Bonnie G. P. Johnson

Neonatal body condition, immune responsiveness, and hematocrit predict longevity in a wild bird population

Measures of body condition, immune function, and hematological health are widely used in ecological studies of vertebrate populations, predicated on the assumption that these traits are linked to fitness. However, compelling evidence that these traits actually predict long-term survival and reproductive success among individuals in the wild is lacking. Here, we show that body condition (i.e., size-adjusted body mass) and cutaneous immune responsiveness to phytohaemagglutinin (PHA) injection among neonates positively predict recruitment and subsequent longevity in a wild, migratory population of house wrens (Troglodytes aedon). However, neonates with intermediate hematocrit had the highest recruitment and longevity. Neonates with the highest PHA responsiveness and intermediate hematocrit prior to independence eventually produced the most offspring during their lifetime breeding on the study site. Importantly, the effects of PHA responsiveness and hematocrit were revealed while controlling for variation in body condition, sex, and environmental variation. Thus, our data demonstrate that body condition, cutaneous immune responsiveness, and hematocrit as a neonate are associated with individual fitness. Although hematocrits effect is more complex than traditionally thought, our results suggest a previously underappreciated role for this trait in influencing survival in the wild.

Female house wrens (Troglodytes aedon) increase the size, but not immunocompetence, of their offspring through extra-pair mating.

House wrens are typically socially monogamous, but frequently engage in extra‐pair matings leading to multisired broods. Because females do not appear to acquire direct material benefits from their extra‐pair mates, we tested the hypothesis that female house wrens derive indirect genetic benefits, such as enhanced immunocompetence (cutaneous immune activity, humoral immunity, and plasma bactericidal activity) and condition (size and haematoserological traits) for their offspring, by mating polyandrously. We predicted that extra‐pair young (EPY) should show greater immune responsiveness and better body condition than their within‐pair maternal half‐siblings (WPY). Contrary to our prediction, WPY had higher cutaneous immune activity than their EPY brood‐mates in two of three years, and EPY and WPY did not differ in measures of innate and humoral immunity. WPY also had higher albumin to γ‐globulin ratios than EPY; however, they were not in better condition based on other measures. EPY had consistently longer tarsi (a measure of long‐bone size) than their WPY half‐siblings, suggesting that females engage in extra‐pair copulations with larger males. The benefits of large structural size in the study population is unknown, but based on evidence from other passerines, we suggest that structural size may be an important fitness‐related trait in house wrens. We conclude that our results are not consistent with the hypothesis that females gain immune‐related benefits for their offspring by engaging in extra‐pair matings. Further study of the fitness consequences of differences in tarsus length is needed to determine whether females acquire size‐related benefits for their offspring from extra‐pair mates.

CHANGES IN EGG SIZE AND CLUTCH SIZE WITH ELEVATION IN A WYOMING POPULATION OF MOUNTAIN BLUEBIRDS

Abstract Few studies have examined how avian life-history traits vary within populations as elevation increases and climate becomes more severe. We compared egg and clutch sizes of Mountain Bluebirds (Sialia currucoides) nesting at two elevations (1500 m and 2500 m above sea level) in the Bighorn Mountains of Wyoming over two years. Eggs laid by females at the high-elevation site were, on average, significantly (6%) smaller in volume than eggs laid by their lower-elevation counterparts. Across elevations, egg size showed a significant positive correlation with female body condition (weight relative to size), and high-elevation females had significantly lower indices of condition than low-elevation females. Temperatures during clutch formation were colder at the high-elevation site, and egg size was negatively related to temperature after controlling for the effects of female condition. Clutches of females at high elevations were, on average, marginally smaller (by 5%, 0.3 eggs) than clutches of low-elevation females. Unlike egg size, clutch size was unrelated to either female condition or temperature during clutch formation. This suggests that, when under energetic or nutritional stress at high elevations, females sacrifice egg size before sacrificing clutch size.

Extra-pair young in house wren broods are more likely to be male than female.

Sex-allocation theory predicts that females should preferentially produce offspring of the sex with greater fitness potential. In socially monogamous animal species, extra-pair mating often increases the variance in fitness of sons relative to daughters. Thus, in situations where offspring sired by a females extra-pair mate(s) will typically have greater fitness potential than offspring sired by the within-pair mate, sex-allocation theory predicts that females will bias the sex of offspring sired by extra-pair mates towards male. We examined the relationship between offspring sex and paternity over six breeding seasons in an Illinois population of the house wren (Troglodytes aedon), a cavity-nesting songbird. Out of the 2345 nestlings that had both sex and paternity assigned, 350 (15%) were sired by extra-pair males. The sex ratio of extra-pair offspring, 0.534, was significantly greater than the sex ratio of within-pair offspring, 0.492, representing an increase of 8.5 per cent in the proportion of sons produced. To our knowledge, this is the first confirmed report of female birds increasing their production of sons in association with extra-pair fertilization. Our results are consistent with the oft-mentioned hypothesis that females engage in extra-pair mating to increase offspring quality.

Evidence for heterozygote instability in microsatellite loci in house wrens

Microsatellite loci have high mutation rates and high levels of allelic variation, but the factors influencing their mutation rate are not well understood. The proposal that heterozygosity may increase mutation rates has profound implications for understanding the evolution of microsatellite loci, but currently has limited empirical support. We examined 20 microsatellite mutations identified in an analysis of 12 260 meiotic events across three loci in two populations of a songbird, the house wren (Troglodytes aedon). We found that for an allele of a given length, mutation was significantly more likely when there was a relatively large difference in size between the allele and its homologue (i.e. a large ‘allele span’). Our results support the proposal of heterozygote instability at microsatellite loci.

Increased extra-pair paternity in broods of aging males and enhanced recruitment of extra-pair young in a migratory bird.

Despite keen interest in extra‐pair mating in birds, its adaptive significance remains unresolved. Here, we use a multi‐year dataset to test whether traits of a females social mate influence her propensity to produce extra‐pair offspring in a population of house wrens, and whether producing extra‐pair young has consequences for a females fitness through effects on offspring survival. Females were most likely to produce extra‐pair offspring when paired with old males and when paired with males on poor‐quality territories, although this latter effect was marginally nonsignificant. Among offspring, the cutaneous immunity of within‐pair young decreased as the age of their sires increased, but cutaneous immunity of extra‐pair young was not affected by the age of their extra‐pair sires or by the age of the males rearing them. Extra‐pair offspring were more likely than within‐pair offspring to return as breeding adults to the local population, with extra‐pair sons being more likely to return as a breeder for multiple years. Our findings support the hypothesis that females produce extra‐pair offspring to enhance their inclusive fitness beyond what they are capable of given the male with which they are socially paired.

Genetic and environmental variation in condition, cutaneous immunity, and haematocrit in house wrens

BackgroundLife-history studies of wild bird populations often focus on the relationship between an individual’s condition and its capacity to mount an immune response, as measured by a commonly-employed assay of cutaneous immunity, the PHA skin test. In addition, haematocrit, the packed cell volume in relation to total blood volume, is often measured as an indicator of physiological performance. A multi-year study of a wild population of house wrens has recently revealed that those exhibiting the highest condition and strongest PHA responses as nestlings are most likely to be recruited to the breeding population and to breed through two years of age; in contrast, intermediate haematocrit values result in the highest recruitment to the population. Selection theory would predict, therefore, that most of the underlying genetic variation in these traits should be exhausted resulting in low heritability, although such traits may also exhibit low heritability because of increased residual variance. Here, we examine the genetic and environmental variation in condition, cutaneous immunity, and haematocrit using an animal model based on a pedigree of approximately 2,800 house wrens.ResultsEnvironmental effects played a paramount role in shaping the expression of the fitness-related traits measured in this wild population, but two of them, condition and haematocrit, retained significant heritable variation. Condition was also positively correlated with both the PHA response and haematocrit, but in the absence of any significant genetic correlations, it appears that this covariance arises through parallel effects of the environment acting on this suite of traits.ConclusionsThe maintenance of genetic variation in different measures of condition appears to be a pervasive feature of wild bird populations, in contradiction of conventional selection theory. A major challenge in future studies will be to explain how such variation persists in the face of the directional selection acting on condition in house wrens and other species.

How males in the house wren, a cavity-nesting songbird, discover that eggs have hatched and transition to provisioning nestlings

In many bird species that conceal nests within cavities or burrows, only females incubate eggs, but both sexes feed young after hatching. How males in such species discover that eggs have hatched and start provisioning offspring is unknown. We video-taped 26 house wren ( Troglodytes aedon ) nests continuously before, during, and after hatching began to test four hypotheses as to how males might learn of hatching: (i) females signal hatching to males; (ii) males hear hatchlings vocalizing; (iii) males observe changes in their mates behaviour (e.g., entering and exiting nests more frequently and/or carrying eggshells or food); and (iv) males enter the nest cavity and encounter hatchlings directly. We did not detect any unique visual or vocal displays by females immediately post-hatching and so could not support the first hypothesis. At only three of 26 nests did it appear that males might have been stimulated to begin feeding solely as a result of either hearing offspring from outside the nest or observing changes in their mates behaviour. Rather, males at most nests did not begin delivering food until after they had entered nest cavities and presumably had direct visual and/or tactile contact with hatchlings, even though most of these males previously had the opportunity to hear offspring from outside nests and/or see their mates acting parentally. Our finding that most males do not start delivering food until they have had direct exposure to young is consistent with recent neurological studies in mammals and birds that suggest direct exposure to young triggers a cascade of gene expression in the brain that induces nurturing behaviour.