Effect of female sexual displays on the endocrine physiology and behaviour of male white-crowned sparrows, Zonotrichia leucophrys

In photoperiodic birds, endocrine responses to behavioural interactions between males and females may be involved in temporally "fine-tuning" the onset of reproduction to yearly variations in the environment. This study examined the endocrine and behavioural responses of male White-crowned sparrows ( Zonotrichia leucophrys ) to changes in the endocrine state of the female, as signalled by changes in her behaviour. Males on different photoperiodic regimes were paired with oestrogen-treated, sexually receptive females. Males exposed to gonadostimulatory long days mounted and copulated with oestrogen-treated females even before gonadal development was complete. These males had higher plasma levels of testosterone and luteinizing hormone and maintained enlarged testes longer than control males paired with untreated, nonreceptive females. Males maintained on nonstimulatory short days also mounted oestrogen-treated females; however, testes of these males remained nonfunctional and their plasma levels of testosterone and luteinizing hormone were basal. Thus, reproductive function of photostimulated males is profoundly affected by changes in the endocrine state and behaviour of the female. However, male sexual behaviours are expressed in response to visual and auditory stimuli from the female regardless of male hormonal condition or photoperiodic treatment.     

Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii)

Exposing vertebrates to pathogenic organisms or inflammatory stimuli, such as bacterial lipopolysaccharide (LPS), activates the immune system and triggers the acute phase response. This response involves fever, alterations in neuroendocrine circuits, such as hypothalamo-pituitary-adrenal (HPA) and -gonadal (HPG) axes, and stereotypical sickness behaviors that include lethargy, anorexia, adipsia, and a disinterest in social activities. We investigated the hormonal, behavioral, and thermoregulatory effects of acute LPS treatment in a seasonally breeding songbird, the white-crowned sparrow (Zonotrichia leucophrys gambelii) using laboratory and field experiments. Captive male and female sparrows were housed on short (8L:16D) or long (20L:4D) day lengths and injected subcutaneously with LPS or saline (control). LPS treatment activated the HPA axis, causing a rapid increase in plasma corticosterone titers over 24 h compared to controls. Suppression of the HPG axis occurred in long-day LPS birds as measured by a decline in luteinizing hormone levels. Instead of a rise in body temperature, LPS-injected birds experienced short-term hypothermia compared to controls. Birds treated with LPS decreased activity and reduced food and water intake, resulting in weight loss. LPS males on long days experienced more weight loss than LPS males on short days, but this seasonal effect was not observed in females. These results paralleled seasonal differences in body condition, suggesting that modulation of the acute phase response is linked to energy reserves. In free-living males, LPS treatment decreased song and several measures of territorial aggression. These studies highlight immune-endocrine-behavior interrelationships that may proximately mediate life-history tradeoffs between reproduction and defense against pathogens.     

Hormonal control of female sexual behavior in the rat

Graded amounts of estradiol benzoate (ranging from 0.48 to 500 μg/kg) were administered to ovariectomized, adrenalectomized female rats in order to analyze the effects of estrogen on the qualitative and quantitative aspects of female reproductive behavior in this species. The interaction of hormone dose and copulatory stimulation was also investigated. In this study, soliciting behavior and lordosis responses were broken down into subcategories. There were three main results. First, it was found that the responses were hierarchically arranged such that, with increasing doses of hormone, the common elements of sexual responding appeared in the same order across individual females. Second, the chronic endocrine background of the female influenced the degree of her receptivity following an acute injection of estrogen. Third, repeated elicitation of lordosis by copulatory stimulation facilitated the subsequent occurrence of lordosis.     

Effects of corticosterone on territorial behavior of free-living male song sparrows Melospiza melodia

A group of 10 territorial male song sparrows, Melospiza melodia, were given subcutaneous implants of corticosterone in Silastic tubing. A second group of 10 territorial males were given empty implants as controls. After 18-24 hr all males were then subjected to a simulated territorial intrusion (STI) by placing a caged male song sparrow in the center of the subject's territory, and playing tape recorded songs through a speaker placed alongside. Significantly fewer males with corticosterone implants responded to STI than to controls, and the latency to respond was longer. Of the 3 experimental males that did respond to STI, all had a lower frequency of songs and did not approach the simulated intruder as closely as controls. Many males were captured 2-7 days after implantation and blood samples collected for measurement of circulating hormone levels. As expected, plasma levels of corticosterone were high in the group given corticosterone implants. However, plasma levels of luteinizing hormone (LH) were not affected by treatment with corticosterone, and although circulating levels of testosterone were depressed slightly compared with controls, they were within the normal range for territorial and breeding males. There were no differences in body mass despite greatly increased fat depots in males treated with corticosterone. These data suggest that high levels of corticosterone, similar to those measured during stressful episodes both in the laboratory and field, may suppress territorial behavior independently of the adenohypophysial-gonad axis. Since plasma levels of LH and testosterone are not depressed markedly, thus maintaining the gonads in a near functional state, renesting can begin as soon as environmental conditions ameliorate. Such mechanisms could potentially increase the probability of raising viable young after unpredictable, severe weather resulted in failure of the previous breeding attempt.     

Evidence for androgen independence of male mounting behavior in white-crowned sparrows (Zonotrichia leucophrys gambelii)

Previous experiments have shown that expression of mounting behavior in sexually inexperienced, adult male white-crowned sparrows does not require elevated plasma levels of androgen; adult males maintained on nonstimulatory short days mount sexually receptive females. The experiments reported here demonstrate that (1) sexually inexperienced, prepubertal males maintained on nonstimulatory short days show very low mounting rates in response to female sexual displays; (2) these males exhibit high mounting rates when exposed to stimulatory long days but androgen treatment on short days is ineffective in stimulating high mounting rates; and (3) prepubertal castration has no effect on the expression of mounting behavior by photostimulated adult males. Thus, there is no evidence that mounting behavior of adult male white-crowned sparrows depends on androgen.     

Hormonal specificity and activation of sexual behavior in male zebra finches

Castrated zebra finches receiving one of six hormone treatments were given three weekly tests with different females and their sexual behavior was contrasted with that of two control groups consisting of intact or castrated males given implants of cholesterol. The six hormone treatments were: two aromatizable androgens, testosterone (T) and androstenedione (AE); two nonaromatizable androgens, androsterone (AN) and dihydrotestosterone (DHT); an estrogen, estradiol (E); or a combination of E + DHT. Half the males receiving DHT received the 5α-isomer, half received the 5β-isomer. Castration significantly reduced the proportion of males which courted females, total courtship displays, high-intensity courtship displays, beak wiping activity, and significantly increased the latencies to show these behaviors compared to intact males. Castrated males never attempted to mount a female. All of these measures of courtship and copulatory behavior were restored to normal levels only by treatments providing both estrogenic and α-androgenic metabolites (i.e., T, AE, E + αDHT). AE was clearly the most effective of these, raising behavior significantly above normal on several measures. AN treatment was more effective than αDHT on all measures and not significantly different from intact birds on some. Treatment with E, αDHT, βDHT, or E + βDHT was totally ineffective. Surprisingly, females only solicited males whose hormone treatments provided estrogenic metabolites. Not only did they solicit males given aromatizable androgens, which showed high rates of courtship activity, they also solicited males given E or E + βDHT, some of which never even courted. Castration and hormone treatment also affected body and syringeal weight, but in opposite directions. Castration increased body weight while decreasing syringeal weight. Hormone treatments providing α-androgenic metabolites decreased body weight and increased syrinx weight. Treatments supplying estrogen as well were slightly more effective.     

Changes in sperm quality and numbers in response to experimental manipulation of male social status and female attractiveness

In promiscuous species, male reproductive success is determined by the interaction between the ability to access and choose females of the highest reproductive quality and, after copulation, the ability to outcompete the ejaculates of rival males. Disentangling the factors regulating the interplay between traits conferring a reproductive advantage before and after copulation is therefore crucial to understanding how sexual strategies evolve. Here we show in the fowl Gallus gallus, where social status determines copulation success, that dominant males produce more sperm than subordinates but that the quality of dominant males' sperm decreases over successive copulations, whereas that of subordinates remains constant. Experimentally manipulating male social status confirmed that ejaculate quality (the number and quality of sperm produced) was a response to the social environment rather than the result of intrinsic differences between dominant and subordinate males. We further show that dominant males responded to variation in female sexual ornamentation, which signals reproductive quality, by adjusting the number and quality of sperm they transferred, whereas subordinate males did not: they transferred ejaculates of similar quality to females with different ornament sizes. These results indicate that trade-offs between traits influencing reproductive success before and after copulation, combined with variation in social dynamics and female quality, may favor the evolution of phenotypically plastic alternative reproductive strategies.     

Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows

In males of several songbird species, the morphology of forebrain nuclei that control song changes seasonally. The only seasonally breeding songbird in which seasonal changes in the structure of song control nuclei have been reported not to occur is the nonmigratory Nuttall's subspecies of white-crowned sparrow. In the present study, we manipulated photoperiod and plasma testosterone concentrations in captive male white-crowned sparrows of the migratory Gambel's subspeices. Males exposed to photoperiods and plasma testosterone concentrations typical of those experienced by wild breeding males had larger song control nuclei than males held on a winter photoperiod. We also found seasonal change in stereotypy of spectral and temporal parameters of song in wild Gambel's white-crowned sparrows. We hypothesize that seasonal changes in song control nuclei may correlate with seasonal changes in song stereotypy. © 1995 John Wiley & Sons, Inc.     

Female Lincoln's sparrows modulate their behavior in response to variation in male song quality

Sexually reproducing organisms should mate with the highest quality individuals that they can. When female songbirds choose a mate, they are thought to use several aspects of male song that reflect his quality. Under resource-limited environmental conditions, male Lincoln's sparrows (Melospiza lincolnii) vary among one another in several aspects of song quality, including song length, song complexity, and trill performance. In a 2-pronged approach, we tested whether variation in song quality of male Lincoln's sparrows influences the behavior of females that are in a reproductive-like state. Over two trials, we exposed females to songs from the high and low ends of the distribution of naturally occurring song quality variation and found a higher level of behavioral activity in females exposed to high-quality songs, especially when they had first been exposed to low-quality songs. We also examined female phonotaxis toward antiphonally played songs with experimentally elevated and reduced trill performance and found that females moved preferentially toward the songs with elevated trill performance. Contrary to most studies investigating the behavioral responses of wild, female songbirds to variation in male song, we obtained our results without administering exogenous estradiol, which can artificially perturb the female's physiology. Our results demonstrate that the behavior of female Lincoln's sparrows is modulated by the quality of male songs to which they are exposed and that trill performance plays a significant role in this behavioral modulation. Furthermore, as the order of song quality presentation matters, it appears that recent song experience also influences female behavior.     

Aspects of risk-aversion in foraging white-crowned sparrows

Two series of aviary experiments with white-crowned sparrows (Zonotrichia leucophrys) are reported. The first series attempts to mimic foraging choices between microhabitats. The second series examines foraging choices made within a single artificial patch, a design intended to resemble dietary selection. In all experiments subjects chose between a constant food reward and a variable reward, the mean of which equalled the constant reward. Each experiment allowed the bird to feed at an overall rate greater than that minimally required for daily energy balance. In both series of experiments, the birds usually preferred the constant reward. Results of the first series do not differ significantly from previously reported preferences of dark-eyed juncos (Junco hyemalis), birds weighing 10 g less than the white-crowned sparrows.     

Decline of sexual behavior in castrated male rats: Effects of female precopulatory behavior

From the population of 89 adult sexually inexperienced Wistar male rats 20 animals that initiated copulatory behavior with females exhibiting low intensity of precopulatory behavior (presenting females) were preselected. Prior to castration all 20 males had the same sexual experience: three ejaculatory series in four weekly sessions with females exhibiting high intensity of precopulatory behavior (darting females). Following castration, the decline of copulatory behavior was much slower for the nine males tested with darting females as compared to the 11 males tested with presenting females. Male precopulatory behaviors (anogenital sniffing, touching flanks, etc) outlasted the loss of copulatory behavior and seem to be less dependent on both external and internal determinants. It is concluded that intensive external sexual stimuli can function to compensate, and therefore mask, the subnormal operation of androgen-dependent mechanisms in initiating the copulatory behavior.     

Corticosterone treatment has no effect on reproductive hormones or aggressive behavior in free-living male tree sparrows, Spizella arborea

We examined the effect of corticosterone on plasma levels of reproductive hormones (testosterone, dihydrotestosterone, and luteinizing hormone) and territorial defense behavior in male tree sparrows, Spizella arborea. Birds receiving Silastic implants filled with corticosterone (B) had significantly higher plasma levels of B than control birds, which received empty implants, and exhibited pectoral muscle wastage and a decrease in body mass. We evaluated the hormonal and agonistic responses of the two implanted groups of birds using a simulated territorial intrusion (STI) 2 to 4 days after they were implanted. Corticosterone-treated and control birds did not differ in their circulating levels of reproductive hormones or in their behavioral responses to STI (latency to respond to intrusion, number of songs, and closest approach to a decoy and tape recording). Unlike previous studies of north temperate passerines, high physiological levels of exogenous B had no effect either on circulating levels of reproductive hormones or on territorial behaviors associated with breeding. Nonetheless, untreated tree sparrows do mount a robust adrenocortical response, having a two- to fourfold increase in plasma B levels during a 1-h period of capture. Thus, adrenocortical responsiveness is maintained in these birds, but elevated levels of glucocorticoids do not suppress reproductive hormones or associated behaviors. We believe that this hormonal and behavioral refractoriness to glucocorticoids-or uncoupling of the stress response from the reproductive axis-may be advantageous for species having extreme temporal constraints on their breeding schedules.     

Integrating stress physiology,environmental change,and behavior in free-living sparrows

As weather deteriorates, breeding animals have a diverse array of options to ensure survival. Because of their mobility, birds can easily abandon territories to seek out benign conditions away from the breeding site. The timing of abandonment, however, may have repercussions for territory size, mate quality, reproductive success, and survival. There is a large body of evidence indicating that the adrenocortical response to stress plays a role in mediating the onset and maintenance of this behavioral switch. Here we develop a model describing the interactions of weather, food availability, body condition, and stress physiology in initiating departure from the breeding site. We tested the model using a population of white-crowned sparrows breeding at high elevation in the Sierra Nevada, where severe weather at the beginning of the breeding season often induces temporary abandonment of breeding territories and facultative altitudinal migration to lower elevation refugia. The data show that (1). during inclement weather, exogenous corticosterone delays return to the breeding site after territory abandonment; (2). during good weather, exogenous corticosterone alone does not induce territory abandonment, but does increase activity range around the breeding site; and (3). the magnitude of the corticosteroid response to stress is inversely related to body condition of the sparrow.     

Olfactory control of sexual behavior in the male and early-androgenized female hamster

Thirty-seven female hamsters, treated with either sesame oil or testosterone postnatally on days 2, 4, or 10 of life, and 25 male hamsters were given either olfactory bulbectomies or sham operations and tested for mounting behavior in adulthood. Extensive lesioning of the olfactory bulbs eliminated mounting in all subjects, suggesting that the mounting of early androgenized females is dependent upon the same sensory channels as the mounting of the males.     

Expression of adult female patterns of sexual behavior by male, female, and pseudohermaphroditic female rhesus monkeys

Gonadally intact pseudohermaphroditic female and normal female and neonatally castrated male rhesus monkeys were given estrogen treatment as adults and evaluated for attractivity, proceptivity, and receptivity during tests with a tethered stud male. Pseudohermaphrodites were produced by injecting their mothers during pregnancy with either testosterone propionate (TP) or dihydrotestosterone propionate (DHTP). Castrated males had reliably lower attractivity than normal females on all indicator responses shown by the tethered males. Additionally, castrated males showed reliably fewer proceptive responses on 4 of 5 measures than normal females. Receptivity could not be assessed in this situation for castrated males, because tethered males never contacted them unless the castrated males were displaying presentation. No reliable differences were observed between pseudohermaphrodites produced by prenatal treatments with TP or DHTP. Pseudohermaphrodites generally showed reliably less attractivity and proceptivity than normal females and reliably more of these traits than castrated males. Attractivity scores for pseudohermaphrodites were not different from those for normal females until proximity to the tethered male was established. Receptivity was not different in pseudohermaphrodites compared with normal females. Results indicate prenatal androgenization and its developmental sequelae lead to a defeminization in adulthood which, in this testing situation, was principally manifested by a deficiency in the performance of proceptive behaviors. Additionally, defeminization in rhesus monkeys, unlike that demonstrated in rodents, does not depend upon actions of an aromatizable androgen.     

Potential contribution of progesterone receptors to the development of sexual behavior in male and female mice

We previously showed that estradiol can have both defeminizing and feminizing effects on the developing mouse brain. Pre- and early postnatal estradiol defeminized the ability to show lordosis in adulthood, whereas prepubertal estradiol feminized this ability. Furthermore, we found that estradiol upregulates progesterone receptors (PR) during development, inducing both a male-and female-typical pattern of PR expression in the mouse hypothalamus. In the present study, we took advantage of a newly developed PR antagonist (ZK 137316) to determine whether PR contributes to either male- or female-typical sexual differentiation. Thus groups of male and female C57Bl/6j mice were treated with ZK 137316 or OIL as control: males were treated neonatally (P0–P10), during the critical period for male sexual differentiation, and females were treated prepubertally (P15–P25), during the critical period for female sexual differentiation. In adulthood, mice were tested for sexual behavior. In males, some minor effects of neonatal ZK treatment on sexual behavior were observed: latencies to the first mount, intromission and ejaculation were decreased in neonatally ZK treated males; however, this effect disappeared by the second mating test. By contrast, female mice treated with ZK during the prepubertal period showed significantly less lordosis than OIL-treated females. Mate preferences were not affected in either males or females treated with ZK during development. Taken together, these results suggest a role for PR and thus perhaps progesterone in the development of lordosis behavior in female mice. By contrast, no obvious role for PR can be discerned in the development of male sexual behavior.     

Vocal performance influences female response to male bird song: an experimental test

Female songbirds are thought to assess males based on aspectsof song, such as repertoire size or amount of singing, thatcould potentially provide information about male quality. Arelatively unexplored aspect of song that also might serve asan assessment signal is a male's ability to perform physicallychallenging songs. Trilled songs, such as those produced byswamp sparrows (Melospiza georgiana), present males with a performancechallenge because trills require rapid and precise coordinationof vocal tract movements, resulting in a trade-off between trillrate and frequency bandwidth. This trade-off defines a constrainton song production observed as a triangular distribution inacoustic space of trill rate by frequency bandwidth, with anupper boundary that represents a performance limit. Given thisbackground on song production constraints, we are able to identifya priori which songs are performed with a higher degree of proficiencyand, thus, which songs should be more attractive to females.We determined the performance limit for a population of swampsparrows and measured how well individual males performed songsrelative to this limit ("vocal performance"). We then comparedfemale solicitation responses to high-performance versus low-performanceversions of the same song type produced by different males.Females displayed significantly more to high-performance songsthan to low-performance songs, supporting the hypothesis thatfemales use vocal performance to assess males.     

Hormonal differentiation of sexual behavior in Japanese quail

The effect of hormones on the development of Japanese quail during the postembryonic period was examined. First, subcutaneous implants of estradiol monobenzoate (EB) and testosterone propionate (TP) were implanted 6–12 hr after hatching. EB and TP had no effect on the differentiation of sexual behavior in genetic males or females. However, EB had marked feminizing effects on plumage in genetic males. Second, the role of gonadal hormones during development was examined by gonadectomizing males and females 6–12 hr after hatching and treating them intramuscularly with EB or TP as adults. EB-treated adult females displayed sexual behavior typical of the genetic female and developed female plumage. A significant proportion of TP-treated females (57%) displayed male sexual behavior patterns. Cloacal gland development and male-type vocalizations were induced. EB-treated males displayed either male or female sexual patterns depending on the stimulus conditions. Third, to test whether bisexuality in gonadectomized males and females is maintained despite steroid treatment and expression of sexual behavior in adulthood, gonadectomized quail which were originally treated with EB received TP and vice versa. The results indicate that in the absence of gonadal hormones after hatching female quail remain bisexual until exposed to estrogen, whereas gonadectomized male quail retain behavioral bisexuality irrespective of prior estrogen or androgen exposure.