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

Date Published: August 23, 2019

Publisher: Public Library of Science

Author(s): Alejandro Cantarero, Lorenzo Pérez-Rodríguez, Ana Ángela Romero-Haro, Olivier Chastel, Carlos Alonso-Alvarez, William J. Etges.


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.

Partial Text

The ultimate and proximate mechanisms involved in the evolution of animal signals have been the subject of intense debate for decades (see e.g. recently [1–3]). Theoretical evolutionary models predict that signals must be reliable to evolve (e.g. [4, 5]). These reliable signals evolve when the signal production or maintenance costs are disproportionally high for low-quality individuals [6–8], or alternatively, when a direct causal link between signaling level and individual quality exists, making signals uncheatable [4, 9]. In both cases, those individuals producing larger or more intense signals should be higher-quality individuals, and be able to survive better and/or reproduce at a higher rate. In other words, higher signal expression should be linked to superior fitness, and not only as a result of direct benefits (fitness returns) of signaling (i.e. leading to a circular reasoning; [10]), but also to intrinsic genetic quality [4, 5, 11, 12]. The ornaments would thus became “honest” signals of high fitness [11–13].

This investigation was approved by the institutional animal welfare committee (University of Castilla-La Mancha’s Committee on Ethics and Animal Experimentation) in accordance with pertinent Spanish legislation under Protocol number: 1011.01. The implanting procedure was performed under veterinary supervision. We used a planned humane endpoint where any bird would be immediately euthanized by cervical dislocation when it rapidly lost more than 20% of body mass.

We show that carotenoid-based colored ornaments can act as fitness signals because their intensity is positively correlated to both lifespan and lifetime fecundity. To our knowledge, this is the first study in any vertebrate species reporting a significant link between the expression level of a carotenoid-based colored ornament and longevity and lifetime fecundity. Simons et al. [39] reported these correlations but during a shorter period of life (part of the sample was still alive at the end of the study), and reproductive success in their study period, i.e. not lifetime, was estimated assuming that extrapair paternity did not affect their results (also [38]). However, they recognized that zebra finch extrapair paternity may reach 29% in similar aviary conditions (citing [92, 93], also Ana Angela Romero-Haro & Carlos Alonso-Alvarez, unpublished data). Here, we avoided this problem as only one pair was housed per cage, and the eggs were immediately removed and artificially incubated. Moreover, we show that the testosterone function throughout life may reduce the link between signal level and fitness, providing further support for a role of sex steroids in the evolution of carotenoid-based signals [45].