Developmental stress affects song learning but not song complexity and vocal amplitude in zebra finches

Several recent studies have tested the hypothesis that song quality in adult birds may reflect early developmental conditions, specifically nutritional stress during the nestling period. Whilst all of these earlier studies found apparent links between early nutritional stress and song quality, their results disagree as to which aspects of song learning or production were affected. In this study, we attempted to reconcile these apparently inconsistent results. Our study also provides the first assessment of song amplitude in relation to early developmental stress and as a potential cue to male quality. We used an experimental manipulation in which the seeds on which the birds were reared were mixed with husks, making them more difficult for the parents to obtain. Compared with controls, such chicks were lighter at fledging; they were thereafter placed on a normal diet and had caught up by 100 days. We show that nutritional stress during the first 30 days of life reduced the birds’ accuracy of song syntax learning, resulting in poorer copies of tutor songs. Our experimental manipulations did not lead to significant changes in song amplitude, song duration or repertoire size. Thus, individual differences observed in song performance features probably reflect differences in current condition or motivation rather than past condition.     

Female response to song reflects male developmental history in swamp sparrows

One explanation for why female songbirds attend to male song is that the quality of a male's song is associated with the quality of his developmental history. We tested this hypothesis by playing back to female swamp sparrows (Melospiza georgiana) songs recorded from males of either inferior or superior developmental histories, as assessed by their rates of mass gain during the first 18 days post-hatching. Females showed significantly higher levels of courtship display in response to songs of males with superior growth than to songs of males with inferior growth. Out of nine song traits measured, only song duration correlated with variation in female response; duration was also the only trait that differed significantly in univariate comparisons between the superior growth songs and the inferior growth songs. In a multivariate analysis, however, inferior growth songs were best discriminated from superior growth songs by combining three song traits: trill rate, stereotypy, and the number of notes per syllable. We suggest that early developmental stress degrades song in many small ways, and that it is the cumulative effect of the resulting deficits that explains lower female response.     

Mate choice in the willow warbler — a field experiment

Summary Females may choose a mate on his own quality or on the quality of his resources, i.e., his territory. We removed willow warbler males and allowed new males to settle, before the arrival of females, in order to test whether the proximate cue for female choice was any male trait or territory characteristics. The experiment indicates that females base their choice on some male trait. No correlation was found between male settlement order and size (tarsus length, wing length), but males arriving early were in better body condition than males arriving late. The most likely male trait for female choice was singing rate, which was a good indicator of male settlement date. The duration of time between mating and egg laying was shorter in early territories, both in the observational and the experimental data. Since male song rate was correlated with territory quality (e.g., food abundance) the ultimate benefit to females choosing males with high song rates could be a high quality territory.Offprint requests to: B.L. Arvidsson     

Developmental stress affects the attractiveness of male song and female choice in the zebra finch (Taeniopygia guttata)

Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.     

Patterns of fluctuating asymmetry in beetle horns: an experimental examination of the honest signalling hypothesis

Recent theoretical arguments have claimed that negative relationships between the size and symmetry of secondary sexual traits are indicative of honest signalling of male quality. The patterns of fluctuating asymmetry in beetle horns have been proposed to support the honest signalling hypothesis. Here we examine three assumptions of the hypothesis, (1) that traits are costly to produce; (2) the levels of fluctuating asymmetry are indicative of stress imposed during development; and (3) that males with larger traits should have more symmetrical traits, using the horned beetle, Onthophagus taurus. Experimental manipulations of brood mass were used to manipulate horn size and asymmetry. The development of horns was found to be environmentally determined and costly in terms of delayed development and increased risk of pre-adult mortality. Decreasing resource availability increased relative horn asymmetry. However, horn height was positively related to absolute horn asymmetry. While the results do support the hypothesis that sexual selection on secondary sexual traits should increase levels of fluctuating asymmetry, they provide no support for the notion that the patterns of asymmetry honestly signal male quality. Horns are used in disputes between males and may be indicative of male parental investment. Thus, we conclude that while horn size may be an indication of male quality, the patterns of fluctuating asymmetry are not. Received: 16 December 1996 / Accepted after revision: 5 May 1997     

Energetic state and the performance of dawn chorus in silvereyes (Zosterops lateralis)

Stochastic dynamic programming (SDP) models predict that males singing to attract a mate should concentrate singing in what has been termed the dawn chorus. This is because male birds should have a variable surplus of fat in the morning that can be used to fuel singing, with the amount of fat available dependent upon such factors as his quality, foraging success and risk of predation. In this manner, the dawn chorus can act as an indicator of male quality in the context of female mate choice. We test a key prediction of SDP models of singing behaviour that males with greater fat levels should sing more. We conducted an experiment where we recorded the dawn chorus of male silvereyes (Zosterops lateralis) on three consecutive days. Each male received supplementary food on the second day, which enabled us to sample his dawn chorus before, during and after food supplementation. We also collected data on the effect of supplementary food on the body mass of silvereyes. As predicted by SDP models, we found that silvereyes sang for a greater proportion of the time after receiving supplementary food. Supplementary food also had a significant effect on the complexity of a male song, indicating that males not only increased the quantity of their song but also the quality of their song when they received extra food. As the provision of supplementary food significantly increased the mass of fed birds, our results support a causal link between male energy reserves and his ability to perform the dawn chorus.     

Sex-specific costs of hatching last: an experimental study on herring gulls (<Emphasis Type="Italic">Larus argentatus</Emphasis>)

An organism’s pattern of development can have important long-term fitness effects. In species where the sexes differ in size or other phenotypic traits, they may also have different optimal developmental rates. This influences both parental sex allocation strategies and susceptibility of the sexes to early developmental conditions. However, sex differences in developmental rate and vulnerability to environment during the embryonic period are not well understood. In birds, sibling competition and hatching asynchrony may select for accelerated embryonic development of the last offspring in order to reduce their competitive disadvantage after hatching. They may advance their hatching in response to vocal stimuli by the older siblings. It is, however, unclear whether this flexibility in developmental rates is sex specific. In this study, we experimentally manipulated between-embryo contact and tested whether this affected the pre-natal developmental rate and post-hatching performance of male and female offspring from last-laid eggs in the herring gull. Post-hatching performance was measured both in competitive and non-competitive situations. Among young incubated in isolation, males hatched faster than females, but both sexes fledged in similar, relatively good condition. Among young incubated with normal between-embryo contact, hatching time did not differ between sexes, but males fledged in poorer condition than females, regardless of whether they were reared singly or in a brood. These results suggest that male and female offspring differ in their ability to mitigate the costs of hatching asynchrony.     

Multiple song repertoire characteristics in the willow warbler (Phylloscopus trochilus): correlations with female choice and offspring viability

Male willow warblers have song repertoires which vary in complexity along several dimensions. We examined whether female choice, as measured by date of pairing, was based on these song characteristics in 4 different years. Pairing date was negatively correlated with song repertoire size in 1 year, and with song versatility in another year, but there was no consistent effect of any song characteristic on pairing throughout the years or in the pooled sample. The variable that best explained how soon a male pairs is male arrival date (only males that had settled territories before the first female arrived were considered in the analysis). This correlation is consistently significant in all years. This is most parsimoniously interpreted as females choosing some habitat characteristic in the same way that males do. A small percentage of males (8.3%) attracted and paired with a second female. The likelihood of becoming polygynous was not explained by any measured song characteristic, but it was related to arrival date: early males were more likely to pair with two females. Males with large repertoires fledged more young in their primary nests, and there was a trend for the offspring of these males to have a greater probability of being recruited into the population. In conclusion, the results show that in most years there is no sexual selection by female preference on song characteristics, although the data on reproductive success is consistent with the idea of repertoire size being an indicator of male quality. Received: 4 June 1999 / Received in revised form: 1 December 1999 / Accepted: 31 December 1999     

The evolution of polyandry by queens in social Hymenoptera: the significance of the timing of removal of diploid males

Summary Multiple mating by queens in social Hymenoptera with single locus sex determination may be an adaptation to reduce the effect of genetic load caused by the production of diploid males, if there is a concave relationship between queen fitness and the proportion of diploid male offspring in the colony. In this situation queens should be selected to reduce the variance in the production of diploid male offspring by multiple mating. It has been suggested that this concave relationship occurs in species such as the honey bee, Apis mellifera, in which reproduction occurs near the peak of colony population. This paper suggests that the timing of diploid male removal may influence mating frequency, with early removal of diploid males favoring multiple mating and late removal of diploid males favoring single mating. This idea is explored in two ways. A mathematical model shows that cell use in the brood area of species that rear young in cells will be more efficient with multiple mating. This would favor multiple mating in species, such as the honey bee, in which brood rearing is constrained by the usable area of the brood chamber. Secondly, comparison of polyandrous honey bees (early removal of diploid males as young larvae) with monandrous fire ants, Solenopsis invicta, and Melipona bees (non-removal of immature diploid males) suggests that in the species without diploid male removal, variance reduction may reduce queen fitness. Suggestions are made for testing this hypothesis.     

An experimental study of paternal behavior in red-winged blackbirds

Summary The effect of brood size and female nesting status on male parental behavior was investigated in red-winged blackbirds Agelaius phoeniceus using brood size manipulation experiments. Male redwings allocated parental effort on the basis of brood size and nestling age. Males began assisting females only at nests with at least three offspring older than three days. Female nesting status had no singificant influence on male parental care. When females were unable to meet a brood's demand for food, males assisted females with nestling feeding. Females did not reduce the amount of food delivered to nestlings when males assisted. The amount of food brought to nestlings by the male was additional to the amount of food provided by the female. Male assistance increased fledgling success. When female provisioning was sufficient to meet a brood's demand for food males did not assist. The value of male parental care varied inversely with the ability of the female to meet nestling food demands. The ability of unassisted females to provide sufficient food and to raise a brood of nestlings successfully appeared to be influenced by resource abundance.     

Song repertoires and density assessment in red-winged blackbirds: further tests of the Beau Geste hypothesis

Summary The Beau Geste hypothesis proposes that song repertoires are advantageous in territory defense because nonterritorial males, who are prospecting for territories, use the number of song types they hear to assess the density of territorial males, and then avoid densely-settled areas. A territorial male can then inflate the apparent density of singers on his territory by singing several distinct song type. This hypothesis assumes (1) a positive correlation between the density of song types and the density of territorial males, and (2) a negative correlation between the rate of trespassing and the densities of both song types and territorial males. We studied the behavior of male red-winged blackbirds (Agelaius phoeniceus) and found support for the first, but not the second, assumption. Results showing a positive correlation between density of song types and density of territorial males show that the proposed method of density assessment is feasible in this species. However, we could find no support for the assumption that nonterritorial male red-winged blackbirds avoid densely settled areas. In contrast to the assumed negative correlation, rate of trespass per territory was not consistently correlated with male density, and trespass rate per unit area was positively correlated with male density. Further, these relationships were retained when we controlled statistically for the effects of territory quality. We conclude that prospecting male red-winged blackbirds to not attempt to avoid densely settled areas, and that, although they do avoid territories defended by many song types, they do not use song type density to assess the density of territorial males. It is thus unlikely that the Beau Geste hypothesis adequately accounts for the evolution of song repertoires in the red-winged blackbird.     

Foster,but not genetic,father plumage coloration has a temperature-dependent effect on offspring quality

Secondary sexual characters have most likely evolved through sexual selection because such traits indicate the genetic or phenotypic quality of the bearer. While genetic variation in such fitness-related traits should be depleted by directional selection, there are many cases in which variation is higher than expected. One hypothesis explaining this variation is that different phenotypes within a population are adapted to different environmental conditions. We tested this hypothesis by comparing the offspring quality of male pied flycatchers, Ficedula hypoleuca, with different degrees of melanin-based dorsal plumage coloration under different environmental conditions. To create different environmental growth conditions and to be able to separate offspring genotype effects from paternal effects on offspring body mass, we used a partial cross-foster design where the brood size was reduced or enlarged by one chick. We also examined the interactive effects of temperature and male phenotype because previous correlative studies suggest such temperature-dependent effects in this species. We show that, while manipulated brood size did not interact with male phenotype to affect offspring quality, temperature during the nestling period influenced the offspring quality of dark and brown foster (but not genetic) fathers. When the temperature was relatively low during the nestling period, foster offspring of black males were lighter than those raised by brown males; the opposite was true if temperature was relatively high. These results add a new aspect to our understanding of how variation in the degree of melanin-based coloration is maintained in wild populations and how phenotypic variation may be maintained in general.     

Nest defence by song sparrows: methodological and life history considerations

Summary Several aspects of nest defence behavior were investigated in song sparrows (Melospiza melodia) in eastern Ontario. Two independent tests were made of the hypothesis that the increase in nest defence observed through a nesting attempt is due to the birds becoming familiar with the nest threat, rather than because the nest contents increase in value to the parents. Neither test supported the hypothesis. As predicted by life history theory for species with age-independent mortality, males did not defend their nest more vigorously as they become older. Parents defended their nests less vigorously through the breeding season, contrary to the expected pattern of increased nest defence in response to declining renesting potential. This result may be attributable to a decline in offspring value through the breeding season. Nest defence behavior of mated individuals was positively correlated, independent of factors such as offspring age, renesting potential and brood size. From this result it is proposed that a source of variation in nest defence behavior may be individuals basing their own response on their mate's response in a positive feedback fashion. Males defended nests less vigorously than females, consistent with the expectation that males have lower certainty of parentage in the offspring. It is proposed that variation in paternal uncertainty could contribute to the unexplained variation reported in nest defence studies.     

Male parental care and monogamy in snow buntings

Summary We experimentally removed males from a random sample of 14 snow bunting (Plectrophenax nivalis) pairs to determine the influence of male parental care on reproductive success. Widowed females increased their rate of food delivery to nestlings by increasing their feeding visit rate but not their load size. However, Widows were only able to achieve 73% of the food delivery rate of Control pairs and, as a result, they raised fewer offspring of lower quality (i.e. lower mass at fledging). Total brood mass raised by Widows was only 55% of that of Control pairs. Thus, in the year of our experiment, male parental care in the nestling period almost doubled the reproductive success realized from a brood. Our experiment, however, was done in a year of poor food availability and data from the previous year, when food supply was higher, indicate that males may not always be so important. Since nestling food supply appears to be unpredictable at the time of pair formation, we suggest that monogamy is a bet-hedging strategy in case of poor food availability. As a consequence the importance of male parental care in some years may explain why snow buntings are almost always monogamous.     

Males are sensitive — sex-dependent effect of rearing conditions on nestling growth

The sex-dependent effect of environmental conditions on nestlings has been extensively studied in size dimorphic birds. Whether males or females are more sensitive to poor conditions is not yet clear; however, the degree of sexual size-dimorphism, brood size and their interactions seem to influence the pattern. Much less is known about sex-dependent environmental sensitivity in size-monomorphic species, even though it may result in biased sex allocation. We altered the rearing conditions by brood size manipulation in the size-monomorphic collared flycatcher and then examined the sex-specific development of the nestlings. In all analyses, we controlled for the effect of paternity, because one may expect extra-pair young to be of better genetic quality and perform better at least under poor conditions. However, this was not the case, because we did not find any difference in growth rate or fledging size between extra- and within-pair young. We found that male nestlings had the potential for faster growth under favourable conditions, but suffered more under poor conditions. We found no sex × environment interaction for fledging size probably because the growth curves level off before fledging, and the disadvantaged nestlings can catch up with their siblings. The larger sensitivity of males does not explain the previously found seasonal shift in brood sex ratios and contradicts previous findings in another size-monomorphic species where females were more sensitive. This suggests that even in size-monomorphic species, no general rule exists, which determines the more sensitive sex.     

Developmental stress impairs song complexity but not learning accuracy in non-domesticated zebra finches (<Emphasis Type="Italic">Taeniopygia guttata</Emphasis>)

Food restrictions early in life can have adverse effects on the development of adult avian song structure. Nutritional deficiencies during brain development are thought to impair the growth of neural circuits responsible for learning and production of song in adulthood. Thus, the quality of song may reflect the quality of the singer due to the costs associated with neural development early in life. Recent investigations have focused on domesticated laboratory strains of zebra finches where early dietary deficiencies have significantly reduced the complexity of song and its sexual attractiveness. Domesticated zebra finches may be more sensitive to the early effects of moderate under-nutrition on song complexity than their non-domesticated counterparts. In an aviary experiment with non-domesticated zebra finch stock, we found that song complexity when measured by a linear combination of six variables was reduced in food-restricted birds, with syllable rate and maximum syllable frequency as the principal variables affected. The restriction had no effect on learning accuracy when song phrases of experimental birds were compared to those of their fathers.This result demonstrates that early nutrition may differentially affect the development of neural processes that influence learning accuracy and song complexity. While the finding of negative effects of dietary restriction on song complexity is robust for zebra finches and is not an artefact of domestication, it does not explain why some nutritionally stressed populations of wild zebra finches have more complex songs than those from other regions of Australia characterised by greater food availability.     

Does song reflect age and viability? A comparison between two populations of the great reed warbler Acrocephalus arundinaceus

Song complexity is often regarded as a sexually selected trait that reflects the overall quality of a male. In many passerine species, old males possess larger song repertoires than younger males. This may be either because individual males improve their performance as they get older (longitudinal increase) or because poor singers have reduced viability and, hence, are underrepresented in old age classes (cross-sectional increase). We studied the age dependence of repertoire size and other song traits in a German and a Swedish great reed warbler (Acrocephalus arundinaceus) population. We found marked differences between longitudinal and cross-sectional approaches, as well as between the two study populations. In the German population, we found that syllable switching, a measure of immediate versatility and strophe length, increased with age in a cross-sectional analysis. This was not because birds improved with age (longitudinally) but because syllable switching was positively correlated with male longevity. However, in Sweden, syllable switching seemed to be unrelated to age and longevity. In the Swedish population, individual males increased their repertoire size as they got older (longitudinal increase), but this did not happen in the German population. Hence, two populations, even when belonging to the same subspecies, may differ in whether or not they show delayed song maturation.     

Parentage and paternal care: consequences of intersexual selection in Savannah sparrows?

Empirical relationships between parentage and male parental care are commonly interpreted in the context of life-history models that consider increased offspring survivorship as the only benefit of paternal effort. However, indirect benefits associated with male care can also influence a male's response to cuckoldry: if females allocate paternity according to their prior experience with male parental care, it may pay for males to provision extra-pair young in early broods. Here, I assess the relationship between first-brood parentage and paternal care in a population of Savannah sparrows (Passerculussandwichensis) where a male's fertilization success in the second brood appears to be influenced by his prior parental performance. Based on the multi-locus DNA fingerprinting of 17 first broods, male feeding effort was influenced by parentage (percent of brood resulting from within-pair fertilizations) but not by brood size, male mating status (monogamous versus polygynous), timing of breeding (hatching date), structural size (wing length) or condition (mass). Males provided more care to broods that contained few within-pair young. This result supports the idea that males provision young to increase their future mating success, but alternative hypotheses involving male quality and timing of breeding cannot be excluded. Received: 13 August 1996 / Accepted after revision: 22 February 1997     

Sex-specific maternal effect on egg mass,laying order,and sibling competition in the Bengalese finch (<Emphasis Type="Italic">Lonchura striata</Emphasis> var. <Emphasis Type="Italic">domestica</Emphasis>)

Maternal effects, such as investment in eggs, have profound effects on offspring fitness. Mothers are expected to skew their investment depending on the laying order and sex when unequal sibling competition occurs within a brood because of sex-specific vulnerability and age hierarchy caused by asynchronous hatching. The Bengalese finch hatches asynchronously and shows a moderate reversed sexual size dimorphism. However, contrary to commonly accepted assumptions of size-dependent vulnerability, the smaller sex (male) is more vulnerable to developmental stress caused by sibling competition. We investigated whether maternal investment would be biased by the position in laying order and the sex of eggs, and also explored the possible differences in growth patterns depending on sex, laying order, and age hierarchy by observing chicks fostered to experimentally manipulated broods where brood composition was controlled and age hierarchy was more enhanced than in natural breeding conditions. We found that overall patterns of maternal investment favored the disadvantageous sectors of sibling competition, i.e., eggs of later laying order and sons over those of early laying order and daughters. We also examined the effect of laying order on adult body size and sex differences in growth patterns. When reared in the subordinate age hierarchy, females could compensate for the deficit of decreased growth rate by taking longer to mature, whereas males could not. We suggest that this sex-specific growth pattern could be the cause of sex differences in vulnerability to early developmental stress.     

Maternal characteristics and the production and recruitment of sons in the eastern kingbird (<Emphasis Type="BoldItalic">Tyrannus tyrannus</Emphasis>)

Sex allocation theory predicts that if variance in reproductive success differs between the sexes, females who are able to produce high-quality young should bias offspring sex ratio towards the sex with the higher potential reproductive success. We tested the hypothesis that high-quality (i.e., heavy) female eastern kingbirds (Tyrannus tyrannus) that bred early in the breeding season would produce male-biased clutches. A significant opportunity for sexual selection also exists in this socially monogamous but cryptically polygamous species, and we predicted that successful extra-pair (EP) sires would be associated with an excess of male offspring. Although population brood sex ratio did not differ from parity, it increased significantly with female body mass and declined with female breeding date, but was independent of the morphology and display (song) behavior (correlates of reproductive success) of social males and EP sires. Male offspring were significantly heavier than female offspring at fledging. Moreover, the probability that male offspring were resighted in subsequent years declined with breeding date, and was greater in replacement clutches, but lower when clutch size was large. Probability of resighting female offspring varied annually, but was independent of all other variables. Given that variance in reproductive success of male kingbirds is much greater than that of females, and that male offspring are more expensive to produce and have a higher probability of recruitment if fledged early in the season, our results support predictions of sex allocation theory: high-quality (heavy) females breeding when conditions were optimal for male recruitment produced an excess of sons.