effects on the neonate's future immunity are potentially costly and thus could limit yolk antibody deposition. The benefits to neonatal immunity must be balanced against costs, which may depend on neonate vulnerability to pathogens, developmental trajectories and the immunological strategies best suited to a species' pace of life. We measured yolk antibodies and life-history features of 23 species of small Neotropical birds and assessed the evidence for each of several hypotheses for life history and ecological effects on the evolution of yolk antibody levels. Developmental period and yolk antibodies are negatively related, which possibly reflect the importance of humoral immune priming through antigen exposure, and selection to avoid autoimmunity, in species with a slower pace of life. There is also a strong relationship between body size and yolk antibody concentration, suggesting that larger species are architecturally equipped to produce and transfer higher concentrations of antibodies. These results suggest that developmental effects of maternally derived antibodies, such as imprinting effects on B-cell diversity or autoimmune effects, are important and deserve more consideration in future research.

Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology

“…Our results thus highlight that the maternal transfer of antibodies may well be a key example of an adaptive transgenerational-induced response with far-reaching implications [52,53]. The only study that investigated the relationship between the transfer of maternal antibodies and the pace of life suggested that slow-living species deposit less immunoglobulin Y (IgY) in the yolk of their eggs [12]. However, this study is based on the quantification of levels of antibodies in the egg yolk and did not consider the persistence of the transferred antibodies in the newborn, nor accounted for the level of circulating antibodies in the mother plasma at the time of egg laying.…”

“…Interestingly, this receptor is also responsible for the uptake of antibodies from the egg yolk in the hatchling [60]. An increase in the expression of the FcRY or in the strength of the FcRY-IgY interaction could thus not only contribute to greater half-lives of IgY but would also help hatchlings achieve high levels of circulating IgY despite a possible lesser investment of females in egg yolk deposition of IgY in longer lived birds [12]. Evidence for the possibility of such mechanisms comes from studies of the mammalian counterpart of FcRY, the neonatal Fc receptor (FcRn), which is implicated in both the transfer of antibodies from mother to young and the recycling of IgG (see [61] for a review).…”

“…The temporal persistence of those maternal antibodies has been shown to be positively related to the level of antibodies initially transferred in the egg yolk within a given species [17], but little is known about the potential role of other factors. In particular, within and among-species variability in the propensity to transfer immune protection has been largely overlooked in vertebrates [9,12], and investigations with non-model species in natural settings have the potential to lead to important findings. The few studies conducted so far with species other than classical avian models have consistently reported a relatively short temporal persistence of those antibodies [17 -23] and some evidence of variability among species [17,23,24].…”

The influence of year, laying date, egg fertility and incubation, individual hen, hen age and mass and clutch size on maternal immunoglobulin Y concentration in captive Steller's and spectacled eider egg yolk

“…Newly hatched ducklings depend on maternal immunoglobulin Y (IgY), which is the primary antibody in serum and the principal antibody involved in defense against systemic infections (Davison et al, 2008;Lundqvist et al, 2006). The passive immunity provided by the mother to the hatchling protects the offspring against disease agents present in the environment, and can be especially important in dense breeding populations where disease transmission may be enhanced (Addison et al, 2009;Garnier et al, 2012). Maternal IgY will form complexes with antigens to protect the duckling and alleviate pressure on the duckling's developing immune system (Addison et al, 2009).…”

Female pipefish can detect the immune status of their mates

“…However, nongenetically based immune information may also influence mate choice and is the focus of the present paper. For example, the transfer of parental immune experience to offspring, socalled trans-generational immune priming (TGIP), can result in an induced offspring immune response against prevailing parasite genotypes (Sadd et al 2005;Boulinier and Staszewski 2008;Addison et al 2009;Jokela 2010;Roth et al 2010;Sepp et al 2011;Moreau et al 2012;Zhang et al 2013). Mate choice favoring individuals with immune experience may also pay off as previous parasitic experience could result in increased investment into reproduction, since the likelihood to survive and reproduce in the future is decreased (terminal investment theory: Clutton-Brock 1984;Simmons 1994;Bonneaud et al 2004).…”