Haemoproteus infected birds have increased lifetime reproductive success.

The impact of haematozoan infection on host fitness has received substantial attention since Hamilton and Zuk posited that parasites are important drivers of sexual selection. However, short-term studies testing the assumption that these parasites consistently reduce host fitness in the wild have produced contradictory results. To address this complex issue, we conducted a long-term study examining the relationship between naturally occurring infection with Haemoproteus and Plasmodium, and lifetime reproductive success and survival of Mountain White-crowned Sparrows. Specifically, we tested the hypothesis that birds infected with haematozoan parasites have reduced survival (as determined by overwinter return rates) and reproductive success. Contrary to expectation, there was no relationship between Haemoproteus and Plasmodium infection and reproduction or survival in males, nor was there a relationship between Plasmodium infection and reproduction in females. Interestingly, Haemoproteus-infected females had significantly higher overwinter return rates and these females fledged more than twice as many chicks during their lifetimes as did uninfected females. We discuss the impact of parasitic infections on host fitness in light of these findings and suggest that, in the case of less virulent pathogens, investment in excessive immune defence may decrease lifetime reproduction.

Natural selection and glucocorticoid physiology.

Glucocorticoid hormones are considered potent modulators of trade-offs between reproduction and survival. As such, selection should affect glucocorticoid physiology, although relatively little is known about how selection may act on glucocorticoid profiles. In general, the evolution of physiology is less studied and less well understood than morphological or life history traits. Here, we used a long-term data set from a population of mountain white-crowned sparrows to estimate natural selection on glucocorticoid profiles. Our study suggests that survival selection favours higher hormone concentrations for multiple components of glucocorticoid physiology (both baseline and stress-induced glucocorticoid levels). Fecundity selection varies depending on the component of hypothalamic-pituitary-adrenal physiology; greater reproductive output was associated with higher baseline glucocorticoid levels, but lower stress-induced glucocorticoid levels. Additionally, the selection gradient was greater for glucocorticoids than for a morphological trait (wing length). These results support the hypothesis that stress-induced glucocorticoids increase survival over reproduction within a wild population (the CORT-trade-off hypothesis). Taken together, these results add to our knowledge of how selection operates on physiological traits and also provide an evolutionary and ecological perspective on several key open issues in the field of glucocorticoid physiology.

Assessing the role of reproduction and stress in the spring emergence of haematozoan parasites in birds.

A spring emergence of avian haemosporidian infections is nearly universal among temperate zone birds and is often described as a cost of reproductive effort. We take advantage of the opportunistic (i.e. aseasonal) breeding schedule of the red crossbill (Loxia curvirostra) to determine the relative contributions of season versus host physiology to the timing and intensity of Haemoproteus infections in the temperate zone. Despite breeding activity in both the winter and summer, Haemoproteus infections were highly seasonal--occurring largely from May through September--and measures of host physiology (i.e. reproductive condition and stress parameters) did not explain parasite prevalence. However, within the spring-summer peak, infection intensity (i.e. parasite density) was positively correlated with plasma levels of testosterone and free corticosterone and negatively correlated with corticosterone binding globulin capacity. These data are discussed in terms of the behavioral ecology of host and vector, and suggest that both seasonal increases in vector activity and relapse of latent (i.e. dormant) infections contribute to the spring emergence in birds. Relapse of latent infections does not appear to be induced by reproductive activity or increased allostatic (i.e. energy) load, but rather by a season-specific change in host or parasite physiology (e.g. melatonin or endogenous rhythms).

Obligate versus rich patch opportunism: evolution and endocrine mechanisms.

Opportunistic breeding has been hypothesized to evolve in response to rare or unpredictable resource pulses. In this traditional view of opportunism, individuals invest heavily in reproduction whenever conditions are permissive for breeding, perhaps at the expense of investment in survival. We term this strategy 'obligate opportunism' (OBO). We also present an additional strategy that could account for the evolution of opportunism. High mobility may allow individuals to move between rich patches of resources that are spatially or temporally unpredictable, reducing exposure to food scarcity and taking advantage of breeding opportunities. This strategy, which we term 'rich patch exploiter' (RPE), predicts that investment in survival-enhancing processes may occur at the expense of reproduction despite high resource availability. We review examples to determine which opportunists better match predictions from the OBO strategy or the RPE strategy and then review endocrine profiles in the context of the two strategies.

Body composition and amino acid concentrations of select birds and mammals consumed by cats in northern and central California.

The diet of the feral domestic cat consists of primarily birds and small mammals, but the nutritional composition is relatively unknown. Because of the increasing popularity of natural diets for cats and other wild captive carnivores, the purpose of this study was to describe the body composition and AA concentrations of select birds and small mammals in northern and central California: wild-caught mice (n = 7), Norway rats (n = 2), roof rats (n = 2), voles (n = 4), moles (n = 2), gophers (n = 3), and birds (n = 4). Body water, crude fat (CFa), CP, ash, and AA composition for each specimen were determined. Results are reported as mean ± SD. All results are reported on a DM basis except body water (as-is basis) and AA (g/16 g N). Combined, carcasses had this mean composition: 67.35 ± 3.19% water, 11.72 ± 6.17% CFa, 62.19 ± 7.28% CP, and 14.83 ± 2.66% ash. Concentrations of Arg, Tau, Cys, and Met were 5.63 ± 0.46, 0.92 ± 0.33, 1.91 ± 0.89, and 1.82 ± 0.19 g/16 g N, respectively. Using NRC physiologic fuel values for CP, CFa, and carbohydrate by difference, the combined average energy content of the carcasses was 3,929 kcal/kg DM, but the fiber content was not determined. With the exception of mice and rats, little historical data exist regarding the body and AA composition of many of the species analyzed in this study. Wild-caught mice and rats were composed of less fat but more ash compared with previously reported data in their purpose-bred counterparts. The CP content of mice in this study was similar to previous reports in purpose-bred mice. The CP content of rats was similar or slightly greater compared with historical findings in purpose-bred rats. The N content of rats and AA concentrations on a per-N basis for both rats and mice were similar to previously published data on purpose-bred rodents. The discrepancies in nutrient composition, especially fat concentration, indicate that using purpose-bred animals to represent the diet of the feral domestic cat may not be valid in many instances. When consumed to meet energy needs, the nutrient content of the species reported in the present study exceed the NRC (2006) recommended allowances (RA) for total fat, CP, and essential AA for felines at all life stages.

Gonadotropin-releasing hormone plasticity: a comparative perspective.

Gonadotropin-releasing hormone 1 (GnRH1) is a key regulator of the reproductive neuroendocrine system in vertebrates. Recent developments have suggested that GnRH1 neurons exhibit far greater plasticity at the cellular and molecular levels than previously thought. Furthermore, there is growing evidence that sub-populations of GnRH1 neurons in the preoptic area are highly responsive to specific environmental and hormonal conditions. In this paper we discuss findings that reveal large variation in GnRH1 mRNA and protein expression that are regulated by social cues, photoperiod, and hormonal feedback. We draw upon studies using histochemistry and immediate early genes (e.g., c-FOS/ZENK) to illustrate that specific groups of GnRH1 neurons are topographically organized. Based on data from diverse vertebrate species, we suggest that GnRH1 expression within individuals is temporally dynamic and this plasticity may be evolutionarily conserved. We suggest that the plasticity observed in other neuropeptide systems (i.e. kisspeptin) may have evolved in a similar manner.

Variation in gonadotrophin-releasing hormone-1 gene expression in the preoptic area predicts transitions in seasonal reproductive state.

In many seasonally reproducing animals, the experience of prolonged exposure to constant photoperiods results in the induction of a state of photorefractoriness, which is defined as a lack of responsiveness to a previously stimulatory photoperiod. The physiological and genetic processes that control photorefractoriness are not well understood; however, the hallmark of photorefractoriness is an endogenous change in the physiological response to a constant photoperiod. It is already known that preoptic area (POA) gnrh1 gene expression declines during the development of refractoriness to long-day stimulation in European starlings. We employed in situ hybridisation histochemistry to characterise changes in POA gnrh1 mRNA expression during the reinstatement of photosensitivity in female starlings. Photorefractory starlings moved to short days (8L:16D) increased optical density of gnrh1 expressing cells within 10 days. Exposure to 30 short days resulted in greater visible gnrh1 cell numbers, with no detectable change in measures of ovarian follicular volume and oviduct mass. We subsequently examined the extent of gnrh1 expression in response to photostimulation after incremental periods on short day lengths. A significant long-day-induced increase in both gnrh1 expression and ovarian and oviduct mass occurred only after at least 30 short days. These findings demonstrate that the recovery of photorefractoriness involves an increase in gnrh1 mRNA expression and expands upon our previous knowledge that the development of photosensitivity is associated with an increase in both the precursor proGnRH1-GAP and GnRH1 peptides in the POA. Importantly, the change in the brain sensitivity occurs well before such changes can be detected via variation in ovarian activity.

Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird.

Stimulus-induced expression of the immediate early gene ZENK (egr-1) in the songbird's auditory forebrain presumably depends on the behavioral significance of the stimulus. Few studies, however, have quantified both the ZENK and behavioral responses to a stimulus in the same individuals. We played conspecific male song of either hatch (local) or foreign dialect to female white-crowned sparrows (Zonotrichia leucophrys oriantha) and quantified both the auditory ZENK response and their behavioral response, which is known to depend on dialect. Birds hearing hatch dialect showed greater ZENK induction in the caudomedial hyperstriatum ventrale and the dorsal portion of the caudomedial neostriatum than birds hearing foreign dialect, supporting previous work showing a relationship between ZENK and salience of the stimulus. In the dorsal portion of the caudomedial neostriatum, ZENK induction was correlated with the amount of non-vocal courtship behavior; however, in the caudomedial hyperstriatum ventrale, ZENK induction was more highly correlated with the females' own vocal behavior and thus may have been partly self-induced. Some females sang and showed a male-like pattern of ZENK induction in their song systems. This study provides the first evidence that the ZENK response in a sensory area to a social stimulus is proportional to the animal's preference for the stimulus.

Differential mechanisms for regulation of the stress response across latitudinal gradients.

We examined plasticity of the stress response among three populations of the white-crowned sparrow (Zonotrichia leucophrys). These populations breed at different elevations and latitudes and thus have breeding seasons that differ markedly in length. We hypothesize that in populations where birds raise only one or rarely two broods in a season, the fitness costs of abandoning a nest are substantially larger than in closely related populations that raise up to three broods per season. Thus individuals with short breeding seasons should be less responsive to stressors and therefore less likely to abandon their young. In our study, baseline and handling-induced corticosterone levels were similar among populations, but corticosteroid-binding globulins differed, leading to a direct relationship between stress-induced free corticosteroid levels and length of breeding season. There were also population-specific differences in intracellular low-affinity (glucocorticoid-like) receptors in both liver and brain tissue. Although investigations of population-based differences in glucocorticoid secretion are common, this is the first study to demonstrate population-level differences in binding globulins. These differences could lead to dramatically different physiological and behavioral responses to stress.

Seasonal changes in brain GnRH immunoreactivity and song-control nuclei volumes in an opportunistically breeding songbird.

White-winged crossbills (Loxia leucoptera) are opportunistic breeders that can nest at almost any time of year if there is sufficient food. Other cardueline finches that have been shown to breed on a strictly seasonal schedule become absolutely refractory to the stimulatory effects of long-day photoperiod, dramatically down-regulate hypothalamic gonadotropin-releasing hormone (GnRH), and reduce the volume of several song-control nuclei in autumn. This study examined whether changes in photoperiod modify the GnRH and song-control systems in white-winged crossbills. Adult male and female crossbills were captured and held on a naturally changing photoperiod. Brains of male and female birds were collected in May, October, and January. GnRH content was assessed by immunocytochemistry and the volumes of Nissl-defined song-control nuclei (HVc, Area X, and the robust nucleus of the archistriatum) were reconstructed. In contrast to other cardueline finches, GnRH immunoreactivity was relatively stable across the year, exhibiting only modest seasonal variation. The song control system, on the other hand, exhibited large seasonal changes as well as sex differences. Thus, crossbills appear to maintain hypothalamic GnRH content year round, perhaps to facilitate a rapid response to favorable breeding conditions, even on short days. However, song control nuclei are dramatically affected by photoperiod. Future work should examine these systems in crossbills breeding on short days to compare photoperiod-dependent and -independent effects on neural plasticity.

Photoperiodic regulation of the reproductive axis in male zebra finches, Taeniopygia guttata.

In arid central Australia, breeding of zebra finches (Taeniopygia guttata) tends to take place immediately after the aperiodic rainfall-this being irrespective of the time of year. As a result, zebra finches have traditionally been considered nonphotoperiodic. Despite this, there are some published reports of photoperiodic effects on behavior in zebra finches. Therefore, we transferred singly housed male zebra finches from a photoperiod of 14 h light and 10 h dark per day (14L:10D) to either 20L:4D or 8L:16D. Control birds remained exposed to 14L:10D. Plasma LH, testicular volume, and body mass were assessed at the start of the experiment and at intervals for a period of 56 days. Testicular mass was measured at the end of the 56-day period. Plasma LH increased significantly in the 20L:4D group after 14 days, but decreased again by 56 days, presumably an effect of increased gonadal steroid negative feedback. Plasma LH did not change significantly in the other two groups. Testicular volume increased steadily in the 20L:4D group during the treatment period and it was significantly higher than that of the 8L:16D group at the end of the experiment. After 56 days of treatment, combined testicular mass in the 20L:4D group was much greater than that of the 8L:16D group, but not quite statistically different from the 14L:10D group. There was no statistical difference in testicular mass between the 14L and 8L groups. Body mass did not differ between any of the groups at any time in the experiment. Our results are consistent with zebra finches being photoperiodic to some degree, despite their opportunistic breeding strategy. When considered in conjunction with recent reports of photoperiodic responses in tropical avian species, these data suggest that the ability to respond to changing photoperiod is more common among avian species than previously hypothesized.

Effects of ambient temperature on photo-induced prolactin secretion in three subspecies of white-crowned sparrow, Zonotrichia leucophrys.

We tested the effects of naturally relevant ambient temperatures (5, 20, and 30 degrees C) on photoinduced prolactin (PRL) secretion in three subspecies of white-crowned sparrow, Zonotrichia leucophrys. In all three subspecies, transfer from short to long days triggered an increase in plasma PRL typical of an avian seasonal breeder. In Z. l. gambelii, which breeds at high latitudes, temperature does not affect the rate of photoinduced gonadal maturation or luteinizing hormone (LH) secretion. In this subspecies, we found that changes in plasma PRL concentrations were similar in all temperature treatments. In Z. l. pugetensis, which breeds in the Pacific Northwest, high temperatures accelerate gonadal development in females but not males and does not affect LH secretion. In this subspecies, we found that like gonadal growth, photoinduced changes in PRL secretion in Z. l. pugetensis vary with ambient temperature in females but not males. In Z. l. oriantha, which breeds in alpine regions of the West, both males and females respond to temperature cues by modulating gonadal growth but not LH secretion. We found in Z. l. oriantha that ambient temperature affects PRL secretion in both sexes. These results suggest that PRL may be involved in the transduction of ambient temperature cues used to time reproductive development and the termination of seasonal breeding. Alternatively, temperature-mediated differences in plasma PRL may be a result rather than a cause of differences in gonadal development, since sex steroids affect PRL secretion in some species.

Seasonal variation in brain GnRH in free-living breeding and photorefractory house finches (Carpodacus mexicanus).

Absolute photorefractoriness in captive birds of several species correlates with reduced hypothalamic content of gonadotropin-releasing hormone (GnRH) relative to photosensitive or photostimulated birds. We used immunocytochemistry to examine GnRH immunostaining in free-living breeding and photorefractory house finches (Carpodacus mexicanus). Photorefractory birds with regressed gonads in early autumn had lower GnRH immunoreactivity (fewer, smaller, less intensely stained cell bodies and fewer immunopositive axon fibers) than did breeding birds with enlarged gonads in spring. These results confirm that absolute refractoriness in house finches is associated with dramatic changes in the hypothalamic GnRH system, as in other species with this type of refractoriness, and show that these changes occur in free-living birds.

Effects of day length and temperature on gonadal development, body mass, and fat depots in white-crowned sparrows, Zonotrichia leucophrys pugetensis.

We tested the effects of ambient temperature (5 degrees, 20 degrees, and 30 degrees) on photoperiodically induced reproductive functions in male and female white-crowned sparrows, Zonotrichia leucophrys pugetensis. Transfer from short days (9L 15D) to long days (16L 8D) resulted in rapid testicular growth and partial ovarian development in all three temperature treatments. There were no differences in sizes of testes and cloacal protuberance following 30 or 70 days of exposure to long days at the different temperatures. However, brood patch and follicular development were enhanced in females at 30 degrees compared with the 5 degrees and 20 degrees groups. Many of these females exposed to 30 degrees had large yolky follicles by Day 70. This enhancement was evident only when females were housed in the same room with males, however. Despite the effects of high temperature on ovarian development, there were no differences among groups in plasma levels of follicle-stimulating hormone or luteinizing hormone, suggesting that differential ovarian development may have been mediated by gonadal sensitivity to gonadotropins rather than by differential secretion of these hormones. We examined circulating levels of corticosterone (B) and both tri-iodothyronine (T3) and thyroxine (T4) as possible regulators of this differential ovarian sensitivity to gonadotropins. Plasma B levels showed transitory increases in males at 5 degrees and 20 degrees, but were suppressed in males at 30 degrees. Titers of B were not influenced by temperature treatments in females. Circulating T4 increased following photostimulation in both sexes, but this increase was reduced at 5 degrees. T3 concentrations in plasma were highly variable and not influenced by either photo-period or temperature in males, but were significantly lower in females exposed to 30 degrees by Day 70. Thus, B and T4 levels do not appear to help explain differential ovarian development, but circulating T3 levels cannot yet be excluded as a regulator of ovarian sensitivity to gonadotropins. Long days resulted in no change, or a gradual decrease, in body mass and fat deposit in males and females, and temperature regimes had no further effects on fattening or body mass. Thus, reproductive development under long days appears to be resistant to naturally relevant temperature extremes in male Z.l. pugetensis, whereas follicular development (i.e., yolk deposition in follicles leading to ovulation and onset of nesting) can be enhanced by high temperature. Reasons for the dimorphism in this response are unknown, but may be explained by the role of females in determining onset of final ovarian maturation and nesting in relation to favorable environmental conditions. In a second experiment, in which the sexes were isolated from one another, we determined the effects of the same treatments on.Z.I. pugetensis. Again there was no effect of temperature on photoperiodically induced testicular growth, and the enhancement of follicular development in females at 30 degrees was greatly reduced in the absence of males. We also continued this experiment up to 116 days of treatment to investigate effects on onset of photorefractoriness (spontaneous gonadal regression) and onset of prebasic moult. In both sexes it was clear that low temperature (5 degrees) retarded gonadal regression and high temperature (30 degrees) advanced it. Similarly, the prebasic moult score was greater at 30 degrees and less at 5 degrees in both sexes. There were no effects of temperature on plasma levels of LH at Day 116 of treatment, but plasma levels of T4 were higher in the 5 degrees group of both males and females sampled at Day 116. Clearly, the effects of temperature can have different effects on gonadal recrudescence, onset of breeding (yolk deposition), and termination of breeding. Whether these influences of temperature on reproductive function at different stages in the breeding cycle have different mechanisms remains to be determ

Interrelationship of day length and temperature on the control of gonadal development, body mass, and fat score in white-crowned sparrows, Zonotrichia leucophrys gambelii.

We tested the effects of naturally relevant environmental temperatures on long day-induced reproductive development in male and female white-crowned sparrows, Zonotrichia leucophrys gambelii. Transfer from short days (8L 16D) to long days (20L 4D) resulted in rapid testicular development and partial ovarian development as has been reported many times previously. Exposure of experimental groups to low (5 degrees), moderate (20 degrees), and high (30 degrees) temperature during photostimulation had only subtle effects on plasma levels of follicle-stimulating hormone and luteinizing hormone over time and no effects on the size of testes, cloacal protuberance, ovaries, or brood patch at Day 30 of treatment. Long days resulted in the well known increase in body mass and fat score, indicative of preparations for migration. In females, treatment with low temperature resulted in a reduction in the premigratory increase in fat and body mass when transferred to long days. This was accompanied by an increase in plasma levels of corticosterone during the early stages of photostimulation at low temperature. Temperature regimes had no effects on fattening or body mass in males, despite an early increase in plasma corticosterone at low temperature. Circulating levels of thyroxine (T4) and triiodothyronine (T3) increased to varying degrees following photostimulation. Temperature treatment had no effect on plasma levels of thyroid hormones in males, but low temperature did inhibit thyroid hormone secretion (particularly T4) in females. Although reproductive development appears to be resistant to naturally relevant temperature extremes in both sexes, low environmental temperature impaired preparations for migration in females but not males. This effect may be mediated through glucocorticosteroids and not thyroid hormones. Reasons for the sexual dimorphism in this response are unknown, but may be related to sexual selection for males to arrive on the breeding grounds ahead of females regardless of local weather conditions.

Changes in brain GnRH associated with photorefractoriness in house sparrows (Passer domesticus).

Temperate zone birds terminate reproduction when they become photorefractory. In many species, refractoriness is "absolute" in that gonadal regression occurs before day length declines, and individuals are reproductively unresponsive even to continuous light. Based on studies of a few species, this form of refractoriness appears to be associated with a reduction (compared with breeding and/or photosensitive birds) in numbers of hypothalamic cells and fibers that are immunoreactive for gonadotropin releasing hormone (GnRH). Some species display "relative" refractoriness, in that day length must decline before gonadal regression occurs, and individuals never lose the capacity to respond to very long days. A few reports suggest that GnRH levels in the brain do not change in relatively refractory birds. House sparrows (Passer domesticus) regress their gonads sooner when day length declines during summer than they do if photoperiod is not permitted to decline after the summer solstice (i.e., they appear to be "relatively" refractory). However, if held on long days they eventually regress the gonads despite no decline in photoperiod (they appear to be "absolutely" refractory). In this experiment, we tested whether gonadal regression was associated with changes in hypothalamic GnRH in adult male house sparrows. We used immunocytochemistry (primary antibody sensitive to both forms of avian GnRH) to compare the distribution and number of GnRH-immunoreactive cells and fibers among reproductively active individuals on long days, "absolutely" refractory individuals on long days, and presumably "relatively" refractory individuals induced to regress by shortened days. Similar reductions in ir-GnRH cell number and cell size occurred in both groups of refractory birds compared with birds still in breeding condition. Gonadal regression also was correlated with reduced staining intensity of cell bodies and reduced fiber staining, but these reductions were somewhat more pronounced in the "absolutely" than the "relatively" refractory birds. We discuss these results in light of other studies of avian GnRH changes with reproductive stage. Our results are consistent with the idea that house sparrows become absolutely refractory, regardless of whether exposed to a decline in photoperiod. However, the results also suggest that relative refractoriness may induce gonadal regression through a cessation of GnRH secretion, whereas absolute refractoriness involves down-regulation of peptide production as well.