The heart of an acrobatic bird.

The courtship behavior of some species of birds can be energetically demanding, but it is unknown if cardiovascular specializations enable such behaviors. While performing a highly acrobatic courtship dance, heart rate in male golden-collared manakins increases briefly to 1300 beats per minute, among the highest heart rates recorded in any bird or mammal. We hypothesize that male manakins have enhanced cardiovascular capabilities to meet these demands on the heart. Using histological and molecular techniques, we examined manakin heart structure as well as expression of genes involved in Ca2+ handling, action potential duration, steroidal signaling and cardiac growth. These measures were also made on the hearts of zebra finches, a similar-sized bird with limited cardiovascular demands. Compared to the zebra finch, the manakin had a significantly thicker left ventricular (LV) muscle (cross-sectional thickness of the free LV wall and septum) with a smaller LV chamber. In addition, compared to zebra finches, manakin hearts had significantly greater gene expression of ryanodine receptors as well as androgen receptors. Testosterone (T) treatment of non-breeding manakins (with low T) increased gene expression of the Ca2+ pump SERCA. These observations suggest that hearts of breeding male manakins require specialized Ca2+ handling and androgens may facilitate manakin cardiovascular function.

Energetics of the acrobatic courtship in male golden-collared manakins (Manacus vitellinus).

In lek mating systems, females choose mates through indicators of quality, which males may exhibit by their performance of courtship displays. In temperate regions, displaying seasons are brief (one to two months), whereas in the tropics courtship seasons may be prolonged. Moreover, in temperate-breeding animals lekking behaviour can be energetically demanding, but little is known about the energy costs of lekking in tropical animals. Daily, over the course of a nearly seven-month-long breeding season, male golden-collared manakins (Manacus vitellinus) of Panamanian rainforests perform acrobatic courtship displays that markedly elevate heart rates, suggesting that they require high energy investment. Typically, animals of tropical lowland forests (such as manakins) exhibit a 'slow pace of life' metabolic strategy. We investigated whether male manakin courtship is indeed metabolically costly or whether the birds retain a low daily energy expenditure (DEE), as seen in other tropical species. To assess these questions, we calibrated manakin heart rate against metabolic rate, examined daily lek activity and, using telemetry, obtained heart rates of individual wild, lekking male manakins. Although metabolic rates peak during courtship displays, we found that males actually invest minimal time (only approx. 5 min d(-1)) performing displays. As a consequence, the DEE of approximately 39 kJ d(-1) for male manakins is comparable to other lowland tropical species. The short, intense bursts of courtship by these birds make up only approximately 1.2% of their total DEE. Presumably, this cost is negligible, enabling them to perform daily at their arenas for months on end.

Neural sensitivity to sex steroids predicts individual differences in aggression: implications for behavioural evolution.

Testosterone (T) regulates many traits related to fitness, including aggression. However, individual variation in aggressiveness does not always relate to circulating T, suggesting that behavioural variation may be more closely related to neural sensitivity to steroids, though this issue remains unresolved. To assess the relative importance of circulating T and neural steroid sensitivity in predicting behaviour, we measured aggressiveness during staged intrusions in free-living male and female dark-eyed juncos (Junco hyemalis). We compared aggressiveness to plasma T levels and to the abundance of androgen receptor (AR), aromatase (AROM) and oestrogen receptor alpha (ORα) mRNA in behaviourally relevant brain areas (avian medial amygdala, hypothalamus and song control regions). We also asked whether patterns of covariation among behaviour and endocrine parameters differed in males and females, anticipating that circulating T may be a better predictor of behaviour in males than in females. We found that circulating T related to aggressiveness only in males, but that gene expression for ORα, AR and AROM covaried with individual differences in aggressiveness in both sexes. These findings are among the first to show that individual variation in neural gene expression for three major sex steroid-processing molecules predicts individual variation in aggressiveness in both sexes in nature. The results have broad implications for our understanding of the mechanisms by which aggressive behaviour may evolve.