Patterns of stress response to foreign eggs by a rejecter host of an obligate avian brood parasite

Abstract

One of the most effective defenses of avian hosts against obligate brood parasites is the ejection of parasitic eggs from the nests. Despite the clear fitness benefits of this behavior, individuals within so-called "egg-rejecter" host species still show substantial variation in their propensity to eliminate foreign eggs from the nest. We argue that this variation can be further understood by studying the physiological mechanisms of host responses to brood parasitic egg stimuli: independent lines of research increasingly support the hypothesis that stress-related physiological response to parasitic eggs may trigger egg rejection. The "stress-mediated egg rejection" hypothesis requires that hosts activate the stress-response when responding to parasitic egg stimuli. We tested this prediction by asking whether hosts showed differential stress response when exposed to host-like (mimetic) or parasite-like (non-mimetic) eggs. We experimentally parasitized incubating American robins Turdus migratorius, a robust egg-rejecter host to obligate brood parasitic brown-headed cowbirds Molothrus ater, with mimetic or non-mimetic model eggs. To assess the stress response, we measured the heart rate in incubating females immediately after experimental parasitism. We also measured plasma corticosterone and, in a subset of birds, used RNA-sequencing to analyze the expression of proopiomelanocortin (POMC), a precursor of adrenocorticotropic hormone, 2 h after experimental parasitism. We found that egg type had no effect on heart rate. Two hours following experimental parasitism, plasma corticosterone did not differ between the differently-colored model egg treatments or between rejecter and accepter females within the non-mimetic treatment. However, females exposed to non-mimetic eggs showed an upregulation of POMC gene expression (before FDR correction) in the pituitary compared with females treated with mimetic eggs. Our findings suggest that in an egg-rejecter host species, non-mimetic parasitic eggs may increase the activity of the stress-related hypothalamic-pituitary-adrenal axis compared with mimetic eggs, although the temporal dynamics of this response are not yet understood.

Keywords: HPA axis; coevolution; egg rejection; host–parasite interactions.

FIGURE 1

Experimental parasitism treatments in a natural American robin nest: (a) mimetic blue model egg and (b) a non‐mimetic beige model egg

FIGURE 2

The effect of model egg treatment on heart rate. Heart rate following the addition of non‐mimetic beige eggs did not differ from heart rate following the addition of mimetic blue egg in a separate set of experimentally parasitized females (n = 21). Black dots show time‐specific average heart rate for individual females.

FIGURE 3

The effect of model egg treatment on corticosterone levels. Baseline corticosterone did not differ between females experimentally parasitized with non‐mimetic beige eggs (n = 21) or mimetic blue eggs (n = 22). Black dots indicate females that had not rejected the model egg within 2 h, while red dots indicate females that rejected the model egg. Within the non‐mimetic egg treatment, females that rejected and accepted the eggs did not differ in their corticosterone levels.

FIGURE 4

The effect of model egg treatment on (a) POMC and (b) ATF3 expression in the pituitary in a subset of female American robins. Prior to FDR correction, females experimentally parasitized with non‐mimetic beige eggs (n = 6) showed higher POMC and ATF3 expression compared with females experimentally parasitized with mimetic blue eggs (n = 7). Black dots indicate females that had had not rejected the model egg within 2 h, while red dots indicate females that rejected the model egg. Neither POMC nor ATF3 expression differences were significant after FDR correction.

FIGURE 5

POMC expression in the pituitary was not correlated with plasma corticosterone concentration 2 h following experimental parasitism (n = 13) of American robins. Shaded area indicates the 95% confidence interval.

FIGURE A1

Microphone‐fitted model egg for heart rate recording. (a) model egg before it is covered by a balloon and painted. The microphone is positioned on the egg equator; (b) finished and painted microphone‐fitted egg (indicated by the red arrow) placed in a natural American robin nest. The egg is positioned so that the microphone (covered by a balloon) makes contact with the brood patch of an incubating female.

FIGURE A2

Example heart rate trace from an incubating female after arrival at the nest. Each dot indicates instantaneous heart rate for each heartbeat. Heartbeats were scored by hand and the instantaneous heart rate calculated using formula 1/(time between two successive heart beats).