Ontogenetic immune challenges shape adult personality in mallard ducks

Abstract

Consistent individual differences in behaviour are widespread in animals, but the proximate mechanisms driving these differences remain largely unresolved. Parasitism and immune challenges are hypothesized to shape the expression of animal personality traits, but few studies have examined the influence of neonatal immune status on the development of adult personality. We examined how non-pathogenic immune challenges, administered at different stages of development, affected two common measures of personality, activity and exploratory behaviour, as well as colour-dependent novel object exploration in adult male mallard ducks (Anas platyrhynchos). We found that individuals that were immune-challenged during the middle (immediately following the completion of somatic growth) and late (during the acquisition of nuptial plumage) stages of development were more active in novel environments as adults relative to developmentally unchallenged birds or those challenged at an earlier developmental time point. Additionally, individuals challenged during the middle stage of development preferred orange and avoided red objects more than those that were not immune-challenged during development. Our results demonstrate that, in accordance with our predictions, early-life immune system perturbations alter the expression of personality traits later in life, emphasizing the role that developmental plasticity plays in shaping adult personality, and lending support to recent theoretical models that suggest that parasite pressure may play an important role in animal personality development.

Neuroendocrine-immune circuits, phenotypes, and interactions

“…Conversely, stimulation of the NEI circuit by infection or immunogens can produce stereotypical and adaptive changes in behavior that are collectively termed sickness behavior (discussed below). In addition, maternal immune challenge can also affect personality of offspring and predisposition to disease (Butler et al, 2012; Grindstaff, 2016; Khan et al., 2014). Thus, behavior affects NEI interactions and vice versa (Fig.…”

Early Environmental Conditions Shape Personality Types in a Jumping Spider

“…To clearly identify underlying processes, experimental studies in which environmental conditions are manipulated are needed. The majority of studies that measured personality development in an experimental setting manipulated either food availability (e.g., Carere et al, 2005;Edenbrow and Croft, 2013), or stress by inducing immune challenge (e.g., Butler et al, 2012;DiRienzo et al, 2015), by increasing antipredator pressure (e.g., Bell and Sih, 2007;Niemelä et al, 2012a;Edenbrow and Croft, 2013), or by preventing access to shelter (Bengston et al, 2014).…”

Developmental immune activation programs adult behavior: insight from research on birds

“…Because state characters influence the adaptive value of behaviors, personality differences may be at least partially due to variation among hosts in state as a function of infection history or susceptibility to infection [21,22,23]. To test this hypothesis, mallard ducklings ( Anas platyrhynchos ) were immune challenged during one of three phases of development, and activity and exploration in a novel environment and response to novel objects of different colors were quantified in adulthood after a subsequent immune challenge [9]. Initial immune challenges administered after completion of somatic growth, but before completion of molt into the nuptial plumage, increased activity in adulthood and altered color-based novel object exploration, but did not influence overall exploratory behavior [9].…”

“…To test this hypothesis, mallard ducklings ( Anas platyrhynchos ) were immune challenged during one of three phases of development, and activity and exploration in a novel environment and response to novel objects of different colors were quantified in adulthood after a subsequent immune challenge [9]. Initial immune challenges administered after completion of somatic growth, but before completion of molt into the nuptial plumage, increased activity in adulthood and altered color-based novel object exploration, but did not influence overall exploratory behavior [9]. A study of zebra finches ( Taeniopygia guttata ) assessed the potential for both maternal and developmental immune challenges to impact neophobia in adulthood measured as response to novel objects.…”

“…For example, exposure to stressors during critical developmental windows early in life may program adult behavioral expression. Stressors that have been demonstrated to influence adult behavior in birds include nutritional stress [2*,3,4,5], brood size [6], and parasite exposure or immune challenge [7,8,9,10]. Birds are an excellent group in which to study programming effects of early life immune activation on behavior because behavior can be readily observed under natural conditions and is well characterized for many species from diverse habitats and with divergent life history strategies.…”