Diego Gil

Chapter 7 Hormones in Avian Eggs: Physiology, Ecology and Behavior

Publisher Summary This chapter discusses the physiology, ecology, and behavior of hormones in avian eggs. The main source of hormones found in avian eggs is the maturing follicles of the female ovary that contain specialized cells creating different hormones during their development. The granulosa cells of the largest preovulatory follicles (F1) are the main source of circulating progesterone. Theca cells produce both estrogen and androgens, and the production decreases with increasing follicular maturation. Postovulatory follicles continue to produce steroids before final atresia, and their low androgen production during incubation is brought about by a decrease in luteinizing hormone stimulation rather than by a reduction of the steroidogenic capacity of the theca interna cells at that stage. Although sexual differentiation takes place in the early embryo by the means of processes based on estradiol, the development of sexually selected characters in birds is tightly linked to hormonal processes in adulthood, of both androgenic and estrogenic nature. While within‐brood distributions of yolk androgens can be highly species‐specific, many differential patterns can be found within the same species. Given the effects of androgens in chick competitiveness, females could use within‐clutch distributions of androgens to balance or reinforce the effects of hatching asynchrony.

Nestling immunocompetence and testosterone covary with brood size in a songbird.

The social and ecological conditions that individuals experience during early development have marked effects on their developmental trajectory. In songbirds, brood size is a key environmental factor affecting development, and experimental increases in brood size have been shown to have negative effects on growth, condition and fitness. Possible causes of decreased growth in chicks from enlarged broods are nutritional stress, crowding and increased social competition, i.e. environmental factors known to affect adult steroid levels (especially of testosterone and corticosteroids) in mammals and birds. Little, however, is known about environmental effects on steroid synthesis in nestlings. We addressed this question by following the development of zebra finch (Taeniopygia guttata) chicks that were cross–fostered and raised in different brood sizes. In line with previous findings, nestling growth and cell–mediated immunocompetence were negatively affected by brood size. Moreover, nestling testosterone levels covaried with treatment: plasma testosterone increased with experimental brood size. This result provides experimental evidence that levels of circulating testosterone in nestlings can be influenced by their physiological response to environmental conditions.

Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird

Research has shown that bird songs are modified in different ways to deal with urban noise and promote signal transmission through noisy environments. Urban noise is composed of low frequencies, thus the observation that songs have a higher minimum frequency in noisy places suggests this is a way of avoiding noise masking. Most studies are correlative and there is as yet little experimental evidence that this is a short-term mechanism owing to individual plasticity. Here we experimentally test if house finches (Carpodacus mexicanus) can modulate the minimum frequency of their songs in response to different noise levels. We exposed singing males to three continuous treatments: low–high–low noise levels. We found a significant increase in minimum frequency from low to high and a decrement from high to low treatments. We also found that this was mostly achieved by modifying the frequency of the same low-frequency syllable types used in the different treatments. When different low-frequency syllables were used, those sung during the noisy condition were longer than the ones sang during the quiet condition. We conclude that house finches modify their songs in several ways in response to urban noise, thus providing evidence of a short-term acoustic adaptation.

Negative effects of elevated testosterone on female fecundity in zebra finches

Although factors influencing androgen deposition in the avian egg and its effects on nestling fitness are recently receiving considerable attention, little is known about the potential costs of high testosterone levels in the females. Our study aimed at determining the effect of injections of testosterone (T) in female zebra finches (Taeniopygia guttata), on clutch size, egg mass, yolk mass, and yolk androgen content. Females were given a single bolus injection of T in a range of doses after laying the first egg. Results show that administration of T negatively affected clutch size; the strength of this effect increased with increasing doses of T. Females injected with the highest testosterone dose showed suppressed oviposition of the third and the fourth eggs. Interestingly, testosterone administration made females produce eggs with relatively large yolks, suggesting that T may mediate the trade-off between number and size of eggs. Testosterone injection resulted in elevated levels of androgen in the eggs, in contrast to control clutches, which showed a decreasing pattern of androgen concentration along the laying sequence. We conclude that high androgen investment in eggs may be limited by physiological requirements of the ovulatory process.

Maternal developmental stress reduces reproductive success of female offspring in zebra finches

Environmental factors play a key role in the expression of phenotypic traits and life-history decisions, specifically when they act during early development. In birds, brood size is a main environmental factor affecting development. Experimental manipulation of brood sizes can result in reduced offspring condition, indicating that developmental deficits in enlarged broods have consequences within the affected generation. Yet, it is unclear whether stress during early development can have fitness consequences projecting into the next generation. To study such trans-generational fitness effects, we bred female zebra finches, Taeniopygia guttata, whose mothers had been raised in different experimental brood sizes. We found that adult females were increasingly smaller with increasing experimental brood size in which their mother had been raised. Furthermore, reproductive success at hatching and fledging covaried negatively with the experimental brood size in which their mothers were raised. These results illustrate that early developmental stress can have long-lasting effects affecting reproductive success of future generations. Such trans-generational effects can be life-history responses adapted to environmental conditions experienced early in life.

Correlated evolution of male and female testosterone profiles in birds and its consequences

Circulating levels of testosterone in adults have mainly evolved as a consequence of selection on males for increased levels, while levels of circulating testosterone in females may be an indirect consequence of selection on males. A review of the literature revealed that intense directional selection for high levels of circulating testosterone in birds is likely to be mainly due to direct selection on males. A comparative study of testosterone levels in birds revealed a strong positive relationship between peak testosterone levels in adult females and peak levels in males. The slope of this relationship was significantly less than unity, implying that the testosterone levels in females have been reduced in species with high levels in males. An analysis of the order of evolutionary events suggested that peak concentration of testosterone in females changed after peak concentrations of testosterone in males. Females in colonial species of birds had significantly higher circulating peak testosterone levels compared to females of solitary species, and relative levels after controlling for the effects of peak levels in males were also larger, suggesting that any costs of high testosterone levels in females are particularly likely in colonial birds. Direct selection on male circulating testosterone levels may increase the costs that females incur from high testosterone titers. For example, high female levels may negatively affect ovulation and laying and may also affect the levels of testosterone that females deposit in their eggs and hence the exposure of pre- and post-hatching offspring to testosterone. This in turn may affect not only offspring behavior, but also offspring development and the trade-offs between growth, development of immune function, and behavior in offspring.

Transgenerational effects on body size caused by early developmental stress in zebra finches.

The nutritional and social conditions that individuals experience during early development can have profound effects on their morphology, physiology, behaviour and life history. Experimental increases in brood size in birds can result in reduced offspring condition and survival, indicating that developmental deficits in enlarged broods have negative fitness consequences within the affected generation. To study long-term effects (i.e. transgenerational effects of developmental stress), we conducted a two-step breeding experiment in which we manipulated early developmental conditions in zebra finches Taeniopygia guttata. We raised zebra finches by manipulating brood sizes and controlled for maternal and genetic effects by cross-fostering. In a previous study, we showed that offspring condition and body size decreased with increasing brood size. Here we show that this effect was carried over to the next generation. Body size in nestlings and at nutritional independence was affected by the brood size in which the mothers were raised. Female offspring did significantly worse than male offspring when the mother had been raised in large broods, suggesting sex-specific influences of maternal effects. These findings directly link early developmental stress in females via maternal effects to the phenotype of the next generation.

Strategies of song adaptation to urban noise in the house finch: syllable pitch plasticity or differential syllable use?

The influence of ambient noise in shaping birdsong attributes has received much attention lately. Recent work shows that some birds sing higher-pitched songs in noisy areas, which may allow them to avoid acoustic interference; yet it is not clear how this is achieved. Higher-pitched songs may be produced either by using the same syllable types in quiet and noisy areas, but singing them at a higher frequency in the latter (syllable pitch plasticity), or by using different syllable types in silent and in noisy circumstances (differential syllable use). Here we explored both strategies in the Mexico City population of house finch (Carpodacus mexicanus), a species known to possess a repertoire of several hundreds of syllable types. Birds produced songs with higher minimum frequencies in noisy than in quiet areas. This was mostly due to the minimum frequency of some syllable types being higher in noisy areas than in quiet locations. Also, males modulated the minimum frequency of the same syllable type during momentary increases of noise. Our results can help explain the high success of house finches at colonizing urban areas, while providing evidence of syllable pitch plasticity.

Food availability affects the maternal transfer of androgens and antibodies into eggs of a colonial seabird

Mothers can improve the quality of their offspring by increasing the level of certain components in their eggs. To examine whether or not mothers increase deposition of such components in eggs as a function of food availability, we food‐supplemented black‐legged kittiwake females (Rissa tridactyla) before and during egg laying and compared deposition of androgens and antibodies into eggs of first and experimentally induced replacement clutches. Food‐supplemented females transferred lower amounts of androgens and antibodies into eggs of induced replacement clutches than did non‐food‐supplemented mothers, whereas first clutches presented no differences between treatments. Our results suggest that when females are in lower condition, they transfer more androgens and antibodies into eggs to facilitate chick development despite potential long‐term costs for juveniles. Females in prime condition may avoid these potential long‐term costs because they can provide their chicks with more and higher quality resources.

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.