Aerobic power and flight capacity in birds: a phylogenetic test of the heart-size hypothesis.

Flight capacity is one of the most important innovations in animal evolution; it only evolved in insects, birds, mammals and the extinct pterodactyls. Given that powered flight represents a demanding aerobic activity, an efficient cardiovascular system is essential for the continuous delivery of oxygen to the pectoral muscles during flight. It is well known that the limiting step in the circulation is stroke volume (the volume of blood pumped from the ventricle to the body during each beat), which is determined by the size of the ventricle. Thus, the fresh mass of the heart represents a simple and repeatable anatomical measure of the aerobic power of an animal. Although several authors have compared heart masses across bird species, a phylogenetic comparative analysis is still lacking. By compiling heart sizes for 915 species and applying several statistical procedures controlling for body size and/or testing for adaptive trends in the dataset (e.g. model selection approaches, phylogenetic generalized linear models), we found that (residuals of) heart size is consistently associated with four categories of flight capacity. In general, our results indicate that species exhibiting continuous hovering flight (i.e. hummingbirds) have substantially larger hearts than other groups, species that use flapping flight and gliding show intermediate values, and that species categorized as poor flyers show the smallest values. Our study reveals that on a broad scale, routine flight modes seem to have shaped the energetic requirements of birds sufficiently to be anatomically detected at the comparative level.

Coronary blood flow in the anesthetized American alligator (Alligator mississippiensis).

Coronary circulation of the heart evolved early within ectothermic vertebrates and became of vital importance to cardiac performance in some teleost fish, mammals and birds. In contrast, the role and function of the coronary circulation in ectothermic reptiles remains largely unknown. Here, we investigated the systemic and coronary arterial responses of five anesthetized juvenile American alligators (Alligator mississippiensis) to hypoxia, acetylcholine, adenosine, sodium nitroprusside, isoproterenol, and phenylephrine. We recorded electrocardiograms, monitored systemic blood pressure, blood flows in both aortae, and blood flow in a major coronary artery supplying most of the right ventricle. Coronary arterial blood flow was generally forward, but there was a brief retrograde flow during a ventricular contraction. Blood pressure was significantly changed in all conditions. Acetylcholine decreased coronary forward flow, but this response was confounded by the concomitant lowered work of the ventricles due to decreased heart rate and blood pressure. Coronary forward flow was poorly correlated with heart rate and mean arterial pressure across treatments. Overall changes in coronary forward flow, significant and not significant, were generally in the same direction as mean arterial pressure and ventricular power, approximated as the product of systemic cardiac output and mean arterial pressure.

Early stress causes sex-specific, life-long changes in behaviour, levels of gonadal hormones, and gene expression in chickens.

Early stress can have long-lasting phenotypic effects. Previous research shows that male and female chickens differ in many behavioural aspects, and respond differently to chronic stress. The present experiment aimed to broadly characterize long-term sex differences in responses to brief events of stress experienced during the first weeks of life. Chicks from a commercial egg-laying hybrid were exposed to stress by inducing periods of social isolation during their first three weeks of life, followed by a broad behavioural, physiological and genomic characterization throughout life. Early stressed males, but not females, where more anxious in an open field-test, stayed shorter in tonic immobility and tended to have delayed sexual maturity, as shown by a tendency for lower levels of testosterone compared to controls. While early stressed females did not differ from non-stressed in fear and sexual maturation, they were more socially dominant than controls. The differential gene expression profile in hypothalamus was significantly correlated from 28 to 213 days of age in males, but not in females. In conclusion, early stress had a more pronounced long-term effect on male than on female chickens, as evidenced by behavioral, endocrine and genomic responses. This may either be attributed to inherent sex differences due to evolutionary causes, or possibly to different stress related selection pressures on the two sexes during commercial chicken breeding.

The strong selective sweep candidate gene ADRA2C does not explain domestication related changes in the stress response of chickens.

Analysis of selective sweeps to pinpoint causative genomic regions involved in chicken domestication has revealed a strong selective sweep on chromosome 4 in layer chickens. The autoregulatory α-adrenergic receptor 2C (ADRA2C) gene is the closest to the selective sweep and was proposed as an important gene in the domestication of layer chickens. The ADRA2C promoter region was also hypermethylated in comparison to the non-selected ancestor of all domesticated chicken breeds, the Red Junglefowl, further supporting its relevance. In mice the receptor is involved in the fight-or-flight response as it modulates epinephrine release from the adrenals. To investigate the involvement of ADRA2C in chicken domestication, we measured gene expression in the adrenals and radiolabeled receptor ligand in three brain regions comparing the domestic White Leghorn strain with the wild ancestor Red Junglefowl. In adrenals ADRA2C was twofold greater expressed than the related receptor gene ADRA2A, indicating that ADRA2C is the predominant modulator of epinephrine release but no strain differences were measured. In hypothalamus and amygdala, regions associated with the stress response, and in striatum, receptor binding pIC50 values ranged between 8.1-8.4, and the level was not influenced by the genotyped allele. Because chicken strains differ in morphology, physiology and behavior, differences attributed to a single gene may be lost in the noise caused by the heterogeneous genetic background. Therefore an F10 advanced intercross strain between White Leghorn and Red Junglefowl was used to investigate effects of ADRA2C alleles on fear related behaviors and fecundity. We did not find compelling genotype effects in open field, tonic immobility, aerial predator, associative learning or fecundity. Therefore we conclude that ADRA2C is probably not involved in the domestication of the stress response in chicken, and the strong selective sweep is probably caused by selection of some unknown genetic element in the vicinity of the gene.

Transgenerational effects of early experience on behavioral, hormonal and gene expression responses to acute stress in the precocial chicken.

Stress during early life can profoundly influence an individual's phenotype. Effects can manifest in the short-term as well as later in life and even in subsequent generations. Transgenerational effects of stress are potentially mediated via modulation of the hypothalamic-pituitary-adrenal axis (HPA) as well as epigenetic mechanisms causing heritable changes in gene expression. To investigate these pathways we subjected domestic chicken (Gallus gallus) to intermittent social isolation for the first three weeks of life. The early life stress resulted in a dampened corticosterone response to restraint stress in affected birds and in their male offspring. Stress-specific genes, such as early growth response 1 (EGR1) and corticotropin releasing hormone receptor 1 (CRHR1), were upregulated immediately after restraint stress, but not under baseline conditions. Treatment differences in gene expression were also correlated across generations which indicate transgenerational epigenetic inheritance. In an associative learning test early stressed birds made more correct choices suggesting a higher coping ability in stressful situations. This study is the first to show transgenerational effects of early life stress in a precocial species by combining behavioral, endocrinological, and transcriptomic measurements.

Fetal development of baroreflex sensitivity: the chicken embryo as a case model.

The baroreflex is the main short term compensatory mechanism to buffer blood pressure changes and maintain circulatory homeostasis. Its ontogeny and importance during prenatal life is not fully understood so we used broiler chickens to investigate the maturation of the baroreflex in late incubation using a novel method that measured changes in heart rate during spontaneous fluctuations in blood pressure. Our results suggest that a baroreflex is already functional at d17 with no indication of further maturation in terms of sensitivity (gain at 17 d was 52.9±8.3 and at 20 d 69.5±16.2 ms kPa(-1)). The physiological relevance of these values is shown using data surrogation methods. Although the results contrast with the progressive baroreflex maturation indicated by the pharmacological method, we sustain that both methods provide information on baroreflex regulation. While the spontaneous method evaluates truly physiological (but small) pressure changes, the pharmacological method provides a more consistent and repetitive challenge for the reflex that requires a different recruitment of baroreflex effectors.