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. 2024 Oct 23;93(12):1972–1982. doi: 10.1111/1365-2656.14205

Inbreeding accelerates reproductive senescence, but not survival senescence, in a precocial bird

Matteo Beccardi 1, Ido Pen 2, Coraline Bichet 3, Barbara Tschirren 4, Oscar Vedder 1,✉
PMCID: PMC11615265  PMID: 39440664

Abstract

  1. Inbreeding depression is predicted to increase with age, because natural selection is less efficient at purging deleterious alleles that are only expressed later in life. However, empirical results are scarce, and equivocal between studies.

  2. Here we performed controlled matings between related and unrelated individuals of domesticated Japanese quail (Coturnix japonica), and monitored the performance of their offspring for all fitness components over their complete life course.

  3. We found rapid senescence in adult survival and egg laying performance, and inbreeding depression at all life stages (reduced embryo viability, increased age at maturity, as well as reduced adult survival and reproduction).

  4. Inbreeding depression did not increase at later ages for survival, but did so for egg laying, thereby accelerating reproductive senescence. Moreover, the effect of inbreeding on egg laying persisted after correcting for lifespan, indicating that both survival and reproduction were independently affected by inbreeding.

  5. We suggest that in heterogeneous populations intra‐generational purging may at earlier ages already select out the individuals that are homozygous for the specific alleles responsible for depressed survival, preventing the appearance of increased inbreeding depression in survival with age. Given that inbreeding affects reproduction independent of survival this should not apply to reproductive senescence or homogeneous populations, which may explain equivocal results between traits and studies.

Keywords: actuarial senescence, ageing, age‐specific inbreeding depression, fecundity, hatching success, laying rate, quail

This research shows that inbreeding depression increases with age for fecundity, but not for viability, in Japanese quail, which offers important new insights into how inbreeding depression interacts with senescence in heterogeneous populations.

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1. INTRODUCTION

A reduced fitness of offspring resulting from matings between relatives (i.e. inbreeding depression) is ubiquitous in both wild and domesticated species (Crnokrak & Roff, 1999; Keller, 2002; Leroy, 2014). Inbreeding depression's persistence can be explained by at least two genetic mechanisms: overdominance and partial dominance (Charlesworth & Charlesworth, 1987; Wright, 1977). Overdominance refers to the superior performance of heterozygotes over homozygotes at individual loci that affect fitness (East, 1908; Shull, 1908), thus allowing overdominant alleles being maintained in the population by balancing selection (Charlesworth & Willis, 2009). Alternatively, partial dominance causes many mutant detrimental recessive alleles to remain present at low frequencies in the population, as they are only strongly purged when homozygous (Charlesworth & Willis, 2009; Davenport, 1908). Because mating between relatives (i.e. inbreeding) increases the probability of homozygosity at individual loci, both scenarios lead to inbreeding depression. Yet, although both explanations are not mutually exclusive and cases of overdominance are known, empirical evidence predominantly points at partial dominance as the main genetic mechanism responsible for inbreeding depression (Charlesworth & Charlesworth, 1999; Charlesworth & Willis, 2009).

After an initial increase due to growth and/or experience, individual performance in fitness‐related traits commonly decreases with age (‘senescence’; Bouwhuis & Vedder, 2017; Nussey et al., 2013). One of the main genetic explanations for the evolution of senescence invokes similar logic as for inbreeding depression. Because selection for survival and reproduction declines with age (Hamilton, 1966) the ‘mutation accumulation theory’ posits that mutant detrimental alleles—including recessive alleles—that express their effects at old age will not be as effectively purged as those that are expressed at young age, causing individual senescence (Medawar, 1952). Combined with partial dominance as the cause for inbreeding depression, this predicts that a greater frequency of late‐expressed recessive mutants will increase inbreeding depression at old age (Charlesworth & Hughes, 1996). Alternatively, senescence is genetically explained by antagonistic pleiotropic expression of alleles with age, with mutations that enhance fitness at young age being favoured by selection, despite negative effects at old age (Williams, 1957). While this explanation does not specifically predict inbreeding depression to be age‐specific (Charlesworth & Hughes, 1996), it also does not exclude the possibility of increased inbreeding depression with age, for example if individuals become increasingly sensitive to the negative effects of pleiotropic alleles with age (Hughes et al., 2002; Keller et al., 2008). Indeed, a more recent theoretical analysis suggests that also the ‘antagonistic pleiotropy theory’ of senescence predicts increased inbreeding depression with age (Moorad & Promislow, 2009). Hence, regardless of the exact explanation for the evolution of senescence, there is good theoretical support for the hypothesis of increased inbreeding depression later in life.

Empirical results regarding changes in the severity of inbreeding depression with age are equivocal and limited to only few taxa. While experimental findings in fruit flies (Drosophila melanogaster) indeed suggest inbreeding depression on survival to increase with age (Charlesworth & Hughes, 1996; Hughes et al., 2002; Snoke & Promislow, 2003; Swindell & Bouzat, 2006; but see Rose et al., 2002), this is not supported for age‐specific survival in two species of seed beetles (Callosobruchus maculatus and Stator limbatus; Fox et al., 2006). Contrary to predictions, in island populations of red deer (Cervus elaphus) and Soay sheep (Ovis aries) inbreeding depression on survival appeared stronger early in life than later in life (Huisman et al., 2016; Stoffel et al., 2021). In birds, inbreeding depression of female reproductive success was found to increase with age in a captive population of canaries (Serinus canaria; de Boer et al., 2018), and of male reproductive success, but not female reproductive success and survival in both sexes, in an island population of song sparrows (Melospiza melodia; Keller et al., 2008). In zebra finches (Taeniopygia guttata) inbreeding depression on viability declined after the embryonic stage (Hemmings et al., 2012), but individuals were not monitored beyond the onset of sexual maturity, that is, the age after which the strength of selection should decline (Hamilton, 1966). Clearly, results are too scant to establish any universal pattern, and more work is needed on this topic. However, this is hampered by observational studies on inbreeding depression suffering from the difficulty in detecting variation in inbreeding among enough individuals across age classes, and the potential for the natural occurrence of inbreeding to be confounded with parental quality (Becker et al., 2016; Kruuk et al., 2002; Reid et al., 2006; Szulkin & Sheldon, 2006). Experimental studies can potentially solve this by creating inbred and outbred offspring from the same set of parents.

In this study we experimentally created a large sample of inbred and outbred offspring in domesticated Japanese quail (Coturnix japonica). Japanese quail are a well‐suited vertebrate model to study the relationship between inbreeding depression and individual age. They are easy to keep and both sexes mate indiscriminately, which allows mating the same individuals with both related and unrelated partners. Their offspring are precocial and can be reared completely independent of their parents, making estimates of inbreeding depression unconfounded by differences in rearing environment or parental quality. Moreover, egg production declines rapidly after the onset of reproduction, causing practically all adult females to experience senescence (Vedder et al., 2022; Woodard & Abplanalp, 1971). Although inbreeding depression has frequently been described for various early‐life traits in Japanese quail (Ihle et al., 2017; Kulenkamp et al., 1973; Sittmann et al., 1966), it has never been quantified in interaction with age, nor over their complete lifespan.

By making crosses within and between lines of domesticated Japanese quail we created both inbred and outbred offspring, for which all major life‐history traits (embryonic survival, survival to maturity, age at maturity, age‐specific egg production, and female age‐specific adult survival) were monitored over the species' complete lifespan. These crosses were made with the same parents, by mating each male and female parent once with a related partner of the same line, and once with an unrelated partner of a different line. This permits one of the strongest tests for causal effects of inbreeding, as by using the same parents to create inbred and outbred offspring it was primarily the homozygous occurrence, and not the frequency, of alleles within the groups of offspring that was manipulated. This way we tested the hypothesis that inbreeding depression increases with age (Charlesworth & Hughes, 1996).

2. MATERIALS AND METHODS

2.1. Experimental procedures and data collection

The experimental matings were performed in 2018 and 2019 at the Institute of Avian Research in Wilhelmshaven, Germany. In each year, 96 (192 in total) unique combinations out of 48 individual one‐year‐old males and 48 individual one‐year‐old females were created, by mating every individual with two partners. Each year, 48 birds (24 males and 24 females) were randomly selected to be first mated with a related partner from the same line (see details below), and the remaining 48 birds first mated with an unrelated partner from a different line. Every individual was mated again with a partner of opposite relatedness status after a minimum period of 10 days, in which males and females were separated to prevent stored sperm of previous males to fertilize any new eggs (Birkhead & Fletcher, 1994). We avoided close inbreeding (i.e. brother–sister and parent‐offspring mating), to prevent extinction of the lines. Mating was conducted by housing pairs in breeding cages (122 cm × 50 cm × 50 cm), in which pairs spent 8–14 days together. Japanese quail readily copulate when placed together (Vedder, 2022), and all eggs laid in the breeding cages were collected at a daily basis. The eggs were marked with an indelible marker upon collection and stored for 0–13 days at 12°C until artificial incubation. Excluding the egg that was laid on the first day after pairing (which was always infertile) for each pair, we collected a total of 1461 eggs, of which 709 (48.5%) came from matings between relatives.

Incubation was performed at 37.7°C and 50% relative humidity in fully automatic incubators (Grumbach, ProCon automatic systems GmbH & Co. KG, Mücke, Germany) that turned eggs every hour. In 2018, after 7 days of incubation a randomly selected subset of 262 eggs was further incubated at 36.0°C, as part of another experiment, which did not have long‐term fitness consequences (Vedder et al., 2022). The other eggs remained at 37.7°C. After 14 days of incubation, all eggs were placed in marked individual compartments to allow the hatchling to be linked to the egg it hatched from. Further incubation until hatching was done at the same temperatures, but with 70% relative humidity and no egg turning, in hatching incubators (Favorit, HEKA Brutgeräte, Rietberg, Germany). From 15 days of incubation onwards, the hatching incubators were checked for hatching, and all chicks that had hatched in the previous 24 h were taken out of the incubators once a day, until all viable embryos had hatched.

After hatching, chicks were marked with a numbered plastic leg ring and randomly placed in heated rearing cages (109 × 57 × 25 cm, Kükenaufzuchtbox Nr 4002/C, HEKA Brutgeräte, Rietberg, Germany) with maximally 30 individuals per cage. In the rearing cages water and food were provided ad libitum, with a 16–8 h light–dark cycle. The temperature of the rearing cages was set at 37.0°C at hatching and gradually lowered to room temperature (20–25°C) over the course of 2 weeks. The standard rearing diet contained 21.0% protein and had a caloric value of 11.4 MJ/Kg (GoldDott, DERBY Spezialfutter GmbH, Münster, Germany). However, in 2019 half of the chicks were randomly allocated to a poor quality diet treatment, as part of another experiment (Vedder et al., 2023). The poor quality diet contained 14.5% protein, but also had a caloric value of 11.4 MJ/Kg (GoldDott, DERBY Spezialfutter GmbH, Münster, Germany). The plastic leg rings were replaced with uniquely numbered aluminium rings when chicks were between 14 and 35 days old, depending on the size of their legs. After two (2018) or three (2019) weeks in the rearing cages the chicks were transferred to outdoor aviaries provided with heat lamps, where they were housed in random groups, and in 2018 received an adult diet with 19.0% protein and a caloric value of 9.8 MJ/Kg (GoldDott, DERBY Spezialfutter GmbH, Münster, Germany). In 2019 they initially received the same diets as in the rearing cages, but upon individual maturation they also received the adult diet. In the outdoor aviaries a minimum of 16 h of light was ensured with additional artificial lighting.

Chicks were sexed based on plumage characteristics, which are different between males and females from the age of 4 weeks. All chicks that died prematurely were molecularly sexed (following Becker & Wink, 2003), except one that was accidentally discarded. From 5 weeks onwards, all chicks were individually checked for their age at sexual maturity, every 2–3 days. For males this was done by checking for the production of cloacal foam, which is a good indicator of sexual activity (Sachs, 1969). For females this was done by checking for the presence of an egg in the oviduct, which can be easily established by palpation. At sexual maturity, each female was temporarily housed in a breeding cage to monitor her laying rate. In 2018 this was done until she laid at least 4 eggs, and in 2019 for a standard period of 7 days. Afterwards, the females were moved into single‐sex outdoor aviaries, with a minimum of 16 h of light per day to ensure the continuation of reproductive activity (Kovach, 1974). All adult females were subsequently monitored for their laying rate (over 7 days) at approximately 0.5 year intervals until ca. 3.5 years after hatching, before which 96% of females had died. All mortality was monitored on a daily basis until ca. 4.5 years after hatching, when the remaining few females had also died. The males were not monitored after sexual maturity, because their sexual behaviour makes them more logistically challenging to keep in large numbers, and their fecundity is difficult to quantify. All procedures involving the quail were done under licence of the “Veterinäramt JadeWeser” (permit nr. 42508_03122020), and all data was collected blind to the inbreeding status of the individuals.

2.2. Data and statistical analyses

Because one male died after first mating and was replaced with a brother for the second mating, and two females did not lay eggs at all, ultimately the total of 1461 eggs were sired by 97 different males, and mothered by 94 different females, in 92 related, and 93 unrelated, pair combinations.

The study population has been maintained for several generations in replicated breeding lines, with controlled matings performed within lines, and the offspring linked to the eggs they hatched from (Pick et al., 2016), and we therefore could make use of a pedigree of at least 10 generations deep to calculate the inbreeding coefficient (F) for each egg in the experiment (see Vedder et al., 2023 for more details). This coefficient (F) represents the probability that two alleles at any locus are identical by descent from common ancestors of the parents (Malécot, 1948). Because the lines originated from a common set of founders (Pick et al., 2016), F values of eggs from crosses between breeding lines ranged from 0.000 to 0.002, and averaged at 0.001 (n = 752). The crosses within breeding lines resulted in more variable F values, and ranged from 0.039 to 0.122, and averaged at 0.074 (n = 709, Figure 1). Hence, the level of inbreeding within the ‘inbred’ group was, on average, slightly above that resulting from a mating between first cousins (F = 0.0625), and did not exceed the value for a mating between half siblings (F = 0.125).

FIGURE 1.

FIGURE 1

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Distribution of inbreeding coefficients (F) of eggs, from matings between breeding lines (in blue, mean = 0.001, n = 752), and matings within breeding lines (in red, mean = 0.074, n = 709).

To test for significance of effects of inbreeding on life‐history traits occurring once per individual we constructed generalized linear mixed models (GLMMs, function “glmer()”, package “lme4”) with binomial error distributions and a logit link function for the binary traits: hatching success per egg, and survival to sexual maturity per hatchling. For effects on the age at sexual maturity and adult lifespan, we used GLMMs with normal error distributions and identity link function. All models included ‘father identity’, ‘mother identity’ and their interaction (‘pair identity’) as random intercepts. As fixed effects all models included year of hatching (2018 or 2019). However, for the model on age at sexual maturity, this fixed effect was subdivided over three categories (2018, 2019 poor diet, and 2019 standard diet) to account for the large effect the diet manipulation in 2019 had on age at sexual maturity (Vedder et al., 2023). Because unhatched eggs were not sexed, and adult performance was only measured in females, only the models on hatchling traits (survival to sexual maturity, age at sexual maturity) included sex (male or female) as fixed effect. Although we experimentally created two main categories of inbreeding (inbred and outbred), the effect of inbreeding was tested with individual inbreeding coefficient (F) as continuous fixed effect in all models. This way we account for the heterogeneity of inbreeding coefficients within the inbred category (Figure 1).

For the adult females the effect of inbreeding on their daily laying probability was studied using Generalized additive models (GAMs, function ‘gam()’, package ‘mgcv’) with a binomial error distribution (logit link function). For their adult age‐specific mortality rate we used a piece‐wise exponential additive mixed model (PAMM), combining the ‘pammtools’ package (Bender et al., 2018) with a GAM model fitted with the ‘mgcv’ package. These spline models have the advantage of being able to model the age‐specific performance without constraining this pattern to a preconceived shape. We used the gam() function's default thin plate splines with 10 knots, estimated using restricted maximum likelihood (REML). In addition to ‘father identity’, ‘mother identity’ and ‘pair identity’, the model on daily laying probability also included ‘individual identity’ as random effect. Splines were fitted with respect to the continuous predictors inbreeding coefficient (F) and age, as well as a smooth tensor product interaction between F and age. We specifically included the interaction term to test if inbreeding depression varied with age. Year of hatching (2018 or 2019) was included as parametric fixed effect. Because a previous study in our quail population has shown that egg laying performance and adult survival are positively correlated among individuals (Vedder et al., 2022), we also tested if age‐specific effects of F on laying performance were independent of effects of F on adult survival. For this we ran an additional GAM model on daily laying probability that also included adult lifespan (in days) as a continuous linear predictor.

Finally, we also ran a parametric mortality model on their age‐specific mortality probability using the function ‘flexsurvreg()’ in the package ‘flexsurv’. First, we tested which survival distribution provided the best fit to the data by comparing six common distributions (generalized‐gamma, Weibull, exponential, log‐logistic, log‐normal, Gompertz). This yielded the Weibull distribution to provide the best fit according to both Kernel density estimator (package ‘muhaz’) and Akaike information criterion (AIC) values (Table S1, Figure S1). Subsequently, we included the inbreeding coefficient (F) as covariate and the year of hatching (2018 or 2019) as a categorical explanatory variable to this Weibull model. In addition, we included a term that allowed the shape parameter (i.e. the effect of age on the mortality hazard) to vary with the inbreeding coefficient (F), to test if inbreeding depression on survival increased with age.

All analyses were done in R software (version 4.1.3, R Foundation for Statistical Computing).

3. RESULTS

3.1. Early life

Inbreeding led to a decline in hatching success, with the eggs from the inbred combinations having a ca. 15% lower hatching success (Figure 2a, Table 1). Yet, after hatching, survival to sexual maturity was very high and not affected by inbreeding (Figure 2b, Table 1). Inbreeding did delay sexual maturity, with inbred chicks reaching maturity ca. 2% later (Figure 2c, Table 1).

FIGURE 2.

FIGURE 2

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Comparison between inbred and outbred offspring with respect to fitness components; (a) hatching success, (b), survival to maturity, (c) age of maturity, and (d) adult lifespan. For visual purposes the graphs represent predicted values (mean ± 95% CI) from GLMMs as in Table 1, but with inbreeding as a categorical variable. All results from analyses presented in the text are with individual inbreeding coefficients (F) as a continuous variable.

TABLE 1.

Summaries of GLMMs testing for effects of the individual inbreeding coefficient (F) on life‐history traits occurring once per individual.

Random effects Variance Fixed effects Estimate S.E. p‐value
Hatching success
Mother identity 0.705 Intercept 0.933 0.178 <0.001
Father identity 0.055 F −5.671 1.792 0.001
Pair identity 0.171 Hatching Year (2019) −1.090 0.229 <0.001
Survival to maturity
Mother identity 0.219 Intercept 4.976 1.075 <0.001
Father identity 1.949 F −7.159 6.893 0.299
Pair identity 1.313 Sex (male) −0.051 0.484 0.916
Hatching Year (2019) 0.024 0.625 0.969
Age at maturity (d)
Mother identity 0.000 Intercept 53.139 0.662 <0.001
Father identity 0.155 F 27.205 9.438 0.004
Pair identity 6.332 Sex (male) −7.491 0.605 <0.001
Hatching Year (2019 poor diet) 19.808 0.845 <0.001
Hatching Year (2019 standard diet) −1.752 0.825 0.035
Lifespan (d)
Mother identity 3668 Intercept 780.99 30.37 <0.001
Father identity 801 F −1178.76 491.24 0.019
Pair identity 13,247 Hatching Year (2019) −0.96 39.26 0.980
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3.2. Adult survival

The adult lifespan was shorter due to inbreeding, with the inbred individuals having a ca. 10% shorter lifespan (Figures 2d and 3, Table 1). This was confirmed by a higher daily mortality hazard (Figure 4, Table 2). The daily mortality hazard increased with age, but there was no indication that the effect of inbreeding on adult survival was age‐specific (Figure 4, Table 2). These results were corroborated with the Weibull mortality model, which also did not indicate that the effect of inbreeding was age‐dependent (Table 3, Figure 5).

FIGURE 3.

FIGURE 3

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Cumulative survival curves of outbred (blue) and inbred (red) adult female quail. For visual purposes the graphs represent values with inbreeding as a categorical variable, but all results from analyses presented in the text are with individual inbreeding coefficients (F) as a continuous variable. The correspondingly coloured shaded areas represent the 95% CI.

FIGURE 4.

FIGURE 4

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Model predicted (a) daily mortality hazard of outbred (blue) and inbred (red) adult female quail, and (b) their relative difference (odds ratio), in relation to age. The correspondingly coloured shaded areas represent the 95% CIs. The dashed line in (b) represents the odds ratio for which there is no difference between outbred and inbred individuals. For visual purposes the graphs represent values with inbreeding as a categorical variable, but all results from analyses presented in Table 2 are with individual inbreeding coefficients (F) as a continuous variable.

TABLE 2.

Summaries of GAMs testing for effects of the individual inbreeding coefficient (F) on age‐specific daily mortality hazard, and age‐specific daily laying probability.

Daily adult mortality hazard
Parametric coefficients Estimate S.E. p‐value
Intercept −6.523 0.104 <0.001
Hatching year (2019) −0.046 0.154 0.762
Smooth terms Edf Chi. sq p‐value
F 1.000 5.494 0.019
Age 2.885 316.807 <0.001
F : Age 1.000 0.577 0.447
Random effects
Mother identity 6.821 8.619 0.415
Father identity 0.007 0.008 0.486
Pair identity 37.459 57.014 0.008
Daily laying probability
Parametric coefficients Estimate S.E. p‐value
Intercept 0.602 0.121 <0.001
Hatching year (2019) −0.025 0.180 0.890
Smooth terms Edf Chi. sq p‐value
F 1.000 4.383 0.036
Age 6.411 1419.64 <0.001
F : Age 9.740 37.195 <0.001
Random effects
Mother identity 2.781 16.773 0.496
Father identity 1.79 × 10−3 0.001 0.853
Pair identity 1.96 × 101 244.310 0.905
Individual identity 2.5 × 102 1608.12 <0.001
Daily laying probability (corrected for lifespan)
Parametric coefficients Estimate S.E. p‐value
Intercept 0.676 0.123 <0.001
Hatching year (2019) −0.010 0.180 0.955
Lifespan 9.04 × 10−4 0.001 0.002
Smooth terms Edf Chi. sq p‐value
F 1.000 3.188 0.074
Age 6.398 1380.60 <0.001
F : Age 9.736 36.757 <0.001
Random effects
Mother identity 8.078 105.331 0.453
Father identity 0.006 0.005 0.879
Pair identity 15.313 137.932 0.970
Individual identity 247.761 1572.83 <0.001
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Note: The model on daily laying probability was repeated with a correction for lifespan to test if the age‐specific effect of F on egg laying was independent of the effect of F on survival.

TABLE 3.

Summary of a Weibull mortality model testing the effect of individual inbreeding coefficient (F) on age‐specific mortality hazard.

Estimate Lower‐95% Upper‐95% S.E.
Shape 2.896 2.590 3.239 0.165
Scale 867.182 815.279 922.388 27.306
F −1.358 −2.518 −0.197 0.592
Hatching year (2019) 0.012 −0.066 0.091 0.040
Shape (F) −1.759 −4.088 0.570 1.188
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FIGURE 5.

FIGURE 5

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Weibull model‐predicted age‐specific mortality hazards of outbred (blue) and inbred (red) adult female quail. A natural logarithm transformation was applied to both mortality hazard and age to allow a linear visualization of the results. For visual purposes the graph represents predictions with inbreeding as a categorical variable, but the results from the analysis presented in Table 3 are with individual inbreeding coefficients (F) as a continuous variable.

3.3. Reproduction

The daily laying probability of adult females started off very high, with almost an egg per day, but decreased considerably to almost zero towards the end of their lifespan (Figure 6, Table 2). Inbreeding decreased the laying probability, the effect of which became stronger at later ages (Figure 6, Table 2). This effect remained statistically significant when correcting for a positive association between lifespan and laying performance (Table 2), indicating that there was an effect of inbreeding on egg laying independent of the negative effect of inbreeding on survival.

FIGURE 6.

FIGURE 6

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Model predicted (a) daily egg laying probability of outbred (blue) and inbred (red) adult female quail, and (b) their relative difference (odds ratio), in relation to age. The correspondingly coloured shaded areas represent the 95% CIs. The datapoints in (a) represent the raw data, and indicate the ages at which individuals were sampled. The dashed line in (b) represents the odds ratio for which there is no difference between outbred and inbred individuals. For visual purposes the graphs represent values with inbreeding as a categorical variable, but all results from analyses presented in Table 2 are with individual inbreeding coefficients (F) as a continuous variable.

4. DISCUSSION

By monitoring the performance of offspring of related and unrelated mating combinations of the same parents over the complete life course in Japanese quail, we found strong evidence for inbreeding depression in almost all components of fitness. Only the survival from hatching to the age at sexual maturity was not detectably affected by inbreeding. However, inbreeding did also affect performance at this life stage, because inbreeding delayed the age at which offspring became sexually mature, indicating a slower development speed of inbred offspring.

In agreement with the prediction that a reduction in the strength of selection on performance with age should lead to less efficient purging of recessive deleterious alleles, and therefore greater inbreeding depression at old age (Charlesworth & Hughes, 1996), we found that the negative effect of inbreeding on egg laying in Japanese quail increased towards old age. Only few studies have previously also tested this prediction for fecundity traits, and they all appear to support the prediction (de Boer et al., 2018; Keller et al., 2008; Snoke & Promislow, 2003). In contrast, we did not find support for the same prediction regarding adult survival. Despite clear evidence for a negative effect of inbreeding on adult survival, this effect did not change with age. Previous studies are equivocal in this context. There is consistent evidence that the detrimental effect of inbreeding on adult viability increases with age in laboratory populations of fruit flies (Charlesworth & Hughes, 1996; Hughes et al., 2002; Snoke & Promislow, 2003; Swindell & Bouzat, 2006), but not in some more natural populations from other species (Fox et al., 2006; Keller et al., 2008; Stoffel et al., 2021).

Studies on fruit flies can, however, use balancer chromosomes to capture and clone entire chromosome copies, such that all inbred individuals are homozygous for the exact same region of the genome (Kaufman, 2017; Sved & Ayala, 1970). Yet, more in line with natural populations, our group of inbred individuals will have been heterogeneous in homozygosity for the specific alleles that are responsible for depressed performance, with individuals having similar F values being homozygous for different alleles. This may allow for intra‐generational purging—selective disappearance—of the individuals that are homozygous for deleterious alleles that are expressed already at earlier ages (Enders & Nunney, 2016), potentially causing the oldest individuals to be less homozygous for the deleterious alleles than predicted based on their F value, and thereby obscuring the appearance of increased inbreeding depression with age.

When the recessive deleterious alleles that affect viability do not have a shared effect on fecundity, such intra‐generational purging should be less relevant for fecundity traits. Indeed, in our study the effect of inbreeding on egg laying persisted after correcting for lifespan, indicating that both survival and reproduction were independently affected by inbreeding. This could explain why we did find inbreeding depression to increase with age for egg laying but not for survival. With inbreeding studies on heterogeneous populations that have simultaneously monitored age‐specific fecundity and viability being rare (Keller et al., 2008), it cannot yet be established if this is a general phenomenon. Another cause for the absence of increased inbreeding depression on survival with age could be a non‐uniform distribution of directional dominance for performance with age. Directional dominance is the phenomenon of alleles underlying a trait predominantly showing dominance in one direction. It has been hypothesized that the closer a trait is associated with fitness the more likely it is that among mutations that have a deleterious effect on the trait, only the recessive ones can persist in the population, albeit in low frequency, thereby increasing directional dominance (DeRose & Roff, 1999; Lynch & Bruce, 1998). Hence, if, due to the reduced strength of selection, poor performance at old age is proportionally less caused by deleterious recessive (as opposed to dominant) alleles this could also prevent increased inbreeding depression with age. However, why this would only affect survival, and not reproduction, is difficult to address with this explanation. Clearly, more empirical studies that simultaneously measure age‐specific inbreeding depression in reproduction and survival would be needed to establish if our results reflect a general pattern, and ultimately predictions for more natural, heterogeneous, populations, may need to specifically incorporate how the balance between inter‐generational purging and intra‐generational purging can cause variation in empirical patterns between traits, populations, or species. With genomic techniques proliferating that relieve from the need for a detailed pedigree to estimate reliable inbreeding coefficients (Kardos et al., 2016), more empirical work from a diverse range of taxa to inform such predictions is highly anticipated, promising a better understanding of the connection between two fundamental influences on individual performance: senescence and inbreeding.

AUTHOR CONTRIBUTIONS

Conceptualization and experimental design: Oscar Vedder, Barbara Tschirren, Ido Pen and Matteo Beccardi. Data collection: Oscar Vedder and Matteo Beccardi. Data analysis: Matteo Beccardi, Ido Pen, Coraline Bichet, with feedback from Oscar Vedder. Writing: Oscar Vedder, Matteo Beccardi, with feedback from Barbara Tschirren, Ido Pen and Coraline Bichet.

CONFLICT OF INTEREST STATEMENT

The authors have no conflict of interest.

ETHICS STATEMENT

All procedures involving the quail were done under licence of the “Veterinäramt JadeWeser” (permit nr. 42508_03122020).

Supporting information

Table S1. AIC values of parametric survival models using six common survival distributions, ranked according to goodness of fit (see also Figure S1).

Figure S1. Fitted model predictions (dashed red lines) of six common survival distributions, with the raw data of age‐specific adult female quail mortality presented as Kernel density estimates (black lines).

JANE-93-1972-s001.docx (184.2KB, docx)

ACKNOWLEDGEMENTS

We thank Adolf Völk for the quail husbandry, and two anonymous reviewers for constructive comments that improved the manuscript. The study was funded by grant number 428800869 from the German Research Foundation (DFG, Deutsche Forschungsgemeinschaft) to O.V.

Beccardi, M. , Pen, I. , Bichet, C. , Tschirren, B. , & Vedder, O. (2024). Inbreeding accelerates reproductive senescence, but not survival senescence, in a precocial bird. Journal of Animal Ecology, 93, 1972–1982. 10.1111/1365-2656.14205

Handling Editor: Jelle Boonekamp

DATA AVAILABILITY STATEMENT

Data available from the Dryad Digital Repository https://doi.org/10.5061/dryad.9s4mw6mrr (Beccardi et al., 2024).

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Associated Data

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

Supplementary Materials

Table S1. AIC values of parametric survival models using six common survival distributions, ranked according to goodness of fit (see also Figure S1).

Figure S1. Fitted model predictions (dashed red lines) of six common survival distributions, with the raw data of age‐specific adult female quail mortality presented as Kernel density estimates (black lines).

JANE-93-1972-s001.docx (184.2KB, docx)

Data Availability Statement

Data available from the Dryad Digital Repository https://doi.org/10.5061/dryad.9s4mw6mrr (Beccardi et al., 2024).

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