Pre‐ and Postnatal Effects of Corticosterone on Fitness‐Related Traits and the Timing of Endogenous Corticosterone Production in a Songbird

Abstract

Maternally-derived corticosterone in the egg and corticosterone produced endogenously by altricial nestling birds play essential roles during development. Although persistently high corticosterone levels can be harmful, moderately elevated levels above baseline can lead to reallocation of resources between growth and maintenance to ensure immediate survival or to enhance the development of fitness-related traits. We tested two hypotheses concerning the fitness consequences of elevated corticosterone during pre-natal and post-natal development in altricial house wrens: (1) elevated corticosterone shifts resources away from growth and immune function and (2) elevated corticosterone serves as a signal to allocate resources to fitness-related traits. We also explored the development of the stress response, hypothesizing that early-stage nestlings have little endogenously produced corticosterone, but that their baseline and stress-induced corticosterone levels increase with age. Nestlings hatching from corticosterone-injected eggs were lighter at hatching, but through compensatory growth, ended up heavier than controls near the time of fledgling, an important, fitness-related trait. Nestlings that hatched from corticosterone-injected eggs and those given oral doses of corticosterone did not differ from controls in three other fitness-related traits: immunoresponsiveness, size, or haematocrit. Early- and late-stage nestlings had similar baseline corticosterone levels, and all nestlings increased their plasma corticosterone levels in response to a capture-and-restraint protocol, with older nestlings mounting a stronger stress-induced response than younger nestlings. These results suggest that pre-natal exposure to corticosterone is important in shaping offspring phenotype, and are consistent with the hypothesis that maternally derived corticosterone in the egg can have long-term, fitness-related effects on offspring phenotype.

Pre‐ and postnatal effects of experimentally manipulated maternal corticosterone on growth, stress reactivity and survival of nestling house wrens

“…There was also a significant postnatal effect of maternal corticosterone treatment (i.e., via its effect on maternal behaviour) on nestling stress reactivity. Collectively, these results parallel earlier, generally positive effects of prenatal corticosterone exposure in house wren nestlings in our study system (Bowers, Bowden, et al., ; Strange et al., ).…”

“…There were positive, prenatal effects of increased maternal plasma corticosterone (i.e., via the egg or, less likely, female incubation behaviour) on size-adjusted body mass and structural body size (i.e., tarsus length) of offspring. There also was a significant interaction between the corticosterone treatment of the female rearing young and the corticosterone treatment to which young had been prenatally exposed via the egg in their Collectively, these results parallel earlier, generally positive effects of prenatal corticosterone exposure in house wren nestlings in our study system (Bowers, Bowden, et al, 2016;Strange et al, 2016).…”

“…For example, in Japanese quail ( Coturnix japonica ), offspring of corticosterone‐manipulated females grew slower in their first week posthatching, but were not significantly different in size from control nestlings by adulthood (Hayward & Wingfield, ). Similarly, nestlings hatching from corticosterone‐injected eggs in our study population were lighter than control nestlings at hatching, but, through compensatory growth, were heavier near the time of nest‐leaving (Strange et al., ), a likely positive effect; however, there are often long‐term costs to compensatory growth (Grace, Froud, Meillère, & Angelier, ; Metcalfe & Monaghan, ; Monaghan, ). There is evidence of positive effects of prenatal corticosterone or cortisol exposure in a variety of taxa (Capelle, Semeniuk, Sopinka, Heath, & Love, ; Meylan & Clobert, ).…”

“…Perhaps the most striking pattern to emerge from the split‐brood cross‐fostering experiment was the interaction between pre‐ and postnatal maternal effects on nestling survival through to fledging: experimental nestlings had higher survival than control young when reared by control mothers, but there was no difference in survival when nestlings were reared by experimental mothers. It is easy to understand why survival of nestlings hatching from eggs laid by corticosterone‐manipulated mothers might be higher: this study and our earlier work have revealed that an increase in maternally derived corticosterone leads to increased body condition, body size and enhanced immune responsiveness of nestlings (Bowers, Bowden, et al., ; Bowers, Bowden, et al., ; Strange et al., ), traits predictive of offspring recruitment and longevity (Bowers et al., ). But why should the effect of maternal corticosterone treatment on nestling survival disappear when nestlings are reared by experimental mothers?…”

“…Development of avian embryos and neonates in an environment with increased maternal corticosterone can often have profound, long-lasting effects on their adult phenotype (e.g., Bowers, Bowden, Thompson, & Sakaluk, 2016;Schoech et al, 2011). Compared with the well-documented effects of corticosterone on adults (e.g., Adkins-Regan, Banerjee, Correa, & Schweitzer, 2013;Astheimer, Buttemer, & Wingfield, 1992;Jimeno, Briga, Hau, & Verhulst, 2018;Lõhmus, Sundström, & Moore, 2006;Love, Chin, Wynne-Edwards, & Williams, 2005) and nestlings and fledglings (e.g., Butler, Leppert, & Dufty, 2009;Crino et al, 2011;Kitaysky, Wingfield, & Piatt, 2001;Patterson, Winkler, & Breuner, 2011;Strange, Bowden, Thompson, & Sakaluk, 2016;Wada & Breuner, 2008), considerably less is known about effects of maternally derived corticosterone in the egg on the development of avian embryos (but see reviews in Henriksen, Rettenbacher, & Groothuis, 2011;Williams & Groothuis, 2015). This paucity of information persists despite the potential for all aspects of prenatal (embryonic) and even postnatal (nestling, fledgling) development to be affected by the presence of maternal corticosterone in the egg.…”