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

Abstract

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.

Keywords: KLH; beak colour; haptoglobin; mate choice; sexual selection; signal; stressor; zebra finch.

Figure 1

Timeline of events for prenatal and postnatal immune challenges and subsequent assessment of sexual signals and female mate-choice trials in zebra finches (Taeniopygia guttata). Dashed lines represent pre-hatch period, and solid lines are post-hatch.

Figure 2

Effect of young treatment on four aspects of zebra finch (Taeniopygia guttata) song quality. KLH=keyhole limpet hemocyanin, LPS=lipopolysaccharide, and PBS=phosphate-buffered saline (control). Different letters denote significant differences between treatments based on post-hoc ANOVAs, and bars reflect mean and standard error.

Figure 3

The relationship between circulating haptoglobin (Hp) levels on Day 28 post-hatch and mean number of song phrases (A), and song duration (B) in zebra finches.

Figure 4

A. Mean phenotypic correlation (r_p) estimates and 95% confidence intervals between the four measures of zebra finch song complexity and four measures of beak colour by early-life treatment: phosphate buffered saline (control), lipopolysaccharide (LPS) and keyhole limpet hemocyanin (KLH). B. Individual r_p estimates for birds that did not receive KLH as nestlings and those that did (both control and LPS groups). Lines connect r_p values between the same traits. See Table S1 in Supporting Information for estimates for each association.