Skip to main content
NCBI home page
Wiley Open Access Collection logoLink to Wiley Open Access Collection
. 2024 Sep 25;343(1):70–80. doi: 10.1002/jez.2868

Early Oxidative Stress May Prevent a Red Ornament From Signaling Longevity

A A Romero‐Haro 1,✉, A Cantarero 2, C Alonso‐Alvarez 3,4,✉
PMCID: PMC11617810  PMID: 39318264

ABSTRACT

Harsh early environmental conditions can exert delayed, long‐lasting effects on phenotypes, including reproductive traits such as sexual signals. Indeed, adverse early conditions can accelerate development, increasing oxidative stress that may, in turn, impact adult sexual signals. Among signals, colorations produced by red ketocarotenoids seem to depend on mitochondrial functioning. Hence, they could reveal individual cell respiration efficiency. It has been hypothesized that these traits are unfalsifiable “index” signals of condition due to their deep connection to individual metabolism. Since mitochondrial dysfunction is frequently linked to aging, red ketocarotenoid‐based ornaments could also be good signals of a critical fitness component: longevity. We tested this red color per longevity correlation in captive zebra finches. In addition, we experimentally decreased the synthesis of glutathione (a critical intracellular antioxidant) during the first days of the birds' life to resemble harsh early environmental conditions (e.g., undernutrition). Longevity was recorded until the death of the last bird (almost 9 years). Males, but not females, exhibiting a redder bill in early adulthood lived longer than males with paler bills, which agrees with some precedent studies. However, such bill redness—longevity connection was absent among males with inhibited glutathione synthesis. These findings may suggest that environmental factors can alter the reliability of red ketocarotenoid‐based sexual signals, making them less unfalsifiable than believed.

Keywords: carotenoid transformation enzymes, index signals, ketocarotenoids, longevity, sexual signaling theory, shared‐pathway hypothesis

Summary

  • Red colorations produced by carotenoids are supposedly be linked to mitochondria function, and probably longevity.

  • We found that the positive link between such coloration and longevity can be distorted by early oxidative stress in an avian species.

1. Introduction

Harsh environmental conditions during early development are expected to cause stronger, long‐lasting effects on phenotypes than conditions impacting later in life (Metcalfe and Monaghan 2001; Yearsley, Kyriazakis, and Gordon 2004). These early environmental conditions can trigger metabolic responses leading to particular phenotypes more or less adapted to future environments (“environmental matching,” “predictive adaptive response,” or “thrifty phenotype” hypotheses; Wells 2007; Monaghan 2008; Bateson, Gluckman, and Hanson 2014). In this context, limited food intake or extreme environmental conditions (e.g., low temperatures, hyperoxia) during early life may increase metabolic rates to accelerate growth (i.e., catch‐up growth; e.g., Arnott et al. 2006; Criscuolo et al. 2008; Owerkowicz, Elsey, and Hicks 2009). This challenge may imbalance the production of reactive oxygen species (ROS) regarding the state of the antioxidant machinery (i.e., oxidative stress), generating oxidative damage on biomolecules (Alonso‐Alvarez et al. 2007; Tarry‐Adkins et al. 2009; Christensen et al. 2016; Kim, Noguera, and Velando 2019; Janssens and Stoks 2020). Thus, early oxidative stress could play a role in determining the phenotypic profiles and individual life history trajectories (Alonso‐Alvarez et al. 2006; Monaghan, Metcalfe, and Torres 2009; Romero‐Haro and Alonso‐Alvarez 2015).

The foremost life‐history traits comprise reproductive parameters (e.g., number or size of the offspring, the age and size at maturity) and longevity (e.g., Braendle, Heyland, and Flatt 2011). Those traits allowing individuals to obtain mates are considered reproductive parameters, and, among them, those conveying information to potential partners and benefiting both transmitter and receptor are considered sexual signals (Maynard Smith and Harper 2003). The conspicuous colorations generated by carotenoid pigments (e.g., many yellow‐to‐red colorations) are among the most intensely studied sexual signals (e.g., McGraw and Ardia 2003; Hartley and Kennedy 2004; Delhey et al. 2023). Carotenoids are acquired with food, allocated to colorations, or used as antioxidants or provitamin molecules for homeostatic functions (Britton, Pfander, and Liaaen‐Jensen 2009; Pérez‐Rodríguez, 2009). The foraging effort needed for acquiring carotenoids and metabolic demands led to the hypothesis that coloration intensity is traded against self‐maintenance (von Schantz et al. 1999; Blount 2004; Alonso‐Alvarez et al. 2008; but see Koch and Hill 2018). Resolving such a trade‐off by investing more in coloration would imply proportionally higher costs for low‐quality individuals (e.g., Weaver et al. 2018; Penn and Számadó 2020). Low‐quality animals should avoid a high investment in coloration, thus converting colored traits into reliable signals of the individual condition.

In addition, carotenoids include many types of compounds. Yellow carotenoids (xanthophylls) are commonly acquired with the diet and directly deposited on ornament tissues (McGraw 2006). In contrast, red carotenoids (ketocarotenoids) are obtained from enzymatic transformations of dietary yellow carotenoids (McGraw 2006; Hill and Johnson 2012). This transformation seems to be made into the inner mitochondrial membrane (Johnson and Hill 2013; Hill et al. 2019). This scenario would add complexity to signal production. Thus, it has been hypothesized that the intensity of red ketocarotenoid‐based coloration reveals individual cell respiration efficiency (Johnson and Hill 2013; Cantarero and Alonso‐Alvarez 2017; Cantarero et al. 2020). Such a deep link to cell function would imply that red ketocarotenoid‐based ornaments could be fully unfalsifiable, resource‐independent, and cost‐free (i.e., the shared‐pathway hypothesis; Hill 2011). This type of unfalsifiable signal is usually called an “index” or “index signal” (Maynard Smith and Harper 2003; Weaver et al. 2018).

Interestingly, given that mitochondrial dysfunction is commonly associated with oxidative stress, and since the latter is linked to aging and aging‐related diseases (Barja 2014; Sun, Youle, and Finkel 2016), the intensity of ketocarotenoid‐based colorations should predict individual lifespan as an ultimate fitness index. This is supported by studies in sticklebacks (Gasterosteus aculeatus; Pike et al. 2007; Simons et al. 2021), zebra finches (Taeniopygia guttata: Simons et al. 2012; Simons, Briga, and Verhulst 2016) and red‐legged partridges (Alectoris rufa; Cantarero et al. 2019).

However, fluctuating environmental conditions throughout development could make sexual signals less reliable as a consequence of individual phenotypic plasticity acting on the trait (signal) expression level (e.g., Higginson and Reader 2009; Ingleby, Hunt, and Hosken 2013; Candolin and Wong 2019). In other words, early development conditions can be so diverse (heterogeneous) that they can deviate the phenotype (within its reaction norm) in such a way that the expression level of the signal may not correlate with individual quality. Thus, when environmental conditions became harder during growth (e.g., by reduced food intake or increased thermal stress), sexual signals in adulthood could transmit dishonest information. In that case, their expression level should not be well correlated to individual fitness traits (i.e., the ultimate indices of individual quality: longevity and fecundity). Here, we test this hypothesis on a red‐ketocarotenoid‐based ornament that could signal individual longevity, that is, the red bill of zebra finches (see Simons et al. 2012; Simons, Briga, and Verhulst 2016). In particular, we hypothesize that early oxidative stress, potentially influenced by environmental changes, may disrupt the information transmission from sexual signals. In a long‐term study, we artificially decreased the blood levels of a key intracellular antioxidant (glutathione) in captive birds during their growth by administering an inhibitor of glutathione synthesis (buthionine sulfoximine; BSO) from 6 to 14 days old (i.e., Romero‐Haro and Alonso‐Alvarez 2015). Glutathione is synthesized from amino acids, and a low amino acid intake decreases glutathione synthesis in mammals and birds (Gould and Pazdro 2019; Kachungwa Lugata, Ortega, and Szabó 2022). Similarly, in avian species, birds raised in artificially enlarged broods (i.e., probably receiving less food per capita; e.g., Saino, Calza, and pape Moller 1997; Westneat et al. 2017) showed lower blood glutathione levels than individuals reared in artificially reduced broods (Gil et al. 2019; Romero‐Haro and Alonso‐Alvarez 2020). Thus, our glutathione synthesis inhibition aims to resemble a situation in which a transient nutritional shortage disrupts the antioxidant machinery. We previously analyzed the effect of this manipulation on phenotypic and life‐history traits for 9 years (until the death of the last bird). Just ending the treatment (i.e., 14 days old), nestlings endured low blood plasma antioxidant levels (Romero‐Haro and Alonso‐Alvarez 2015). In early adulthood (100 days old), these BSO‐treated birds showed higher oxidative damage (lipid peroxidation in erythrocytes), with longevity not differing between experimental groups (Romero‐Haro and Alonso‐Alvarez 2015; Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). Here, we tested the impact of this manipulation on the capacity of a sexual signal expressed during early life to reveal the individuals' longevity potential. Sexual signaling theory would predict that zebra finches with redder bills should live longer (high‐quality birds), whereas life‐history theory and the associated trade‐offs predict birds investing more in (early) reproduction (here sexual signaling) living shorter (Stearns 1992; Braendle, Heyland, and Flatt 2011). The latter should be expected among BSO‐treated birds since color investment when enduring high oxidative stress would imply physiological costs. Hence, a color‐per‐treatment interaction on longevity would reveal a life‐history trade‐off in signal expression rather than supporting a deeply constrained index signaling mechanism. Finally, we may also predict the color per longevity association will differ among sexes considering differences in sex‐specific selection pressures (e.g., carotenoid investment in egg yolk in females; Bertrand, Faivre, and Sorci 2006) and coloration (male zebra finches show redder bills due to higher bill ketocarotenoid content; McGraw 2006).

2. Methods

This study is part of a long‐term experiment that tested the influence of experimentally decreased early‐life levels of a critical intracellular antioxidant (i.e., glutathione) on the expression of life‐history traits in captive zebra finches (Romero‐Haro and Alonso‐Alvarez 2015, 2020; Romero‐Haro, Canelo, and Alonso‐Alvarez 2015; Romero‐Haro, Sorci, and Alonso‐Alvarez 2016; Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). Eighty randomly formed pairs (F0 birds) were placed in breeding cages (details in (Romero‐Haro and Alonso‐Alvarez 2015) for 5 months, and the breeding pairs produced 409 nestlings (F1). Among them, 206 randomly selected individuals were treated with the glutathione inhibitor BSO, and 203 were control‐treated (experimental chronogram in Figure 1). An experimental treatment was applied to nestlings reaching 3 g minimum (mean ± SE: 4.82 g ± 0.03). Half of the nestlings in a brood were assigned to the treatment receiving DL‐buthionine‐S, R‐sulfoximine (BSO; Sigma, ref. B2640) in saline solution (0.90% w/v of NaCl; BSO individuals). The other half of the brood was assigned to the control group and only received saline. We randomly assigned one treatment to the heaviest chick in a brood and then alternated the treatment assignation among the siblings (e.g., control, BSO, control, BSO). The BSO solution was 50 mg BSO in 1 mL of saline solution. Birds received 0.06 mL of BSO solution (BSO individuals) or 0.06 mL of saline (controls). The cited volume was subcutaneously injected into the back every other day from 6 to 12 days old (i.e., four injections). To validate the manipulation, total glutathione levels in erythrocytes were determined in 14 days old (mean age) nestlings using a spectrophotometer (A25‐Autoanalyzer, Biosystems) and following Griffith, (1980) method with modifications (Romero‐Haro and Alonso‐Alvarez 2014). BSO nestlings reported significantly lower glutathione levels than controls (see Figure 2 in Romero‐Haro and Alonso‐Alvarez 2015).

Figure 1.

Figure 1

Open in a new tab

Chronogram of the experiment. BSO, buthionine sulfoximine.

Figure 2.

Figure 2

Open in a new tab

Cumulative survival of male zebra finches depending on their bill color at early adulthood (average: 100 days old). Above: controls. Below: birds early and transitorily exposed to buthionine sulfoximine (BSO; an inhibitor of glutathione synthesis). Bill hue residuals grouped birds into tertiles (Methods). The birds with the reddest bills were included in the lowest tertile (red line). The birds with intermediate coloration were in the mid‐tertile (orange line), and those with the palest bills were in the highest tertile (yellow line). Note that Table 1 models tested bill hue as a continuous covariate.

Males and females (F1) were housed in different indoor aviaries (2.80 × 3 × 2.50 m each; details in Romero‐Haro, Canelo, and Alonso‐Alvarez 2015) at 40 days of age (average). The adult bird's bill was photographed at 99 days (average; “100d” to simplify; details in Romero‐Haro and Alonso‐Alvarez 2015). This age is higher than the earliest first egg‐laying age reported in the field (Zann 1996) and also in outdoor aviaries in another population (median 94 days old; Alonso‐Alvarez et al. 2006). Also, note that mate choice occurs before the first egg‐laying date. The black surfaces present in the beaks of immature birds (Zann 1996; Boruszewska, Witkowski, and Jaszczak 2007) were fully absent in the birds assessed for red coloration. Moreover, there was no difference between treatments (or treatment × sex interaction) in the proportion of the black surface in the beak when early measured (40 days of age; all p values > 0.30; Supporting Information). The sample of birds assessed for bird coloration and longevity was statistically balanced (control males: 86; BSO males: 79; control females: 72; BSO females: 76; χ 2 = 0.376, p = 0.540).

To avoid physiological stress due to high social density (Poot et al. 2012), among all individuals reaching at least 110 days of life (n = 283; mean ± SE: 137d ± 1.52 days old), 65% were randomly chosen and released into a large outdoor aviary (223 m3). The treatment and sex categories were balanced in this subsample (χ 2 = 1.26, p = 0.26; Supporting Information), and BSO‐treated birds also showed lower glutathione levels at 14 days of age than controls (p < 0.001; Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). These individuals were monitored throughout their entire lifetime. First, the birds mated and bred freely for 7 months after release (Romero‐Haro and Alonso‐Alvarez 2020; Romero‐Haro, Sorci, and Alonso‐Alvarez 2016). Treatment did not influence reproductive parameters (Romero‐Haro, Sorci, and Alonso‐Alvarez 2016; Romero‐Haro and Alonso‐Alvarez 2020; Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). After the reproductive period, males and females (F1) were separated, and each sex was placed in each half of the aviary with similar social density, with their lifespan being monitored every 2 or 3 days throughout the 8 years (2012–2020) until the death of the oldest bird (104 months).

The longevity data of animals whose date of natural death could not be well established were censored in Cox models (below). In this case, the last date a bird was found alive was used to assign its minimum lifespan. This included three situations: (1) missing birds that could only be identified when capturing all the birds during sampling events (mainly a consequence of ants making corpses quickly disappear; see Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023), (2) birds that died due to causes unrelated to natural aging (e.g., accidents, predation by thin snakes entering the facilities), and (3) individuals not released in the outdoor aviary (see above). In the latter case, the minimum longevity was calculated until the cohort members were released. The comparison of the presence/absence of censored data between the sexes, treatments, or the four sex × treatment combinations did not provide significant biases (χ 2 tests p values > 0.27; also Supporting Information).

2.1. Zebra Finch Bill Color Measurement

Digital images of the upper surface of the upper mandible were obtained using a Nikon D3100 under standardized conditions (see details in Supporting Information). The mean red, green, and blue (RGB) values were determined (Alonso‐Alvarez et al. 2008) using Adobe Photoshop CS3. A standard red chip (Kodak, NY) was placed close to the bird's head. The bill and red chip hue and brightness were calculated using Foley and Van Dam (1984). High hue values indicate less redness than low hue values. Three pictures were not analyzed because of a lack of focus or incorrect bird position. Bill color parameters were finally obtained from 165 males and 148 females (full details in Supporting Information).

2.2. Statistical Analyses

We tested whether bill color intensity predicted longevity. We ran a mixed‐effects Cox model that included sex and early treatment as fixed factors and bill hue as a covariate, including all possible interactions between them. The brood ID nested into the cage ID where the bird was born was included as a random factor. The hue values included were residuals previously obtained from a mixed‐effect linear model. In this previous model, the bill brightness and red chip hue were added as covariates to control the amount of light reflected by the bill surface or subtle illumination variability among pictures, respectively (Romero‐Haro and Alonso‐Alvarez 2015; Cantarero et al. 2020). Here, the random term was also the brood ID nested into the cage ID.

The analyses were performed in R version 4.2.3. (R Core Team 2021). The R package lme4 (Bates et al. 2015) was used to perform mixed models to obtain residuals for the color covariate. The coxme and survival packages were used for mixed Cox models (Therneau, Grambsch, and Pankratz 2003). The predictors' significance was obtained using the analysis of variance (ANOVA) function from the car package to perform likelihood‐ratio tests for mixed models and Wald χ 2 tests for Cox models (Fox and Weisberg 2019). Normality and homoscedasticity of residuals from mixed models were met.

3. Results

First, it should be noted that a negative slope in Cox models indicates that the hazard (mortality) decreases with increasing levels of the covariate values. Thus, a positive slope indicates that paler individuals (higher hue values) had a higher mortality risk (or reduced longevity). We found a significant interaction between sex and bill color hue (p = 0.012 in Table 1, model above). To understand this result, we tested the influence of bill hue on longevity for each sex separately and excluding the treatment. Here, the bill hue predicted longevity in males, with paler individuals showing a higher mortality risk (β = 0.497, SE = 0,128, χ 2 = 15.01, df = 1, p < 0.001, n = 165). This relationship was not significant when testing only females (β = 0.024, SE = 0.107, χ 2 = 0.051, df = 1, p = 0.821, n = 148).

Table 1.

Generalized Cox models testing the influence of bill hue at 100 days of age, sex and early treatment (glutathione synthesis inhibition; see Section 2) on zebra finch longevity.

Predictors β SE χ 2 df p
Both sexes (n = 313)
Treatment (control) 0.218 0.249 0.413 1 0.521
Sex (males) −0.056 0.268 0.216 1 0.642
Bill hue −0.033 0.159 9.325 1 0.002
Treatment (control) × Sex (males) −0.153 0.358 0.223 1 0.637
Treatment (control) × Bill hue 0.121 1.128 3.539 1 0.060
Sex (males) × Bill hue 0.078 0.275 6.302 1 0.012
Treatment (control) × Sex (males) × Bill hue 0.496 0.339 2.144 1 0.143
Males (n = 165)
Treatment (control) 0.060 0.269 0.0003 1 0.987
Bill hue 0.129 0.229 17.656 1 < 0.001
Treatment (control) × Bill hue 0.547 0.270 4.112 1 0.043
Females (n = 148)
Treatment (control) 0.184 0.249 0.592 1 0.442
Bill hue −0.041 0.157 0.049 1 0.825
Treatment (control) × Bill hue 0.119 0.212 0.312 1 0.577
Open in a new tab

Note: Bold values indicate significant tests at p < 0.05.

Nonetheless, even when the three‐order interaction between treatment, sex, and hue values did not reach significance (p = 0.143 in Table 1), we explored the color and longevity correlation separately for each sex, including the treatment and its interaction with hue (Table 1). The treatment × bill hue interaction was only significant in males (p = 0.043, in Table 1). The cited correlation (paler individuals living shorter) was detected among control males (β = 0.631, SE = 0.141, χ 2 = 20.09, df = 1, p < 0.001, n = 86) but not among BSO males (β = 0.202, SE = 0.211, χ 2 = 0.918, df = 1, p = 0.338, n = 79; see Table 1 and Figure 2). The result is illustrated in Figure 2, representing cumulative survival for birds in tertiles that divided the color distribution into high, intermedia, or low values. The difference between control and BSO males could not be attributed to a sample size difference. The statistical power of a model with the same effect size that was found in male controls (0.631) but the sample size used in the BSO group (79) provided a very high power (0.998), which is only subtly different from that found in male controls (0.999; XLSTAT 2024 software, Supporting Information).

4. Discussion

Our longitudinal study supports the hypothesis that red ketocarotenoid‐based signals transmit information about the longevity potential of the trait bearer, at least among male zebra finches. However, exposure to adverse conditions during development (high levels of oxidative stress) would weaken the information transfer, making the signal unreliable.

First, we should mention that the coloration of birds was assessed early in adult life, some days later than the first reproduction reported for this species (Zann 1996). The trait assumedly subject to sexual selection (i.e., the red bill) was fully developed in all the birds (i.e., no sign of the blackish color characteristic of immature birds; see Section 2). Thus, our approach focusing on young but eligible‐for‐reproduction birds would have increased the sample size, allowing the detection of small but significant statistical effects. Furthermore, from a male's life history point of view, the investment in coloration at the first opportunity should be critical as the first reproduction is crucial in short‐lived species where future reproductive events are subject of unpredictable mortalities (Stearns 1992; Braendle, Heyland, and Flatt 2011; Griffith 2019, 2021). Moreover, we should also consider that the reproductive potential of a younger bird would be higher than that of an older individual. Therefore, the benefit of making a good choice for a young mate should be higher than the benefit of making a good choice for an older bird. This is particularly important here since zebra finches are considered monogamous birds with lifetime pair‐bonds (e.g., Zann 1994; Adkins‐Regan and Tomaszycki 2007; Griffith 2019).

In our longitudinal study, the males with the reddest bills lived longer. Such a result agrees with some previous works in zebra finches but differs from others, perhaps due to differences in the approaches. Price and Burley (1994) did not detect a significant correlation between bill redness and longevity in males but a negative association in females. However, they used a smaller sample size (30 birds per sex) than ours and stopped monitoring birds when > 50% of birds were still alive. Similar to our results, Simons et al. (2012) reported a positive link for males and a quadratic (first positive) association for females, with approximately 70 birds per sex and 40% remaining alive. However, their color measurements were performed at around 660 days of age, precluding testing the entire life range. Lastly, Simons, Briga and Verhulst (2016) tested whether annual bill redness predicted yearly mortality, finding a significant positive correlation in males but not in females. The latter study was conducted on the Simons et al. (2012) population but on a larger sample size (about 180 birds per sex) and during a more extended period. Overall, a positive link between the intensity of ketocarotenoid‐based coloration and longevity is supported by zebra finch studies, although females seem to show a weaker association, perhaps due to sex‐specific selection pressures (e.g., carotenoid investment in egg yolk; Bertrand, Faivre, and Sorci 2006; Price 1996).

Male longevity was explained by the interaction of color and treatment (Table 1). The link between color and longevity was not detected in males exposed to early low glutathione levels. BSO birds did not show a significant negative correlation as initially predicted. Some of the reddest BSO males could have paid the cost of investing carotenoids in coloration, dying earlier and making the positive correlation fade. Also, some of the palest BSO males could live longer (see Figure 2) due to a potential mobilization of carotenoids from coloration into protection (homeostasis) under oxidative stress. Such extended longevity among the palest BSO males could be explained at the proximate level by physiological compensatory responses controlled by mitochondria (see mito‐hormesis; Yun and Finkel 2014; Zhang and Hood 2016). Regarding the latter, we should highlight that astaxanthin (a red ketocarotenoid in the zebra finch beak; McGraw and Toomey 2010) seems able to penetrate the mitochondrial membrane and modulate its function (Nishida et al. 2022; see also Hill et al. 2019). In any case, the results overall suggest a life‐history trade‐off between early investment in sexual signaling and longevity, disagreeing with the nonplastic signaling implicit in the index concept (Maynard Smith and Harper 2003; Hill 2011) and opening the possibility of signal dishonesty (cheating) in some circumstances.

We should note that avian colorations in nonfeathered body parts are particularly dynamic (e.g., Alonso‐Alvarez et al. 2022; Iverson and Karubian 2017). Thus, in zebra finches, males can intensify bill color in a few days when housed with females (Gautier et al. 2008; but see also Romero‐Haro, Canelo, and Alonso‐Alvarez 2015). Even the handling stress increased the red bill coloration of male zebra finches in a few weeks (McGraw, Lee, and Lewin 2011). The latter can be interpreted as birds investing in coloration when perceiving a high predation risk, trying to advance reproduction (i.e., a terminal investment strategy; Clutton‐Brock 1984; Velando, Drummond, and Torres 2006). Similarly, we have previously shown that BSO birds faced oxidative stress but simultaneously increased bill redness (Romero‐Haro and Alonso‐Alvarez 2015), suggesting a terminal investment strategy triggered by stressful conditions. Several studies on ketocarotenoid‐based ornaments support this scenario. In male sticklebacks, low food availability increased red skin coloration (Candolin 2000b). Old zebra finches exposed to bacterial antigens increased coloration, whereas the opposite was found among younger birds (Cote et al. 2010). In male red‐legged partridges, exposure to a ROS generator (diquat) produced oxidative stress but intensified the red coloration by converting yellow carotenoids to ketocarotenoids (García‐de Blas, Mateo, and Alonso‐Alvarez 2016). In all these examples, we should note that terminal investment could have been induced by mito‐hormetic responses (i.e., as a potential proximate mechanism; see above). In any event, the lack of signal reliability under early oxidative stress highlights the relevance of genotype × environment (GxE) interactions on sexual signaling evolution (Greenfield and Rodriguez 2004; Higginson and Reader 2009; Ingleby, Hunt, and Hosken 2013). Such a lack of reliability can sustain sexual selection in some circumstances (e.g., when immigrants are not well adapted to the new environment; Getty 2014; Holman and Kokko 2014).

Nevertheless, animals can evolve mechanisms to avoid reliability fluctuations. Female sticklebacks change how they assess males' sexiness by focusing on other traits instead of red coloration, such as the nest size (made by the male), when the environmental conditions change (Head, Fox, and Barber 2017). Indeed, the influence of environmental factors disrupting the link between the signal level and individual quality seems to promote the evolution of multiple signals in the same individual (Bro‐Jørgensen, 2010; Candolin 2000a, 2003; Lozano 2009). The analysis of several signals would improve mating decisions. Male zebra finches exhibit different ornamental colors in plumage, songs, and displays, thus adding complexity to female choice. Unraveling the influence of harsh early conditions on potential signaling traits of individuals, as a whole, is an avenue for a better understanding of signal evolution.

Finally, our longitudinal and transgenerational studies support the role of glutathione as a connector of multiple functionally related traits (see “phenotypic integration” in, e.g., Costantini, Monaghan, and Metcalfe 2013; Cox, McGlothlin, and Bonier 2016). Individuals whose glutathione levels were experimentally decreased suffered a widespread loss of integration among physiological traits, coloration, and longevity. Erythrocyte glutathione concentrations were negatively related to blood total carotenoid levels in nestlings from another independent captive zebra finch population (i.e., Romero‐Haro and Alonso‐Alvarez 2014) and again in the present population (Romero‐Haro and Alonso‐Alvarez 2015). This link suggests that developing birds with low glutathione levels mobilized carotenoids to avoid oxidative stress or vice versa. However, this compensatory mechanism was absent when birds endured decreased glutathione synthesis due to BSO (Romero‐Haro and Alonso‐Alvarez 2015). Early glutathione levels were also associated with telomere length in the present population (Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). Telomeres are protective, highly repetitive, noncoding DNA sequences at the end of chromosomes that shorten in each cell division (Blackburn 1991; Harley et al. 1992), being considered predictors of individuals' longevity (e.g., Heidinger et al. 2012; Reichert et al., 2015; Srinivas, Rachakonda, and Kumar 2020). The erythrocyte glutathione level of nestlings was positively correlated to erythrocyte telomere length when birds became adults (Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023), suggesting that glutathione protects telomeres from oxidative stress‐mediated shortening (Stauffer, Panda, and Ilmonen 2018; Yadav and Maurya 2022). However, BSO tended to make such a link significantly negative, pointing to a telomere compensatory mechanism (e.g., via telomerase) triggered by low early glutathione levels (Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). Moreover, control females with low early glutathione levels but long telomeres at adulthood (perhaps better in compensating for harsh early conditions) lived longer than other phenotypic profiles (Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). This association between glutathione levels, telomere length, and longevity was absent among BSO females (Romero‐Haro, Figuerola, and Alonso‐Alvarez 2023). Here, the association between bill redness and longevity appears only among control males and not among BSO males, once again supporting the role of glutathione as a phenotypic integrator.

In conclusion, the bill redness predicts lifespan in male zebra finches, but an early harsh environment, inducing low levels of the antioxidant glutathione, would make this sexual signal less reliable. The findings support that investment in coloration would be traded against longevity, highlighting the integrative role of glutathione in shaping phenotypes. However, the correlation between the signal level and fitness should be estimated from more than longevity but also from reproductive success and offspring fitness. In this line, we have previously found that BSO birds produced smaller offspring than controls (Romero‐Haro and Alonso‐Alvarez 2020). Thus, in environments constraining glutathione synthesis, choosing a redder partner could be risky not only because its color does not correctly reveal longevity but also because these individuals could lead to small offspring (negative transgenerational effects).

Author Contributions

C.A.‐A. and A.A.R.‐H. conceived and performed the experimental study and analyzed samples. A.C. contributed to animal monitoring for some years. A.A.R.‐H. performed statistical models on experimental data. C.A.‐A. wrote a first draft. A.A.R.‐H. and A.C. contributed to the first draft, and all the authors reviewed the final text.

Ethics Statement

The University of Castilla La Mancha's animal experimentation committee approved this research project under licence number CEEA: 1201_08.

Conflicts of Interest

The authors declare no conflicts of interest.

Supporting information

Supporting information.

JEZ-343-70-s001.xlsx (70.1KB, xlsx)

Supporting information.

JEZ-343-70-s002.docx (25.6KB, docx)

Acknowledgments

We acknowledge the personnel in charge of some maintenance duties in the bird housing facilities of Finca Galiana (Diputación Provincial de Ciudad Real, Ciudad Real, Spain) and FIEB Foundation (Casarrubios del Monte, Toledo, Spain). We also thank M. E. Ferrero, E. García‐de Blas, L. Ramírez and L. Pérez‐Rodriguez for their help during the glutathione laboratory analyses and blood sampling. A.A.R.‐H. was funded by a Formación de Personal de Investigación grant (BES‐2010‐035013; Ministerio de Economía y Competitividad, MINECO, Spanish Government) and supported by the European Union's Horizon 2020 research and innovation program under the Marie Skłodowska‐Curie grant agreement 842085 and by a postdoctoral contract María Zambrano (Castilla‐La Mancha University) from the Program of Requalification of the Spanish University System (Spanish Ministry of Universities) financed by the European Union – NextGenerationEU (grant agreement MZ2021: 2022‐POST‐21023). AC was funded by grant RYC2022‐035559‐I funded by MICIU/AEI/10.13039/501100011033 and by “ESF + ”. Financial support was obtained from projects CGL‐2009‐10883‐C02‐02, CGL2012‐40229‐C02‐01, and CGL2015‐69338‐C2‐2‐P and PID2019‐109303GB‐I00 from MINECO (Spain). We acknowledge support of the publication fee by the CSIC Open Access Publication Support Initiative through its Unit of Information Resources for Research (URICI).

Contributor Information

A. A. Romero‐Haro, Email: ana.romero@uclm.es.

C. Alonso‐Alvarez, Email: carlos.alonso@csic.es.

Data Availability Statement

The data that supports the findings of this study are available in the supplementary material of this article.

References

  1. Adkins‐Regan, E. , and Tomaszycki M.. 2007. “Monogamy on the Fast Track.” Biology Letters 3: 617–619. 10.1098/rsbl.2007.0388. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alonso‐Alvarez, C. , Bertrand S., Devevey G., et al. 2006. “An Experimental Manipulation of Life‐History Trajectories and Resistance to Oxidative Stress.” Evolution 60, no. 9: 1913–1924. 10.1111/j.0014-3820.2006.tb00534.x. [DOI] [PubMed] [Google Scholar]
  3. Alonso‐Alvarez, C. , Andrade P., Cantarero A., Morales J., and Carneiro M.. 2022. “Relocation to Avoid Costs: A Hypothesis on Red Carotenoid‐Based Signals Based on Recent CYP2J19 Gene Expression Data.” Bioessays 44, no. 12: 2200037. 10.1002/bies.202200037. [DOI] [PubMed] [Google Scholar]
  4. Alonso‐alvarez, C. , Bertrand S., Faivre B., and Sorci G.. 2007. “Increased Susceptibility to Oxidative Damage As a Cost of Accelerated Somatic Growth in Zebra Finches.” Functional Ecology 21, no. 5: 873–879. 10.1111/j.1365-2435.2007.01300.x. [DOI] [Google Scholar]
  5. Alonso‐alvarez, C. , Pérez‐rodríguez L., Mateo R., Chastel O., and Viñuela J.. 2008. “The Oxidation Handicap Hypothesis and the Carotenoid Allocation Trade‐Off.” Journal of Evolutionary Biology 21, no. 6: 1789–1797. 10.1111/j.1420-9101.2008.01591.x. [DOI] [PubMed] [Google Scholar]
  6. Arnott, S. A. , Chiba S., Conover D. O., Arnott S. A., Chiba S., and Conover D. O.. 2006. “Evolution of Intrinsic Growth Rate: Metabolic Costs Drive Trade‐Offs Between Growth and Swimming Performance in Menidia menidia .” Evolution 60, no. 6: 1269–1278. [PubMed] [Google Scholar]
  7. Barja, G. 2014. “The Mitochondrial Free Radical Theory of Aging.” In Mitochondrion in Aging and Disease, Progress in Molecular Biology and Translational Science, edited by Osiewacz H. D..127, 1–27. Cambridge, Massachusetts: Academic Press. [DOI] [PubMed] [Google Scholar]
  8. Bates, D. , Mächler M., Bolker B., and Walker S.. 2015. “Fitting Linear Mixed‐Effects Models Using lme4.” Journal of Statistical Software 67, no. 1: 1–48. 10.18637/jss.v067.i01. [DOI] [Google Scholar]
  9. Bateson, P. , Gluckman P., and Hanson M.. 2014. “The Biology of Developmental Plasticity and the Predictive Adaptive Response Hypothesis.” The Journal of Physiology 592, no. 11: 2357–2368. 10.1113/jphysiol.2014.271460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bertrand, S. , Faivre B., and Sorci G.. 2006. “Do Carotenoid‐Based Sexual Traits Signal the Availability of Non‐Pigmentary Antioxidants?” Journal of Experimental Biology 209, no. 22: 4414–4419. 10.1242/jeb.02540. [DOI] [PubMed] [Google Scholar]
  11. Blackburn, E. H. 1991. “Structure and Function of Telomeres.” Nature 350, no. 6319: 569–573. 10.1038/350569a0. [DOI] [PubMed] [Google Scholar]
  12. Blount, J. D. 2004. “Carotenoids and Life‐History Evolution in Animals.” Archives of Biochemistry and Biophysics 430, no. 1: 10–15. 10.1016/j.abb.2004.03.039. [DOI] [PubMed] [Google Scholar]
  13. Boruszewska, K. , Witkowski A., and Jaszczak K.. 2007. “Selected Growth and Development Traits of the Zebra Finch (Poephila guttata) Nestlings in Amateur Breeding.” Animal Science Papers and Reports 25: 97–110. [Google Scholar]
  14. Braendle, C. , Heyland A., and Flatt T.. 2011. “Integrating Mechanistic and Evolutionary Analysis of Life History Variation.” In Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade‐Offs, edited by Flatt In. T., and Heyland A., 3–10. Oxford: Oxford University Press. [Google Scholar]
  15. Britton, G. , Pfander H., and Liaaen‐Jensen S.. 2009. Carotenoids Volume 5: Nutrition and Health. Basel: Birkhäuser Basel. [Google Scholar]
  16. Bro‐Jørgensen, J. 2010. “Dynamics of Multiple Signalling Systems: Animal Communication in a World in Flux.” Trends in Ecology & Evolution 25, no. 5: 292–300. 10.1016/j.tree.2009.11.003. [DOI] [PubMed] [Google Scholar]
  17. Candolin, U. 2000a. “Changes in Expression and Honesty of Sexual Signalling Over the Reproductive Lifetime of Sticklebacks.” Proceedings of the Royal Society B‐Biological Sciences 267, no. 1460: 2425–2430. 10.1098/rspb.2000.1301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Candolin, U. 2000b. “Increased Signalling Effort When Survival Prospects Decrease: Male‐Male Competition Ensures Honesty.” Animal Behaviour 60: 417–422. 10.1006/anbe.2000.1481. [DOI] [PubMed] [Google Scholar]
  19. Candolin, U. 2003. “The Use of Multiple Cues in Mate Choice.” Biological Reviews 78, no. 4: 575–595. 10.1017/s1464793103006158. [DOI] [PubMed] [Google Scholar]
  20. Candolin, U. , and Wong B. B. M.. 2019. “Mate Choice in a Polluted World: Consequences for Individuals, Populations and Communities.” Philosophical Transactions of the Royal Society B: Biological Sciences 374, no. 1781: 20180055. 10.1098/rstb.2018.0055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Cantarero, A. , and Alonso‐Alvarez C.. 2017. “Mitochondria‐Targeted Molecules Determine the Redness of the Zebra Finch Bill.” Biology Letters 13, no. 10: 20170455. 10.1098/rsbl.2017.0455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Cantarero, A. , Andrade P., Carneiro M., Moreno‐Borrallo A., and Alonso‐Alvarez C.. 2020. “Testing the Carotenoid‐Based Sexual Signalling Mechanism By Altering CYP2J19 Gene Expression and Colour in a Bird Species.” Proceedings of the Royal Society B: Biological Sciences 287, no. 1938: 20201067. 10.1098/rspb.2020.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Cantarero, A. , Pérez‐Rodríguez L., Romero‐Haro A. Á., Chastel O., and Alonso‐Alvarez C.. 2019. “Carotenoid‐Based Coloration Predicts Both Longevity and Lifetime Fecundity in Male Birds, but Testosterone Disrupts Signal Reliability.” Plos One 14, no. 8: e0221436. 10.1371/journal.pone.0221436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Christensen, L. L. , Selman C., and Blount J. D., et al. 2016. “Marker‐Dependent Associations Among Oxidative Stress, Growth and Survival During Early Life in a Wild Mammal.” Proceedings of the Royal Society B 283, no. 1840: 20161407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Clutton‐Brock, T. H. 1984. “Reproductive Effort and Terminal Investment in Iteroparous Animals.” The American Naturalist 123, no. 2: 212–229. 10.1086/284198. [DOI] [Google Scholar]
  26. Costantini, D. , Monaghan P., and Metcalfe N.. 2013. “Loss of Integration Is Associated With Reduced Resistance to Oxidative Stress.” Journal of Experimental Biology 216, no. 12: 2213–2220. 10.1242/jeb.083154. [DOI] [PubMed] [Google Scholar]
  27. Cote, J. , Arnoux E., Sorci G., Gaillard M., and Faivre B.. 2010. “Age‐Dependent Allocation of Carotenoids to Coloration Versus Antioxidant Defences.” Journal of Experimental Biology 213, no. 2: 271–277. 10.1242/jeb.035188. [DOI] [PubMed] [Google Scholar]
  28. Cox, R. M. , McGlothlin J. W., and Bonier F.. 2016. “Hormones As Mediators of Phenotypic and Genetic Integration: An Evolutionary Genetics Approach.” Integrative and Comparative Biology 56, no. 2: 126–137. 10.1093/icb/icw033. [DOI] [PubMed] [Google Scholar]
  29. Criscuolo, F. , Monaghan P., Nasir L., and Metcalfe N. B.. 2008. “Early Nutrition and Phenotypic Development: ‘Catch‐Up’ Growth Leads to Elevated Metabolic Rate in Adulthood.” Proceedings of the Royal Society B: Biological Sciences 275, no. 1642: 1565–1570. 10.1098/rspb.2008.0148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Delhey, K. , Valcu M., Dale J., and Kempenaers B.. 2023. “The Evolution of Carotenoid‐Based Plumage Colours in Passerine Birds.” Journal of Animal Ecology 92, no. 1: 66–77. 10.1111/1365-2656.13791. [DOI] [PubMed] [Google Scholar]
  31. Foley, J. D. , and Van Dam A.. 1984. Fundamentals of Interactive Computer Graphics. Reading, MA: Addison‐Wesley. [Google Scholar]
  32. Fox, J. , and Weisberg S.. 2019. An R Companion to Applied Regression (Third ed.). Sage. [Google Scholar]
  33. García‐de Blas, E. , Mateo R., and Alonso‐Alvarez C.. 2016. “Specific Carotenoid Pigments in the Diet and a Bit of Oxidative Stress in the Recipe for Producing Red Carotenoid‐Based Signals.” PeerJ 4: e2237. 10.7717/peerj.2237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Gautier, P. , Barroca M., Bertrand S., et al. 2008. “The Presence of Females Modulates the Expression of a Carotenoid‐Based Sexual Signal.” Behavioral Ecology and Sociobiology 62, no. 7: 1159–1166. 10.1007/s00265-008-0544-1. [DOI] [Google Scholar]
  35. Getty, T. 2014. “GEIs When Information Transfer is Uncertain or Incomplete.” In Genotype‐by‐Environment Interactions and Sexual Selection, edited by Hunt In. J., and Hosken D., 19–40. Hoboken, New Jersey, U.S.: John Wiley & Sons, Ltd. [Google Scholar]
  36. Gil, D. , Alfonso‐Iñiguez S., Pérez‐Rodríguez L., Muriel J., and Monclús R.. 2019. “Harsh Conditions During Early Development Influence Telomere Length in an Altricial Passerine: Links With Oxidative Stress and Corticosteroids.” Journal of Evolutionary Biology 32, no. 1: 111–125. 10.1111/jeb.13396. [DOI] [PubMed] [Google Scholar]
  37. Gould, R. L. , and Pazdro R.. 2019. “Impact of Supplementary Amino Acids, Micronutrients, and Overall Diet on Glutathione Homeostasis.” Nutrients 11, no. 5: 1056. 10.3390/nu11051056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Greenfield, M. D. , and Rodriguez R. L.. 2004. “Genotype‐Environment Interaction and the Reliability of Mating Signals.” Animal Behaviour 68: 1461–1468. 10.1016/j.anbehav.2004.01.014. [DOI] [Google Scholar]
  39. Griffith, O. W. 1980. “Determination of Glutathione and Glutathione Disulfide Using Glutathione Reductase and 2‐vinylpyridine.” Analytical Biochemistry 106, no. 1: 207–212. 10.1016/0003-2697(80)90139-6. [DOI] [PubMed] [Google Scholar]
  40. Griffith, S. C. 2019. “Cooperation and Coordination in Socially Monogamous Birds: Moving Away From a Focus on Sexual Conflict.” Frontiers in Ecology and Evolution 7: 455. 10.3389/fevo.2019.00455. [DOI] [Google Scholar]
  41. Griffith, S. C. , Ton R., Hurley L. L., McDiarmid C. S., and Pacheco‐Fuentes H.. 2021. “The Ecology of the Zebra Finch Makes it a Great Laboratory Model but an Outlier Amongst Passerine Birds.” Birds 2: 60–76. 10.3390/birds2010004. [DOI] [Google Scholar]
  42. Harley, C. B. , Vaziri H., Counter C. M., and Allsopp R. C.. 1992. “The Telomere Hypothesis of Cellular Aging.” Experimental Gerontology 27, no. 4: 375–382. 10.1016/0531-5565(92)90068-B. [DOI] [PubMed] [Google Scholar]
  43. Hartley, R. C. , and Kennedy M. W.. 2004. “Are Carotenoids a Red Herring in Sexual Display?” Trends in Ecology & Evolution 19, no. 7: 353–354. 10.1016/j.tree.2004.04.002. [DOI] [PubMed] [Google Scholar]
  44. Head, M. L. , Fox R. J., and Barber I.. 2017. “Environmental Change Mediates Mate Choice for an Extended Phenotype, but not for Mate Quality.” Evolution 71, no. 1: 135–144. 10.1111/evo.13091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Heidinger, B. J. , Blount J. D., Boner W., Griffiths K., Metcalfe N. B., and Monaghan P.. 2012. “Telomere Length in Early Life Predicts Lifespan.” Proceedings of the National Academy of Sciences 109, no. 5: 1743–1748. 10.1073/pnas.1113306109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Higginson, A. D. , and Reader T.. 2009. “Environmental Heterogeneity, Genotype‐By‐Environment Interactions and the Reliability of Sexual Traits as Indicators of Mate Quality.” Proceedings of the Royal Society B: Biological Sciences 276, no. 1659: 1153–1159. 10.1098/rspb.2008.1592. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Hill, G. E. 2011. “Condition‐Dependent Traits As Signals of the Functionality of Vital Cellular Processes.” Ecology Letters 14, no. 7: 625–634. 10.1111/j.1461-0248.2011.01622.x. [DOI] [PubMed] [Google Scholar]
  48. Hill, G. E. , Hood W. R., Ge Z., et al. 2019. “Plumage Redness Signals Mitochondrial Function in the House Finch.” Proceedings of the Royal Society B: Biological Sciences 286, no. 1911: 20191354. 10.1098/rspb.2019.1354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Hill, G. E. , and Johnson J. D.. 2012. “The Vitamin A‐Redox Hypothesis: A Biochemical Basis for Honest Signaling Via Carotenoid Pigmentation.” The American Naturalist 180, no. 5: E127–E150. 10.1086/667861. [DOI] [PubMed] [Google Scholar]
  50. Holman, L. , and Kokko H.. 2014. “Local Adaptation and the Evolution of Female Choice.” In Genotype‐by‐Environment Interactions and Sexual Selection, edited by Hunt J., and Hosken D., 41–62. [Google Scholar]
  51. Ingleby, F. C. , Hunt J., and Hosken D. J.. 2013. “Heritability of Male Attractiveness Persists Despite Evidence for Unreliable Sexual Signals in Drosophila Simulans .” Journal of Evolutionary Biology 26, no. 2: 311–324. 10.1111/jeb.12045. [DOI] [PubMed] [Google Scholar]
  52. Iverson, E. N. K. , and Karubian J.. 2017. “The Role of Bare Parts in Avian Signaling.” The Auk 134, no. 3: 587–611. 10.1642/auk-16-136.1. [DOI] [Google Scholar]
  53. Janssens, L. , and Stoks R.. 2020. “Oxidative Stress Mediates Rapid Compensatory Growth and Its Costs.” Functional Ecology 34: 2087–2097. 10.1111/1365-2435.13616. [DOI] [Google Scholar]
  54. Johnson, J. D. , and Hill G. E.. 2013. “Is Carotenoid Ornamentation Linked to the Inner Mitochondria Membrane Potential? A Hypothesis for the Maintenance of Signal Honesty.” Biochimie 95, no. 2: 436–444. 10.1016/j.biochi.2012.10.021. [DOI] [PubMed] [Google Scholar]
  55. Kachungwa Lugata, J. , Ortega A. D. S. V., and Szabó C.. 2022. “The Role of Methionine Supplementation on Oxidative Stress and Antioxidant Status of Poultry‐A Review.” Agriculture 12, no. 10: 1701. 10.3390/agriculture12101701. [DOI] [Google Scholar]
  56. Kim, S. Y. , Noguera J. C., and Velando A.. 2019. “Carry‐Over Effects of Early Thermal Conditions on Somatic and Germline Oxidative Damages Are Mediated by Compensatory Growth in Sticklebacks.” Journal of Animal Ecology 88, no. 3: 473–483. 10.1111/1365-2656.12927. [DOI] [PubMed] [Google Scholar]
  57. Koch, R. E. , and Hill G. E.. 2018. “Do Carotenoid‐Based Ornaments Entail Resource Trade‐Offs? An Evaluation of Theory and Data.” Functional Ecology 32, no. 8: 1908–1920. 10.1111/1365-2435.13122. [DOI] [Google Scholar]
  58. Lozano, G. A. 2009. “Multiple Cues in Mate Selection: the Sexual Interference Hypothesis.” Bioscience Hypotheses 2, no. 1: 37–42. 10.1016/j.bihy.2008.09.001. [DOI] [Google Scholar]
  59. Maynard Smith, J. , and Harper D.. 2003. Animal signals. Oxford: Oxford University Press. [Google Scholar]
  60. McGraw, K. J. , and Ardia D. R.. 2003. “Carotenoids, Immunocompetence, and the Information Content of Sexual Colors: An Experimental Test.” The American Naturalist 162, no. 6: 704–712. 10.1086/378904. [DOI] [PubMed] [Google Scholar]
  61. McGraw, K. J. 2006. “Mechanics of Carotenoid‐Based Coloration.” In Bird Coloration, Volume 1: Mechanisms and Measurements, edited by Hill G. E., and McGraw K. J., 177–242. Cambridge (MA): Harvard University Press. [Google Scholar]
  62. McGraw, K. J. , Lee K., and Lewin A.. 2011. “The Effect of Capture‐and‐Handling Stress on Carotenoid‐Based Beak Coloration in Zebra Finches.” Journal of Comparative Physiology A 197, no. 6: 683–691. 10.1007/s00359-011-0631-z. [DOI] [PubMed] [Google Scholar]
  63. McGraw, K. J. , and Toomey M. B.. 2010. “Carotenoid Accumulation in the Tissues of Zebra Finches: Predictors of Integumentary Pigmentation and Implications for Carotenoid Allocation Strategies.” Physiological and Biochemical Zoology 83: 97–109. 10.1086/648396. [DOI] [PubMed] [Google Scholar]
  64. Metcalfe, N. B. , and Monaghan P.. 2001. “Compensation for a Bad Start: Grow Now, Pay Later?” Trends in Ecology & Evolution 16, no. 5: 254–260. 10.1016/s0169-5347(01)02124-3. [DOI] [PubMed] [Google Scholar]
  65. Monaghan, P. 2008. “Early Growth Conditions, Phenotypic Development and Environmental Change.” Philosophical Transactions of the Royal Society B: Biological Sciences 363, no. 1497: 1635–1645. 10.1098/rstb.2007.0011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Monaghan, P. , Metcalfe N. B., and Torres R.. 2009. “Oxidative Stress as a Mediator of Life History Trade‐Offs: Mechanisms, Measurements and Interpretation.” Ecology Letters 12, no. 1: 75–92. 10.1111/j.1461-0248.2008.01258.x. [DOI] [PubMed] [Google Scholar]
  67. Nishida, Y. , Nawaz A., Hecht K., and Tobe K.. 2022. “Astaxanthin as a Novel Mitochondrial Regulator: A New Aspect of Carotenoids, Beyond Antioxidants.” Nutrients 14: 107. 10.3390/nu14010107. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Owerkowicz, T. , Elsey R. M., and Hicks J. W.. 2009. “Atmospheric Oxygen Level Affects Growth Trajectory, Cardiopulmonary Allometry and Metabolic Rate in the American Alligator (Alligator mississippiensis).” Journal of Experimental Biology 212, no. 9: 1237–1247. 10.1242/jeb.023945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Penn, D. J. , and Számadó S.. 2020. “The Handicap Principle: How an Erroneous Hypothesis Became a Scientific Principle.” Biological Reviews 95, no. 1: 267–290. 10.1111/brv.12563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Pérez‐Rodríguez, L. 2009. “Carotenoids in Evolutionary Ecology: Re‐Evaluating the Antioxidant Role.” Bioessays 31, no. 10: 1116–1126. 10.1002/bies.200900070. [DOI] [PubMed] [Google Scholar]
  71. Pike, T. W. , Blount J. D., Bjerkeng B., Lindström J., and Metcalfe N. B.. 2007. “Carotenoids, Oxidative Stress and Female Mating Preference for Longer Lived Males.” Proceedings of the Royal Society B: Biological Sciences 274, no. 1618: 1591–1596. 10.1098/rspb.2007.0317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Poot, H. , ter Maat A., Trost L., Schwabl I., Jansen R. F., and Gahr M.. 2012. “Behavioural and Physiological Effects of Population Density on Domesticated Zebra Finches (Taeniopygia guttata) Held in Aviaries.” Physiology & Behavior 105, no. 3: 821–828. 10.1016/j.physbeh.2011.10.013. [DOI] [PubMed] [Google Scholar]
  73. Price, D. K. 1996. “Sexual Selection, Selection Load and Quantitative Genetics of Zebra Finch Bill Colour.” Proceedings of the Royal Society of London. Series B: Biological Sciences 263 1367: 217–221. 10.1098/rspb.1996.0034. [DOI] [Google Scholar]
  74. Price, D. K. , and Burley N. T.. 1994. “Constraints on the Evolution of Attractive Traits—Selection in Male and Female Zebra Finches.” The American Naturalist 144, no. 6: 908–934. 10.1086/285718. [DOI] [Google Scholar]
  75. R Core Team . 2021. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/. [Google Scholar]
  76. Reichert, S. , Criscuolo F., Zahn S., Arrivé M., Bize P., and Massemin S.. 2014. “Immediate and Delayed Effects of Growth Conditions on Ageing Parameters in Nestling Zebra Finches.” Journal of Experimental Biology 218, no. 3: 491–499. 10.1242/jeb.109942. [DOI] [PubMed] [Google Scholar]
  77. Romero‐Haro, A. A. , and Alonso‐Alvarez C.. 2014. “Covariation in Oxidative Stress Markers in the Blood of Nestling and Adult Birds.” Physiological and Biochemical Zoology 87, no. 2: 353–362. 10.1086/674432. [DOI] [PubMed] [Google Scholar]
  78. Romero‐Haro, A. A. , and Alonso‐Alvarez C.. 2015. “The Level of an Intracellular Antioxidant During Development Determines the Adult Phenotype in a Bird Species: A Potential Organizer Role for Glutathione.” The American Naturalist 185, no. 3: 390–405. 10.1086/679613. [DOI] [PubMed] [Google Scholar]
  79. Romero‐Haro, A. A. , and Alonso‐Alvarez C.. 2020. “Oxidative Stress Experienced During Early Development Influences the Offspring Phenotype.” The American Naturalist 196, no. 6: 704–716. 10.1086/711399. [DOI] [PubMed] [Google Scholar]
  80. Romero‐Haro, A. A. , Canelo T., and Alonso‐Alvarez C.. 2015. “Early Development Conditions and the Oxidative Cost of Social Context in Adulthood: An Experimental Study in Birds.” Frontiers in Ecology and Evolution 3: 35. 10.3389/fevo.2015.00035. [DOI] [Google Scholar]
  81. Romero‐Haro, A. A. , Figuerola J., and Alonso‐Alvarez C.. 2023. “Low Antioxidant Glutathione Levels Lead to Longer Telomeres: A Sex‐Specific Link to Longevity?” Integrative Organismal Biology 5: obad034. 10.1093/iob/obad034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Romero‐Haro, A. A. , Sorci G., and Alonso‐Alvarez C.. 2016. “The Oxidative Cost of Reproduction Depends on Early Development Oxidative Stress and Sex in a Bird Species.” Proceedings of the Royal Society B: Biological Sciences 283, no. 1833: 20160842. 10.1098/rspb.2016.0842. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Saino, N. , Calza S., and pape Moller A.. 1997. “Immunocompetence of Nestling Barn Swallows in Relation to Brood Size and Parental Effort.” The Journal of Animal Ecology 66, no. 6: 827–836. 10.2307/5998. [DOI] [Google Scholar]
  84. von Schantz, T. , Bensch S., Grahn M., Hasselquist D., and Wittzell H.. 1999. “Good Genes, Oxidative Stress and Condition‐Dependent Sexual Signals.” Proceedings of the Royal Society B‐Biological Sciences 266 1414: 1–12. 10.1098/rspb.1999.0597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  85. Simons, M. J. P. , Briga M., Koetsier E., et al. 2012. “Bill Redness Is Positively Associated With Reproduction and Survival in Male and Female Zebra Finches.” Plos One 7, no. 7: e40721. 10.1371/journal.pone.0040721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  86. Simons, M. J. P. , Briga M., and Verhulst S.. 2016. “Stabilizing Survival Selection on Presenescent Expression of a Sexual Ornament Followed By a Terminal Decline.” Journal of Evolutionary Biology 29, no. 7: 1368–1378. 10.1111/jeb.12877. [DOI] [PMC free article] [PubMed] [Google Scholar]
  87. Simons, M. J. P. , Sebire M., Verhulst S., and Groothuis T. G. G.. 2021. “Androgen Elevation Accelerates Reproductive Senescence in Three‐Spined Stickleback.” Frontiers in Cell and Developmental Biology 9. 10.3389/fcell.2021.752352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Srinivas, N. , Rachakonda S., and Kumar R.. 2020. “Telomeres and Telomere Length: A General Overview.” Cancers 12, no. 3: 558. 10.3390/cancers12030558. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Stauffer, J. , Panda B., and Ilmonen P.. 2018. “Telomere Length, Sibling Competition and Development of Antioxidant Defense in Wild House Mice.” Mechanisms of Ageing and Development 169: 45–52. 10.1016/j.mad.2017.10.002. [DOI] [PubMed] [Google Scholar]
  90. Stearns, S. 1992. The evolution of life histories. Oxford, UK: Oxford University Press. [Google Scholar]
  91. Sun, N. , Youle R. J., and Finkel T.. 2016. “The Mitochondrial Basis of Aging.” Molecular Cell 61, no. 5: 654–666. 10.1016/j.molcel.2016.01.028. [DOI] [PMC free article] [PubMed] [Google Scholar]
  92. Tarry‐Adkins, J. L. , Chen J. H., Smith N. S., Jones R. H., Cherif H., and Ozanne S. E.. 2009. “Poor Maternal Nutrition Followed By Accelerated Postnatal Growth Leads to Telomere Shortening and Increased Markers of Cell Senescence in Rat Islets.” The FASEB Journal 23: 1521–1528. 10.1096/fj.08-122796. [DOI] [PubMed] [Google Scholar]
  93. Therneau, T. M. , Grambsch P. M., and Pankratz V. S.. 2003. “Penalized Survival Models and Frailty.” Journal of Computational and Graphical Statistics 12, no. 1: 156–175. 10.1198/1061860031365. [DOI] [Google Scholar]
  94. Velando, A. , Drummond H., and Torres R.. 2006. “Senescent Birds Redouble Reproductive Effort When Ill: Confirmation of the Terminal Investment Hypothesis.” Proceedings of the Royal Society B: Biological Sciences 273, no. 1593: 1443–1448. 10.1098/rspb.2006.3480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Weaver, R. J. , Santos E. S. A., Tucker A. M., Wilson A. E., and Hill G. E.. 2018. “Carotenoid Metabolism Strengthens the Link Between Feather Coloration and Individual Quality.” Nature Communications 9, no. 1: 73. 10.1038/s41467-017-02649-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Wells, J. C. K. 2007. “The Thrifty Phenotype As an Adaptive Maternal Effect.” Biological Reviews 82, no. 1: 143–172. 10.1111/j.1469-185X.2006.00007.x. [DOI] [PubMed] [Google Scholar]
  97. Westneat, D. F. , Mutzel A., Bonner S., and Wright J.. 2017. “Experimental Manipulation of Brood Size Affects Several Levels of Phenotypic Variance in Offspring and Parent Pied Flycatchers.” Behavioral Ecology and Sociobiology 71, no. 6: 91. 10.1007/s00265-017-2315-3. [DOI] [Google Scholar]
  98. Yadav, S. , and Maurya P. K.. 2022. “Correlation between Telomere Length and Biomarkers of Oxidative Stress in Human Aging.” Rejuvenation Research 25, no. 1: 25–29. 10.1089/rej.2021.0045. [DOI] [PubMed] [Google Scholar]
  99. Yearsley, J. M. , Kyriazakis I., and Gordon I. J.. 2004. “Delayed Costs of Growth and Compensatory Growth Rates.” Functional Ecology 18, no. 4: 563–570. 10.1111/j.0269-8463.2004.00879.x. [DOI] [Google Scholar]
  100. Yun, J. , and Finkel T.. 2014. “Mitohormesis.” Cell Metabolism 19, no. 5: 757–766. 10.1016/j.cmet.2014.01.011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Zann, R. A. 1994. “Reproduction in a Zebra Finch Colony in South‐Eastern Australia: The Significance of Monogamy, Precocial Breeding and Multiple Broods in a Highly Mobile Species.” Emu ‐ Austral Ornithology 94: 285–299. 10.1071/MU9940285. [DOI] [Google Scholar]
  102. Zann, R. A. 1996. The Zebra Finch. A synthesis of field and laboratory studies. Oxford: Oxford University Press. [Google Scholar]
  103. Zhang, Y. , and Hood W. R.. 2016. “Current Versus Future Reproduction and Longevity: A Re‐Evaluation of Predictions and Mechanisms.” Journal of Experimental Biology 219: 3177–3189. 10.1242/jeb.132183. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supporting information.

JEZ-343-70-s001.xlsx (70.1KB, xlsx)

Supporting information.

JEZ-343-70-s002.docx (25.6KB, docx)

Data Availability Statement

The data that supports the findings of this study are available in the supplementary material of this article.

Articles from Journal of Experimental Zoology. Part A, Ecological and Integrative Physiology are provided here courtesy of Wiley

RESOURCES