Carotenoid-based coloration predicts both longevity and lifetime fecundity in male birds, but testosterone disrupts signal reliability

PLoS One. 2019 Aug 23;14(8):e0221436. doi: 10.1371/journal.pone.0221436. eCollection 2019.

Abstract

Sexual selection promotes the evolution of conspicuous animal ornaments. To evolve as signals, these traits must reliably express the "quality" of the bearer, an indicator of individual fitness. Direct estimates of individual fitness may include the contribution of longevity and fecundity. However, evidence of a correlation between the level of signal expression and these two fitness components are scarce, at least among vertebrates. Relative fitness is difficult to assess in the wild as age at death and extra-pair paternity rates are often unknown. Here, in captive male red-legged partridges, we show that carotenoid-based ornament expression, i.e., redness of the bill and eye rings, at the beginning of reproductive life predicts both longevity (1-7 years) and lifetime breeding output (offspring number and hatching success). The recently proposed link between the individual capacity to produce red (keto) carotenoid pigments and the efficiency of cell respiration could, ultimately, explain the correlation with lifespan and, indirectly, fecundity. Nonetheless, in males of avian species, carotenoid-based coloration in bare parts is also partially controlled by testosterone. We also manipulated androgen levels throughout life by treating males with testosterone or antiandrogen compounds. Treatments caused correlations between signal levels and both fitness components to disappear, thus making the signals unreliable. This suggests that the evolution of carotenoid-based sexual signals requires a tightly-controlled steroid metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Birds / physiology*
  • Carotenoids / metabolism*
  • Fertility / physiology*
  • Longevity / physiology*
  • Male
  • Phenotype
  • Pigmentation*
  • Proportional Hazards Models
  • Regression Analysis
  • Testosterone / metabolism*

Substances

  • Carotenoids
  • Testosterone

Grants and funding

Financial support was obtained from the projects PII1I09-0271-5037, PII1C09-0128-4724, SBPLY/17/180501/000468 from the JCCM (co-financed with European Regional Development Fund –ERDF), CGL2009-10883-C02-02 from Ministerio de Ciencia e Innovación (MICIN, Spain) and CGL2015-69338-C2-2-P from Ministerio de Economía, Industria y Competitividad (MINECO). AC and LP-R were supported by a “Juan de la Cierva-formación” postdoctoral grant (MINECO, FJCI-2015-23536) and a SECTI postdoctoral contract from the University of Castilla-La Mancha (UCLM), respectively. AC is currently supported by a postdoctoral fellowship from Fundación Ramón Areces.