Stabilizing survival selection on presenescent expression of a sexual ornament followed by a terminal decline

Abstract

Senescence is a decrease in functional capacity, increasing mortality rate with age. Sexual signals indicate functional capacity, because costs of ornamentation ensure signal honesty, and are therefore expected to senesce, tracking physiological deterioration and mortality. For sexual traits, mixed associations with age and positive associations with life expectancy have been reported. However, whether these associations are caused by selective disappearance and/or within‐individual senescence of sexual signals, respectively, is not known. We previously reported that zebra finches with redder bills had greater life expectancy, based on a single bill colour measurement per individual. We here extend this analysis using longitudinal data and show that this finding is attributable to terminal declines in bill redness in the year before death, with no detectable change in presenescent redness. Additionally, there was a quadratic relationship between presenescent bill colouration and survival: individuals with intermediate bill redness have maximum survival prospects. This may reflect that redder individuals overinvest in colouration and/or associated physiological changes, while below‐average bill redness probably reflects poorer phenotypic quality. Together, this pattern suggests that bill colouration is defended against physiological deterioration, because of mate attraction benefits, or that physiological deterioration is not a gradual process, but accelerates sharply prior to death. We discuss these possibilities in the context of the reliability theory of ageing and sexual selection.

Age‐dependent trajectories differ between within‐pair and extra‐pair paternity success

“…). We detected a marginal terminal decline in within‐pair (but not in extra‐pair) paternity success, which could be caused by a decline in physiological condition (Coulson & Fairweather, ; Hammers et al ., ; Simons et al ., ). This result was consistent with a previous study on the same population, in which we detected a terminal decline in annual productivity (Schroeder et al ., ).…”

“…A terminal effect would be different from a more gradual decline due to senescence. However, terminal effects can potentially confound age‐related effects and thus must be accounted for (Simons et al ., ). We therefore modelled the terminal effect with a binary variable indicating whether an individual died between the current and following breeding seasons (died = 1, survived = 0).…”

The rate of telomere loss is related to maximum lifespan in birds

“…Since our study is cross-sectional in nature due to the lack of long-term study populations and the long lifespans of some species, the relationship between TROC and lifespan could be a result of selective loss of short-lived individuals from the environment. This selective disappearance of particular individuals [ 41 , 64 ]—those with short telomeres—can cloud the relationship between telomere loss and age in a cross-sectional context [ 65 ]. For example, the positive relationship between telomere length and age seen in Leach's storm petrels ( O. leucorhoa ) is most likely due to the longest-lived individuals starting with the longest telomeres and variation in telomere length decreasing with age owing to the selective disappearance of individuals with short telomeres [ 65 ].…”

The role of bare parts in avian signaling

“…Signals of age may serve as de facto signals of quality, because older individuals are those that have survived longest (Andersson 1994, Buchholz 1995, although ornament expression can decline with age as well. In male Blue-footed Boobies and Zebra Finches, carotenoid-based bare-part color declines in senescence, and older birds show a greater decline in color following an immune challenge (Torres and Velando 2007, Cote et al 2010, Simons et al 2016). However, under carotenoid supplementation, older male Blue-footed Boobies actually increase foot coloration more than younger ones, perhaps trading off somatic maintenance for enhanced reproduction in what may be their last breeding attempt (Beamonte-Barrientos et al 2014).…”