Effects of early-life conditions on innate immune function in adult zebra finches

Abstract

Early life conditions can impact individuals for life, with harsh developmental conditions resulting in lower fitness, but the underlying mechanisms are not well understood. We hypothesised that immune function may be part of the underlying mechanism, when harsh developmental conditions result in less effective immune function. We tested this hypothesis by comparing innate immune function between zebra finches (Taeniopygia guttata) in adulthood (n=230; age 108 – 749 days) that were reared in either small or large broods. We used this experimental background to follow up our earlier finding that finches reared in large broods have a shorter lifespan. To render a broad overview of innate immune function, we used an array of six measures: bacterial killing capacity, haemagglutination, haemolysis, haptoglobin, nitric oxide, and ovotransferrin. We found no convincing evidence for effects of natal brood size on any of the six measures of innate immune function. This raised the question whether the origin of variation in immune function was genetic, and we therefore estimated heritabilities using animal models. However, we found heritability estimates to be low (range 0.04 – 0.11) for all measured immune variables, suggesting variation in innate immune function can largely be attributed to environmental effects independent of early-life conditions as modified by natal brood size.

Experimentally manipulated food availability affects offspring quality but not quantity in zebra finch meso-populations

“…Average brood sizes after cross-fostering were 2.6 (SD = 0.58, n = 48) and 5.5 (SD = 0.59, n = 34) for small and large broods respectively. As described in detail in Driessen et al ( 2021 ), growth rate from cross-fostering to day 15 was lower by 0.13 (range 0.10–0.17) grams per day in large broods; a notable difference as the average growth rate over all nestlings was 0.73 (SD 0.14) grams per day. Birds were kept with their parents until 35 days old, and subsequently moved to single-sex indoor aviaries (153 × 76 ×110 cm), together with four adults, two of each sex, to facilitate sexual imprinting.…”

Effects of manipulated food availability and seasonality on innate immune function in a passerine

“…We also investigated the effects of natal brood size manipulation and its interaction with the food availability manipulation. Previous work shows that growing up in a large brood did not affect innate immune function in adulthood within a benign foraging environment (Driessen et al, 2021 ), but the interaction with harsh foraging conditions was previously found to affect ageing and life span (Briga et al, 2017 ). These foraging and brood size manipulations are known to be effective in this model species (Briga et al, 2016 , 2017 ; Jimeno et al, 2017 ; Koetsier & Verhulst, 2011 ), in which immune function is also relatively well studied (Deerenberg et al, 1997 ; Driessen et al, 2021 ; Kriengwatana et al, 2013 ; Naguib et al, 2004 ; Tschirren et al, 2009 ; Verhulst et al, 2005 ).…”

“…Previous work shows that growing up in a large brood did not affect innate immune function in adulthood within a benign foraging environment (Driessen et al, 2021 ), but the interaction with harsh foraging conditions was previously found to affect ageing and life span (Briga et al, 2017 ). These foraging and brood size manipulations are known to be effective in this model species (Briga et al, 2016 , 2017 ; Jimeno et al, 2017 ; Koetsier & Verhulst, 2011 ), in which immune function is also relatively well studied (Deerenberg et al, 1997 ; Driessen et al, 2021 ; Kriengwatana et al, 2013 ; Naguib et al, 2004 ; Tschirren et al, 2009 ; Verhulst et al, 2005 ). One plausible outcome we predict is that, since harsh foraging and developmental conditions negatively affected life span, these manipulations will have a negative effect on overall immune function, thereby potentially contributing to the effect on life span.…”

“…They observed no effects of the food manipulation on immune function, although the sample size was small. We here report the effects of foraging environment in adulthood on a broad array of innate immune measures in zebra finches (Taeniopygia guttata, Vieillot 1817) reared in either small or large broods (Driessen et al, 2021), in a full 2 × 2 design measured over multiple years and seasons. To manipulate the foraging environment, we applied a technique to permanently increase foraging costs (Koetsier & Verhulst, 2011), allowing us to estimate effects of manipulated food availability without confounding effects of predation and competition.…”

“…Variation in traits is the outcome of an interplay of genetic and environmental components, but for the immune system, the variation that can be explained through additive genetic effects is often low (e.g. Ardia & Rice, 2006 ; Driessen et al, 2021 but see also Clapperton et al, 2009 ; Henryon et al, 2006 ), pointing to the environment as the dominant factor explaining immune variation. Environmental differences can indeed often be related to changes in various parts of the immune system.…”