Male Song Quality, Egg Size and Offspring Sex in Captive Canaries (Serinus canaria)

Life history theory predicts that females should vary their investment in offspring according to the quality of their mate. In birds, several studies have now shown that females do vary investment according to perceived male quality, by producing larger eggs, investing more in parental care or by manipulating the sex of their offspring. In a captive breeding colony of canaries, we first show that under normal conditions larger eggs in a clutch are more likely to hatch male offspring. In canaries, male song functions in female attraction and females respond more to complex structures in male song called sexy syllables. In a series of experiments, we go on to show first, that females exposed to playback of male song produce larger eggs than those who heard no song. Next, using synthetic songs, we show that females exposed to playback of more attractive songs containing sexy syllables, produced larger eggs than those exposed to simpler songs containing no sexy syllables. However, in a final analysis, we found no evidence from our experiments that females exposed to playback of more attractive songs also produced more male offspring.     

Eavesdropping on Male Singing Interactions Leads to Differential Allocation in Eggs

Females invest differently in their eggs depending on the quality of their mates. In oscines, female investment is influenced by the quality of male song. In domestic canaries Serinus canaria, as well as in black‐capped chickadees Poecile atricapillus, females pay attention not only to the intrinsic quality of male song but can also gather information, by eavesdropping on male–male singing interactions, on the relative quality of males. During these interactions, overlapping the song of the rival is more threatening than alternating. Moreover eavesdropping female canaries have been shown to prefer the overlapping song rather than the overlapped song. The present study was designed to assess the effect of the information gathered by eavesdropping on female investment in eggs. First, we broadcasted overlapping interactions to female canaries. Then, we broadcasted to each female one of the two songs previously heard and collected eggs. Females exposed to overlapping songs laid eggs with greater yolk ratio than females exposed to overlapped songs. In contrast, yolk testosterone quantity and concentration were not affected by the treatment. Moreover, we found a variation between eggs with regard to the testosterone deposited in yolk: both quantity and concentration increased with laying order. Our results suggest that female canaries use information gathered by eavesdropping to differentially allocate resources into the eggs. They suggest that singing interactions could influence chick quality via female investment.     

Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.     

Do female spotless starlings Sturnus unicolor adjust maternal investment according to male attractiveness?

In birds, female egg allocation patterns have a strong influence in offspring development and differential investment in egg size and composition has been shown to respond to male attractiveness. In this study we experimentally manipulated the perceived attractiveness of male starlings Sturnus unicolor by increasing the amount of green material in some nests (a male courtship display in this species). We predicted that, if female investment before laying is related to male attractiveness, experimental females would increase their reproductive investment in response to the addition of plants in their nests when compared to control females. We found that our manipulation caused variations in female reproductive investment in a way that seems to influence offspring quantity but not offspring quality: Females laid larger clutch sizes but not larger eggs when green plant material was added. However, yolk androgens contents were not related to the experimental manipulation. Contrary to expectations, females breeding in experimental nests laid eggs with smaller amounts of eggshell pigments. Interestingly, we found that eggs laid later in the sequence had higher testosterone levels and showed more intense egg colouration than eggs laid earlier in the sequence. These differences at the within-clutch level suggest that selection has favoured compensatory strategies for hatching asynchrony. Alternatively, since nest sabotages by other females are most common at the beginning of laying, this could be seen as female strategy to minimise losses due to nest sabotages. As far as we know, this is the first study to show that an external egg characteristic such as blue-green colouration reflects yolk androgen concentration.     

Intrinsic Factors Affecting Female Choice in House Crickets: Time Cost, Female Age, Nutritional Condition, Body Size, and Size-Relative Reproductive Investment

Few studies have examined potential costs of female choice and factors intrinsic to females that affect choice. To examine these factors, female house crickets, Acheta domesticus, were presented with a simultaneous choice between tapes of a priori attractive and unattractive male chirps. Females varied in age, nutritional condition, body size (potential fecundity), and size-relative reproductive investment. Female age had a significant effect on female choosiness: young females were selective, whereas older females were not selective. Nutritional condition, body size, and size-relative reproductive investment did not affect female choice. Females that chose the call of the attractive male spent approximately twice as long choosing as females that chose the unattractive male call.     

Do females invest more into eggs when males sing more attractively? Postmating sexual selection strategies in a monogamous reed passerine

Maternal investment can play an important role for offspring fitness, especially in birds, as females have to provide their eggs with all the necessary nutrients for the development of the embryo. It is known that this type of maternal investment can be influenced by the quality of the male partner. In this study, we first verify that male song is important in the mate choice of female Eurasian reed warblers, as males mate faster when their singing is more complex. Furthermore, female egg investment varies in relation to male song characteristics. Interestingly, clutch size, egg weight, or size, which can be considered as an high‐cost investment, is not influenced by male song characteristics, whereas comparably low‐cost investment types like investment into diverse egg components are adjusted to male song characteristics. In line with this, our results suggest that female allocation rules depend on investment type as well as song characteristics. For example, egg white lysozyme is positively correlated with male song complexity. In contrast, a negative correlation exists between‐song speed and syllable repetitiveness and egg yolk weight as well as egg yolk testosterone concentration. Thus, our results suggest that female egg investment is related to male song performance in several aspects, but female investment patterns regarding various egg compounds are not simply correlated.     

Sexual conflict and cryptic female choice in the black field cricket, Teleogryllus commodus

The prevalence and evolutionary consequences of cryptic female choice (CFC) remain highly controversial, not least because the processes underlying its expression are often concealed within the female reproductive tract. However, even when female discrimination is relatively easy to observe, as in numerous insect species with externally attached spermatophores, it is often difficult to demonstrate directional CFC for certain male phenotypes over others. Using a biological assay to separate male crickets into attractive or unattractive categories, we demonstrate that females strongly discriminate against unattractive males by removing their spermatophores before insemination can be completed. This results in significantly more sperm being transferred by attractive males than unattractive males. Males respond to CFC by mate guarding females after copulation, which increases the spermatophore retention of both attractive and unattractive males. Interestingly, unattractive males who suffered earlier interruption of sperm transfer benefited more from mate guarding, and they guarded females more vigilantly than attractive males. Our results suggest that postcopulatory mate guarding has evolved via sexual conflict over insemination times rather than through genetic benefits of biasing paternity toward vigorous males, as has been previously suggested.     

The importance of calling song and courtship song in female mate choice in the variable field cricket

Male field crickets produce calling songs, courtship songs, tactile signals and chemical signals. Although calling songs are known to play an important role in female mate choice, the importance of the other signals in mate choice is poorly understood. In the variable field cricket, Gryllus lineaticeps, females select mates, in part, based on variation in male calling song. Females prefer higher chirp rates, a trait which is partially dependent on male nutrient intake, and females prefer longer chirp durations, a trait which appears to be independent of male nutrient intake. We tested whether females also have preferences based on variation in male courtship song, and whether the structure of male courtship song varies with nutrient intake. First, we reexamined female preference for calling song chirp rate. Then, we examined: (1) female preference based on courtship song chirp rate; (2) the relative importance of calling song and courtship song chirp rate; (3) the nutrition dependence of courtship song chirp rate; and (4) the correlation between calling song and courtship song chirp rate. As reported previously, females preferred higher calling song chirp rates, and in addition, preferred higher courtship song chirp rates. Females were more likely to switch from a speaker broadcasting more attractive calling song to a speaker broadcasting less attractive calling song when the attractive calling song was associated with an unattractive courtship song than when it was associated with an attractive courtship song. Preferences based on courtship song may thus cause females to alter the choices that they made based on calling song. Males that received greater nutrients did not produce higher courtship song chirp rates. There was no correlation between calling song and courtship song chirp rate. As a result, the two traits may provide information to females about different aspects of male quality. Copyright 2000 The Association for the Study of Animal Behaviour.     

Differential investment in the Banggai cardinalfish: can females adjust egg size close to egg maturation to match the attractiveness of a new partner?

To test whether females can change their egg investment according to the different attractiveness (  i.e . size as measured by standard length, L _s) of a new mate after eggs have already matured in response to an earlier mate, female Banggai cardinalfish Pterapogon kauderni were first allowed to produce eggs for small (unattractive) or large (attractive) males. Then, when spawning was initiated, but prior to actual spawning, their partner was switched to either a significantly larger or a significantly smaller partner, respectively. A strong positive correlation between egg size and days until spawning with the second male was found for the females initially paired to a small and then a large male. Within a few days, these females apparently increased their egg size to match the attractiveness of their new male. No correlation between days until spawning and egg size in females initially paired to a large and then a small male, however was found, so apparently females were unable to adjust egg size in response to a decrease in mate attractiveness. Consequently, it is suggested that females can increase their egg size investment even after the onset of egg maturation and that this change can be quite rapid.     

Male Song Stimulation of Female Reproduction in Canaries: Features Relevant to Sexual Displays are not Relevant to Nest-building or Egg-laying

Recent studies conducted in our laboratory have demonstrated that a special type of song phrase (‘sexy’ phrases) containing bipartite syllables composed of abrupt frequency falls and short silences stimulate female canaries to solicit for copulation. The study was undertaken to determine whether sexy phrases also facilitated other aspects of the reproductive activity of the female canary, namely, nest-building and egg-laying. During the first experiment, we studied the effect of sexy and non-sexy songs on copulation solicitation displays in 1-year-old females without reproductive experience and in mature females with previous reproductive experience. We confirmed that sexy songs elicited more sexual responses than did non-sexy songs in yearlings and in mature females. During the second experiment, we studied the effect of male songs on nest-building activities and egg-laying in 1-year-old inexperienced females, and in mature, experienced females. The songs of conspecific males significantly triggered and increased nest-building behaviour in female canaries whatever their age or reproductive experience. In contrast, song effects on egg-laying were only found in young females. One-year-old inexperienced females exposed to sexy or non-sexy songs laid more eggs and laid earlier than did 1-year-old inexperienced controls; no such differences were observed in mature, experienced females. The efficiency of songs in promoting nest-building or egg-laying appeared to be unrelated to their efficiency in eliciting sexual responses. No difference was found between females exposed to sexy songs and females exposed to non-sexy songs; differences were only found between control and the two groups of song-exposed females. This result demands further experiments in order to determine whether other song phrase types may account for the stimulating effects of male song on female nest-building and egg-laying.     

Male dominance determines female egg laying rate in crickets

A key prediction of theories of differential allocation and sexual conflict is that male phenotype will affect resource allocation by females. Females may adaptively increase investment in offspring when mated to high quality males to enhance the quality of their offspring, or males may vary in their ability to manipulate female investment post-mating. Males are known to be able to influence female reproductive investment, but the male traits underlying this ability have been little studied in taxa other than birds. We investigated the relationship between male dominance and female oviposition rate in two separate experiments using the field cricket, Gryllus bimaculatus. In both experiments, females mated to more dominant (but not larger) males laid more eggs. This reveals that either females allocate more effort to reproduction after mating with a dominant male or that dominance status is associated with male ability to manipulate their mates. This is the first evidence that dominance, rather than male attractiveness, has a post-copulatory effect on reproductive investment by females.     

Experience Affects Female Responses to Male Song in the Variable Field Cricket Gryllus lineaticeps (Orthoptera, Gryllidae)

Search theory predicts that females will use information on search costs and the characteristics of potential mates to adjust their search behavior and mate choices. We examined the effect of previous acoustic experience on female mating responses in the variable field cricket Gryllus lineaticeps . Females of this species prefer calling songs with higher chirp rates to those with lower chirp rates. In this study we examined how female responses to male calling songs change with experience by measuring the responses of females to male calls over a sequence of three trials. Females in one group (group I) were exposed to a sequence of three identical low chirp rate songs and females in a second group (group II) were exposed to two identical low chirp rate songs interspersed by a high chirp rate song. Females in group I did not show a significant difference in their responses to the initial and final low chirp rate presentations, whereas females in group II showed a significantly reduced response to the final low chirp rate song. In addition, the degree to which female responses to the initial and final low chirp rate song changed differed significantly between the treatment groups. Thus acoustic experience appears to affect female mating preferences in this species; exposure to either more attractive songs or more variable songs makes normally unattractive songs even less attractive. These results suggest that females do not use a fixed-threshold search rule in which they mate with any male with a phenotype that exceeds a given threshold. Instead, G. lineaticeps females appear to use a more complex search rule in which they adjust their searching behavior based on the local distribution of male phenotypes.     

Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song

Courtship vocalizations of male songbirds can profoundly enhance the reproductive physiology and behavior of conspecific females. However, no study has fully investigated the selectivity of conspecific song effects on reproductive development in birds. We studied the effects of conspecific and heterospecific song on reproductive development in domesticated (canaries) and wild songbirds (song sparrows). As expected, conspecific song enhanced follicular development. Unexpectedly, however, birds exposed to heterospecific song also underwent enhanced follicular development (compared to birds exposed to no song); conspecific and heterospecific songs were equally effective in enhancing ovarian development. In canaries exposed to 18L:6D, conspecific song induced oviposition earlier and at a greater frequency than in heterospecific and no song groups, with the fewest eggs being laid in the no song group. These results indicate that conspecific and heterospecific male song can enhance reproductive activity in female songbirds. Whether or not activation of the reproductive axis in female songbirds by heterospecific song occurs in the wild remains unclear. It is also unclear as to whether the ability of the reproductive axis to respond to heterospecific song performs a specific function, or whether it is simply a consequence of greater selection pressure acting upon behavioral responses to song.     

Indirect benefits for choosy female grasshoppers (Chorthippus biguttulus)?

Since direct benefits are likely to be absent in the grasshopper Chorthippus biguttulus, indirect genetic benefits are a potential explanation for costly female preference. Choosy females may improve their fitness in terms of enhanced attractiveness of sons alone or additionally by improved viability of offspring. We tested the predictions of these two hypotheses by comparing attractiveness-related song traits and viability in offspring of attractive and unattractive grasshopper males. The experiment was conducted with larvae reared under semi natural lab conditions in one year and under natural conditions in the field in the following year. If reared under natural conditions no significant differences in viability and song traits between offspring of attractive and unattractive males could be found. Offspring reared in the lab produced calling songs with a significantly more exact song rhythm when sired by attractive males than offspring of unattractive males. Offspring of attractive males should thus have a theoretical advantage in mate choice, which, however, did not translate into higher attractiveness values in acoustic female choice experiments. Therefore our experiments could not resolve whether female choice in C. biguttulus evolved according to the sexy son hypothesis. Since viability in offspring of attractive males did not differ from offspring of unattractive males, “good genes” seems unlikely to be the underlying mechanism of female choice.     

Fitness consequences of increased testosterone levels in female spotless starlings

The role of testosterone in female fitness is poorly known in most vertebrates. It has been proposed that the dynamics of female testosterone may represent a correlated response to selection acting on male testosterone. However, several costs and benefits of enhancing the circulating levels of testosterone in females have been documented in a number of species, suggesting that female testosterone may be the product of direct selection. Despite this, no study has tried to quantify the long-term fitness consequences of manipulating female testosterone. We report the results of an experiment in which we implanted females with testosterone (T-females) and recorded the consequences of this manipulation on investment and reproductive success throughout their lifetime in relation to control females (C-females). Our results show that T-females bred more years in the colony than C-females. The onset of laying was delayed in T-females compared with C-females, but this effect decreased in the years following manipulation. The T-females laid fewer eggs per year, but eggs were heavier than those laid by C-females. The T-females fed nestlings at a lower rate than C-females in the 3 years in which feeding rates were measured and raised fewer fledglings than C-females in the manipulation year. However, since T-females accomplished more breeding attempts than C-females, as a result of their longer stay in the colony, there were no significant differences between the lifetime reproductive success of T- and C-females. There were no overall differences in body size of nestlings raised by T- and C-females, but the body mass of fledglings reached a peak 2-3 years after manipulation for C-females, a tendency not recorded in offspring of T-females. Also, young that were fledged in broods of C-females tended to recruit into the study colony more frequently than those fledged in T-females' nests. All these results indicate that our testosterone manipulation improved the ability of females to acquire and maintain a breeding site but interfered with their reproductive biology and parental investment. Thus, our main conclusion is that under the ecological conditions of our experiment, the addition of exogenous testosterone reduced female fitness. However, differences in population density and female-female competition are likely to alter the fitness landscape of this trait and change the adaptiveness of increased testosterone as a component of female reproductive strategies.     

Negative impact of urban noise on sexual receptivity and clutch size in female domestic canaries

In oscines, male song stimulates female reproduction and females are known to adjust both their sexual preferences and their maternal investment according to song quality. Female domestic canaries are especially responsive to wide frequency bandwidth (4 kHz) male songs emitted with a high‐repetition syllable rate and low minimal frequencies (1 kHz). We previously showed that low‐frequency urban noise decreases female sexual responsiveness for these low‐frequency songs (1–5 kHz) through auditory masking. Based on the differential allocation hypothesis, we predicted that urban noise exposure will equally affect female maternal investment. Using a crossover design, we broadcast low‐frequency songs to females either in an overlapping noise condition or in an alternating noise condition. Females decreased both their sexual responsiveness and their clutch size in the overlapping noise treatment relative to the alternative noise treatment. No differences were found concerning egg size or egg composition (yolk and albumen mass, testosterone concentration). Due to our experimental design, we can exclude a general impact of noisy conditions and thereby provide evidence for a detrimental effect through masking on avian courtship and reproductive output. These results suggest that noisy conditions may also affect avian communication in outdoor conditions, which may partly explain field reports on noise‐dependent breeding success and reduced breeding densities at noisy sites.     

Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches

Yolk androgens affect offspring hatching, begging, growth and survival in many bird species. If these effects are sex-specific, yolk androgen deposition may constitute a mechanism for differential investment in male and female offspring. We tested this hypothesis in zebra finches. In this species, females increase yolk-testosterone levels and produce male-biased sex ratios when paired to more attractive males. We therefore predicted that especially sons benefit from elevated yolk androgens. Eggs were injected with testosterone or sesame oil (controls) after 2 days of incubation. Testosterone had no clear effect on sex-specific embryonic mortality and changed the pattern of early nestling mortality independent of offspring sex. Testosterone-treated eggs took longer to hatch than control eggs. Control males begged significantly longer than females during the first days after hatching and grew significantly faster. These sex differences were reduced in offspring from testosterone-treated eggs due to prolonged begging durations of daughters, enhanced growth of daughters and reduced growth of sons. The results show that variation in maternal testosterone can play an important role in avian sex allocation due to its sex-specific effects on offspring begging and growth.     

Copulatory behaviors and body condition predict post-mating female hormone concentrations, fertilization success, and primary sex ratios in Japanese quail

Environmental cues and social interactions are known to influence reproductive physiology and behavior in vertebrates. In female birds, male courtship displays can result in the growth of ovarian follicles, the production of reproductive hormones, and stimulation of oviduct development, all of which have the potential to influence maternal investment. Male Japanese quail follow a typical sequence of copulatory behaviors during a mating interaction and often force copulations with unreceptive females. We hypothesized that female Japanese quail could adjust maternal investment in response to male copulatory behaviors during a single mating interaction. We investigated the relationships between 1) male copulatory behaviors and post-mating concentrations of steroids in the female, 2) female steroid concentrations and fertilization success of inseminations and 3) female steroid concentrations and the offspring sex ratio. We found that male condition and copulatory behaviors predicted female steroid concentrations and maternal investment in eggs laid after a mating trial. The body condition of one or both mates was a significant predictor of the changes in female corticosterone and testosterone concentrations after mating, whereas specific male copulatory behaviors significantly predicted changes in female progesterone concentrations. Male and female body condition, male neck grabs and post-mating concentrations of female corticosterone, progesterone, and testosterone were all significant predictors of egg fertilization rates. Female body condition, male copulation efficiency, and female testosterone concentrations were significant predictors of offspring sex ratios. Our results show that phenotypic and behavioral characteristics of male Japanese quail modulate female steroid concentrations and result in changes in maternal investment.     

Testosterone-induced Singing in Female European Starlings (Sturnus vulgaris)

Adult female starlings (Sturnus vulgaris) were injected with testosterone in order to determine the song structures they had in memory. Those females had been caught in the wild in different geographical areas and had different ages. This hormone treatment clearly stimulated singing behaviour of females in isolation and revealed their ability to sing quite complex songs. Both categories of songs observed in males (warbling and whistles) were demonstrated and large repertoires were observed. Although the testosterone treatment may have altered the female song system and induced male-like vocalizations, it is interesting that none of the species-typic elements of male starlings was produced by the experimental females. Large changes were found in both repertoire size and composition over a year, revealing a high plasticity, even in older birds. We also found evidence that even under testosterone treatment, females do not necessarily sing all the songs they may have in memory.     

Genetic benefits of mate choice separated from differential maternal investment in red junglefowl (Gallus gallus)

Abstract Females may choose more attractive mates to obtain better viability or attractiveness genes for their offspring. A number of studies have demonstrated a positive relationship between paternal attractiveness and offspring quality. However, this pattern could be due to inheritance of paternal genes and/or it could be due to increased maternal investment in the offspring of more attractive males. To isolate female responses to male appearance from paternal genetic effects, I housed female red junglefowl ( Gallus gallus ) with vasectomized (sterile) males and artificially inseminated them. Male junglefowl with larger combs are more attractive to females. Females laid more eggs when housed with a large-combed, as opposed to a small-combed, vasectomized mate. Neither egg volume nor offspring body condition was associated with comb size of the mother's vasectomized mate. Paternal genetics appeared important. Body condition and comb size were greater for the sons of large-combed sperm donor males. This is consistent with the hypothesis that genetic benefits to offspring maintain female preference for the most ornate males. It is possible that greater body condition and comb size in sons of large-combed sires was not caused by genetic differences, but instead was due to compounds in the ejaculate of large-combed sperm donors inducing greater reproductive investment from females. However, females artificially inseminated by large-combed males did not produce more or larger eggs than females artificially inseminated by small-combed males, and thus there is no other evidence consistent with ejaculate-induced differential investment. Furthermore, only in older chicks was body condition significantly related to sire comb size, suggesting genetic rather than differential investment mechanisms.