Signal Traits and Oxidative Stress: A Comparative Study across Populations with Divergent Signals

Diverging populations often shift patterns of signal use – a process that can contribute to reproductive isolation and speciation. Yet it is not clear why most traits gain or lose signal value during divergence. One reason this could occur is because changes in the relationship between signals and relevant physiological parameters degrade the reliability of a signal, or even change its underlying information content. Here we test the hypothesis that the relationship between signal trait elaboration and a central component of organismal health – oxidative stress – differs across closely related populations that have diverged in signal use and preferences. In the recently diverged barn swallow subspecies complex (Hirundo rustica, Family: Hirundinidae), different populations use different traits as sexual signals. Two of these traits, ventral breast plumage color and tail streamer length, differ markedly between North American H. r. erythrogaster and European H. r. rustica. Despite this divergence, variation in ventral plumage color was similarly associated with measures of oxidative damage across both populations. However, the directionality of these relationships differed between the sexes: darker male barn swallows had higher levels of plasma oxidative damage than their lighter counterparts, while the opposite relationship was seen in females. In contrast, relationships between tail streamer length and measures of oxidative stress were not consistent across populations. Some analyses indicated that in European H. r. rustica, where males bearing elongated streamers are preferred as mates, longer-streamered males were more oxidatively stressed; however, the opposite pattern was suggested in North American H. r. erythrogaster. Tail streamer length was not associated with measures of oxidative stress in females of either population. Differences in the physiological state of stronger signalers across populations and between the sexes may be related to costs or constraints on signal elaboration (e.g., biochemical pathways associated with melanogenesis), or reflect differences in how signal-mediated social interactions influence oxidative stress. Overall, our results suggest that while some phenotypic traits appear to be capable of conveying similar physiological information regardless of their use as signals, divergence in other phenotypic traits may be associated with shifts in their information content

Signal Traits and Oxidative Stress: A Comparative Study across Populations with Divergent Signals

Diverging populations often shift patterns of signal use – a process that can contribute to reproductive isolation and speciation. Yet it is not clear why most traits gain or lose signal value during divergence. One reason this could occur is because changes in the relationship between signals and relevant physiological parameters degrade the reliability of a signal, or even change its underlying information content. Here we test the hypothesis that the relationship between signal trait elaboration and a central component of organismal health – oxidative stress – differs across closely related populations that have diverged in signal use and preferences. In the recently diverged barn swallow subspecies complex (Hirundo rustica, Family: Hirundinidae), different populations use different traits as sexual signals. Two of these traits, ventral breast plumage color and tail streamer length, differ markedly between North American H. r. erythrogaster and European H. r. rustica. Despite this divergence, variation in ventral plumage color was similarly associated with measures of oxidative damage across both populations. However, the directionality of these relationships differed between the sexes: darker male barn swallows had higher levels of plasma oxidative damage than their lighter counterparts, while the opposite relationship was seen in females. In contrast, relationships between tail streamer length and measures of oxidative stress were not consistent across populations. Some analyses indicated that in European H. r. rustica, where males bearing elongated streamers are preferred as mates, longer-streamered males were more oxidatively stressed; however, the opposite pattern was suggested in North American H. r. erythrogaster. Tail streamer length was not associated with measures of oxidative stress in females of either population. Differences in the physiological state of stronger signalers across populations and between the sexes may be related to costs or constraints on signal elaboration (e.g., biochemical pathways associated with melanogenesis), or reflect differences in how signal-mediated social interactions influence oxidative stress. Overall, our results suggest that while some phenotypic traits appear to be capable of conveying similar physiological information regardless of their use as signals, divergence in other phenotypic traits may be associated with shifts in their information content

Multimodal signalling in the North American barn swallow: a phenotype network approach

Complex signals, involving multiple components within and across modal- ities, are common in animal communication. However, decomposing complex signals into traits and their interactions remains a fundamental challenge for studies of phenotype evolution. We apply a novel phenotype network approach for studying complex signal evolution in the North American barn swallow (Hirundo rustica erythrogaster). We integrate model testing with correlation-based phenotype networks to infer the contributions of female mate choice and male–male competition to the evolution of barn swallow communication. Overall, the best predictors of mate choice were distinct from those for competition, while moderate functional overlap suggests males and females use some of the same traits to assess potential mates and rivals. We interpret model results in the context of a network of traits, and suggest this approach allows researchers a more nuanced view of trait clustering patterns that informs new hypotheses about the evolution of communication systems. 3 supplemental files attached below

Positive Carotenoid Balance Correlates with Greater Reproductive Performance in a Wild Bird

Background: Carotenoids can confer somatic and reproductive benefits, but most evidence is from captive animal experimentation or single time-point sampling. Another perhaps more informative means by which to assess physiological contributions to animal performance is by tracking an individual’s ability to increase or sustain carotenoids or other health-related molecules over time, as these are likely to be temporally variable. Methodology/Principal Findings: In a field study of North American barn swallows (Hirundo rustica erythrogaster), we analyzed within-individual changes in carotenoid concentrations by repeatedly sampling the carotenoid profiles of individuals over the course of the breeding season. Our results demonstrate that carotenoid concentrations of individuals are temporally dynamic and that season-long balance of these molecules, rather than single time-point samples, predict reproductive performance. This was true even when controlling for two important variables associated with reproductive outcomes: (1) timing of breeding and (2) sexually selected plumage coloration, which is itself positively correlated with and concomitantly changes with circulating carotenoid concentrations. Conclusions/Significance: While reproduction itself is purported to impose health stress on organisms, these data suggest that free-ranging, high-quality individuals can mitigate such costs, by one or several genetic, environmental (diet), or physiological mechanisms. Moreover, the temporal variations in both health-linked physiological measures and morphological traits we uncover here merit further examination in other species, especially when goals include the estimation of signal information content or the costs of trait expression

Sensitive periods during the development and expression of vertebrate sexual signals: A systematic review

Many sexually selected traits exhibit phenotypic plasticity. Despite a growing appreciation for the ecological context in which sexual selection occurs, and for the role of plasticity in shaping traits associated with local adaptation and divergence, there is an important gap in knowledge about the onset and duration of plasticity in sexual trait expression. Integrating this temporal dimension of plasticity into models of sexual selection informs our understanding of the information conveyed by sexual traits and our predictions related to trait evolution, and is critical in this time of unprecedented and rapid environmental change. We conducted a systematic review of 869 studies to ask how trait modalities (e.g., visual and chemical) relate to the onset and duration of plasticity in vertebrate sexual signals. We show that this literature is dominated by studies of coloration in birds and fish, and most studies take place during the breeding season. Where possible, we integrate results across studies to link physiology of specific trait modalities with the life stage (e.g., juvenile, breeding, or nonbreeding) during which plasticity occurs in well-studied traits. Limitations of our review included a lack of replication in our dataset, which precluded formal analysis. We argue that the timing of trait plasticity, in addition to environmental context, is critical for determining whether and how various communication signals are associated with ecological context, because plasticity may be ongoing or occur at only one point in an individual's lifetime, and determining a fixed trajectory of trait expression. We advocate for careful consideration of the onset and duration of plasticity when analyzing how environmental variation affects sexual trait expression and associated evolutionary outcomes.</p

Positive Carotenoid Balance Correlates with Greater Reproductive Performance in a Wild Bird

Background: Carotenoids can confer somatic and reproductive benefits, but most evidence is from captive animal experimentation or single time-point sampling. Another perhaps more informative means by which to assess physiological contributions to animal performance is by tracking an individual’s ability to increase or sustain carotenoids or other healthrelated molecules over time, as these are likely to be temporally variable. Methodology/Principal Findings: In a field study of North American barn swallows (Hirundo rustica erythrogaster), we analyzed within-individual changes in carotenoid concentrations by repeatedly sampling the carotenoid profiles of individuals over the course of the breeding season. Our results demonstrate that carotenoid concentrations of individuals are temporally dynamic and that season-long balance of these molecules, rather than single time-point samples, predict reproductive performance. This was true even when controlling for two important variables associated with reproductive outcomes: (1) timing of breeding and (2) sexually selected plumage coloration, which is itself positively correlated with and concomitantly changes with circulating carotenoid concentrations. Conclusions/Significance: While reproduction itself is purported to impose health stress on organisms, these data suggest that free-ranging, high-quality individuals can mitigate such costs, by one or several genetic, environmental (diet), or physiological mechanisms. Moreover, the temporal variations in both health-linked physiological measures an

The importance of cross-validation, accuracy, and precision for measuring plumage color: A comment on Vaquero-Alba et al. (2016)

Vaquero-Alba and colleagues published a study in The Auk: Ornithological Advances comparing objective color measurements of plumage taken in the field directly on a bird’s body to those taken in the lab on collected feathers arranged to emulate the appearance of a bird’s natural plumage. Although the field measures of plumage color were less repeatable than lab measures, the authors concluded that measurements taken in the field were more representative of a bird’s ‘‘true color.’’ Accordingly, they recommend that researchers should bring spectrophotometers into the field to measure color on live birds. We question the assumption that their field measurements represent true color and highlight concerns regarding their experimental design and methodology. Because they did not measure color of live birds in the lab or the color of plucked feathers in the field, they cannot directly test whether the assessment of color in the field on a live bird is superior. Also, rather than assume field measures are the most accurate or precise way to assess plumage color, we suggest cross-validation with other methodologies, such as digital photography, pigment biochemistry, or measures of a known color standard in both environments. Importantly, researchers should be aware of the limitations and advantages of various methods for measuring plumage color so they can use the method most appropriate for their study. Vaquero-Alba y sus colaboradores publicaron un estudio en The Auk comparando medidas objetivas del color del plumaje tomadas en el campo directamente en el cuerpo del ave con medidas tomadas en el laboratorio en plumas recolectadas y organizadas para emular la apariencia natural del plumaje. Aunque las medidas de campo del color del plumaje fueron menos repetibles que las de laboratorio, los autores concluyeron que las medidas tomadas en el campo fueron ma´s representativas del ‘‘color verdadero’’ de un ave. En consecuencia, recomendaron que los investigadores deben llevar espectrofot ´ ometros a los sitios de campo para medir el color en aves vivas. Cuestionamos la suposici ´on de que sus mediciones de campo representan el ‘‘color verdadero’’ y resaltamos nuestras preocupaciones con respecto a su dise ˜no experimental y metodolog´ıa. Debido a que ellos no midieron el color de las aves vivas en el laboratorio ni el color de las plumas sueltas en el campo, no pueden evaluar directamente si la evaluaci ´on del color en el campo en un ave viva es superior. Tambi´en, en vez de asumir que las medidas de campo son la forma ma´s exacta o precisa de determinar el color del plumaje, sugerimos que se haga una validaci ´on cruzada con otras metodolog´ıas como la fotograf´ıa digital, la bioqu´ımica de los pigmentos o las medidas de un esta´ndar de un color conocido en ambos ambientes. Es importante que los investigadores tengan en cuenta las limitaciones y avances en varios m´etodos para medir el color del plumaje para que puedan usar el m´etodo ma´s apropiado para su estudio

The importance of cross-validation, accuracy, and precision for measuring plumage color: A comment on Vaquero-Alba et al. (2016)

Vaquero-Alba and colleagues published a study in The Auk: Ornithological Advances comparing objective color measurements of plumage taken in the field directly on a bird’s body to those taken in the lab on collected feathers arranged to emulate the appearance of a bird’s natural plumage. Although the field measures of plumage color were less repeatable than lab measures, the authors concluded that measurements taken in the field were more representative of a bird’s ‘‘true color.’’ Accordingly, they recommend that researchers should bring spectrophotometers into the field to measure color on live birds. We question the assumption that their field measurements represent true color and highlight concerns regarding their experimental design and methodology. Because they did not measure color of live birds in the lab or the color of plucked feathers in the field, they cannot directly test whether the assessment of color in the field on a live bird is superior. Also, rather than assume field measures are the most accurate or precise way to assess plumage color, we suggest cross-validation with other methodologies, such as digital photography, pigment biochemistry, or measures of a known color standard in both environments. Importantly, researchers should be aware of the limitations and advantages of various methods for measuring plumage color so they can use the method most appropriate for their study. Vaquero-Alba y sus colaboradores publicaron un estudio en The Auk comparando medidas objetivas del color del plumaje tomadas en el campo directamente en el cuerpo del ave con medidas tomadas en el laboratorio en plumas recolectadas y organizadas para emular la apariencia natural del plumaje. Aunque las medidas de campo del color del plumaje fueron menos repetibles que las de laboratorio, los autores concluyeron que las medidas tomadas en el campo fueron ma´s representativas del ‘‘color verdadero’’ de un ave. En consecuencia, recomendaron que los investigadores deben llevar espectrofot ´ ometros a los sitios de campo para medir el color en aves vivas. Cuestionamos la suposici ´on de que sus mediciones de campo representan el ‘‘color verdadero’’ y resaltamos nuestras preocupaciones con respecto a su dise ˜no experimental y metodolog´ıa. Debido a que ellos no midieron el color de las aves vivas en el laboratorio ni el color de las plumas sueltas en el campo, no pueden evaluar directamente si la evaluaci ´on del color en el campo en un ave viva es superior. Tambi´en, en vez de asumir que las medidas de campo son la forma ma´s exacta o precisa de determinar el color del plumaje, sugerimos que se haga una validaci ´on cruzada con otras metodolog´ıas como la fotograf´ıa digital, la bioqu´ımica de los pigmentos o las medidas de un esta´ndar de un color conocido en ambos ambientes. Es importante que los investigadores tengan en cuenta las limitaciones y avances en varios m´etodos para medir el color del plumaje para que puedan usar el m´etodo ma´s apropiado para su estudio