Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia)

Models of sexual selection propose that exaggerated secondary sexual ornaments indicate a male's own fitness and the fitness of his offspring. These hypotheses have rarely been thoroughly tested in free-living individuals because overall fitness, as opposed to fitness components, is difficult to measure. We used 20 years of data from song sparrows (Melospiza melodia) inhabiting Mandarte Island, British Columbia, Canada, to test whether a male's song repertoire size, a secondary sexual trait, predicted overall measures of male or offspring fitness. Males with larger song repertoires contributed more independent and recruited offspring, and independent and recruited grandoffspring, to Mandarte's population. This was because these males lived longer and reared a greater proportion of hatched chicks to independence from parental care, not because females mated to males with larger repertoires laid or hatched more eggs. Furthermore, independent offspring of males with larger repertoires were more likely to recruit and then to leave more grandoffspring than were offspring of males with small repertoires. Although we cannot distinguish whether observed fitness variation reflected genetic or environmental effects on males or their offspring, these data suggest that female song sparrows would gain immediate and intergenerational fitness benefits by pairing with males with large song repertoires.     

Heritability of female extra-pair paternity rate in song sparrows (Melospiza melodia)

The forces driving the evolution of extra-pair reproduction in socially monogamous animals remain widely debated and unresolved. One key hypothesis is that female extra-pair reproduction evolves through indirect genetic benefits, reflecting increased additive genetic value of extra-pair offspring. Such evolution requires that a female's propensity to produce offspring that are sired by an extra-pair male is heritable. However, additive genetic variance and heritability in female extra-pair paternity (EPP) rate have not been quantified, precluding accurate estimation of the force of indirect selection. Sixteen years of comprehensive paternity and pedigree data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) showed significant additive genetic variance and heritability in the proportion of a female's offspring that was sired by an extra-pair male, constituting major components of the genetic architecture required for extra-pair reproduction to evolve through indirect additive genetic benefits. However, estimated heritabilities were moderately small (0.12 and 0.18 on the observed and underlying latent scales, respectively). The force of selection on extra-pair reproduction through indirect additive genetic benefits may consequently be relatively weak. However, the additive genetic variance and non-zero heritability observed in female EPP rate allow for multiple further genetic mechanisms to drive and constrain mating system evolution.     

The effects of sample size on population genetic diversity estimates in song sparrows Melospiza melodia

To empirically determine the effects of sample size on commonly used measures of average genetic diversity, we genotyped 200 song sparrows Melospiza melodia from two populations, one genetically depauperate (n=100) and the other genetically diverse (n=100), using eight microsatellite loci. These genotypes were used to randomly create 10,000 datasets of differing sizes (5 to 50) for each population to determine what the effects of sample size might be on several estimates of genetic diversity (number of alleles per locus, average observed heterozygosity, and unbiased average expected heterozygosity) in natural populations of conservation concern. We found that at small sample sizes of 5 to 10 individuals, estimates of unbiased heterozygosity outperformed those based on observed heterozygosity or allelic diversity for both low- and high-diversity populations. We also found that when comparing across populations in which different numbers of individuals were sampled, rarefaction provided a useful way to compare estimates of allelic diversity. We recommend that standard errors should be reported for all diversity estimators, especially when sample sizes are small. We also recommend that at least 20 to 30 individuals be sampled in microsatellite studies that assess genetic diversity when working in a population that has an unknown level of diversity. However, research on critically endangered populations (where large sample sizes are impossible or extremely difficult to obtain) should include measures of genetic diversity even if sample sizes are less than ideal. These estimates can be useful in assessing the genetic diversity of the population.     

Long-term maternal effect on offspring immune response in song sparrows Melospiza melodia

Knowledge of the causes of variation in host immunity to parasitic infection and the time-scales over which variation persists, is integral to predicting the evolutionary and epidemiological consequences of host-parasite interactions. It is clear that offspring immunity can be influenced by parental immune experience, for example, reflecting transfer of antibodies from mothers to young offspring. However, it is less clear whether such parental effects persist or have functional consequences over longer time-scales, linking a parent's previous immune experience to future immune responsiveness in fully grown offspring. We used free-living song sparrows (Melospiza melodia) to quantify long-term effects of parental immune experience on offspring immune response. We experimentally vaccinated parents with a novel antigen and tested whether parental vaccination influenced the humoral antibody response mounted by fully grown offspring hatched the following year. Parental vaccination did not influence offspring baseline antibody titres. However, offspring of vaccinated mothers mounted substantially stronger antibody responses than offspring of unvaccinated mothers. Antibody responses did not differ between offspring of vaccinated and unvaccinated fathers. These data demonstrate substantial long-term effects of maternal immune experience on the humoral immune response of fully grown offspring in free-living birds.     

Male song sparrows Melospiza melodia do not announce their female's fertility

We tested the fertility announcement hypothesis, whereby male song during a female's fertile period functions as both a paternity guard and an advertisement for extra-pair copulations, in an eastern population of song sparrows Melospiza melodia over two broods within a breeding season. Our results did not support one of its main predictions: male song rate was not significantly higher in the female's fertile period than in her post-fertile period. Song rate peaked prior to pairing, when males were establishing territories and trying to attract females. Once paired, song rate dropped by a factor of about ten, and was consistently low through all stages of the nesting cycle. Males who failed to pair continued singing at high rates throughout the breeding season. Our results do not support the fertility announcement hypothesis, therefore song rate is not used primarily as a paternity assurance strategy by song sparrows.     

Local song elements indicate local genotypes and predict physiological condition in song sparrows Melospiza melodia

Geographical variation in birdsong is taxonomically widespread and behaviourally salient, with females often preferring local over non-local song. However, the benefits associated with this preference remain poorly understood. One potential explanation is that song may reflect a male's place of origin and thus allow females to obtain genes well adapted to the local environment. We studied naturally occurring variation in the degree to which the elements of a male's song repertoire matched those of the local population ('syllable sharing') in migratory song sparrows (Melospiza melodia melodia). Syllable sharing was correlated with genetic similarity to the local population, suggesting that song reflects population of origin. Males sharing more syllables also had larger testosterone-dependent traits, fewer blood-borne parasites and reduced indicators of stress. Our findings are consistent with locally good genes models. Alternatively, immigrants' condition may suffer due to unfamiliarity with the breeding site or inability to match song elements during territorial interactions. Females preferring 'local-sounding' males may thus obtain genetic and/or direct benefits for their offspring.     

Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia)

The consequences of inbreeding for host immunity to parasitic infection have broad implications for the evolutionary and dynamical impacts of parasites on populations where inbreeding occurs. To rigorously assess the magnitude and the prevalence of inbreeding effects on immunity, multiple components of host immune response should be related to inbreeding coefficient (f) in free-living individuals. We used a pedigreed, free-living population of song sparrows (Melospiza melodia) to test whether individual responses to widely used experimental immune challenges varied consistently with f. The patagial swelling response to phytohaemagglutinin declined markedly with f in both females and males in both 2002 and 2003, although overall inbreeding depression was greater in males. The primary antibody response to tetanus toxoid declined with f in females but not in males in both 2004 and 2005. Primary antibody responses to diphtheria toxoid were low but tended to decline with f in 2004. Overall inbreeding depression did not solely reflect particularly strong immune responses in outbred offspring of immigrant-native pairings or weak responses in highly inbred individuals. These data indicate substantial and apparently sex-specific inbreeding effects on immune response, implying that inbred hosts may be relatively susceptible to parasitic infection to differing degrees in males and females.     

Offspring fitness varies with parental extra-pair status in song sparrows, Melospiza melodia

Numerous studies have tested for indirect selection on female extra-pair reproduction (EPR) by quantifying whether extra-pair young (EPY) are fitter than their within-pair young (WPY) maternal half-siblings. In contrast, the hypothesis that offspring of EPY and WPY (rather than the EPY and WPY themselves) differ in fitness has not been tested, even though inter-generational effects of parental extra-pair status on offspring fitness could alter the magnitude and direction of indirect selection on EPR. We tested whether offspring of EPY song sparrows, Melospiza melodia, were more likely to recruit or produce hatched or recruited offspring over their lifetimes than offspring of WPY. Hatchlings with one or two EPY parents were more likely to recruit and produce hatched offspring than hatchlings with two WPY parents. Furthermore, these relationships differed between maternal versus paternal extra-pair status. Hatchlings with EPY fathers were more likely to recruit and produce offspring than hatchlings with WPY fathers. In contrast, hatchlings with EPY mothers were as likely to recruit as hatchlings with WPY mothers and tended to be less likely to produce recruited offspring. Depending on the causal genetic and environmental mechanisms, such conflicting inter-generational relationships between parental extra-pair status and offspring fitness could substantially influence the evolutionary dynamics of EPR.     

Sex-specific differential survival of extra-pair and within-pair offspring in song sparrows, Melospiza melodia

It is widely hypothesized that the evolution of female extra-pair reproduction in socially monogamous species reflects indirect genetic benefits to females. However, a critical prediction of this hypothesis, that extra-pair young (EPY) are fitter than within-pair young (WPY), has rarely been rigorously tested. We used 18 years of data from free-living song sparrows, Melospiza melodia, to test whether survival through major life-history stages differed between EPY and WPY maternal half-siblings. On average, survival of hatched chicks to independence from parental care and recruitment, and their total lifespan, did not differ significantly between EPY and WPY. However, EPY consistently tended to be less likely to survive, and recruited EPY survived for significantly fewer years than recruited WPY. Furthermore, the survival difference between EPY and WPY was sex-specific; female EPY were less likely to survive to independence and recruitment and lived fewer years than female WPY, whereas male EPY were similarly or slightly more likely to survive and to live more years than male WPY. These data indicate that extra-pair paternity may impose an indirect cost on females via their female offspring and that sex-specific genetic, environmental or maternal effects may shape extra-pair reproduction.     

Extra-pair fertilization and effective population size in the song sparrow Melospiza melodia

The concept of effective population size (N_e) is used widely by conservation and evolutionary biologists as an indicator of the genetic state of populations, but its precision and relation to the census population size is often uncertain. Extra-pair fertilizations have the potential to bias estimates of N_e when they affect the number of breeders or their estimated reproductive success tallied from social pedigrees. We tested if the occurrence of extra-pair fertilizations influenced estimates of N_e in a resident population of song sparrows Melospiza melodia using four years of detailed behavioural and genetic data. Estimates of N_e based on social and genetic data were nearly identical and averaged c. 65% of the census population size over four years, despite that 28% of 471 independent young were sired outside of social pairs. Variance in male reproductive success also did not differ between estimates based on social and genetic data, indicating that extra-pair mating had little effect on the distribution of reproductive success in our study population. Our results show that the genetic assignment will not always be necessary to estimate N_e precisely.     

Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia)

Complex birdsong is a classic example of a sexually selected ornamental trait. In many species, females prefer males with large song repertoires, possibly because repertoire size is limited by the size of song control nuclei which reflect developmental success. We investigated whether song repertoire size was indicative of brain area and male quality in song sparrows (Melospiza melodia) by determining if repertoire size was related to the volume of song control nucleus HVC, as well as several morphological, immunological and genetic indices of quality. We found that males with large repertoires had larger HVCs and were in better body condition. They also had lower heterophil to lymphocyte ratios, indicating less physiological stress and a robust immune system as measured by the number of lymphocytes per red blood cell. Song repertoire size also tended to increase with neutral-locus genetic diversity, as assessed by mean d2, but was not related to internal relatedness. Our results suggest several mechanisms that might explain the finding of a recent study that song sparrows with large song repertoires have higher lifetime fitness.     

Inbreeding depresses immune response in song sparrows (Melospiza melodia): direct and inter-generational effects

A thorough knowledge of relationships between host genotype and immunity to parasitic infection is required to understand parasite-mediated mechanisms of genetic and population change. It has been suggested that immunity may decline with inbreeding. However, the relationship between inbreeding level and a host's response to a novel immune challenge has not been investigated in a natural population. We used the pedigreed population of song sparrows (Melospiza melodia) inhabiting Mandarte Island, Canada, to test the hypothesis that a sparrow's cell-mediated immune response (CMI) to an experimental challenge would decline with individual or parental inbreeding. CMI in 6-day-old chicks declined significantly with their mother's coefficient of inbreeding, demonstrating an inter-generational effect of maternal inbreeding on offspring immunity. In fledged juveniles and adult sparrows, CMI declined markedly with an individual's own coefficient of inbreeding, but not its mother's. This relationship was consistent across seasons, and was not attributable solely to heterosis in offspring of immigrant breeders. CMI also declined with age and increased with body condition in adult sparrows, but inbreeding explained 37% of the total variation. We emphasize the implications of this dramatic inbreeding depression in cell-mediated immunity for theories of parasite-mediated evolution and the susceptibility of small, inbred populations.     

No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia)

We studied mate choice and inbreeding avoidance a natural population of song sparrows (Melospiza melodia) on Mandarte Island, Canada. Inbreeding occurred regularly: 59% all matings were between known relatives. We tested for inbreeding avoidance by comparing the observed levels of inbreeding to those expected if mate choice had been random with respect to relatedness. Independent of our assumptions about the availability of mates in the random mating model, we found that the expected and observed distributions of inbreeding coefficients were similar, as was the expected and observed frequency of close (f >/= 0.125) inbreeding. Furthermore, there was no difference in relatedness observed pairs and those that would have resulted had birds mated instead with their nearest neighbors. The only evidence to suggest any inbreeding avoidance was a reduced rate of parent-offspring matings as compared to one random mating model but not the other. Hence, despite substantial inbreeding depression in this population, we found little evidence for inbreeding avoidance through mate choice. We present a simple model to suggest that variation in inbreeding avoidance behaviors in birds may arise from differences in survival rates: in species with low survival rates, the costs of forfeiting matings to avoid inbreeding may exceed the costs of inbreeding.     

The effects of contemporary processes in maintaining the genetic structure of western song sparrows (Melospiza melodia)

Historic events and contemporary processes work in concert to create and maintain geographically partitioned variation and are instrumental in the generation of biodiversity. We sought to gain a better understanding of how contemporary processes such as movement and isolation influence the genetic structure of widely distributed vagile species such as birds. Song sparrows (Melospiza melodia) in western North America provide a natural system for examining the genetics of populations that have different patterns of geographic isolation and migratory behavior. We examined the population genetics of 576 song sparrows from 23 populations using seven microsatellite loci to assess genetic differentiation among populations and to estimate the effects of drift and immigration (gene flow) on each population. Sedentary, isolated populations were characterized by low levels of immigration and high levels of genetic drift, whereas those populations less isolated displayed signals of high gene flow and little differentiation from other populations. Contemporary dispersal rates from migratory populations, estimated by assignment test, were higher and occurred over larger distances than dispersal from sedentary populations but were also probably too low to counter the effects of drift in most populations. We suggest that geographic isolation and limited gene flow facilitated by migratory behavior are responsible for maintaining observed levels of differentiation among Pacific coastal song sparrow populations.     

Influences of weather on reproductive function in male Song sparrows, Melospiza melodia

The avian reproductive cycle is integrated and timed by a variety of environmental factors that include day length, availability of food, nest sites, presence of a mate, etc. However, reproduction can be delayed or disrupted by inclement weather and, until recently, the endocrine responses of avian species to storms were entirely unknown. This communication describes changes in endocrine state in free-living male Song sparrows, Melospiza melodia, during gonadal recrudescence after a severe winter, and in response to storms in early spring and summer. Both the severe winter weather and an early spring snow storm delayed testicular development, and depressed circulating levels of testosterone. The sparrows did not appear to be stressed, however, since body mass and fat deposits were higher than in birds sampled during the previous spring after a less severe winter.
A second storm occurred in late May and early June when Song sparrows were feeding young. Curiously, plasma levels of testosterone were not affected, but the sparrows did appear to be stressed since there was a significant decline in body mass, and a marked increase in circulating levels of corticosterone. These data suggest that the effects of inclement weather on reproductive function can vary in relation to the stage in the reproductive cycle when the storm strikes, and that the endocrine mechanisms underlying acclimatization to severe meteorological conditions are also different.     

Influences of weather on reproductive function in female Song sparrows, Melospiza melodia

Prolonged and severe periods of inclement weather can retard gonadal development in early spring or disrupt the breeding cycle in summer. Previous investigations on the endocrine responses of free-living avian species to storms have been restricted almost entirely to males. This communication presents the endocrine responses of free-living female Song sparrows, Melospiza melodia, during gonadal recrudescence after a severe winter, and during storms in early spring and summer. As in males, gonadal recrudescence was delayed by the severe winter weather, and this effect was exacerbated by an aseasonal snow storm in early spring. Unlike males, female Song sparrows did appear to be stressed by this snow storm, since body mass and fat deposit decreased, and plasma levels of corticosterone increased. A second storm in early summer did not, however, prove to be stressful to females, although males were apparently stressed by the same storm. At the time the early summer storm occurred, young had been fledged and were being fed mostly by the male. Females begin preparing for a second clutch of eggs and do not feed fledglings to the same extent as males. Thus it is possible that males are stressed by storms at this time, because they are feeding several young as well as themselves during a period of reduced availability of food, whereas females are feeding themselves only. These data suggest that, not only do the endocrine responses to inclement weather vary in relation to stage in the reproductive cycle when storms strike, but also that there are sex differences in those responses.     

Short-term changes in plasma levels of hormones during establishment and defense of a breeding territory in male song sparrows, Melospiza melodia

When territorial male song sparrows are captured and removed from their territories, previously unmated and nonterritorial males will take over those vacant territories within 12-72 hr. Plasma levels of testosterone are elevated in these replacement males as well as in their neighbors. Since the latter already have territories, it is suggested that the agonistic interactions over territory boundaries, or behavioral stimuli from challenging males, rather than ownership of a territory per se, stimulates secretion of testosterone. To test this hypothesis further, male song sparrows were challenged by experimental simulation of a territorial intrusion. This procedure involved placing a caged male song sparrow in the center of the subject's territory and playing tape recorded conspecific song through an adjacent speaker. Responding males were then captured at intervals after onset of the intrusion. Plasma levels of testosterone were significantly higher in males exposed to experimental territorial intrusion than they were in controls, supporting the hypothesis that behavioral stimuli emanating from an intruding male can act as supplementary information stimulating secretion of testosterone.     

Early nutritional stress impairs development of a song-control brain region in both male and female juvenile song sparrows (Melospiza melodia) at the onset of song learning

Birdsong is a sexually selected trait and is often viewed as an indicator of male quality. The developmental stress hypothesis proposes a model by which song could be an indicator; the time during early development, when birds learn complex songs and/or local variants of song, is of rapid development and nutritional stress. Birds that cope best with this stress may better learn to produce the most effective songs. The developmental stress hypothesis predicts that early food restriction should impair development of song-control brain regions at the onset of song learning. We examined the effect of food restriction on song-control brain regions in fledgling (both sexes, 23-26 days old) song sparrows (Melospiza melodia). Food restriction selectively reduced HVC volume in both sexes. In addition, sex differences were evident in all three song-control regions. This study lends further support to a growing body of literature documenting a variety of behavioural, physiological and neural detriments in several songbird species resulting from early developmental stress.     

Species song discrimination in adult female song and swamp sparrows

Six female song sparrows (Melospiza melodia) and six female swamp sparrows (Melospiza georgiana) were treated with oestradiol, and their response to song measured by frequency and intensity of copulation-solicitation display. Test stimuli were synthetic songs composed of either song sparrow or swamp sparrow syllables assembled in either song-sparrow-like or swamp-sparrow-like temporal patterns. Female song sparrows responded preferentially to songs containing their own species' syllables and to songs containing their own species' temporal patterns. Swamp sparrows were also sensitive to both syllable type and temporal, pattern, in contrast to male swamp sparrows, which show no preference for swamp sparrow temporal patterns.     

Juvenile sparrows preferentially eavesdrop on adult song interactions

Recent research has demonstrated that bird song learning is influenced by social factors, but so far has been unable to isolate the particular social variables central to the learning process. Here we test the hypothesis that eavesdropping on singing interactions of adults is a key social event in song learning by birds. In a field experiment, we compared the response of juvenile male song sparrows (Melospiza melodia) to simulated adult counter-singing versus simulated solo singing. We used radio telemetry to follow the movements of each focal bird and assess his response to each playback trial. Juveniles approached the playback speakers when exposed to simulated interactive singing of two song sparrows, but not when exposed to simulated solo singing of a single song sparrow, which in fact they treated similar to heterospecific singing. Although the young birds approached simulated counter-singing, neither did they approach closely, nor did they vocalize themselves, suggesting that the primary function of approach was to permit eavesdropping on these singing interactions. These results indicate that during the prime song-learning phase, juvenile song sparrows are attracted to singing interactions between adults but not to singing by a single bird and suggest that singing interactions may be particularly powerful song-tutoring events.