Within-clutch patterns of yolk testosterone vary with the onset of incubation in black-headed gulls

Hatching asynchrony in birds produces an age and size hierarchyamong siblings. Later-hatching chicks have a competitive disadvantage,and brood reduction may occur when food availability is insufficientto raise all chicks. When early-hatched chicks fail to surviveor if the circumstances allow raising all chicks, mothers shouldreverse the disadvantage to later-hatched chicks. Increasingdeposition of maternal androgens with the laying sequence hasbeen suggested to compensate for detrimental effects of hatchingasynchrony, allowing a more precise adjustment of the survivalprobabilities of each chick. Here, we show for black-headedgulls that the increase in yolk testosterone with each successiveegg is greater when the mother incubates longer before clutchcompletion, which is the major determinant of the degree ofhatching asynchrony. This finding supports the idea that yolktestosterone has a compensatory function in the context of hatchingasynchrony. Our data further show that if the time needed tocomplete a clutch is lengthened, the developmental differencesdue to incubation between the first- and the last-laid eggsincrease. In addition, the onset of incubation before clutchcompletion occurs sooner as the breeding season progresses.Both long inter-egg intervals and the seasonal shift in incubationbehavior enhance the necessity of compensation for later-hatchingchicks. Indeed, yolk levels of testosterone increased more steeplyover the laying order, if the duration of the egg-laying periodwas extended and in later-laid clutches. We suggest that prolactinplays a key role in the adjustment of testosterone allocationto the incubation pattern.     

Yolk testosterone reduces oxidative damages during postnatal development

Conditions experienced during early life can influence the development of an organism and several physiological traits, even in adulthood. An important factor is the level of oxidative stress experienced during early life. In birds, extra-genomic egg substances, such as the testosterone hormone, may exert a widespread influence over the offspring phenotype. Interestingly, testosterone can also upregulate the bioavailability of certain antioxidants but simultaneously increases the susceptibility to oxidative stress in adulthood. However, little is known about the effects of maternally derived yolk testosterone on oxidative stress in developing birds. Here, we investigated the role of yolk testosterone on oxidative stress of yellow-legged gull chicks during their early development by experimentally increasing yolk testosterone levels. Levels of antioxidants, reactive oxygen species and lipid oxidative damage were determined in plasma during nestlings'' growth. Our results revealed that, contrary to control chicks, birds hatched from testosterone-treated eggs did not show an increase in the levels of oxidative damage during postnatal development. Moreover, the same birds showed a transient increase in plasma antioxidant levels. Our results suggest that yolk testosterone may shape the oxidative stress-resistance phenotype of the chicks during early development owing to an increase in antioxidant defences and repair processes.     

Interspecific variation in egg testosterone levels: implications for the evolution of bird song

Although interspecific variation in maternal effects via testosterone levels can be mediated by natural selection, little is known about the evolutionary consequences of egg testosterone for sexual selection. However, two nonexclusive evolutionary hypotheses predict an interspecific relationship between egg testosterone levels and the elaboration of sexual traits. First, maternal investment may be particularly enhanced in sexually selected species, which should generate a positive relationship. Secondly, high prenatal testosterone levels may constrain the development of sexual characters, which should result in a negative relationship. Here we investigated these hypotheses by exploring the relationship between yolk testosterone levels and features of song in a phylogenetic study of 36 passerine species. We found that song duration and syllable repertoire size were significantly negatively related to testosterone levels in the egg, even if potentially confounding factors were held constant. These relationships imply that high testosterone levels during early development of songs may be detrimental, thus supporting the developmental constraints hypothesis. By contrast, we found significant evidence that song-post exposure relative to the height of the vegetation is positively related to egg testosterone levels. These results support the hypothesis that high levels of maternal testosterone have evolved in species with intense sexual selection acting on the location of song-posts. We found nonsignificant effects for intersong interval and song type repertoire size, which may suggest that none of the above hypothesis apply to these traits, or they act simultaneously and have opposing effects.     

Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them?

Over the past decade, birds have proven to be excellent models to study hormone-mediated maternal effects in an evolutionary framework. Almost all these studies focus on the function of maternal steroid hormones for offspring development, but lack of knowledge about the underlying mechanisms hampers further progress. We discuss several hypotheses concerning these mechanisms, point out their relevance for ecological and evolutionary interpretations, and review the relevant data. We first examine whether maternal hormones can accumulate in the egg independently of changes in hormone concentrations in the maternal circulation. This is important for Darwinian selection and female physiological trade-offs, and possible mechanisms for hormone accumulation in the egg, which may differ among hormones, are reviewed. Although independent regulation of plasma and yolk concentrations of hormones is conceivable, the data are as yet inconclusive for ovarian hormones. Next, we discuss embryonic utilization of maternal steroids, since enzyme and receptor systems in the embryo may have coevolved with maternal effect mechanisms in the mother. We consider dose-response relationships and action pathways of androgens and argue that these considerations may help to explain the apparent lack of interference of maternal steroids with sexual differentiation. Finally, we discuss mechanisms underlying the pleiotropic actions of maternal steroids, since linked effects may influence the coevolution of parent and offspring traits, owing to their role in the mediation of physiological trade-offs. Possible mechanisms here are interactions with other hormonal systems in the embryo. We urge endocrinologists to embark on suggested mechanistic studies and behavioural ecologists to adjust their interpretations to accommodate the current knowledge of mechanisms.     

MHC genotype predicts mate choice in the ring-necked pheasant Phasianus colchicus

Females of several vertebrate species selectively mate with males on the basis of the major histocompatibility complex (MHC) genes. As androgen-mediated maternal effects have long-lasting consequences for the adult phenotype, both mating and reproductive success may depend on the combined effect of MHC genotype and exposure to androgens during early ontogeny. We studied how MHC-based mate choice in ring-necked pheasants (Phasianus colchicus) was influenced by an experimental in ovo testosterone (T) increase. There was no conclusive evidence of in ovo T treatment differentially affecting mate choice in relation to MHC genotype. However, females avoided mating with males with a wholly different MHC genotype compared with males sharing at least one MHC allele. Females also tended to avoid mating with MHC-identical males, though not significantly so. These findings suggest that female pheasants preferred males with intermediate MHC dissimilarity. Male MHC heterozygosity or diversity did not predict the expression of ornaments or male dominance rank. Thus, MHC-based mating preferences in the ring-necked pheasant do not seem to be mediated by ornaments' expression and may have evolved mainly to reduce the costs of high heterozygosity at MHC loci for the progeny, such as increased risk of autoimmune diseases or disruption of coadapted gene pools.     

Maternal immune factors and the evolution of secondary sexual characters

Secondary sexual characters have been hypothesized to revealthe ability of males to resist debilitating parasites. Althoughsuch reliable signaling of parasite resistance may be maintainedby parasite–host coevolution, maternal effects potentiallyprovide a previously neglected factor that could affect thelevel of genetic variation in resistance to parasites. Thatcould be the case because maternal effects have an entirelyenvironmental basis, or because they can maintain considerableamounts of genetic variation through epistatic effects, evenin the presence of strong directional selection. Maternal effectshave been shown to occur as maternal allocation of immune factorsto offspring, and such allocation may depend on the mating prospectsof sons, causing mothers to differentially allocate maternaleffects to eggs in species subject to intense sexual selection.Here we show that a maternal effect through innate antibacterialimmune defense, lysozyme, which is transferred from the motherto the egg in birds, is positively associated with the evolutionof secondary sexual characters. Previous studies have shownthat females differentially allocate lysozyme to their eggswhen mated to attractive males, and elevated levels of lysozymeare associated with reduced hatching failure and superior healthamong neonates and adults. In this study, comparative analysesof lysozyme from eggs of 85 species of birds showed a strongpositive relationship between brightness of male plumage andegg lysozyme, even when controlling for potentially confoundingvariables. These findings suggest that maternal immune factorsmay play a role in the evolution of secondary sexual characters.     

鸡胚发育后期心电图的无损测定及心率变化

目的：测量鸣胚发育后期心电图,测定鸡胚发育后期心率及其变化.方法：利用壳膜外电极测量鸡胚心电图,根据RR间期计算鸡胚心率。结果：引出了具有较为清晰Q波、R波（振幅在8—20μV波动）、S波的鸡胚心电图。鸡胚的QRs间期在发育后期无明显变化,心率在D14～D20早期的心率变化较小,在D20后期和D21显著增加（P〈0．01）。结论：建立了壳膜外记录鸡胚心电图的方法,鸡胚在啄壳期心率显著增加.     

Indirect genetic effects underlie oxygen-limited thermal tolerance within a coastal population of chinook salmon

With global temperatures projected to surpass the limits of thermal tolerance for many species, evaluating the heritable variation underlying thermal tolerance is critical for understanding the potential for adaptation to climate change. We examined the evolutionary potential of thermal tolerance within a population of chinook salmon (Oncorhynchus tshawytscha) by conducting a full-factorial breeding design and measuring the thermal performance of cardiac function and the critical thermal maximum (CT_max) of offspring from each family. Additive genetic variation in offspring phenotype was mostly negligible, although these direct genetic effects explained 53% of the variation in resting heart rate (f_H). Conversely, maternal effects had a significant influence on resting f_H, scope for f_H, cardiac arrhythmia temperature and CT_max. These maternal effects were associated with egg size, as indicated by strong relationships between the mean egg diameter of mothers and offspring thermal tolerance. Because egg size can be highly heritable in chinook salmon, our finding indicates that the maternal effects of egg size constitute an indirect genetic effect contributing to thermal tolerance. Such indirect genetic effects could accelerate evolutionary responses to the selection imposed by rising temperatures and could contribute to the population-specific thermal tolerance that has recently been uncovered among Pacific salmon populations.     

Allocation of maternal- and ejaculate-derived proteins to reproduction in female crickets, Teleogryllus oceanicus

Female fitness has traditionally been thought to be maximized with one or a few matings. More recent research suggests that polyandry, mating with two or more males, can generate an increase in the viability of offspring females produce. However, the mechanism(s) underlying enhanced offspring viability remain largely unknown. The Australian field cricket Teleogryllus oceanicus has proved a useful model for examining the evolutionary significance of polyandry. Embryo viability appears to be associated with a male's investment in accessory gland tissue, implicating a role for seminal fluid. Here, I used amino acids labelled with different radio isotopes to identify proteins manufactured by males and females before they engaged in reproduction. Males incorporated 95% of the radiolabel into the testes, accessory glands and the ejaculate that was transferred to the female at mating. Male ejaculate compounds were incorporated predominantly into the female's somatic tissue. Relatively more female compounds were incorporated into the ovaries and into laid eggs than ejaculate compounds, and relatively fewer female compounds were sequestered in the somatic tissue than ejaculate compounds. The patterns observed suggest that while ejaculate compounds may be incorporated directly into eggs, they are likely to have a larger effect on maternal allocation to offspring.     

Atlantic salmon growth in strongly food-limited environments: Effects of egg size and paternal phenotype?

I manipulated egg size and followed individual mass trajectories from the egg stage in Atlantic salmon to test for effects of size, and for interactions between size and paternal body mass, on offspring performance in strongly food-limited environments. Egg size had a strong effect on body mass at yolk absorption, causing juveniles originating from large eggs to outgrow their siblings from small eggs. This corroborates previous findings of egg size effects under more benign environments, and demonstrates that positive effects of egg size on offspring success are manifested even under strong food-limitation. Previously reported negative effects of being large during the critical period for survival in dense populations are thus likely related to social interactions, rather than to effects of density on total food abundance in the environment. The effect of egg size on offspring performance, and hence the optimal egg size, was independent of paternal body mass.     

Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses

Maternal effects such as androgen in avian eggs can mediate evolutionary responses to selection, allowing manipulation of offspring phenotype and promoting trans-generational adaptive effects. We tested the predictions of two adaptive hypotheses that have been proposed to explain female variation in yolk androgen allocation in birds, using the barn swallow Hirundo rustica as a model. We found no support for the first hypothesis proposing that yolk androgen varies as a function of breeding density in order to prepare offspring for different breeding densities. However, we found experimental support for the hypothesis that female yolk androgen allocation depends on mate attractiveness and that it constitutes an example of differential allocation. Females increased the concentration of androgens in their eggs when mated to males with experimentally elongated tails. Female phenotypic quality as measured by arrival date and clutch size was positively related to egg androgen concentration, consistent with the hypothesis that this is a costly investment, constrained by female condition. We found correlative evidence of a direct relationship between egg androgen concentration and performance of offspring as measured by mass increase.     

Old experiments and new trends in avian sex differentiation

Summary The influence of steroid hormones on sex differentiation was first demonstrated in birds in 1935. Steroid female hormones injected in vivo into male embryos determined a partial or total feminization of gonads and genital ducts. Male hormones determined only the sex reversal of the ducts. Some substances of the group of androgens, such as dehydroandrosterone, had a paradoxical effect; they feminized males and masculinized females. Similar effects were observed later by several authors in all groups of vertebrates. In placentary mammals, only genital ducts were transformed. Castration of avian embryos also demonstrated the role of embryonic sexual hormones on genital ducts. These results, first obtained in vivo, were confirmed by experiments in vitro. Since then numerous studies have been undertaken on the nature of the hormone responsible for the regression of müllerian ducts in embryos of birds and other groups of vertebrates. Some authors assumed that these substances are proteins; many offered new evidence for the role of steroid sexual hormones during sex differentiation. Thus the problem appeared more complicated than it was thought at first. In recent years, synthesis of steroid sexual hormones have been demonstrated in young embryos during or even before sex differentiation; and enzymes that catalyze the synthesis of these hormones, such as hydroxysteroiddehydrogenase, also have been discovered. Further research has been oriented toward the characterization of steroid hormones by techniques of immunochemistry and labeled isotopes confirming the results obtained by other techniques. Specific proteins are being isolated in the effectors; they work as receptors of steroid hormones. Nuclear receptors of estradiol have been discovered in the embryonic gonads and in the cloacal wall at the time of sexual differentiation. Thus a mechanism can be conceived in which proteins and steroid hormones play mutual roles in the process of sex differentiation. Presented in the formal symposium on Sexual Differentiation in Vitro and in Vivo at the 29th Annual Meeting of the Tissue Culture Association, Denver, Colorado, June 4–8, 1978.     

吗啡对鸡胚胎发育的影响

目的：研究吗啡对胎动、心率、孵化率、孵化时间、雏鸡体重等的影响。方法：以气室给药的方式给鸡胚注射吗啡,记录胎动、心率、孵化率、孵化时间、雏鸡体重。结果：吗啡可以缩短雏鸡的孵化时间,降低雏鸡的孵化率,并导致雏鸡出现运动障碍;20mg／kg吗啡剂量和12—16胚龄的给药时间,鸡胚孵化率最高,残疾率最低;吗啡导致胚胎心率加快,胎动减少（P〈0．05）。结论：吗啡对胚胎发育有损伤作用,损伤程度与吗啡剂量和给药时间有关。