Glucocorticoids and “Stress” Are Not Synonymous

Synopsis Reference to glucocorticoids as “stress hormones” has been growing in prevalence in the literature, including in comparative and environmental endocrinology. Although glucocorticoids are elevated in response to a variety of stressors in vertebrate animals, the primary functions of glucocorticoids are not responding to stressors and they are only one component of complex suite of physiological and behavioral responses to stressors. Thus, the use of the short-hand phrase “stress hormone” can be misleading. Further, simply measuring glucocorticoids is not equivalent to measuring a stress response, nor is manipulating glucocorticoids equivalent to exposing an animal to a stressor. In this commentary we highlight the problems with using functional names for hormones, and of treating cortisol or corticosterone as synonymous with stress. We provide recommendations to add clarity to the presentation of research on this topic, and to avoid conflation of glucocorticoids with stressors and the stress response in the design of experiments. Synopsis Los Glucocorticoides y el “Estrés” no Son Sinónimos (Glucocorticoids and “Stress” Are Not Synonymous) La referencia a los glucocorticoides como “hormonas del estrés” ha aumentado en prevalencia en la literatura, incluso en endocrinología comparativa y ecológica. Aunque los glucocorticoides están elevados en respuesta a una variedad de factores de estrés en animales vertebrados, las funciones primarias de los glucocorticoides no responden a los factores de estrés y son solo un componente de un conjunto complejo de respuestas fisiológicas y de comportamiento a los factores de estrés. Por lo tanto, el uso de la frase abreviada “hormona del estrés” puede ser engañoso. Además, simplemente medir glucocorticoides no es equivalente a medir una respuesta al estrés, ni manipular glucocorticoides equivalente a exponer a un animal a un factor estresante. En este comentario destacamos los problemas con el uso de nombres funcionales para las hormonas y con el tratamiento del cortisol o la corticosterona como sinónimo de estrés. Brindamos recomendaciones para agregar claridad a la presentación de investigaciones sobre este tema y para evitar la combinación de glucocorticoides con factores estresantes y la respuesta al estrés en el diseño de los experimentos. Translated to Spanish by J. Heras ([email protected]) Synopsis Glucocorticoide und “Stress” Sind Keine Synonyme (Glucocorticoids and “Stress” Are Not Synonymous) Die Bezugnahme auf Glucocorticoide als “Stresshormone” hat in der Literatur zugenommen, auch in der vergleichenden und ökologischen Endokrinologie. Obwohl Glucocorticoide als Reaktion auf eine Vielzahl von Stressoren bei Wirbeltieren erhöht sind, antworten die primären Funktionen von Glucocorticoiden nicht auf Stressoren und sind nur eine Komponente einer komplexen Reihe von physiologischen und Verhaltensreaktionen auf Stressoren. Daher kann die Verwendung der Kurzformel “Stresshormon” irreführend sein. Darüber hinaus ist das einfache Messen von Glucocorticoiden nicht gleichbedeutend mit dem Messen einer Stressreaktion und das Manipulieren von Glucocorticoiden nicht gleichbedeutend damit, ein Tier einem Stressor auszusetzen. In diesem Kommentar werden wir die Probleme bei der Verwendung funktioneller Bezeichnungen für Hormone und bei der Betrachtung von Cortisol oder Corticosteron als Synonym für Stress hervorheben. Wir geben Empfehlungen, um die Präsentation der Forschungsergebnisse zu diesem Thema klarer zu gestalten und die Verschmelzung von Glucocorticoiden mit Stressoren und der Stressreaktion bei der Versuchsplanung zu vermeiden. Translated to German by F. Klimm ([email protected]) Synopsis Glucocorticóides e “Stress” Não São Sinônimos (Glucocorticoids and “Stress” Are Not Synonymous) A referência aos glicocorticóides como “hormônios do estresse” vem se tornando prevalente em literatura, inclusive na endocrinologia comparada e ecológica. Embora os glicocorticóides sejam elevados em resposta a uma variedade de estressores em vertebrados, as funções primárias de glicocorticóides são a de não responder aos causadores do stress e eles são apenas um componente dentro de um complexo conjunto de respostas fisiológicas e comportamentais aos estressores. Assim, o uso da frase curta “hormônio do estresse” pode ser errôneo. Além disso, simplesmente medir glicocorticóides não é equivalente a medir uma resposta ao estresse, nem a manipulação de glicocorticoides é equivalente a expor um animal a um estressor. Neste comentário, destacamos os problemas com o uso de nomes funcionais para hormônios e o tratamento de cortisol ou corticosterona como sinônimos de estresse. Nós provemos recomendações para adicionar clareza à apresentação de pesquisas deste tópico e para evitar a o tratamento direto de glicocorticoides como estressores e a resposta ao estresse no planejamento de experimentos. Translated to Portuguese by Diego Vaz ([email protected]

The levels of analysis revisited.

The term levels of analysis has been used in several ways: to distinguish between ultimate and proximate levels, to categorize different kinds of research questions and to differentiate levels of reductionism. Because questions regarding ultimate function and proximate mechanisms are logically distinct, I suggest that distinguishing between these two levels is the best use of the term. Integrating across levels in research has potential risks, but many benefits. Consideration at one level can help generate novel hypotheses at the other, define categories of behaviour and set criteria that must be addressed. Taking an adaptationist stance thus strengthens research on proximate mechanisms. Similarly, it is critical for researchers studying adaptation and function to have detailed knowledge of proximate mechanisms that may constrain or modulate evolutionary processes. Despite the benefits of integrating across ultimate and proximate levels, failure to clearly identify levels of analysis, and whether or not hypotheses are exclusive alternatives, can create false debates. Such non-alternative hypotheses may occur between or within levels, and are not limited to integrative approaches. In this review, I survey different uses of the term levels of analysis and the benefits of integration, and highlight examples of false debate within and between levels. The best integrative biology reciprocally uses ultimate and proximate hypotheses to generate a more complete understanding of behaviour

Developmental stress, condition, and birdsong: a case study in song sparrows.

Sexual-selection theory posits that ornaments and displays can reflect a signaler\u27s condition, which in turn is affected both by recent and developmental conditions. Moreover, developmental conditions can induce correlations between sexually selected and other traits if both types of traits exhibit developmental phenotypic plasticity in response to stressors. Thus, sexually selected traits may reflect recent and/or developmental characteristics of signalers. Here, we review data on the relationships between birdsong, a sexually selected trait, and developmental and current condition of birds from a long-term study of a population of song sparrows (Melospiza melodia). Field studies of free-living birds indicate that the complexity of a male\u27s songs, a permanent trait, reflects the size of a song-control region of his brain (HVC), and is correlated with body size and several parameters of immunity, specifically investment in protective proteins. However, the performance of a male\u27s songs, a dynamic trait, is not correlated to immune investment. Complexity of song is correlated with the glucocorticoid stress-response, and in some years response to stress predicts overwinter survival. Experimental manipulations have revealed that stressors in early life impair development of HVC, but that HVC recovers in size by adulthood. These manipulations result in impaired song-complexity and song-learning, but not song-performance. Experimental developmental stressors also affect growth, endocrine physiology, metabolism, and immune-function, often in a sex-specific manner. Combined, these studies suggest that song-complexity provides reliable information about early developmental experience, and about other traits that have critical developmental periods. Birdsong thus provides a multi-faceted sexually selected trait that may be an indicator both of developmental and recent conditions

Long-term winter-site fidelity in Song Sparrows (Melospiza melodia)

In migratory animals, the degree to which individuals return to the same wintering sites across multiple years can affect fitness and population dynamics, and thus has important implications for conservation. Despite this, long-term evaluations of wintering-site fidelity are rare for migratory birds: many populations are intensively studied on their breeding grounds but tracking the migratory movements of small birds once they leave the breeding grounds is challenging. To evaluate patterns of overwintering location and fidelity, we collected winter-grown claw tissue from 301 Song Sparrows (Melospiza melodia; 449 samples) captured in spring at their breeding grounds over six consecutive years and assessed stable hydrogen isotope (δ2Hc) values to determine within-individual repeatability and between-year variation in wintering latitudes. We also retrieved useable data from eight geolocators over two consecutive winters. Geolocator-derived wintering positions correlated with origins based on δ2Hc values. Consistent with previous findings, male δ2Hcvalues reflected more northerly wintering areas than those of females, indicating shorter latitudinal migration distances for males, but the magnitude of the sex difference varied across years. The distribution of wintering latitudes was generally consistent among years, except for the 2015 – 2016 winter that had unusually negative δ2Hc values. Values of δ2Hc were repeatable for males but not for females, suggesting that winter-site fidelity could differ between sexes. The data presented here emphasize the importance of tracking migratory populations across multiple years to uncover factors affecting population dynamics

Zebra finches go wild! Experimental cultural evolution of birdsong

Vocal learning in songbirds is guided by experience and experience-independent factors. Previously, lineages of zebra finches founded by isolate-reared tutors showed cultural evolution to wild-type song. This suggests that experience-independent biases affect song development even in the absence of wild-type song. We hypothesized that cultural evolution of song depends on both experience-independent biases and tutor songs available. We predicted that songs more distant from wild-type would take longer to culturally evolve toward wild-type features. We bred zebra finches in three groups of lineages in which offspring of each generation served as tutors for the next. Lineages were founded with males singing wild-type song, isolate song, or heterospecific song. The two experimental lineages exhibited rapid cultural evolution of song with many temporal and spectral features converging to wild-type within two generations. However the rate of change differed depending on song features measured, and took longer for lineages founded with heterospecific song

Immune Profiles Vary Seasonally, But Are Not Significantly Related To Migration Distance Or Natal Dispersal, In A Migratory Songbird

A central tenet of ecoimmunology is that an organism’s environment shapes its optimal investment in immunity. For example, the benefits of acquired (relatively pathogen-specific) versus innate (non-specific) immune defences are thought to vary with the risk of encountering familiar versus unfamiliar pathogens. Because pathogen communities vary geographically, individuals that travel farther during seasonal migration or natal dispersal are predicted to have higher exposure to novel pathogens, and lower exposure to familiar pathogens, potentially favoring investment in innate immunity. During the breeding season, migratory animals’ exposure to familiar pathogens should increase, potentially favoring investment in acquired immunity. We hypothesized that song sparrows Melospiza melodia adjust their constitutive immune profiles in response to risk of encountering novel versus familiar pathogens. We predicted that individuals migrating longer distances (inferred from stable hydrogen isotope analysis of claws) and less philopatric individuals (inferred from microsatellite assignment testing) would rely more heavily on acquired than innate defences. We also predicted that reliance on acquired defences would increase throughout the early breeding season. Consistent with trade-offs between acquired and innate defences, levels of immunoglobulin Y (acquired) varied negatively with macrophage phagocytosis activity (innate). Levels of acquired relative to innate immunity did not vary significantly with migration distance or philopatry, but increased throughout the early breeding season. Macrophage phagocytosis was not significantly repeatable between years. Song sparrows appear to shift from innate defences immediately after migration, to acquired defences with increasing time at the breeding grounds. These patterns highlight the plasticity of constitutive immune defences in migratory animals

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

No Evidence that Songbirds Use Odour Cues to Avoid Malaria-infected Conspecifics

Many animals have evolved mechanisms to detect and avoid parasitized conspecifics, primarily through odour cues, but whether birds are capable of odour-mediated parasite avoidance is unknown. Recently, we showed that exposing song sparrows (Melospiza melodia) to avian malaria parasites (Plasmodium sp.) alters the chemical composition of their preen oil, which is the major source of body odour in birds. Here, we presented song sparrows with preen oil from uninfected (sham-inoculated) and malaria-infected conspecifics, predicting that birds would spend more time with odour cues from uninfected than infected birds. Birds without detectable malarial infections spent about 50% more time with preen oil from uninfected than infected conspecifics, and females spent nearly twice as much time with preen oil from uninfected than infected conspecifics. However, neither difference was statistically significant. Song sparrows may be unable to detect odour cues of infection, but further experiments are needed to confirm or refute this

High Rates of Exposure to Simulated Winter Storm Cues Negatively Affect White-Throated Sparrow (Zonotrichia albicollis) Energy Reserves

Birds are often able to cope with, and respond to, inclement weather with physiological and behavioral responses. As storms become more severe or frequent as a result of climate change, the adaptive coping responses of many species may be pushed beyond current tolerance limits. We investigated the effects of experimental recurrent inclement winter weather cues on body composition, glucocorticoid hormones, and behavior of white-throated sparrows (Zonotrichia albicollis). We used a hypobaric climatic wind tunnel to simulate storms by transiently decreasing barometric pressure and temperature, and measured behavioral responses, body composition, and baseline corticosterone levels in birds exposed, or not exposed (control), to different frequencies of simulated storms. In study 1, experimental birds were exposed to one storm per week over 9 weeks. In study 2, experimental birds were exposed to two storms per week over 12 weeks. Birds exposed to one simulated storm per week had higher fat and lean masses than control birds, with no differences in the amount of time groups spent feeding. This change in body composition suggests that birds were coping by increasing energy stores. In contrast, birds exposed to two simulated storms per week had lower fat masses compared to control birds, even though they spent more time feeding. Experimental birds in study 2 also had lower baseline corticosterone levels than controls. These changes suggest that the coping response observed in study 1 was not possible in study 2. These findings provide novel experimental evidence that birds detect and respond to changes in temperature and barometric pressure independent of other storm-related cues. One simulated storm per week resulted in potentially adaptive responses of increased mass. However, increasing the frequency of storm exposure to twice per week exceeded the birds’ capacity to maintain these energy reserves. These results also experimentally demonstrate that repeated exposure to inclement weather cues can directly affect birds’ energy reserves, even in the absence of a storm itself, with strong implications for survival as severe weather events continue to become more prevalent

Seasonal change in the avian hippocampus.

The hippocampus plays an important role in cognitive processes, including memory and spatial orientation, in birds. The hippocampus undergoes seasonal change in food-storing birds and brood parasites, there are changes in the hippocampus during breeding, and further changes occur in some species in association with migration. In food-storing birds, seasonal change in the hippocampus occurs in fall and winter when the cognitively demanding behaviour of caching and retrieving food occurs. The timing of annual change in the hippocampus of food-storing birds is quite variable, however, and appears not to be under photoperiod control. A variety of factors, including cognitive performance, exercise, and stress may all influence seasonal change in the avian hippocampus. The causal processes underlying seasonal change in the avian hippocampus have not been extensively examined and the more fully described hormonal influences on the mammalian hippocampus may provide hypotheses for investigating the control of hippocampal seasonality in birds