Wilson's Phalarope (Phalaropus tricolor) is a sex role-reversed species in which incubation of eggs and care of young is performed exclusively by the male. Plasma levels of prolactin (PRL), the hormone most associated with parental care in birds, are higher in incubating males than in nonincubating males or females. Conversely, plasma testosterone levels are reduced in males during incubation. In an attempt to characterize the physiological basis of this unusual parental care system, we used quantitative film autoradiography and densitometry to measure the specific binding in vitro of 125I-ovine PRL to 12 brain regions in females, nonincubating males, and incubating males during the normal breeding season. We also measured hypothalamic chicken gonadotropin-releasing hormone I (cGnRH-I) in three brain areas in these same birds, as well as plasma levels of PRL and testosterone. Analysis revealed that cGnRH-I concentrations in the preoptic area and plasma testosterone levels were significantly lower in incubating males than in nonincubating males. Specific binding of 125I-ovine PRL was detected in choroid plexus and in several diencephalic brain regions of both sexes, with highest binding activity recorded in the dorsolateral thalamus, medial habenula, nucleus subrotundus, and preoptic area. When adjustments were made for the large number of comparisons performed, specific binding did not vary significantly by sex or breeding stage in any single brain region. However, average specific binding values in nonincubating males exceeded those of incubating males in 9 of the 11 PRL-sensitive regions examined. Increased occupancy of the receptor by endogenous PRL during incubation could have contributed to this result, since plasma PRL levels were elevated in incubating males. In addition, PRL binding activity in several of these brain regions tended to correlate negatively with plasma PRL. The two exceptions to this general pattern were the preoptic area and the lateral septum, where mean specific binding was 14-15% higher in incubating males than in nonincubating males. This raises the interesting possibility that PRL sensitivity is up-regulated during incubation in some regions of the male phalarope brain, such as the preoptic area and lateral septum, that have been implicated in PRL-modulated changes in behavior and reproductive activity during this breeding stage.
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We thank Robert Hnasko for his expert technical assistance in conducting PRL binding assays and densitometric analysis of autoradiographs and Nicola Thompson for her work in tissue preparation for the cGnRH-I assay. We also acknowledge the National Hormone and Pituitary Program, NIDDK, NICHHD for supplying purified ovine PRL for these studies. This work was supported by NIMH Grant MH41447 to J.B. and by NRI Grant 92-37203-7742 to M.A.O. This is scientific contribution 9261 of the Maryland Agriculture Experiment Station.