Robert E. Hegner

The "Challenge Hypothesis": Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies

A combination of field and laboratory investigations has revealed that the temporal patterns of testosterone (T) levels in blood can vary markedly among populations and individuals, and even within individuals from one year to the next. Although T is known to regulate reproductive behavior (both sexual and aggressive) and thus could be expected to correlate with mating systems, it is clear that the absolute levels of T in blood are not always indicative of reproductive state. Rather, the pattern and amplitude of change in T levels are far more useful in making predictions about the hormonal basis of mating systems and breeding strategies. In these contexts we present a model that compares the amplitude of change in T level with the degree of parental care shown by individual males. On the basis of data collected from male birds breeding in natural or captive conditions, polygynous males appear less responsive to social environmental cues than are monogamous males. This model indicates that there may be widely different hormonal responses to male-male and male-female interactions and presumably equally plastic neural mechanisms for the transduction of these signals into endocrine secretions. Furthermore, evidence from other vertebrate taxa suggests strongly that the model is applicable to other classes

Effects of Experimental Manipulation of Testosterone Levels on Parental Investment and Breeding Success in Male House Sparrows

-Breeding male House Sparrows (Passer domesticus) were implanted with testosterone (T), the antiandrogen flutamide (F), or an empty capsule as a control (C). Parental feeding rates by C-treated males were high until nestlings reached 10 days of age, then declined significantly. This is the typical temporal pattern of parental behavior for free-living males. In contrast, F-treated males fed young at a high rate throughout the nestling stage, while T-treated males fed young much less frequently and were more involved in male-male competition during this period of time. There was a significant decrease in the breeding success of T-treated males resulting from increased starvation of their nestlings. Despite lowered levels of testosterone, F-treated males were able to maintain control of their nest boxes and exhibited normal sexual behavior. During the subsequent brood, breeding success of T-treated males again was reduced by nestling starvation. Our results demonstrate that high levels of testosterone inhibit the expression of parental care in male House Sparrows. Moreover, they suggest that the typical pattern of testosterone levels in males (high when mate guarding and low when feeding young) represents an optimal compromise between allocation of effort to male-male competition vs. parental care. Received 10 July 1986, accepted 1 March 1987. CORRELATIONAL and experimental studies on House Sparrows (Passer domesticus) have suggested that the activities of breeding males represent a trade-off between investment in malemale competition vs. parental care. In males, circulating levels of testosterone reflect this trade-off, being elevated when male-male competition is high and low when parental investment is high. We have suggested that this pattern maximizes an individuals overall reproductive output, even if it results occasionally in a reduction of fecundity (Hegner and Wingfield 1986a, 1987). In this study, we tested experimentally whether the variable pattern of male investment represents an optimization by artificially altering that pattern. This was achieved by altering the endocrine and behavioral state of males with subcutaneous hormone implants. We tested specifically whether elevated levels of testosterone during the last portion of the nestling stage, the interbrood interval, and the egglaying stage are critical for (1) defense of the I Present address: Department of Zoology, NJ-15, University of Washington, Seattle, Washington 98195 USA. nesting site, (2) normal sexual behavior, and (3) successful mate guarding. We also tested (4) whether lowered levels of testosterone during incubation and the early portion of the nestling stage are necessary for the expression of parental care.

Effects of brood-size manipulations on parental investment, breeding success, and reproductive endocrinology of house sparrows

-Brood sizes of House Sparrows (Passer domesticus) were altered experimentally by adding or subtracting 2 nestlings. Unaltered broods served as controls, and experimental brood sizes were within the normal range found under natural conditions. Feeding rates of both parents increased with brood size, and although nestling mass decreased with brood size, most pairs were able to fledge the extra young added to their broods. Males rearing larger broods invested less in nest-site defense and mate-guarding activities, and females rearing larger broods took longer to initiate subsequent broods and produced smaller subsequent clutches. However, the productivity of the subsequent broods did not decrease. Adult survivorship was not affected by the brood manipulations. In males, circulating levels of dihydrotestosterone increased significantly with brood size. Levels of other hormones, including luteinizing hormone (LH), testosterone, estradiol-17#, and corticosterone (B), were not related to brood size in either sex, although in females LH and B titers tended to increase with brood size. Males feeding larger broods tended to have less body fat, but otherwise there was no relationship between brood size and body condition. These results suggest that adults tending larger broods were not unduly stressed by their extra efforts, at least when feeding nestlings. However, the increased interbrood interval and decreased subsequent clutch size associated with rearing larger broods may have resulted either from the increased energetic and nutrient demand on females after the young fledged or simply from the extra time required to rear the additional fledglings to independence. Received 10 July 1986, accepted 1 March 1987. IMPLICIT in many discussions of life-history phenomena is the assumption that organisms trade off two or more conflicting activities in a manner that maximizes their overall reproductive output (e.g. Williams 1966, Charnov and Krebs 1974). For example, most iteroparous organisms are assumed to forgo maximum annual productivity to increase subsequent survivorship, thereby maximizing lifetime fecundity (e.g. Kluyver 1963, Williams 1966, Charnov and Krebs 1974). Moreover, even within a given breeding season, other trade-offs may occur (e.g. McGillivray 1983). For males, Trivers (1972) proposed a fundamental trade-off between competing with other males to fertilize the ova of females and providing parental care to the offspring they produce. Ecological restrictions on these two options have been used to explain mating systems (e.g. Emlen and Oring 1977). We have suggested that endocrine and associ1 Present address: Department of Zoology, NJ-15, University of Washington, Seattle, Washington 98195 USA. ated behavioral changes of monogamous male House Sparrows (Passer domesticus) during the breeding season reflect a compromise between these two options (Hegner and Wingfield 1986a). In our study area, a given pair of House Sparrows may attempt from 3 to 5 broods within a nesting season. In adults, circulating levels of reproductive hormones vary considerably during different stages of nesting. Plasma concentrations of luteinizing hormone (LH), androgens, and estrogens are maximum during the egg-laying stage of each brood, decline rapidly during incubation, remain low after the young hatch, and rise again as the young approach fledging. In females, rising levels of LH and estradiol (E2) following fledging are indications of physiological preparation for laying the next clutch (Hegner and Wingfield 1986b). In males, levels of LH and testosterone rise rapidly to maximum concentrations when nestlings reach 9-10 days of age, well before the young fledge (typically when 14-15 days old). This reflects a transition between a state of high investment in parental care, when testosterone levels are 470 The Auk 104: 470-480. July 1987 This content downloaded from 157.55.39.4 on Fri, 09 Sep 2016 04:28:40 UTC All use subject to http://about.jstor.org/terms Julv 19871 Brood Manipulations in House Sparrows 471 low, to one of high investment in male-male competition, when testosterone levels are high (Hegner and Wingfield 1986a). We examined the physiological and reproductive effects of altering the demand for parental care on free-living House Sparrows. For some pairs we increased the demand for parental care by adding two young to the nest, for others we decreased that demand by removing two young from the nest, and for a third group the number of nestlings was unchanged. We subsequently determined the effects of these manipulations on investment in parental care, investment by males in male-male competition, circulating levels of reproductive hormones, body condition, breeding success in the experimental and subsequent broods, and adult survival to the next year.

Behavioral and endocrine correlates of multiple brooding in the semicolonial house sparrow Passer domesticus. I. Males.

Behavioral and endocrine changes associated with reproductive events were studied in free-living male house sparrows (Passer domesticus). Circulating levels of luteinizing hormone (LH), testosterone (T), and dihydrotestosterone (DHT) were maximal during egg-laying and declined during incubation and the first 2/3 of the nestling stage. As the young approached fledging, levels of LH and T rose to levels similar to those of the first egg-laying stage. This pattern was repeated three to five times during the prolonged breeding season of this species. Multivariate statistical analysis demonstrated that elevated levels of LH and androgens during egg-laying stages were associated with high rates of intrusion at nests by conspecifics, especially other adult males, and elevated levels of agonistic activity, nest defense, and mate-guarding behavior by breeding males. Feeding rates of males declined significantly as plasma levels of T began to rise. Concentrations of corticosterone (B) were high during each egg-laying and nestling stage and were correlated with high or rising levels of reproductive hormones. This suggests that reproductive activity, while energetically demanding, was not overly stressful to these birds. Body mass and fat depots were lowest during the final brood of the season. We suggest that the temporal pattern of circulating levels of T in male house sparrows is an adaptation which compromises between two conflicting selective pressures: a high level of male-male competition for limiting nesting sites in a semicolonial setting, and a strong demand for parental care associated with large broods of altricial young.

Hormonal responses to removal of a breeding male in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali

The white-browed sparrow weaver (Plocepasser mahali) is a cooperatively breeding Ploceid finch that lives in groups of up to 11 individuals. Each group consists of a dominant breeding male and female and a varying number of nonreproductive birds that help feed young and defend the group territory. Experimental removal of the dominant male resulted in attempts by other males to take over the group. Removal of a subordinate, nonbreeding male, as a control, resulted in no change of status among group members. During takeover, there was a transitory increase in plasma levels of luteinizing hormone in the new dominant male, but no change in testosterone levels. As reported in previous investigations, dominant males tended to have higher levels of testosterone than females or subordinate males, but this was not related to the heightened aggression of the takeover. Plasma levels of luteinizing hormone, testosterone, and corticosterone did not differ between the other status groups. The possibility that luteinizing hormone, or a hitherto unidentified androgen, may regulate aggression in the white-browed sparrow weaver is discussed.