Examining the disconnect between prolactin and parental care in avian brood parasites

Abstract

Prolactin is often referred to as the “parental hormone” but there are examples in which prolactin and parental behavior are disconnected. One intriguing example is in avian obligate brood parasites; species exhibiting high circulating prolactin but no parental care. To understand this disconnect, we examined transcriptional and behavioral responses to prolactin in brown‐headed (Molothrus ater) and bronzed (M aeneus) brood parasitic cowbirds. We first examine prolactin‐dependent regulation of transcriptome wide gene expression in the preoptic area (POA), a brain region associated with parental care across vertebrates. We next examined prolactin‐dependent abundance of seven parental care‐related candidate genes in hypothalamic regions that are prolactin‐responsive in other avian species. We found no evidence of prolactin sensitivity in cowbirds in either case. To understand this prolactin insensitivity, we compared prolactin receptor transcript abundance between parasitic and nonparasitic species and between prolactin treated and untreated cowbirds. We observed significantly lower prolactin receptor transcript abundance in brown‐headed but not bronzed cowbird POA compared with a nonparasite and no prolactin‐dependent changes in either parasitic species. Finally, estrogen‐primed female brown‐headed cowbirds with or without prolactin treatment exhibited significantly greater avoidance of nestling begging stimuli compared with untreated birds. Taken together, our results suggest that modified prolactin receptor distributions in the POA and surrounding hypothalamic regions disconnect prolactin from parental care in brood parasitic cowbirds.

The neuroethology of avian brood parasitism

“…Saline-treated females spent more time near nestling begging sounds than random tones; however, this pattern reversed in females treated with either estrogen or estrogen and prolactin, resulting in significant interactions between hormone treatment and type of sound (Fig. 2A; Lynch et al, 2020). In this case, hormone-treated females avoided the begging nestling sound by spending more time near tones.…”

“…S2). Exogenous prolactin in female brown-headed cowbirds does not stimulate development of a brood patch, nest building or egg incubation even if administered with estradiol, progesterone or a combination of these hormones (Selander, 1960;Selander and Kuich, 1963;Selander and Yang, 1966;Lynch et al, 2020), although these hormones have been linked to parental behavior in other bird species (Angelier et al, 2016). These collective studies indicate a disconnect between prolactin and parental care in brood-parasitic species.…”

“…Candidate gene analysis also revealed no significant differences in transcript abundance between treatments in surrounding hypothalamic brain regions (Fig. S2), which included the paraventricular nucleus (PVN), ventromedial hypothalamic nucleus (VMN), lateral hypothalamic (LH) and tuberal hypothalamic regions (TU; Lynch et al, 2020; Fig. 1C-J).…”

“…This possibility was examined by comparing POA transcriptomes and candidate genes in surrounding hypothalamic regions of prolactintreated and untreated female brown-headed and bronzed (Molothrus aeneus) cowbirds. Transcriptome comparisons revealed only four transcripts were differentially expressed between prolactin-treated and untreated birds (Lynch et al, 2020;Fig. 1A,B), none of which were relevant to parental or other social behaviors.…”

“…Although transcriptome comparisons indicate prolactin insensitivity, this does not appear to be the case at the behavioral level as the hormonal milieu necessary for the onset of parental care in other birds and mammals does not stimulate maternal-like behavior in female brown-headed cowbirds. On the contrary, it appears to stimulate nestling avoidance (Lynch et al, 2020). Female brown-headed cowbirds treated with estrogen, estrogen plus prolactin, or saline were placed in approach/avoidance tests with nests containing sounds of begging nestlings or random tones.…”