Across taxa, we see wide variation in life-history traits, such as the number of offspring produced and time spent raising young (Lack, 1947; Harvey and Clutton-Brock, 1985; Ricklefs, 2000). The central idea in life-history theory is that resources are finite, forcing trade-offs, meaning that investment in one aspect of life requires the sacrifice of another (Stearns, 1976; van Noordwijk and de Jong, 1986; Kirkwood and Rose, 1991; Lemaître and Gaillard, 2017). As reproduction is one of the most resource-demanding life stages, it is expected that within-species variation in offspring production will be constrained by the cost of producing and raising young. It is thought that the fitness costs of reproduction are largely incurred as a decrement to parental survival, explaining why a species evolved a certain amount of reproductive effort, whilst also explaining the fast–slow life-history continuum between reproduction and lifespan observed across species (Kirkwood and Rose, 1991). As reproduction and survival are the two components of life-history most closely related to fitness, this central trade-off has been the subject of much theoretical and empirical research, branching fields ranging from ecology, evolutionary biology to ageing research (Reznick, 1992; Kirkwood and Austad, 2000; Flatt and Partridge, 2018).

Brood size manipulations of birds in natural conditions have provided arguably the best experimental paradigm in which to test the survival costs of reproduction as they directly alter parental care investment. Experimental increases in brood size result in increased parental effort, suggesting that parents can typically cope with increased reproductive demands (Pettifor et al., 1988; Lessells, 1986; Monaghan and Nager, 1997; Conrad and Robertson, 1992; Hegner and Wingfield, 1987). However, the expected increased costs of reproductive effort are not always detected and the current estimate of the cost to reproduce across studies suggests only a small and inconsistent effect (Reznick, 1985; Zera and Harshman, 2001; Santos and Nakagawa, 2012; Cohen et al., 2020). The absence of a cost of reproduction (determined through experimental studies) on survival means that costs must arise elsewhere or, alternatively, that individuals may differ in quality (determined through observational studies). By quality, we refer to individuals operating at their own maximum reproductive output, determined by their phenotypic condition, local or temporal genetic adaptation, and the surrounding environment, and should manifest as a positive correlation between two fitness-associated traits (such as reproduction and survival) (Pettifor et al., 1988; Cohen et al., 2020; Charnov and Krebs, 1974; Wilson and Nussey, 2010; Drent and Daan, 2002). The relative importance of the trade-off between reproductive effort and survival to life-history theory and the biology of ageing (Kirkwood and Austad, 2000), therefore, remains unclear. In addition, the compelling theoretical explanation for the lack of an apparent trade-off due to the confounding effects of individual quality has not often been investigated on a quantitative level (van Noordwijk and de Jong, 1986; Cohen et al., 2020; Descamps et al., 2016; Vedder and Bouwhuis, 2018). Our study aims to separate the effects of a trade-off between reproductive effort and parental survival and the effects of individual quality by comparing studies of brood manipulations and naturally varying clutch size.

Here, we present a meta-analysis that distinguishes between individual quality effects and the costs of reproduction. To do this, we tested how parental annual survival in birds is affected by the clutch size they cared for using brood manipulation studies (costs of reproduction) and observational studies of natural variation in clutch size (individual quality effects) (note brood size and clutch size are used interchangeably throughout this article). We find the effect of quality is associated with higher survival chances given an increase in reproductive effort, and that this effect is opposite but equal in magnitude to the costs of reproduction. Our analysis also allowed us to transform the response variable, scaling for variance and mean, given that a per-egg increase in clutch size does not equate to the same proportional increase in reproductive effort for all species equally. Our findings suggest that species that generally lay smaller clutches are affected more severely by brood size manipulations.

To predict the evolutionary consequences of the effect sizes that we estimated using the meta-analysis, we projected the fitness consequences for a change in clutch size life-history strategy. We found that the costs to parental survival as estimated from brood size manipulation studies translate into negligible fitness costs, with a relatively flat fitness landscape, suggesting that birds underproduce in terms of clutch size, given the absence of fitness costs. Our results therefore suggest that, in wild populations, parental survival costs are, at most, a small component of the total fitness costs of investing parental effort. We therefore infer that, though the survival–parental care trade-off does exist within species, it not strong enough to constrain clutch size and can therefore not explain clutch size evolution and thus variation within species.

The relationship between clutch size and survival was significantly different and opposite between observational and brood manipulation studies, irrespective of how clutch size was scaled (p<0.01, Figure 1, Table 1). Within natural variation (observational studies), parents with larger clutches showed increased survival (or parents with smaller clutches showed reduced survival). In contrast, when broods were experimentally manipulated, the opposite relationship was found; increasing brood sizes decreased survival. Although the difference in overall effect size between experimental and natural variation in clutch size was strongly significant in each comparison made, the individual overall effect sizes only became significantly different from zero when clutch size was expressed as a proportional increase. Expressing clutch size as a proportional increase corrects for the variation in average clutch size observed across the species included in this analysis, which ranged from 2 to 11. The parental effort required to raise two instead of one chick is potentially doubled, whereas one additional chick in a brood of 11 is likely to require only a marginal increase in effort. Indeed, also when using a between-species comparison, the effects of clutch size manipulation and quality were strongest in the species that laid the smallest clutches, suggesting that costs to survival were only observed when a species was pushed beyond its natural limits (Figure 2, Figure 2—figure supplement 1, Appendix 1—table 1).

Figure 1 with 2 supplements see all

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Figure 2 with 1 supplement see all

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Males and females did not differ in their survival response to changing clutch size (Appendix 1 - table 2, Figure 1—figure supplement 1, contrary to Santos and Nakagawa, 2012). The variance assigned to the random effects in the model was largely accounted for by study (Appendix 1—table 3). Species identity accounted for more variation than the phylogeny, indicating that species vary in the relationship between survival and reproductive effort, irrespective of their shared evolutionary ancestry. However, our dataset included few closely related species, which reduces our ability to estimate phylogenetic effects (Figure 3).

Figure 3

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Projected fitness consequences of the costs of reproduction

From our meta-analysis, we now have a quantifiable and comparable effect size for the survival costs of reproduction that we can use to predict the evolutionary consequences of individuals in a given population increasing their clutch size across a range of life histories. To this end, we projected the fitness consequences of increased reproductive effort, starting with the average effect size estimate per egg (–0.05, Table 1) across a range of life histories, for a range of annual survival rates and clutch sizes (Figure 4). Overall, the effect size estimated in the meta-analysis (–0.05) resulted in a gain of fitness when reproductive output increased, especially in hypothetical species with low survival and small clutches. If we used a stronger effect size (–0.15, the lower confidence interval of our meta-analysis), this led to a reduction in fitness in almost all cases. Conversely, the benefit of higher reproductive output was largely offset by the cost of survival when a species’ survival rate and clutch size were high. When we increased the effect size up to fivefold, fitness costs of reproduction became more pronounced, but were still not present in species with small clutches and short lifespans.

Figure 4

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Under long-term evolution, these selection differentials should lead to individual hypothetical species moving towards the diagonal (bottom-left to the right-top corner). This diagonal represents the observed fast–slow pace of life continuum observed among species (Healy et al., 2019). Exemplar species (i.e., with survival and average clutch size combinations observable in wild populations), for which we predicted the fitness consequences of the costs of reproduction, lie on this comparative diagonal in life-history. In these exemplar species, the selection differential was observed to lie slightly above one, indicating that individuals having a higher clutch size than the species’ average would gain a slight fitness benefit. The fitness costs and benefits did, in general, not diverge substantially with the addition of chicks, but flattened, suggesting that the costs of survival counterbalance the benefits of reproduction across a range of reproductive outputs within a species.

The low costs of reproduction that we estimated could still be responsible for between-species life-history evolution, constraining species reproductive output and survival combination to fall along the diagonal of the fast–slow pace of life continuum. How selection pressures translate into short-term and longer-term evolutionary trajectories is uncertain. Often directional selection estimated in the wild does not translate to the inter-generational change on the population level (Pujol et al., 2018). Note, however, that only far away from the diagonal did our fitness projections reach a magnitude that would be predicted to lead to rapid evolutionary change (Gingerich, 2009; see Appendix 2). The weak selection effects that lie on the diagonal are probably to be counterbalanced in the wild by factors such as environmental effects and genetic effects (e.g., gene flow from immigration or random mutation) (Postma et al., 2007). We argue that within-species the minimal costs of reproduction, a flat fitness landscape and quality effects (Figure 1) together explain why individuals appear to under-produce. Only when individuals are pushed beyond the observed between-species constraint do costs become apparent (Figures 1 and 2).

Our interpretation of the reproduction/lifespan life-history trade-off, based on our quantitative meta-analysis and subsequent fitness projections, explains several key observations and contradictions in the field. A strong trade-off is observed between species, but within species this trade-off is not apparent and variation in reproductive output is maintained within fitness boundaries similar to those that determine the between-species life-history trade-off. The implication of this conclusion is that the costs of reproduction are likely to operate on a physiological level, but that the fitness consequences will remain largely flat over a species’ observed variation in reproductive output. These effects are further obscured by the effects of quality (observational studies), which are opposite in sign and magnitude to the cost of reproduction (experimental studies) (Figure 1) and are likely to further flatten the fitness landscape.

Our results provide the first meta-analytic evidence that differences in individual quality drive variation in clutch size and that parental survival costs do not constrain within-species variation in reproductive effort (Figure 5). Here, we use the definition of quality as a combination of traits that give an individual higher fitness (van Noordwijk and de Jong, 1986). The finding of individual quality being a driver of variation in clutch size is not necessarily a surprising one, even though this contradicts the general theory that trade-offs drive variation in clutch size, as among-individual heterogeneity is also a well-established effect across populations in the field of ecology and evolution (such as age-specific reproductive performance) (van Noordwijk and de Jong, 1986; Vedder and Bouwhuis, 2018). There has previously been discussion of why positive genetic correlations have been found in the wild and result from, for example, positive pleiotropy (Maklakov et al., 2015). Furthermore, empirical data has also found an absence of a trade-off between reproduction and survival (Reznick et al., 2004; Žák and Reichard, 2021; Kimber and Chippindale, 2013). A recent meta-analysis on genetic life-history trade-offs found several positive genetic correlations between survival and other life-history traits, which is in conflict with life-history trade-off theory (Chang et al., 2024). Brood manipulations often fail to take into account that variation in resource acquisition may be larger than variation in resource allocation, and though intuitively manipulation of effort tests variation in resource allocation, it fails to account for the baseline variation in reproductive performance (van Noordwijk and de Jong, 1986). This presents a fundamental flaw which our results demonstrate – variation in resource allocation can be present and testable through experiments (i.e. brood manipulations) but may only account for a small proportion of variation observed in reproductive output. Perhaps fitting with this interpretation or with additional costs from recurring bouts of enhanced reproductive effort, Jackdaws (Corvus monedula) show costs of increased brood size only when applied sequentially across years, but note that for this study there is no control group that is only manipulated in single years (Boonekamp et al., 2014).

Figure 5

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The reason selection is not acting on ‘high-quality’ individuals is currently unknown, but it is likely that environmental variability leads to alternative phenotypes being selected for at different points in space and time (also discussed in Pujol et al., 2018). It is also possible that the quality effect could represent a terminal effect, where individuals have lower reproductive output in the year preceding their death, thereby driving the trend for naturally lower laying birds to have lower survival when estimated between individuals (e.g. Coulson and Fairweather, 2001; Rattiste, 2004; Simons et al., 2016; Coulson and Fairweather, 2001; Rattiste, 2004; Simons et al., 2016; also see Hammers et al., 2012 for age-related changes in reproductive output). The effect on parental annual survival of having naturally larger clutches was significantly opposite to the result of increasing clutch size through brood manipulation and quantitatively similar. Parents with naturally larger clutches are thus expected to live longer, and this counterbalances the ‘cost of reproduction’ when their brood size is experimentally manipulated. It is, therefore, possible that quality effects mask trade-offs. Furthermore, it could be possible that individuals that lay larger clutches have smaller costs of reproduction, that is, would respond less in terms of annual survival to a brood size manipulation, but with our current dataset we cannot address this hypothesis (Figure 5). The effect of a change in clutch size on parental survival may also be non-linear, but it remains to be determined what shape, if not linear, the relationship would be. Although these possible non-linear effects warrant investigation, these relationships likely differ between species and inclusion in our current work here could lead to spurious relationships being reported.

For both costs of reproduction and quality effects, we found that species that laid the smallest clutches showed the largest effects. Brood manipulations that affect parental survival are thus likely to be the result of pushing parental effort beyond its natural optima (Figure 2—figure supplement 1) and so arguably that brood manipulations are not necessarily a good test of whether trade-offs happen in the wild. The classic trade-off between adult survival and the clutch size cared for is only apparent when an individual is forced to raise a clutch outside of its individual optimum, and these effects are confounded or even fully counterbalanced by differences in quality (as theorised in van Noordwijk and de Jong, 1986).

Our fitness projections of the consequences of the costs of reproduction using the overall effect size we estimated suggest that, for current extant species, the within-species fitness landscape of the reproduction survival trade-off is flat. Species’ life-history decisions are constrained within a broader fast–slow life-history continuum, explaining why variation within species in reproductive effort, such as in clutch size, is large and near universal. Of course, this analysis does not fully explore more complex variation in clutch size observed in the wild, such as that observed between temperate and tropical reproductive strategies. Such work would prove useful in understanding why variation in clutch size is maintained across species with different life-history strategies. Our results do, however, provide a key step in understanding the generalised relationship between reproductive effort and survival across species (Figure 5). Our interpretation also assumes that other fitness costs of reproduction are smaller or at least less relevant than survival costs. However, it is possible that such costs are actually more important, and it should be noted that effects such as those on offspring quality (e.g. Conrad and Robertson, 1992 and Smith et al., 1989), parental condition other than survival (e.g. Reid, 1987 and Kalmbach et al., 2004), and future reproductive effort e.g. Järvistö et al., 2016 have been observed (also see Figure 5). However, the importance of these effects is likely to vary considerably in different species. Using offspring quality as an example, some species produce sacrificial offspring, others experience catch-up growth, meaning that though the effect of increasing offspring number on offspring quality is important for certain species, drawing generalised across-species conclusions is unlikely to be possible. Conversely, the survival cost to reproduce is thought to be universal across both bird species and across taxa, and it is perhaps for this reason that the reproduction–survival trade-off has been considered to contribute more to variation in reproductive effort than other trade-offs. Our work refutes this idea directly. Indeed, the few studies that have measured the different domains that contribute to fitness in brood size manipulation studies concluded that only in combination do these costs result in balancing selection for the current most common brood size in the population (Daan et al., 1990; Verhulst and Tinbergen, 1991; Tinbergen and Daan, 1990). Such classic trade-off explanations do, however, fail to explain why variation in reproductive effort is prevalent within species and why between-species life-history trade-offs appear so much stronger and conclusive. Our analysis and interpretation suggest that, at its optimum, the within-species trade-off between survival and reproduction is relatively flat, and thus neutral to selection (supporting the theory presented in Cohen et al., 2020). We suggest that the lack of evidence supporting trade-offs driving within-species variation does not necessarily mean that physiological costs of reproduction are non-existent (e.g. Smith et al., 1989 and Lemaître et al., 2015), but rather that, within the wild and within the natural range of reproductive activities, such costs are not relevant to fitness. One key explanation for this effect supported by our meta-analysis (Figure 5) and prior theory (van Noordwijk and de Jong, 1986) is that individuals differ in quality.

All data and code used in this study can be found at: https://doi.org/10.5061/dryad.q83bk3jnk.

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Author details

1. Lucy A Winder

   Ecology & Evolutionary Biology, School of Biosciences, The University of Sheffield, Sheffield, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Writing – original draft, Project administration

   For correspondence

   lucy.anne.winder@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-8100-0568

2. Mirre JP Simons

   Ecology & Evolutionary Biology, School of Biosciences, The University of Sheffield, Sheffield, United Kingdom

   Contribution

   Conceptualization, Supervision, Writing – review and editing

   Competing interests

   No competing interests declared

3. Terry Burke

   Ecology & Evolutionary Biology, School of Biosciences, The University of Sheffield, Sheffield, United Kingdom

   Contribution

   Conceptualization, Supervision, Funding acquisition, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3848-1244

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