Early‐life immune activation increases song complexity and alters phenotypic associations between sexual ornaments

Abstract

Summary Early-life adversity can have long-lasting effects on physiological, behavioural, cognitive, and somatic processes. Consequently, these effects may alter an organism’s life-history strategy and reproductive tactics.In response to early-life immune activation, we quantified levels of the acute phase protein haptoglobin (Hp) during development in male zebra finches (Taeniopygia guttata). Then, we examined the long-term impacts of early-life immune activation on an important static sexual signal, song complexity, as well as effects of early-life immune activation on the relationship between song complexity and a dynamic sexual signal, beak colouration. Finally, we performed mate-choice trials to determine if male early-life experience impacted female preference.Challenge with keyhole limpet hemocyanin (KLH) resulted in increased song complexity compared to lipopolysaccharide (LPS) treatment or the control. Hp levels were inversely correlated with song complexity. Moreover, KLH-treatment resulted in negative associations between the two sexual signals (beak colouration and song complexity). Females demonstrated some preference for KLH-treated males over controls and for control males over LPS-treated males in mate choice trials.Developmental immune activation has variable effects on the expression of secondary sexual traits in adulthood, including enhancing the expression of some traits. Because developmental levels of Hp and adult song complexity were correlated, future studies should explore a potential role for exposure to inflammation during development on song learning.Early-life adversity may differentially impact static versus dynamic signals. The use of phenotypic correlations can be a powerful tool for examining the impact of early-life experience on the associations among different traits, including sexual signals.

Early‐life patterns of growth are linked to levels of phenotypic trait covariance and postfledging mortality across avian species

“…It is not yet clear, however, how well this concept explains emerging patterns of trait covariance in work examining the effects of different early‐life conditions. As documented previously (Careau et al, 2014 ; Hebert et al, 1994 ; Killen et al, 2013 ; Merrill & Grindstaff, 2018 ; Merrill et al, 2017 ), challenging early‐life conditions can result in more positive trait covariance. However, they can also result in more negative trait covariance, such that two traits are inversely correlated with one another (Merrill & Grindstaff, 2018 ; Merrill et al, 2017 ).…”

“…For instance, if values for two traits are plotted against one another (e.g., wing length on the x ‐axis and body mass on the y ‐axis), points may be expected to tightly covary (a high correlation, or high r p ) or may only be loosely correlated (a low correlation, or low r p ). Phenotypic trait covariance strength has proven to be a powerful tool for uncovering costs associated with developmental stress (Careau et al, 2014 ; Hebert et al, 1994 ; Killen et al, 2013 ; Merrill & Grindstaff, 2018 ; Merrill et al, 2017 ). Recent work in zebra finches ( Taeniopygia guttata ), for example, documented that stress during development resulted in near‐universal increases in trait covariance strength for a broad range of physiological and morphological traits (e.g., mass, tarsus, wing length, and concentrations of corticosterone, antibodies, and haptoglobin; Merrill & Grindstaff, 2018 ).…”

Early Life Stress Strengthens Trait Covariance: A Plastic Response That Results in Reduced Flexibility

“…Early life stress has been shown to impact mean trait expression across a wide range of taxa and trait types (Lindström 1999; Monaghan 2008; Schmidt et al 2014; Merrill et al 2017). The influence of developmental stress on within- and among-trait associations, however, has received less attention.…”

“…These early life challenges can have transient or permanent impacts on phenotypic expression depending on the type, duration, and magnitude of the stressors, the developmental stage at which the stress occurs (e.g., Matthews 2002; Monaghan and Haussmann 2015), and the traits examined. There is a large body of work documenting short- and long-term effects of early life stress on trait expression across taxa and across trait types (e.g., behavior [Nowicki et al 2002; Pechtel and Pizzagalli 2011; Merrill et al 2016, 2017], morphology [Denver et al 1998; Schmidt et al 2014], and physiology [Merrill and Grindstaff 2015; Monaghan and Haussmann 2015]), indicating that most organisms exhibit some degree of phenotypic plasticity in response to early life challenges.…”

“…These are generally ephemeral changes in somatic or physiological condition, and once the stressor is removed, organisms are typically able to return to the prior somatic and physiological state. Exposure to CORT or stress during development, conversely, can lead to permanent phenotypic programming (Lindström 1999; Monaghan 2008; Schmidt et al 2014; Merrill et al 2017). Whether these altered phenotypes are adaptive or maladaptive depends on the ecological context (sensu Gluckman et al 2005; Monaghan 2008) and how stressed individuals perform relative to the normal, non-stressed phenotype.…”