Hormone levels predict individual differences in reproductive success in a passerine bird

Hormones mediate major physiological and behavioural components of the reproductive phenotype of individuals. To understand basic evolutionary processes in the hormonal regulation of reproductive traits, we need to know whether, and during which reproductive phases, individual variation in hormone concentrations relates to fitness in natural populations. We related circulating concentrations of prolactin and corticosterone to parental behaviour and reproductive success during both the pre-breeding and the chick-rearing stages in both individuals of pairs of free-living house sparrows, Passer domesticus. Prolactin and baseline corticosterone concentrations in pre-breeding females, and prolactin concentrations in pre-breeding males, predicted total number of fledglings. When the strong effect of lay date on total fledgling number was corrected for, only pre-breeding baseline corticosterone, but not prolactin, was negatively correlated with the reproductive success of females. During the breeding season, nestling provisioning rates of both sexes were negatively correlated with stress-induced corticosterone levels. Lastly, individuals of both sexes with low baseline corticosterone before and high baseline corticosterone during breeding raised the most offspring, suggesting that either the plasticity of this trait contributes to reproductive success or that high parental effort leads to increased hormone concentrations. Thus hormone concentrations both before and during breeding, as well as their seasonal dynamics, predict reproductive success, suggesting that individual variation in absolute concentrations and in plasticity is functionally significant, and, if heritable, may be a target of selection.     

Malarial parasites decrease reproductive success: an experimental study in a passerine bird

Malarial parasites are supposed to have strong negative fitness consequences for their hosts, but relatively little evidence supports this claim due to the difficulty of experimentally testing this. We experimentally reduced levels of infection with the blood parasite Haemoproteus prognei in its host the house martin Delichon urbica, by randomly treating adults with primaquine or a control treatment. Treated birds had significantly fewer parasites than controls. The primaquine treatment increased clutch size by 18%; hatching was 39% higher and fledging 42% higher. There were no effects of treatment on quality of offspring, measured in terms of tarsus length, body mass, haematocrit or T-cell-mediated immune response. These findings demonstrate that malarial parasites can have dramatic effects on clutch size and other demographic variables, potentially influencing the evolution of clutch size, but also the population dynamics of heavily infected populations of birds.     

Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.     

Correlates of lifetime reproductive success in three species of European ducks

Number of breeding attempts is a strong correlate of lifetime reproductive success (LRS) in birds, but the relative importance of potentially interacting factors affecting LRS has rarely been fully evaluated. We considered simultaneously five main factors hypothesized to influence LRS (age at first breeding, nesting date, number of breeding attempts, female traits, brood parasitism) by analyzing with path analysis 22-year data sets for 1,279 individually marked females and their offspring in tufted duck (Aythya fuligula), common pochard (A. ferina) and northern shoveler (Anas clypeata). We recaptured marked offspring as breeding adults (n=496 females) and obtained more complete estimates of LRS by incorporating information about banded ducklings of both sexes shot by hunters 12 months after banding (n=138). In tufted ducks and especially pochard (both diving duck species), late-hatched females tended to delay nesting until 2-years old. Most females (tufted duck, 74%; pochard, 71%; shoveler, 59%) apparently produced no breeding-age offspring. Number of breeding attempts (i.e., longevity) was the strongest correlate of LRS in all species, after controlling effects of age at first breeding, relative nest initiation date, wing length and body mass. Percentage of females producing recruits increased gradually with number of breeding attempts for all three species. Also, as expected, females nesting early in the breeding season had higher LRS than late-nesting individuals. In shoveler, female-specific characteristics of relatively longer wings and heavier late incubation body mass had positive effects on LRS, the latter feature being more common in 2-year-old nesters. In diving ducks, no relationships were detected between LRS and female-specific traits like wing length or body mass, and nor did acceptance of parasitic eggs have any deleterious impact on fitness estimates. Overall, number of fledged ducklings and LRS were related in tufted duck, weakly associated in pochard and unrelated in shoveler, implying that fledging success is not always a reliable measure of LRS.     

Rainfall during parental care reduces reproductive and survival components of fitness in a passerine bird

Adverse weather conditions during parental care may have direct consequences for offspring production, but longer‐term effects on juvenile and parental survival are less well known. We used long‐term data on reproductive output, recruitment, and parental survival in northern wheatears (Oenanthe oenanthe) to investigate the effects of rainfall during parental care on fledging success, recruitment success (juvenile survival), and parental survival, and how these effects related to nestling age, breeding time, habitat quality, and parental nest visitation rates. While accounting for effects of temperature, fledging success was negatively related to rainfall (days > 10 mm) in the second half of the nestling period, with the magnitude of this effect being greater for breeding attempts early in the season. Recruitment success was, however, more sensitive to the number of rain days in the first half of the nestling period. Rainfall effects on parental survival differed between the sexes; males were more sensitive to rain during the nestling period than females. We demonstrate a probable mechanism driving the rainfall effects on reproductive output: Parental nest visitation rates decline with increasing amounts of daily rainfall, with this effect becoming stronger after consecutive rain days. Our study shows that rain during the nestling stage not only relates to fledging success but also has longer‐term effects on recruitment and subsequent parental survival. Thus, if we want to understand or predict population responses to future climate change, we need to consider the potential impacts of changing rainfall patterns in addition to temperature, and how these will affect target species' vital rates.     

Immune challenge mediates vocal communication in a passerine bird: an experiment

Secondary sexual characters may have evolved in part to signalresistance to parasites. Avian song has been hypothesized tobe involved in this process, but the role of parasites in modulatingacoustic communication systems in birds remains largely unknown,owing to lack of experiments. We studied the relationship betweenparasitism, testosterone, song performance, and mating successin male collared flycatchers (Ficedula albicollis) by experimentallychallenging their immune system with a novel antigen. We predictedthat a challenge of the immune system would reduce song performance,and that this reduction would be conditional on the size ofa visual sexual signal, the forehead patch that was previouslyfound to reflect resistance. An antagonistic linkage betweentestosterone and immune function would predict that a challengeof the immune system should suppress testosterone level. Animmunological treatment by sheep red blood cells (SRBCs) triggereda decrease in body mass, testosterone level, and song rate,but other song traits were not significantly affected by theantigen challenge. Initial testosterone level was associatedwith forehead patch size and all song traits except song rate.SRBC injection caused stronger reduction in song rate amongmales with smaller forehead patches, and the change in songrate was also predictable by song features such as strophe complexityand length. We show that song rate and other song characteristicsmay be important cues in male-male competition and female choice.These results suggest that parasite-mediated sexual selectionhas contributed in shaping a complex acoustic communicationsystem in the collared flycatcher, and that testosterone mayplay an important role in this process. Parasitism may drivea multiple signaling mechanism involving acoustic and visualtraits with different signal function.     

Early growth,dominance acquisition and lifetime reproductive success in male and female cooperative meerkats

In polygynous species, variance in reproductive success is higher in males than females. There is consequently stronger selection for competitive traits in males and early growth can have a greater influence on later fitness in males than in females. As yet, little is known about sex differences in the effect of early growth on subsequent breeding success in species where variance in reproductive success is higher in females than males, and competitive traits are under stronger selection in females. Greater variance in reproductive success has been documented in several singular cooperative breeders. Here, we investigated consequences of early growth for later reproductive success in wild meerkats. We found that, despite the absence of dimorphism, females who exhibited faster growth until nutritional independence were more likely to become dominant, whereas early growth did not affect dominance acquisition in males. Among those individuals who attained dominance, there was no further influence of early growth on dominance tenure or lifetime reproductive success in males or females. These findings suggest that early growth effects on competitive abilities and fitness may reflect the intensity of intrasexual competition even in sexually monomorphic species.     

Female variation in allocation of steroid hormones,antioxidants and fatty acids: a multilevel analysis in a wild passerine bird

The environment where an embryo develops can be influenced by components of maternal origin, which can shape offspring phenotypes and therefore maternal fitness. In birds that produce more than one egg per clutch, females differ in the concentration of components they allocate into the yolk along the laying sequence. However, identification of processes that shape female yolk allocation and thus offspring phenotype still remains a major challenge within evolutionary ecology. A way to increase our understanding is by acknowledging that allocation patterns can differ depending on the level of analysis, such as the population versus the among‐female (within‐population) level. We employed mixed models to analyze at both levels the variation in allocation along the laying sequence of four steroid hormones, three antioxidants, and four groups of fatty acids present in the egg yolks of wild great tits Parus major. We also quantified repeatabilities for each component to study female consistency. At a population level, the concentrations/proportions of five yolk components varied along the laying sequence, implying that the developmental environment is different for offspring developing in first versus last eggs. Females varied substantially in the mean allocation of components and in their plasticity along the laying sequence. For most components, these two parameters were negatively correlated. Females were also remarkably repeatable in their allocation. Overall, our data emphasize the need to account for female variation in yolk allocation along the laying sequence at multiple levels, as variation at a population level is underpinned by different individual patterns. Our findings also highlight the importance of considering both levels of analysis in future studies investigating the causes and fitness consequences of yolk compounds. Finally, our results on female repeatability confirm that analyzing one egg per nest is a suitable way to address the consequences of yolk resource deposition for the offspring.     

Multiple mating and lifetime reproductive output in female dobsonflies that receive nuptial gifts

In mating of the dobsonfly, Protohermes grandis (Thunberg), the male attaches the spermatophore externally to the female genitalia. The spermatophore includes a large gelatinous mass which the female detaches and feeds on after mating. While the female consumes this nuptial food gift, sperm is evacuated from the remaining portion of the spermatophore (sperm package) into her reproductive tract. Under laboratory conditions, mated females maintained receptivity throughout their lifetime, and they remated even on the day following copulation. A single insemination may supply enough sperm, as females mated only once deposited fertile eggs throughout life and, when dissected after death, all females had sperm in the spermatheca. There was a positive correlation between longevity and the number of matings. Lifetime fecundity also increased as mating multiplied. However, the size of eggs and hatchlings was not influenced by the number of matings. It seems that large spermatophore consumption by female P. grandis provides nutrients that increase fitness not in offspring quality, but in their quantity.     

Early‐life telomere length predicts lifespan and lifetime reproductive success in a wild bird

Poor conditions during early development can initiate trade‐offs that favour current survival at the expense of somatic maintenance and subsequently, future reproduction. However, the mechanisms that link early and late life‐history are largely unknown. Recently it has been suggested that telomeres, the nucleoprotein structures at the terminal end of chromosomes, could link early‐life conditions to lifespan and fitness. In wild purple‐crowned fairy‐wrens, we combined measurements of nestling telomere length (TL) with detailed life‐history data to investigate whether early‐life TL predicts fitness prospects. Our study differs from previous studies in the completeness of our fitness estimates in a highly philopatric population. The association between TL and survival was age‐dependent with early‐life TL having a positive effect on lifespan only among individuals that survived their first year. Early‐life TL was not associated with the probability or age of gaining a breeding position. Interestingly, early‐life TL was positively related to breeding duration, contribution to population growth and lifetime reproductive success because of their association with lifespan. Thus, early‐life TL, which reflects growth, accumulated early‐life stress and inherited TL, predicted fitness in birds that reached adulthood but not noticeably among fledglings. These findings suggest that a lack of investment in somatic maintenance during development particularly affects late life performance. This study demonstrates that factors in early‐life are related to fitness prospects through lifespan, and suggests that the study of telomeres may provide insight into the underlying physiological mechanisms linking early‐ and late‐life performance and trade‐offs across a lifetime.     

Testosterone, testes size, and mating success in birds: a comparative study

Reproductive behaviors of vertebrates are often underpinned by temporal patterns of hormone secretion. We investigated interspecific patterns of circulating testosterone in male birds to test the hypothesis that testosterone plays a crucial role in sexual selection as determined by degree of polygyny and extra-pair paternity. We predicted that the evolution of increased levels of polygyny and extra-pair paternity would have resulted in the evolution of increased levels of testosterone to allow males more efficiently to compete for mates. This hypothesis was tested in comparative analyses of 116 species of birds using Generalized Least Squares Models. We assessed the importance of latitudinal distribution, because this can confound the relationship between testosterone and mating success. There were weak positive phylogenetic correlations between measures of testosterone and estimates of mating success at the social level, but this association appeared to be confounded by latitudinal distribution, a significant correlate of testosterone titers. However, we found a significantly positive relationship between peak and residual peak testosterone (which is the peak testosterone level that is controlled for the baseline level) and extra-pair paternity independent of latitude. These results suggest that selection pressures arising from social and sexual mating differently affected testosterone levels with the former being mediated by factors associated with latitudinal distribution. An analysis of residual testes size revealed a positive association between peak and residual testosterone and testes size relative to body size. In a path analysis, we show that relative testis size primarily evolved in association with intense sperm competition and thus high sperm production, and these mechanisms had a secondary impact on blood testosterone levels at a phylogenetic scale. Our results suggest that sperm competition has played an important role in the evolution of reproductive mechanisms in birds.     

The contribution of multiple mating and spermatophore consumption to the lifetime reproductive success of female field crickets (Gryllus bimaculatus)

ABSTRACT.

• 1 The adaptive significance of multiple mating by female Gryllus bimaculatus (De Geer) was investigated.
• 2 Multiple mating prevented the depletion of sperm stores and, therefore, maintained high hatching success. This may not, however, explain the high frequency of remating in this species.
• 3 Male-derived egg stimulants known to be passed with sperm at mating increased the number of eggs produced only when females mated throughout their lifespans.
• 4 Spermatophore consumption appeared to provide nutrients which, while they did not increase the quantity of eggs, increased egg quality as indicated by weight. Females who consumed spermatophores had a greater hatching success.
• 5 While females may derive non-genetic benefits from mating, these are apparently long-term benefits; females must mate throughout their lives in order to accrue them.
• 6 Since the benefits of mating may not be derived from individual males, the spermatophores and their contents in this species are best considered as mating effort.

     

Female mating status affects male mating tactic expression in the wolf spider Rabidosa punctulata

Males and females have conflicting interests on the frequency and outcomes of mating interactions. Males maximize their fitness by mating with as many females as possible, whereas choosy females often reduce receptivity following copulation. Alternative male mating tactics can be adaptive in their expression to a variety of mating contexts, including interactions with a relatively unreceptive mated female. Male Rabidosa punctulata wolf spiders can adopt distinctive mating tactics when interacting with a female, a complex courtship display, and/or a more coercive direct mount tactic that often involves grappling with females for copulation. In this study, we set up female mating treatments with initial trials and then paired mated and unmated females with males to observe both female remating frequencies and the male mating tactics used during the interactions. Males adopted different mating tactics depending on the mating status of the female they were paired with. Males were more likely to adopt a direct mount tactic with already-mated females and courtship with unmated females. Already-mated females were considerably less receptive to males during experimental trials, although they did remate 34% of the time, the majority of which were with males using a direct mount tactic. Whereas males adjusting to these contextual cues were able to gain more copulations, the observation of multiple mating in female R. punctulata introduces the potential for sperm competition. We discuss this sexual conflict in terms of the fitness consequences of these mating outcomes for both males and females.     

Female reproductive signaling, and male mating behavior, in the olive baboon

Baboon sexual swellings are among the largest and most colorful signals displayed by any mammal, and many baboon studies have shown an association between sexual swellings and both female and male sexual behavior. However, the extent to which female behavior and sexual swellings combine to signal the timing of ovulation and the fertile period to males, and the extent to which males use these and other signals when determining patterns of mating behavior, remain key topics of research. Here we assess the social and sexual behavior of both female and male olive baboons with respect to detailed measures of swelling size made from digital photographs, measures of fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period based on those levels. Female aggression and grooming behavior were unrelated to fecal progestogen and estrogen levels, but there were some significant relationships between these hormonal measures and presenting behaviors. Measures of female behavior collected during the study did not appear to reveal the timing of ovulation or the fertile period. Male consortship behavior was closely tied to fine-scale changes in sexual swelling size, but copulation behavior was not. Copulation behavior of consorting males was, however, linked to the timing of both ovulation and the fertile period, suggesting that males did have knowledge about these timings. Together these results suggest that males used fine-scale swelling size changes when deciding when to consort, but that consorting males did not use fine-scale swelling size changes in deciding when to copulate. We propose that swelling size may advertise the period during which males should consort with females, with other signals available only from closer inspection then used by consorting males to assess the timing of the fertile period more accurately. An important implication of this interpretation is that different males may have access to different signals of ovulation at any one time. Such a system would allow females to offer different males different information simultaneously, perhaps offering a solution to the ‘female dilemma’ of how females can simultaneously assure and confuse paternity in multi-male societies.     

Resource availability, breeding site selection, and reproductive success of red-winged blackbirds

Red-winged blackbirds are polygynous and show strong breeding site preferences, but it is unclear which environmental factors regulate their reproductive success and are ultimately responsible for shaping their patterns of habitat selection and their mating system. We evaluated the effect of variation in insect emergence rates on the reproductive success of male and female redwings nesting on replicate ponds. The number of male and female redwings that settled on a pond varied two- to three-fold among ponds, but was not related to insect emergence rates. Insect emergence rates had a positive effect on the number of nestlings successfully fledged by females, the number of nestlings fledged from male territories, and on the mass of nestlings at fledging. Typha stem density also varied widely among ponds, and was positively related to male and female settling density and mass of nestlings at fledging, but not to the number of nestlings fledged by females or males. We conclude that alternative breeding sites differ in their ability to support redwing reproduction, and that the availability of emerging odonates is an important environmental factor influencing the reproductive success of both male and female red-winged blackbirds. Received: 31 March 1997 / Accepted: 3 July 1997     

Mhc‐linked survival and lifetime reproductive success in a wild population of great tits

Major histocompatibility complex (Mhc) genes are frequently used as a model for adaptive genetic diversity. Although associations between Mhc and disease resistance are frequently documented, little is known about the fitness consequences of Mhc variation in wild populations. Further, most work to date has involved testing associations between Mhc genotypes and fitness components. However, the functional diversity of the Mhc, and hence the mechanism by which selection on Mhc acts, depends on how genotypes map to the functional properties of Mhc molecules. Here, we test three hypotheses that relate Mhc diversity to fitness: (i) the maximal diversity hypothesis, (ii) the optimal diversity hypothesis and (iii) effect of specific Mhc types. We combine mark–recapture methods with analysis of long‐term breeding data to investigate the effects of Mhc class I functional diversity (Mhc supertypes) on individual fitness in a wild great tit (Parus major) population. We found that the presence of three different Mhc supertypes was associated with three different components of individual fitness: survival, annual recruitment and lifetime reproductive success (LRS). Great tits possessing Mhc supertype 3 experienced higher survival rates than those that did not, whereas individuals with Mhc supertype 6 experienced higher LRS and were more likely to recruit offspring each year. Conversely, great tits that possessed Mhc supertype 5 had reduced LRS. We found no evidence for a selective advantage of Mhc diversity, in terms of either maximal or optimal supertype diversity. Our results support the suggestion that specific Mhc types are an important determinant of individual fitness.     

Male mating success and female mate choice in the river sculpin,Cottus nozawae (Cottidae)

Synopsis Mating success of males and its correlates were investigated in a natural population of the polygynous fluvial sculpinCottus nozawae. Furthermore, the female mate preference of this species was examined experimentally under alternative conditions for mating in a stream. The mating success of individual males (the number of females with which a male mated) ranged between 0 and 8 with a mean of 2.41 in 1983 and 2.52 in 1989, in a population of which the sex ratio was about 1 : 2 in both years, skewed toward females. Mainly due to the excess of nests without egg masses and the few nests with one egg mass, the distribution of male mating success did not fit a Poisson distribution, indicating its non-randomness. Male mating success was not correlated either with the size of the nest rocks or with the male size, suggesting that these two variables are not determinants of mating success. The mate choice experiments demonstrated that females of this species more frequently chose smaller males as mates whose nests already contained eggs than large males without eggs. Additionally, an analysis of stomach contents of guarding males suggested that the parental males ate their own eggs during egg guarding (filial-cannibalism). Based on these results and on a comparison of reproductive characteristics with congeneric species, it is suggested that one of the most important determinants for female mate choice inCottus species may be whether or not parental males are filial egg cannibals.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

Male size,mating potential and lifetime reproductive success in the field cricket,Gryllus bimaculatus (De Geer)

Male size is known to influence short-term, competitive mating success in the field cricket, Gryllus bimaculatus. Short-term measures of mating success are, however, potentially misleading when considering the influence of sexual selection on male morphology and behaviour. The lifetime mating success of males was investigated in the absence of competition to determine the effects of male size per se on reproductive potential and any effects of female behaviour on male lifetime mating success. The cost of spermatophore production was relatively greater for small males who consequently had a longer refractory period between matings, thus limiting their reproductive potential. Large males had a mating advantage resulting from a differential response of females to the courtship attempts of large and small males. Furthermore, small males were ‘sexually incompetent’ in terms of their ability to attach spermatophores once mounted. There was, therefore, an overall positive relationship between male size and lifetime reproductive success.