Divergent Patterns of Age-Dependence in Ornamental and Reproductive Traits in the Collared Flycatcher

Abstract

Sexual ornaments are predicted to honestly signal individual condition. We might therefore expect ornament expression to show a senescent decline, in parallel with late-life deterioration of other characters. Conversely, life-history theory predicts the reduced residual reproductive value of older individuals will favor increased investment in sexually attractive traits. Using a 25-year dataset of more than 5000 records of breeding collared flycatchers (Ficedula albicollis) of known age, we quantify cross-sectional patterns of age-dependence in ornamental plumage traits and report long-term declines in expression that mask highly significant positive age-dependency. We partition this population-level age-dependency into its between- and within-individual components and show expression of ornamental white plumage patches exhibits within-individual increases with age in both sexes, consistent with life-history theory. For males, ornament expression also covaries with life span, such that, within a cohort, ornamentation indicates survival. Finally, we compared longitudinal age-dependency of reproductive traits and ornamental traits in both sexes, to assess whether these two trait types exhibit similar age-dependency. These analyses revealed contrasting patterns: reproductive traits showed within-individual declines in late-life females consistent with senescence; ornamental traits showed the opposite pattern in both males and females. Hence, our results for both sexes suggest that age-dependent ornament expression is consistent with life-history models of optimal signaling and, unlike reproductive traits, proof against senescence.

Life-History Differences in Age-Dependent Expressions of Multiple Ornaments and Behaviors in a Lekking Bird

“…Therefore, yearling males may need to allocate most of their limited resources to the growth of vital traits, leaving limited resources for the expression of their ornaments. Such a pattern has been reported in species with conspicuous secondary sexual traits (Nussey et al 2009;Evans et al 2011) and might play a role in mate choice through discrimination against young but active males that have not undergone viability selection (Manning 1985;Alatalo et al 1991). These age-dependent patterns differed from male tarsus length, which reached its final length during the first year of life.…”

“…In particular, previous studies have focused on socially monogamous birds with limited potential for sexual selection (e.g., Balbontín et al 2011;Evans et al 2011;Bouwhuis et al 2012;Froy et al 2013). However, since male-male competition and female choice can dampen or strengthen the effects of aging on life histories (Bonduriansky et al 2008), patterns of age-dependent trait expression in these species with low variation in male mating success may differ substantially from those observed in species with strong sexual selection.…”

“…However, only longitudinal studies can separate within-individual (i.e., phenotypic plasticity, individual improvement, senescence) and between-individual (i.e., selective appearance or disappearance of certain phenotypes) effects of age on trait expression (van de Pol and Verhulst 2006;van de Pol and Wright 2009). As individual trajectories can be hidden by demographic heterogeneity (Bouwhuis et al 2009;van de Pol and Wright 2009;Evans et al 2011), neglecting within-individual effects might lead to incorrect conclusions about the effects of aging on life histories.…”

“…Most longitudinal studies published to date have analyzed key life-history traits, such as reproductive success (e.g., Dugdale et al 2011;Froy et al 2013) and survival (e.g., Bouwhuis et al 2012), but there is growing interest in age-dependent variation in secondary sexual traits (Balbontín et al 2011;Evans et al 2011) and behavior (Mainguy and Côté 2008;Nussey et al 2009). This is crucial because secondary sexual traits act as honest indicators of individuals' overall genetic quality if their elaboration and maintenance are associated with fitness costs, which in turn depend on individual body condition (Zahavi 1975;Kotiaho 2001).…”

“…Moreover, many previous studies have focused on single sexually selected traits (e.g., antler size [Nussey et al 2009] and tail feather length [Balbontín et al 2011]). However, sexual selection is clearly a multifaceted process, so investigating multiple traits simultaneously is needed to unravel the constraints and trade-offs acting on these traits (Evans et al 2011) and to accurately quantify the overall fitness costs of trait expression (Kotiaho 2001;Lecomte et al 2010). Finally, age-dependent expressions of sexual traits has not yet been quantified in relation to temporal scheduling of individual reproductive effort, where peak reproductive effort is expected to differ among individuals depending on their current body condition and, hence, may be the only opportunity during which all traits are expressed at their maximum.…”