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.     

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.     

Testosterone,migration distance,and migratory timing in song sparrows Melospiza melodia

In seasonally migratory animals, migration distance often varies substantially within populations such that individuals breeding at the same site may overwinter different distances from the breeding grounds. Shorter migration may allow earlier return to the breeding grounds, which may be particularly advantageous to males competing to acquire a breeding territory. However, little is known about potential mechanisms that may mediate migration distance. We investigated naturally-occurring variation in androgen levels at the time of arrival to the breeding site and its relationship to overwintering latitude in male and female song sparrows (Melospiza melodia). We used stable isotope analysis of hydrogen (δ²H) in winter-grown claw tissue to infer relative overwintering latitude (migration distance), combined with 14 years of capture records from a long-term study population to infer the arrival timing of males versus females. Relative to females, males had higher circulating androgen levels, migrated shorter distances, and were more likely to be caught early in the breeding season. Males that migrate short distances may benefit from early arrival at the breeding grounds, allowing them to establish a breeding territory. Even after controlling for sex and date, androgen levels were highest in individuals that migrated shorter distances. Our findings indicate that androgens and migration distance are correlated traits within and between sexes that may reflect individual variation within an integrated phenotype in which testosterone has correlated effects on behavioral traits such as migration.     

Comprehensive paternity assignment: genotype,spatial location and social status in song sparrows,Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.     

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 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.     

Covariance of paternity and sex with laying order explains male bias in extra-pair offspring in a wild bird population

It has been hypothesized that parents increase their fitness by biasing the sex ratio of extra-pair offspring (EPO) towards males. Here, we report a male bias among EPO in a wild population of blue tits (Cyanistes caeruleus). This resulted from a decline in both the proportion of males and EPO over the laying order of eggs in the clutch. However, previous studies suggest that, unlike the decline in EPO with laying order, the relationship between offspring sex ratio and laying order is not consistent between years and populations in this species. Hence, we caution against treating the decline in proportion of males with laying order, and the resulting male bias among EPO, as support for the above hypothesis. Variable patterns of offspring sex and paternity over the laying order may explain inconsistent associations between offspring sex and paternity, between and within species.     

Reed bunting females increase fitness through extra-pair mating with genetically dissimilar males

Females of many socially monogamous species accept or even actively seek copulations outside the social pair bond. As females cannot increase the number of offspring with promiscuous behaviour, the question arises why they engage in extra-pair mating. We used microsatellite data to determine paternity, heterozygosity and genetic relatedness in the reed bunting (Emberiza schoeniclus), a species with high levels of extra-pair paternity (EPP). We found that extra-pair young (EPY) were more heterozygous than within-pair young (WPY). The high heterozygosity of the EPY resulted from a low genetic similarity between females and their extra-pair mates. EPY were heavier and larger when compared with their maternal half-siblings shortly before they left the nest. Recapture data indicated a higher fledgling survival of EPY compared with WPY. Our data suggest that reed bunting females increase the viability of their offspring and thus fitness through extra-pair mating with genetically dissimilar males.     

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.     

Heterosis and outbreeding depression in descendants of natural immigrants to an inbred population of song sparrows (Melospiza melodia)

We studied heterosis and outbreeding depression among immigrants and their descendants in a population of song sparrows on Mandarte Island, Canada. Using data spanning 19 generations, we compared survival, seasonal reproductive success, and lifetime reproductive success of immigrants, natives (birds with resident-hatched parents and grandparents), and their offspring (F1s, birds with an immigrant and a native parent, and F2s, birds with an immigrant grandparent and resident-hatched grandparent in each of their maternal and paternal lines). Lifetime reproductive success of immigrants was no worse than that of natives, but other measures of performance differed in several ways. Immigrant females laid later and showed a tendency to lay fewer clutches, but had relatively high success raising offspring per egg produced. The few immigrant males survived well but were less likely to breed than native males of the same age that were alive in the same year. Female F1s laid earlier than expected based on the average for immigrant and native females, and adult male F1s were more likely to breed than expected based on the average for immigrant and native males. The performance differences between immigrant and native females and between F1s and the average of immigrants and natives are consistent with the hypothesis that immigrants were disadvantaged by a lack of site experience and that immigrant offspring benefited from heterosis. However, we could not exclude the possibility that immigrants had a different strategy for optimizing reproductive success or that they experienced ecological compensation for life-history parameters. For example, the offspring of immigrants may have survived well because immigrants laid later and produced fewer clutches, thereby raising offspring during a period of milder climatic conditions. Although sample sizes were small, we found large performance differences between F1s and F2s, which suggested that either heterosis was associated with epistasis in F1s, that F2s experienced outbreeding depression, or that both phenomena occurred. These findings indicate that the performance of dispersers may be affected more by fine-scale genetic differentiation than previously assumed in this and comparable systems.     

Superiority of extra-pair offspring: maternal but not genetic effects as revealed by a mixed cross-fostering design

Extra-pair copulations (EPC) are the rule rather than an exception in socially monogamous birds, but despite widespread occurrences, the benefits of female infidelity remain elusive. Most attention has been paid to the possibility that females gain genetic benefits from EPC, and fitness comparisons between maternal half-siblings are considered to be a defining test of this hypothesis. Recently, it was shown that these comparisons may be confounded by within-brood maternal effects where one such effect may be the distribution of half-siblings in the laying order. However, this possibility is difficult to study as it would be necessary to detect the egg from which each chick hatched. In this study, we used a new approach for egg-chick assignment and cross-fostered eggs on an individual basis among a set of nests of the collared flycatcher Ficedula albicollis. After hatching, chicks were ascribed to mothers and therefore to individual eggs by molecular genetic methods. Extra-pair young predominated early in the laying order. Under natural conditions, this should give them a competitive advantage over their half-siblings, mediated by hatching asynchrony. However, we experimentally synchronized hatching, and after this treatment, extra-pair young did not outperform within-pair young in any studied trait including survival up to recruitment and several indicators of reproductive success and attractiveness. We obtained only modest sample sizes for the last two traits and did not test for extra-pair success of male offspring. Thus, we cannot exclude the possibility of advantages of extra-pair young during the adult phase of life. However, our data tentatively suggest that the more likely reason for females' EPCs is the insurance against the infertility of a social mate.     

Predicting evolutionary responses to selection on polyandry in the wild: additive genetic covariances with female extra-pair reproduction

The evolutionary forces that underlie polyandry, including extra-pair reproduction (EPR) by socially monogamous females, remain unclear. Selection on EPR and resulting evolution have rarely been explicitly estimated or predicted in wild populations, and evolutionary predictions are vulnerable to bias due to environmental covariances and correlated selection through unmeasured traits. However, evolutionary responses to (correlated) selection on any trait can be directly predicted as additive genetic covariances (cov_A) with appropriate components of relative fitness. I used comprehensive life-history, paternity and pedigree data from song sparrows (Melospiza melodia) to estimate cov_A between a female''s liability to produce extra-pair offspring and two specific fitness components: relative annual reproductive success (ARS) and survival to recruitment. All three traits showed non-zero additive genetic variance. Estimates of cov_A were positive, predicting evolution towards increased EPR, but 95% credible intervals overlapped zero. There was therefore no conclusive prediction of evolutionary change in EPR due to (correlated) selection through female ARS or recruitment. Negative environmental covariance between EPR and ARS would have impeded evolutionary prediction from phenotypic selection differentials. These analyses demonstrate an explicit quantitative genetic approach to predicting evolutionary responses to components of (correlated) selection on EPR that should be unbiased by environmental covariances and unmeasured traits.     

Parental ecological history can differentially modulate parental age effects on offspring physiological traits in Drosophila

Parents adjust their reproductive investment over their lifespan based on their condition, age, and social environment, creating the potential for inter-generational effects to differentially affect offspring physiology. To date, however, little is known about how social environments experienced by parents throughout development and adulthood influence the effect of parental age on the expression of life-history traits in the offspring. Here, I collected data on Drosophila melanogaster offspring traits (i.e., body weight, water content, and lipid reserves) from populations where either mothers, fathers both, or neither parents experienced different social environments during development (larval crowding) and adulthood. Parental treatment modulated parental age effects on offspring lipid reserves but did not influence parental age effects on offspring water content. Importantly, parents in social environments where all individuals were raised in uncrowded larval densities produced daughters and sons lighter than parental treatments which produced the heaviest offspring. The peak in offspring body weight was delayed relative to the peak in parental reproductive success, but more strongly so for daughters from parental treatments where some or all males in the parental social environments were raised in crowded larval densities (irrespective of their social context), suggesting a potential father-to-daughter effect. Overall, the findings of this study reveal that parental ecological history (here, developmental and adult social environments) can modulate the effects of parental age at reproduction on the expression of offspring traits.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

Parental and developmental temperature effects on the thermal dependence of fitness in Drosophila melanogaster

Cross-generational effects refer to nongenetic influences of the parental phenotype or environment on offspring phenotypes. Such effects are commonly observed, but their adaptive significance is largely unresolved. We examined cross-generational effects of parental temperature on offspring fitness (estimated via a serial-transfer assay) at different temperatures in a laboratory population of Drosophila melanogaster. Parents were reared at 18 degrees C, 25 degrees C, or 29 degrees C (Tpar) and then their offspring were reared at 18 degrees C, 25 degrees C, or 29 degrees C (Toff) to evaluate several competing hypotheses (including an adaptive one) involving interaction effects of parental and offspring temperature on offspring fitness. The results clearly show that hotter parents are better; in other words, the higher the temperature of the parents, the higher the fitness of their offspring, independent of offspring thermal environment. These data contradict the adaptive cross-generational hypothesis, which proposes that offspring fitness is maximal when the offspring thermal regime matches the parental one. Flies with hot parents have high fitness seemingly because their own offspring develop relatively quickly, not because they have higher fecundity early in life.     

Genetic covariance between components of male reproductive success: within‐pair vs. extra‐pair paternity in song sparrows

The evolutionary trajectories of reproductive systems, including both male and female multiple mating and hence polygyny and polyandry, are expected to depend on the additive genetic variances and covariances in and among components of male reproductive success achieved through different reproductive tactics. However, genetic covariances among key components of male reproductive success have not been estimated in wild populations. We used comprehensive paternity data from socially monogamous but genetically polygynandrous song sparrows (Melospiza melodia) to estimate additive genetic variance and covariance in the total number of offspring a male sired per year outside his social pairings (i.e. his total extra‐pair reproductive success achieved through multiple mating) and his liability to sire offspring produced by his socially paired female (i.e. his success in defending within‐pair paternity). Both components of male fitness showed nonzero additive genetic variance, and the estimated genetic covariance was positive, implying that males with high additive genetic value for extra‐pair reproduction also have high additive genetic propensity to sire their socially paired female's offspring. There was consequently no evidence of a genetic or phenotypic trade‐off between male within‐pair paternity success and extra‐pair reproductive success. Such positive genetic covariance might be expected to facilitate ongoing evolution of polygyny and could also shape the ongoing evolution of polyandry through indirect selection.     

Offspring performance is linked to parental identity and male breeding ornamentation in whitefish

The 'good genes' hypothesis predicts that males advertise their quality with different sexual ornaments and that females are able to recognize the genetic quality of males by evaluating these characteristics. In the present study, we investigated the parental effects on offspring performance (feeding and swimming ability of newly-hatched larvae) and examined whether male ornamentation indicates offspring success in performance trials of whitefish ( Coregonus lavaretus Linnaeus). Offspring first-feeding success had a strong paternal effect and it was also positively correlated with the size of male breeding tubercles, indicating that breeding ornamentation of males can function as an honest indicator of their genetic quality. In addition, the observed positive correlation between male tubercle size and condition factor suggests that highly ornamented males are efficient foragers and that this trait may have a heritable basis. By contrast to feeding success, only a maternal effect was found in the swimming ability of the larvae. Clear family-specific differences observed in both measures of performance strongly suggest that parental identity may have important effects on larval survival in the wild.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 532–539.     

Changes in plasma levels of testosterone during male-male interactions in the song sparrow,Melospiza melodia: time course and specificity of response

Summary Previous investigations have shown that malemale interactions over territory boundaries result in an increase in plasma levels of testosterone (T). In order to determine the time course of this increase following an agonistic challenge, male song sparrows, Zonotrichia (= Melospiza) melodia, were exposed to simulated territorial intrusions. Responding males were captured at intervals after onset of the intrusion for up to 60 min. Plasma levels of T were elevated by 10 min after onset of the challenge, and remained high in birds sampled 10–60 min after onset of the intrusion. In addition, plasma levels of luteinizing hormone (LH) increased and were significantly elevated after 10 min of stimulation. The results suggest that at least the prolonged elevation of T secretion precipitated by a male-male interaction was mediated via an increase in LH release. However, the initial surge of T levels in plasma may be LH independent. p Investigations of captive birds confirmed that circulating LH and T levels increased when male song sparrows were challenged by a conspecific male. Challenges involving a male house sparrow, Passer domesticus, had no effect suggesting that responses to male intrusions were species characteristic and not a result of general arousal. Further, auditory stimuli (vocalizations) alone, and visual stimuli (a devocalized male) alone were less effective in stimulating an increase in secretion of T than a combination of auditory and visual stimuli.Abbreviations DHT dihydrotestosterone - LH luteinizing hormon; - T testosterone     

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet     

Offspring diet supersedes the transgenerational effects of parental diet in a specialist herbivore Neolema abbreviata under manipulated foliar nitrogen variability

Diet quality influences organismal fitness within and across generations.For herbivorous insects,the transgenerational effecets of diet remain relatively underexplored.Usinga3×3×2 factorial experiment,we evaluated how N enrichment in parental diets of Neolemd abbreviata(Larcordaire)(C oleoptera:Chrysomelidae),a biological control agent for Tradescantia fluminensis Vell.(Commelinaceae),may influence life history and performance of Fi and F2 offspring under reciprocal experiments.We found limited transgenerational effects of foliar nitrogen variability among life-history traits in both larvae and adults.Larval weight gain and mortality were responsive to parental diet contrary to feeding damage,pupal weight and duration taken to pupate.There were significant parental diet x test interactions in larval feeding damage,weight gain,pupal weight and time to pupation.Generally,offspring from parents under high N plants performed better even under low N test plants.Adult traits including oviposition selection,feeding weight and longevity did not respond to the efects of parental diet nor its interaction with test diet as was the case in the larval stage.However,the main efects of test diet were more important in determining adult performance in both generations suggesting limited sensitivity to parental diet in the adult stage.Our results show conflicting responses to parental diet between larvae and adults ofthe same generation among an insec species with both actively feeding larual and adult life stagee These tranegeneratinonal efferte,or lack thereof,may have implications on the field performance of N.abbrevita under heterogencous nutritional landscapes.