Testosterone-induced depression of male parental behavior in the barn swallow: female compensation and effects on seasonal fitness

In birds, many aspects of male socio-sexual and parental behavior are influenced by androgens, most notably testosterone (T). We report the effects of subcutaneous T-implants in male barn swallows (Hirundo rustica) on male and female parental behavior and on seasonal reproductive success. Males were assigned to one of three experimental groups: (i) implanted with a T-filled Silastic tube; (ii) implanted with an empty Silastic tube; and (iii) not implanted. T-implanted males provided a smaller proportion of feedings (number of feedings by the male/total number of feedings by both parents) and fed nestlings less frequently (number of feedings/h) than males of the other two groups. Females paired to T-implanted males fed nestlings significantly more often than females paired with unimplanted males. Females almost fully compensated for their mates' shortfall, and this resulted in similar combined feeding efforts among treatments. Reproductive success in their first broods or during the entire breeding season was unaffected by T- treatment. These results confirm earlier reports of the suppressive effects of T on male parental behavior. However, they are inconsistent with current ESS models that predict partial compensation as the optimal response by one individual to reduction of parental effort by its mate in monogamous, biparental systems.     

Polygyny and male parental care in Savannah sparrows: effects on female fitness

Summary To determine the effects of male mating status on female fitness, we compared the reproductive success, survival, and future fecundity of female Savannah sparrows (Passerculus sandwichensis) mated to monogamous vs. polygynous males in a 5-year study on Kent Island, New Brunswick, Canada. The proportion of males with more than one mate varied from 15 to 43% between years and sites. Polygynous and monogamous males fledged young of equal size in every year of the study. Females who shared paternal care with other females laid as many eggs per clutch and clutches per season as monogamously mated females. In most years polygynously mated females showed no delay in laying a second clutch, and they suffered no reduction in fecundity the following year. Recruitment of a female's offspring into the breeding population was generally independent of her mating status. Fitness costs of being mated to a polygynous male were only apparent in one year of the study, during which females mated to polygynous males had higher over-winter mortality than those mated to monogamous males. That same year, young raised by polygynous males were only one-third as likely to survive to reproductive maturity (as inferred by returns) as those raised by monogamous males. A male's mating status had no effect on his own survivorship. A male's mating status did not necessarily reflect his contributions to raising nestlings, which may partially explain why monogamously and polygynously mated females had equal fitness. At 35 nests the proportion of food deliveries brought by individual males varied from 0 to 75%; on average, males brought fewer than 30% of all food deliveries. Yet parental care by polygynous males was no less than that of monogamous males, at least at the nests of their primary females. Secondary females tended to receive less male assistance during the nestling stage, but their reproductive success was indistinguishable from that of primary females. Females feeding young without male assistance made as many food deliveries/h as did pairs in which males brought at least 30% of all food deliveries. Unassisted females did not suffer diminished fledging success or produce smaller fledglings. The benefits of polygyny for male Savannah sparrows are clear: polygynous males recruit more surviving offspring into the breeding population than monogamous males. The fitness of females, on the other hand, appears to be unaffected by whether their mate was monogamous or polygynous except in occasional years. Polygyny may be maintained in this population by the constraints of a female-biased sex ratio, the inability of females to predict a male's paternal care based on his morphology or behavior, the poor correlation between a male's mating status and his assistance at the nest, and inconsistent natural selection against mating with a polygynous male. Correspondence to: N.T. Wheelwright     

Replacement males in the western bluebird: opportunity for paternity, chick-feeding rules, and fitness consequences of male parental care

In western bluebirds (Sialia mexicana), most pairs remain together for life and share equally in post-hatching parental care. We removed resident males of socially monogamous pairs during laying and after clutch completion to examine chick-feeding rules used by replacement males and current and future fitness consequences of paternal care. Replacement males were not infanticidal and 7 (47%) fed nestlings. Feeding replacement males and the females they joined fed at rates similar to controls. Females without a feeding replacement male compensated by feeding more themselves so that overall feeding rates were not compromised, but they reduced their brooding time. Unlike assisted females, unassisted females exhibited reduced nesting success and their 14-day-old chicks weighed less than controls. Field metabolic rates of unassisted females were 17% higher than those of control females, but the difference was not statistically significant. Older females were better able to raise young without the male's help than were yearling females. Female condition was not affected by male provisioning and unassisted females were as likely to survive to the next breeding season as assisted females. We found no future benefits of provisioning by replacement males; those that fed were no more likely to breed with the female on her subsequent attempt than were males that did not feed, and subsequent clutch sizes were not reduced for females rearing young without the male's help. These experiments suggest that male parental care increases nesting success in western bluebirds and that replacement males use an all-or-none rule to determine whether or not to feed chicks: if they are present during the fertile period they feed at typical rates; if they are not, they usually do not feed at all. Because chick-feeding by males is tied to opportunity for paternity, influences success in the current nest, and does not affect the male's future breeding success, it appears to be parental rather than mating effort. Received: 8 May 1998 / Accepted after revision: 23 July 1998     

High paternal investment in unrelated young: extra-pair paternity and male parental care in house martins

The response of males to reduced paternity has important consequences for the evolution and maintenance of a mixed reproductive strategy. Paternity is predicted to affect directly the level of male parental care in some cases but not in others. The response of males to reduced paternity will be influenced by their ability to assess their paternity, the predictability of cuckoldry and the costs and benefits of parental care. Although male house martins (Delichon urbica) provide among the highest levels of male parental care known in passerines (incubation, brooding and feeding nestlings), there was no evidence that cuckolded males substantially reduced their level of parental care, and, as a result, all young fledged successfully. Thus, extra-pair fertilizations enhanced the reproductive success of some males because they were able to parasitize the parental care of cuckolded males. We discuss several conditions which may favor extensive male parental care even when the male's paternity is very low.     

Sexual selection and variation in reproductive strategy in male yellow warblers (Dendroica petechia)

Summary Male yellow warblers (Dendroica petechia) exhibit extensive variation in the amount and conspicuousness of the sexually distinctive brown streaking on the breast. We investigated this intraspecific variation in degree of sexual dichromatism to see if male plumage rank (essentially the amount of brown streaking) is correlated with the amount of reproductive effort allocated to parental investment, as sexual selection theory would predict. As predicted, the average rate of feeding visits to the nest by males was negatively correlated with the plumage rank of the male in 1982 (Fig. 1) and 1983 (Fig. 2), and varied little between years or among study areas. Within one study area, the higher nest visit rate of dull (low plumage rank) males was correlated with higher nestling growth rates. But in the other two study areas, where bright (high plumage rank) males predominated, nestlings of bright males tended to have the highest growth rates despite minimal nest visit rates. Thus, overall there was no correlation between male plumage rank and nestling growth rate, a potential index of relative reproductive success, in either year (Figs. 3 and 4). This overall equal nest success likely helps to maintain the behavioral and plumage polymorphism. Since we could find no evidence that the high nestling growth rates of bright males were due to an adjustment of female parental effort to compensate for low male parental effort, there must be some other benefit of being bright which contributes to nest success. To address this, we used the relationship between parental feeding rates and nestling growth rates for each nest as an index of relative territory quality. This analysis suggests that bright males generally occupy the best territories available, possibly because they are more aggressive in obtaining and defending them than dull males. Dull males appear to be relegated to poorer territories, where an increase in male parental contribution would be necessary to achieve high nestling growth rates. We propose that different males are using alternative but evolutionarily stable reproductive strategies, in a way that is consistent with the predictions of sexual selection theory. Allocation of limited reproductive effort to parental investment decreases as sexual dichromatism increases, which probably reflects an increased investment in intermale competition for the best territories.     

Carry-over effects of male extra-pair copulation opportunity on biparental effort in zebra finches

Whether parental effort can be negotiated between partners over ecological time and adjusted across different contexts is not well understood. We manipulated male extra-pair copulation (EPC) opportunity in captive zebra finches, Taeniopygia guttata, to test whether males adjust incubation effort to the mating context and to examine how females respond to their partner’s effort. Birds without previous breeding experience were paired randomly and bred with the same partner twice. In the first breeding attempt, half the males received EPC opportunities with ‘extra-pair females’ during incubation, while the other half did not. Males that received EPC opportunities in the first breeding attempt did not in the second breeding attempt and vice versa. We recorded incubation effort on days when EPC opportunities were not presented. In their first breeding attempt, males with EPC opportunities incubated less than those without. Females compensated fully for the deficit in male care so that a pair’s combined incubation effort was unchanged. In the second attempt, when a male’s opportunity for EPCs was switched, individuals showed the same level of incubation effort that they had previously, irrespective of the current availability of extra-pair females. This suggests that division of effort was negotiated in the first breeding attempt and maintained without significant adjustments in the second attempt. The effects of male EPC opportunity in the first breeding attempt on subsequent incubation effort suggests that individual parental decisions can be shaped by previous experience and this may partly explain conflicting results in studies where individuals’ histories were not known.     

Elaborately ornamented males avoid costly parental care in the house finch (<Emphasis Type="Italic">Carpodacus mexicanus</Emphasis>): a proximate perspective

Selection should favor flexibility in reproductive tactics when the combination of sexual traits and reproductive behaviors that achieve the highest fitness differs between males within a population. Understanding the functional significance of variation in male reproductive tactics can provide insight into their evolution. Male house finches (Carpodacus mexicanus) in a Montana population display continuous variation in parental tactics: males with more elaborated (redder) plumage color provide little or no parental care compared to less elaborated (dull) males. Here, we first determined whether elevation of prolactin (a pituitary hormone) was related to variation in male parental tactics and, second, we used the relationship between prolactin levels and parental behavior to investigate why redder males avoid a high investment in parental care. We found that prolactin elevation was closely associated with paternal care. In addition, males with redder plumage color had low prolactin levels, whereas dull males, which provision twice as frequently, had high levels of prolactin. We also found that male condition was unrelated to plumage color but negatively related to prolactin levels. These results suggest that the low provisioning of redder males was not due to physiological constraints, but instead reflected a tactic to avoid the costs associated with parental care. The condition benefits accrued by redder males may explain their higher post-breeding survival compared to dull males. Moreover, dull males were previously shown to have higher pairing success than redder males, suggesting that the relationship between male plumage color and parental care may reflect individually optimized parental tactics.Communicated by H. Kokko     

Extra-pair paternity in the facultatively polygynous spotless starling,<Emphasis Type="Italic"> Sturnus unicolor</Emphasis>

A potential cost of polygyny that may have restrained its evolution in some avian species is the presence of extra-pair offspring in the nests of males mated with several females. However, this relationship is not frequently found and an experimental approach investigating the association between extra-pair offspring and polygyny, while controlling for male traits related to polygyny, has not been undertaken. In this study, we manipulated the testosterone levels of facultatively polygynous spotless starlings, Sturnus unicolor, to establish experimentally different groups of polygyny and analyse its influence on levels of extra-pair offspring in males for which other traits were randomised. During two consecutive breeding seasons, we examined the effects of harem size on the ability of males to assure genetic paternity, assessed by DNA fingerprinting, and on reproductive success in their own nests. The frequency of extra-pair fertilisations varied between 10% (14/140) in 1996 and 20% (39/194) in 1997. Year-to-year analyses of extra-pair paternity variables with treatment as factor and harem size (number of simultaneous mated females) as covariate, were significant only in relation to harem size. Males with few simultaneously mated females were less cuckolded than more polygynous males in 1997 but not in 1996, indicating that mating costs of polygyny occurred, at least in the year with the higher rate of extra-pair paternity. Because polygynous males have more social mates, they may accrue higher reproductive success irrespective of their risk of being cuckolded. However, our results suggest that to be polygynous is costly in terms of paternity loss when we experimentally induce mating status controlling for individual male traits. However, the low values of our power tests for the statistically non-significant results of hormone on cuckoldry do not allow us to discard this hormone effect altogether.     

Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird

Previous studies have suggested that testosterone (T) profiles of male birds reflect a trade-off between mate attraction behaviours (requiring high T levels) and parental care activities (requiring low T levels). In this study, we experimentally elevated T levels of monogamous males in the facultatively polygynous European starling (Sturnus vulgaris), and compared mate attraction and paternal behaviour of T-treated males with those of controls (C-males). T-males significantly reduced their participation in incubation and fed nestlings significantly less often than C-males. Females paired to T-treated males did not compensate for their mate’s lower paternal effort. The observed reduction in a male’s investment in incubating the eggs was accompanied by an increased investment in typical female-attracting behaviours: T-males spent a significantly higher proportion of their time singing to attract additional females. They also occupied more additional nestboxes than C-males, although the differences just failed to be significant, and carried significantly more green nesting materials into an additional nestbox (a behaviour previously shown to serve a courtship function). T-males also behaved significantly more aggressively than C-males. During the nestling period, the frequency of mate-attracting behaviours by T-treated and control males no longer differed significantly. Despite the reduced paternal effort by T-males and the lack of compensation behaviour by females, hatching and breeding success did not differ significantly between T- and C-pairs. Received: 7 February 2000 / Revised: 10 August 2000 / Accepted: 3 September 2000     

Sexual conflict in the house sparrow: interference between polygynously mated females versus asymmetric male investment

Summary The reproductive success of female house sparrows mated with polygynous males depended to some extent on the aid received from their mates. Polygynous males fed nestlings at the same rate as monogamous males although polygynous males gave aid almost exclusively to one of their mates (the preferred). As a consequence, the number and quality of young raised by preferred females were similar to those of monogamous females, whereas nonaided females experienced a reduction of clutch size, hatching success, and fledgling quality. Males aided the harem female that hatched her clutch earliest (in 11 out of 12 cases). However, harem females that laid eggs earliest (i.e., the potential preferred) lost eggs and/or nestlings more frequently than harem females that delayed laying. This resulted from competing females' infanticide suited for redirecting males' aid. All polygynously mated females delayed the start of a new clutch and reproduced fewer times per season than monogamous females. Consequently, monogamy seems to be the optimum mating situation for females; whereas polygynous males raised more young per year than monogamous males, interference between harem females reduced their maximum expected success.