Maternally transmitted parasite defence can be beneficial in the absence of parasites

Abstract

Newborn animals do not have a fully functional immune system and are thus impaired in their ability to fight parasites. Mothers can therefore increase the survival probability of their young by providing them with passive immunity, e.g. in the form of maternal antibodies transferred via the placenta or the eggs. The maternal responses are only induced when parasites are present, and have been observed not only in vertebrates but also in invertebrates. However, while these parasite‐induced maternal effects are known to reduce the harmful effects of common parasites, they may also impose costs for the young, either because the maternal response impairs parental performance, or because maternally transmitted products moderate offspring development. We experimentally tested these two hypotheses in a wild great tit population. We exposed birds to a common ectoparasite before egg‐laying to induce the maternal response, and thereafter separated egg‐mediated maternal effects from effects on post‐laying parental performance by cross‐fostering whole clutches. To assess the costs of this response without its confounding benefits, we kept nests free of parasites after hatching. Since the costs of maternal effects can be expressed differently under relaxed and harsh rearing conditions, we simultaneously manipulated clutch size. First, parasite‐exposed parents raised lighter young, suggesting that parasite defence or the induced maternal response are costly to the parents and reduce their capacity to raise young. Second, under relaxed but not under harsh rearing conditions, young with the flea‐induced maternal effect were heavier and were in better body condition than controls, suggesting that the maternally transferred products can be allocated to physiological functions beyond parasite defence.

Offspring quality and tick infestation load in brood rearing great titsParus major

“…One of the mechanisms may be that poor quality parents have less effective resistance mechanisms against ticks and/or attract more ticks, while also spending less effort in food provisioning to the nestlings. For example, in great tit parents the capacity to raise young was reduced when being experimentally exposed to a common nest ectoparasite ( Ceratophyllus gallinae , Gallizzi et al 2008b), while also the tick loads of exposed parents were higher than in unexposed parents (Gallizzi et al 2008a). Another mechanism may be that in conditions with poor food availability – causing a reduction in nestlings’ body condition – a change in parental microhabitat use (i.e.…”

Predation risk affects offspring growth via maternal effects

“…In order to prevent any parasite related maternal effects (Tschirren, Richner & Schwabl 2004;Gallizzi, Guenon & Richner 2008; we heat-treated the nest material of all the nests when it reached 2 cm in height, and additionally cleaned the nest box thoroughly using a hard brush to remove any remaining fleas or larvae from the box, thus eliminating all naturally occurring ectoparasites in the nest at this stage (Richner, Oppliger & Christe 1993). Reproductive cycles of fleas take about 3 weeks (Tripet & Richner 1999), and flea immigration into nests is weak (Heeb et al 1996).…”

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

“…Because most IgY is produced in a specific response to an immune challenge, neonates receive protection against pathogens likely to be relevant within their lifetime, and thus their passive immunity is shaped by their mothers' previous disease exposure. Maternally derived antibodies benefit chicks through two documented routes; first, they directly interfere with pathogenicity by coating pathogens (Carlier & Truyens 1995;Leuridan & Van Damme 2007;Nemeth et al 2008), and second, they reduce the demands on the neonate immune system, and thus free resources to be directed towards other growth or maintenance needs (Pihlaja et al 2006;Gallizzi et al 2008;Grindstaff 2008). There has also been a proposed imprinting effect of maternal antibodies on immune development of offspring (Lemke & Lange 1999), where the B-cell repertoire is proposed to be modelled after the antibodies present during development.…”