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

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

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

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

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

Symposium overview: Integrating cognitive, motivational, and sensory biases underlying acoustic- and multimodal-based mate choice

The goal of this symposium Integrating Cognitive, Motivational and Sensory Biases Underlying Acoustic and Multimodal-Based Mate Choice was to build a more complete framework in which to understand the mate choice brain. The presentations and papers within this symposium incorporate studies of motivational, cognitive, sensory and salience components of mate choice and highlight future directions that are needed to understand the biological basis of mate choice decision-making

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

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

Sex Differences in Spatial Memory in Brown-Headed Cowbirds: Males Outperform Females on a Touchscreen Task

Spatial cognition in females and males can differ in species in which there are sex-specific patterns in the use of space. Brown-headed cowbirds are brood parasites that show a reversal of sex-typical space use often seen in mammals. Female cowbirds, search for, revisit and parasitize hosts nests, have a larger hippocampus than males and have better memory than males for a rewarded location in an open spatial environment. In the current study, we tested female and male cowbirds in breeding and non-breeding conditions on a touchscreen delayed-match-to-sample task using both spatial and colour stimuli. Our goal was to determine whether sex differences in spatial memory in cowbirds generalizes to all spatial tasks or is task-dependant. Both sexes performed better on the spatial than on the colour touchscreen task. On the spatial task, breeding males outperformed breeding females. On the colour task, females and males did not differ, but females performed better in breeding condition than in non-breeding condition. Although female cowbirds were observed to outperform males on a previous larger-scale spatial task, males performed better than females on a task testing spatial memory in the cowbirds\u27 immediate visual field. Spatial abilities in cowbirds can favour males or females depending on the type of spatial task, as has been observed in mammals, including humans