Neuroendocrine patterns underlying seasonal song and year-round territoriality in male black redstarts

Camila P Villavicencio,Manfred Gahr,Pietro B D’Amelio,Wolfgang Goymann,René Quispe,Harriet Windley

doi:10.1186/s12983-021-00389-x

Abstract

BackgroundThe connection between testosterone and territoriality in free-living songbirds has been well studied in a reproductive context, but less so outside the breeding season. To assess the effects of seasonal androgenic action on territorial behavior, we analyzed vocal and non-vocal territorial behavior in response to simulated territorial intrusions (STIs) during three life-cycle stages in free-living male black redstarts: breeding, molt and nonbreeding. Concurrently, we measured changes in circulating testosterone levels, as well as the mRNA expression of androgen and estrogen receptors and aromatase in the preoptic, hypothalamic and song control brain areas that are associated with social and vocal behaviors.ResultsTerritorial behavior and estrogen receptor expression in hypothalamic areas did not differ between stages. But plasma testosterone was higher during breeding than during the other stages, similar to androgen receptor and aromatase expression in the preoptic area. The expression of androgen receptors in the song control nucleus HVC was lower during molt when birds do not sing or sing rarely, but similar between the breeding and the nonbreeding stage. Nevertheless, some song spectral features and the song repertoire differed between breeding and nonbreeding. Territorial behavior and song rate correlated with the expression of steroid receptors in hypothalamic areas, and in the song control nucleus lMAN.ConclusionsOur results demonstrate seasonal modulation of song, circulating testosterone levels, and brain sensitivity to androgens, but a year-round persistency of territorial behavior and estrogen receptor expression in all life-cycle stages. This suggests that seasonal variations in circulating testosterone concentrations and brain sensitivity to androgens is widely uncoupled from territorial behavior and song activity but might still affect song pattern. Our study contributes to the understanding of the complex comparative neuroendocrinology of song birds in the wild.

Highlights

The connection between testosterone and territoriality in free-living songbirds has been well studied in a reproductive context, but less so outside the breeding season
Territorial behaviors Non-vocal territorial behaviors measured during the simulated territorial intrusions (STIs) were similar between seasons (Fig. 1): Approach latency (F (2, 30) = 0.75, p = 0.48, R2 = − 0.01), time spent in a five meter radius around the decoy (F (2, 30) = 0.99, p = 0.38, R2 = − 0.0004), nodding frequency (F (2, 30) = 2.06, p = 0.15, R2 = 0.06), and closest approach (F (2, 30) = 0.45; p = 0.64, R2 = − 0.04) did not differ between seasons
Regarding the extent of non-vocal territorial behaviors and androgen/estrogen receptor, or aromatase mRNA expression measured in the hypothalamic areas (POA and posterior hypothalamus) we found that the frequency of nodding behavior correlated positively with the expression of aromatase in the preoptic area (POA) when corrected for stage (Faro=7.33, Fstage = 2.36, p = 0.02, R2 = 0.25)

Summary

Introduction

The connection between testosterone and territoriality in free-living songbirds has been well studied in a reproductive context, but less so outside the breeding season. Male birds sing and establish a territory at the onset of the breeding season when circulating levels of testosterone are high Thereby, testosterone can influence several reproductive traits, including vocal and non-vocal territorial behavior [3,4,5]. Androgenic control of vocal and non-vocal territoriality is more evident in species that are territorial and sing only during the breeding season. Plasma testosterone may facilitate vocal and non-vocal territorial behavior during breeding, but not outside the breeding season [9,10,11,12], especially in species that sing year-round or during extended periods [7, 13]. The relationship between circulating testosterone and territorial behaviors can vary among species with different life histories, and within species among different life-cycle stages

Methods

Results

Discussion

Conclusion