Telomere length is reflected by plumage coloration and predicts seasonal reproductive success in the barn swallow

Abstract

Individuals differ in realized fitness but the genetic/phenotypic traits that underpin such variation are often unknown. Telomere dynamics may be a major source of variation in fitness traits because physiological telomere shortening depends on environmental and genetic factors and may impair individual performance. Here, we showed that, in a population of a socially monogamous, biparental passerine bird, the barn swallow (Hirundo rustica), breeding in northern Italy, telomere length (TL) of both adult males and females positively correlated with seasonal reproductive and fledging success, as expected because long telomeres are supposed to boost performance. Telomere length was correlated with sexually dimorphic coloration in both sexes, showing for the first time in any species that coloration reliably reflects TL and may mediate mutual mate choice, leading to the observed positive assortative mating for TL in the barn swallow. Thus, TL appears to be associated with variation in a major fitness trait and may be an ultimate target of mate choice, as individuals of both sexes can use coloration to adaptively choose high-quality mates that possess long telomeres.

Is telomere length a molecular marker of individual quality? Insights from a long‐lived bird

“…Furthermore, we also found that telomere length was positively associated with body size in both male and female black‐browed albatrosses (prediction 2), as previously reported in passerine species (Angelier, Vleck, Holberton, & Marra, ; Costanzo et al, ; Parolini et al, ). This result could appear surprising because telomere length is dynamic throughout the life of individuals while body size is determined during the developmental period in this species with determinate growth.…”

“…This supports the idea that long telomeres may be related to foraging skills, although the functional and causal link between telomere length and foraging behaviour remains to be elucidated. Furthermore, we also found that telomere length was positively associated with body size in both male and female black-browed TA B L E 2 Relationship between telomere length and offspring productivity calculated using different time frame windows (from 2 to 10 years of monitoring after the initial telomere length measurement) albatrosses (prediction 2), as previously reported in passerine species (Angelier, Vleck, Holberton, & Marra, 2015;Parolini et al, 2017). This result could appear surprising because telomere length is dynamic throughout the life of individuals while body size is determined during the developmental period in this species with determinate growth.…”

“…Supporting this interpretation, longer telomeres are associated with higher survival in numerous studies (Asghar, Hasselquist et al, ; Barrett et al, ; Bize et al, ; Fairlie et al, ; Haussmann et al, ; Heidinger et al, ; Salomons et al, ; Stier et al, ), although we still lack experimental data demonstrating the causal link between telomere length and survival. In our study, we only detected a non‐significant positive trend between telomere length and survival (possibly because of a lack of statistical power, see Supporting Information Appendix S1) Furthermore, three studies have reported that telomere length is associated with lifetime reproductive success (reptile: Olsson et al, ; birds: Asghar, Hasselquist et al, ; Bauch et al, ), and several proxies of breeding success, such as arrival date, brood size or the number of recruits (Bauch et al, ; Hall et al, ; Ouyang et al, ; Parolini et al, ; Pauliny et al, ; Plot, Criscuolo, Zahn, & Georges, ). Supporting this link between telomere length and reproductive performance, we found marginally significant positive trends between telomere length, success probability and, to a lesser extent, breeding probability.…”

“…Only a few studies have examined whether telomere length is associated with better reproductive performance and results are mixed (Bauch et al, 2013;Hall et al, 2004;Ouyang, Lendvai, Moore, Bonier, & Haussmann, 2016;Parolini et al, 2017;Pauliny, Wagner, Augustin, Szep, & Blomqvist, 2006). For example, Bauch et al (2013) found that birds with shorter telomeres surprisingly reproduced better in Common terns (Sterna hirundo) and this seems to be related to the cost of reproduction, which is associated with an important telomere shortening in successful chick-rearing birds (Bauch, Riechert, Verhulst, & Becker, 2016).…”

Protoporphyrin‐based eggshell pigmentation predicts hatching success and offspring sex ratio in the barn swallow

“…We plucked 2-3 feathers from the left paramedial breast plumage region to quantify breast colouration by spectrometric analyses. Breast plumage colouration is a sexually selected trait in the barn swallow (Safran et al 2005, even if its role in our study subspecies seems relatively weak , Parolini et al 2017b. As a proxy of ectoparasite load, we counted the number of holes in wing and tail feathers produced by chewing lice (Order Mallophaga; hereafter 'ectoparasite load'; Saino et al 2012Saino et al , 2014.…”