Immune Activation Generates Corticosterone-Mediated Terminal Reproductive Investment in a Wild Bird

Abstract

Despite classical expectations of a trade-off between immune activity and reproduction, an emergent view suggests that individuals experiencing activation of their immune system actually increase reproductive effort and allocation to offspring as a form of terminal investment in response to reduced survival probability. However, the components and mechanisms of increased parental investment following immunostimulation are currently unknown. We hypothesize that increased glucocorticoid production following immunostimulation modulates the increase in reproductive effort that constitutes terminal investment. We activated the immune system of breeding female house wrens (Troglodytes aedon) with an immunogen and cross-fostered the eggs they subsequently produced to separate pre- and post-natal components of maternal investment. Cross-fostering revealed an increase in both pre- and post-natal allocation from immunostimulated females, which was confirmed by quantification of egg constituents and maternal provisioning behavior. The increase in maternal provisioning was mediated, at least in part, by increased corticosterone in these females. Offspring immune responsiveness was also enhanced through transgenerational immune priming via the egg. Thus, our results indicate that maternal immunostimulation induces transgenerational effects on offspring through both pre- and post-natal parental effects, and support an important role for corticosterone in mediating parental investment.

Elevated corticosterone during egg production elicits increased maternal investment and promotes nestling growth in a wild songbird

“…We left the remaining eggs in the nest to develop and hatch naturally, and monitored the subsequent development of these nestlings. In a recent cross-fostering experiment in this population, we fostered offspring among nests prior to hatching and found that the concentration of corticosterone in egg yolks produced by females positively predicts the rate at which they deliver food to unrelated foster offspring after hatching; moreover, we found that offspring hatching from eggs with increased corticosterone attain enhanced body condition when reared by foster parents (Bowers et al 2015b). Thus, if corticosterone in mothers and their eggs modifies offspring behavior according to the environmental conditions they are likely to encounter after hatching, we predicted that offspring hatching from eggs produced by experimental females, with increased yolk-corticosterone concentrations, would beg for food at a higher rate than offspring of control females ( sensu Love and Williams 2008; Smiseth et al 2011; Sheriff and Love 2013), and that these offspring would attain better body condition prior to fledging than those of control females.…”

“…In the laboratory, we weighed (± 0.001 g) and measured the size of these eggs (length and breadth; ± 0.01 mm), before storing them at −20ºC. The concentration of yolk corticosterone in each egg was subsequently measured using competitive-binding radioimmunoassay (RIA) following a standardized protocol (Paitz et al 2011; Bowers et al 2015b). For the RIAs, we diluted yolk samples in 500 μL water and added radiolabeled (tritiated) steroid tracer to quantify recoveries of the extracted corticosterone following column chromatography.…”

“…In birds, for example, ostensibly stressful events, such as interactions with potential predators, often result in dramatic increases in glucocorticoids that promote self-maintenance at a cost to reproduction (Wingfield 2003; Romero et al 2009; Lothery et al 2014; Vitousek et al 2014; Jones et al 2016). However, in the absence of imminent threats, increased glucocorticoids can positively affect foraging, allocation to eggs, and parental care (Sinervo and DeNardo 1996; Crossin et al 2012; Love et al 2014; Bowers et al 2015b), and enhance survival in free-living populations (Sinervo and DeNardo 1996; Rivers et al 2012). There is also evidence that glucocorticoids can affect offspring phenotype (Sinervo and DeNardo 1996; McCormick 1998; Love et al 2005, 2013; Love and Williams 2008; Sheriff et al 2010; Giesing et al 2011; Sheriff and Love 2013).…”

“…Thus, egg-yolk corticosterone can serve as an integrated, non-invasive proxy of maternal physiology and may affect offspring development (Bowers et al 2015b). Moreover, conditions experienced prior to breeding are known to affect investment in eggs (Martin 1987; Nooker et al 2005; Ruffino et al 2012), and integrated measures of circulating corticosterone prior to the breeding season, as measured by corticosterone accumulated in feathers, recently have been found to predict egg size (Kouwenberg et al 2013), a trait that by itself has strong and persistent effects on offspring (Whittingham et al 2007; Krist 2011; Love and Williams 2011; Rollinson and Hutchings 2013; but see also Giordano et al 2014).…”

Experimental manipulation of incubation period reveals no apparent costs of incubation in house wrens

“…Parental provisioning at brood-days 4–5 is especially germane, as this is the age at which nestling growth is most rapid, and the amount of food delivered by parents at this age is positively correlated with nestling growth, fledging success and the recruitment of offspring to the breeding population (Bowers et al, 2014; Bowers, Bowden, Sakaluk, & Thompson, 2015). Recordings were made using pocket-sized digital video cameras (Kodak Sport Zx5, Eastman Kodak, Rochester, NY, U.S.A.) positioned about 1.5 m from the nestbox and secured at the end of a 1.5 m length of metal conduit (1.5 cm diameter) using a cell-phone holster (Barnett, Clairardin, Thompson, & Sakaluk, 2011; DeMory, Thompson, & Sakaluk, 2010; Dorset, Sakaluk, & Thompson, 2017; Will, Dorset, Thompson, Sakaluk, & Bowers, 2017).…”