Global changes in land use and climate are currently having negative influences on numerous taxa (Spooner et al., 2018; Northrup et al., 2019; Rosenberg et al., 2019; Halupka et al., 2023), with effects predicted to increase over the next several decades (Visconti et al., 2016; Newbold, 2018; Powers and Jetz, 2019). As animals are exposed to novel environmental conditions caused by the loss of habitat and climate change, it is important to understand the long-term fitness consequences of varying conditions, including those experienced during early life. Studies across diverse taxa have shown that early life conditions, including environmental quality and parental effects (reviewed in Lindström, 1999), can have persistent, or carry-over, effects into adulthood affecting the fitness prospects of entire cohorts of individuals born or hatched in the same year (Ancona and Drummond, 2013; Herfindal et al., 2015; Payo-Payo et al., 2023). Therefore, a better understanding of how varying early life conditions may influence fitness is important for the conservation of numerous taxa, including migratory birds, as it may provide deeper insights into mechanisms underlying spatially-varying population trends of species across their range.

“Good” or “poor” early life conditions that are positively or negatively associated with adult fitness, respectively, are called “silver-spoon effects” (Grafen, 1988). For example, offspring born or hatched in years with “good” environmental conditions, such as favorable weather, high-quality habitats, or plentiful prey availability, are generally higher quality, i.e., heavier or in better body condition (Hamel et al., 2009; Ancona and Drummond, 2013) and may perform better at later life stages regardless of the adult conditions experienced (Reid et al., 2003; van de Pol et al., 2006; Brown et al., 2022; Poli et al., 2022). However, even in years of “good” environmental conditions, it is possible that offspring may experience poor-quality or degraded environmental conditions if food resources or local weather vary temporally or deteriorate seasonally during the breeding season at temperate latitudes (Harriman et al., 2017; Shipley et al., 2020). While studies have demonstrated evidence in support of silver-spoon effects (van de Pol et al., 2006; Spagopoulou et al., 2020; Poli et al., 2022), fitness outcomes of early life conditions may also depend on the environment individuals experience as adults (e.g., environmental matching hypothesis; Monaghan, 2008).

Parental effects, such as the quality of parents themselves and/or decisions about when in a season to breed, may influence the early life conditions experienced by offspring during development (Lindström, 1999; Rödel et al., 2009; Bouwhuis et al., 2010). For instance, parents in good body condition, because they can invest more care or resources, often produce offspring that are heavier or in better condition with greater fitness prospects, regardless of environmental quality (i.e., silver-spoon condition-transfer effects; Bonduriansky and Crean, 2018). Likewise, across taxa, offspring produced earlier in the season are often heavier (Plard et al., 2015), more likely to recruit to the breeding population (Blums et al., 2002), and sometimes have higher fitness as adults (Rödel et al., 2009; Saino et al., 2012). This could be due to having higher quality parents (i.e., older, more experienced, in better condition) or better access to food resources during development (reviewed in Verhulst and Nilsson, 2008). Therefore, in seasonally deteriorating environments there could be interactions between parental quality and environmental conditions. For example, even in years with “good” conditions, offspring may still have lower fitness prospects if they are raised by poor-quality parents and/or later in the season. Alternatively, in “good” conditions, offspring may have high fitness prospects even when raised by parents that are poor quality and/or later in the season, as such parental effects may be more pronounced or only detected in poor-quality environments (Engqvist and Reinhold, 2016).

Early life conditions can have both short- and long-term consequences for fitness-related traits of offspring (Lindström, 1999). Short-term effects of early life conditions on offspring have been well characterized, and shown to affect offspring quality (e.g., pre-fledging body mass or condition) and survival, or probability of recruitment to the breeding population (Ancona et al., 2018; Halliwell et al., 2023). However, short-term effects of early life conditions on offspring are not always detected on fitness components over the long term, i.e., after local recruitment to the breeding population (Nevoux et al., 2010; Cam and Aubry, 2011; Mumme et al., 2015). Nevertheless, evidence of early life conditions having carry-over effects on adult survival after recruitment (Brown et al., 2022; Poli et al., 2022) or lifetime reproductive success (van de Pol et al., 2006; Rödel et al., 2009; Plard et al., 2015) have been demonstrated. For example, red-billed choughs (Pyrrhocorax pyrrhocorax) hatched in good environments were more likely to recruit to the breeding population and produced more recruits themselves as adults (Reid et al., 2003). Regardless, the context in which early life conditions carry-over to affect fitness and how they may vary across ecological conditions have not been fully evaluated.

In an aerial insectivore, the tree swallow (Tachycineta bicolor), we have previously explored the short-term fitness consequences of variation in early life (natal) conditions at two distinct breeding populations in Canada (Saskatchewan [SK] and British Columbia [BC]) that experience strongly contrasting local environments ( Figure 1 ; Table 1 ). In SK, located in the Canadian prairies, temperatures during the breeding season are generally warmer and there are few days with temperatures below 18.5°C (Berzins et al., 2020), i.e., “cold snaps” (the critical temperature for insect flight; Winkler et al., 2013). This contrasts the BC site, located in the interior of the province, where temperatures are cooler and cold snaps are more frequent (Griebel and Dawson, 2019). However, warmer temperatures during development at both sites, e.g., ambient temperature (SK) (Berzins et al., 2021) or experimentally heated nest boxes (BC) (Dawson et al., 2005), enhance the pre-fledging body mass of nestlings, and therefore reflect “good” environmental conditions. Wetter natal conditions at the semi-arid SK site are indicative of a “good” environment reflecting a high abundance of ponds (i.e., wetland basins containing water; Weegman et al., 2017; Clark et al., 2018). Abundant ponds during development have positive effects on the quality (i.e., pre-fledging body mass) and apparent first-year survival of offspring (Harriman, 2014; Berzins et al., 2021), presumably because of greater insect food availability or quality. In contrast, wetter natal conditions at the BC site are indicative of a “poor” environment, strongly associated with severe weather, such as cold snaps and precipitation, which negatively affect fledging survival (Berzins et al., 2020). Overall, the unfavorably cooler and wetter natal conditions likely underly the reported lower fledging success, and lighter nestling body mass prior to fledging, at the BC site compared to SK (Harriman et al., 2017; Weegman et al., 2017).

Maternal effects, such as timing of egg laying within a season, can also have short-term benefits for nestlings, with those hatching from nests initiated earlier both in SK and BC being more likely to recruit locally (Shutler et al., 2006; Harriman, 2014). The quality of the female parent, i.e., body condition, age class (second-year [SY] or after-second-year [ASY]), or breeding site experience (previously banded or unbanded when captured), also appear to benefit nestlings in the short-term, although the patterns appear site- and/or possibly year-dependent. Specifically, Harriman et al. (2017) reported that in SK, females in better body condition produced nestlings with better body condition prior to fledging (see also Griebel et al., 2019), but this was not observed at the BC site, although other studies in BC have shown that the age class of females can influence nestling body mass (Bitton and Dawson, 2017). Maternal breeding site experience was also found to be a predictor of apparent first-year survival of offspring in SK, but not at the BC site (Harriman, 2014). Finally, Lombardo et al. (2020) reported that the influence of maternal quality traits on the recruitment potential of nestling tree swallows in Michigan, USA, varied annually but were not found to be influential when the data were pooled over a 12-year time series.

In the current study, we tested whether natal conditions, i.e., environmental conditions, maternal effects, or pre-fledging quality, influenced the lifetime reproductive success (LRS) of locally recruited adult tree swallows. Local recruits are defined as nestlings hatched at our study sites that returned to breed in subsequent years. Given that nestlings which permanently emigrated from our study sites were rarely detected, we hereafter use “apparent LRS” (LRS_a; see Berzins et al., 2020). Based on the short-term benefits of “good” natal conditions in these study systems, we hypothesized ( Supplementary Table S1 ) that local recruits experiencing warmer temperatures during development (SK/BC) or hatched in years with abundant ponds (SK) or relatively drier conditions (i.e., lower Palmer drought severity index (PDSI); BC) would have higher LRS_a (environmental conditions), consistent with the silver-spoon hypothesis. Furthermore, we hypothesized that LRS_a of local recruits would be higher if reared by mothers in better body condition or that bred earlier in the breeding season (maternal effects), and that these effects on LRS_a may depend on environmental conditions in the natal year (maternal effect*environmental condition interactions). For instance, LRS_a of local recruits may be (1) lower if reared by mothers in poor body condition or later in the season even when environmental conditions are good, i.e., warmer temperatures, or higher pond abundance (SK) or relatively drier PDSI (BC); or (2) higher if reared by mothers in better body condition or breeding earlier in the season when temperatures are cooler, or pond abundance is lower (SK) or PDSI is relatively wet (BC). Lastly, while natal environmental conditions may have direct effects on long-term fitness (van de Pol et al., 2006; Spagopoulou et al., 2020), some studies have shown that natal environmental conditions can affect fitness indirectly via their effects on juvenile or yearling body mass which persist into adulthood (Plard et al., 2015; Brown et al., 2022). We hypothesized that local recruits fledging with heavier body mass, and therefore being higher quality individuals, would achieve greater LRS_a as adults. Again, positive effects of pre-fledging body mass may be more pronounced if local recruits were hatched earlier within the season or reared by mothers in better body condition (pre-fledging body mass*maternal effects interactions).

The quality of natal conditions experienced by offspring is predicted to have carry-over effects on adult lifetime fitness. In a short-lived aerial insectivore, we showed that the best-supported models explaining LRS_a were those containing environmental conditions. Therefore, environmental conditions, specifically T_max and/or pond abundance or PDSI, that local recruits experienced as nestlings during development, appear to have long-term effects on LRS_a in tree swallows. These results demonstrating consequences of variation in the natal environment on adult fitness are consistent with silver-spoon effects reported previously in diverse taxa (Reid et al., 2003; van de Pol et al., 2006; Plard et al., 2015). However, while evaluating two geographically distinct populations with contrasting environments on the breeding grounds, we also show that silver-spoon effects were context-specific depending on the populations’ response to the local environment. Maternal effects and pre-fledging quality models, including those containing interactions with environmental conditions, were not supported. As a consequence, we found no evidence that the maternal effects variables we studied, i.e., mother body condition or timing of breeding, or pre-fledging quality of local recruits influenced LRS_a. This suggests that the benefits to offspring of maternal effects or heavier pre-fledging body mass previously detected in this species (Harriman, 2014; Berzins et al., 2021) may (1) not extend beyond initial recruitment to the breeding population (Nevoux et al., 2010; Mumme et al., 2015) and therefore provide only short-term benefits, and/or (2) be less influential, or outweighed by, the stronger effect of the environmental conditions (Verhulst et al., 1995; Pärt et al., 2017) that we observed on LRS_a. Overall, results indicate that variation in LRS_a of locally recruited adult tree swallows is shaped, at least in part, by the local environment they experienced as developing nestlings.

Maternal traits and environmental factors we measured to characterize natal conditions can be important determinants of nestling quality and recruitment in tree swallows, yet not all variables were related to LRS_a. For instance, while maternal decisions on when to breed within a season are strongly related to the fitness prospects of nestlings (Verhulst et al., 1995; Verhulst and Nilsson, 2008), we did not find that an earlier hatching date within a season enhanced LRS_a. This finding contrasts with a study in another aerial insectivore, the barn swallow (Hirundo rustica; Saino et al., 2012), where recruits from nests hatched early had higher LRS than recruits hatched later in the season. It is possible that these contrasting results are due to the differing proxies of lifetime reproductive success, i.e., probability of producing a recruit (sexes pooled; this study) versus total eggs (males only; Saino et al., 2012), which may differ in their ability to reliably predict fitness (Alif et al., 2022). Indeed, a previous study in song sparrows (Melospiza melodia) using a proxy similar to ours, i.e., number of offspring surviving to independence, also reported no effect of maternal laying date on LRS of local recruits (Tarwater et al., 2018). However, in some species, it is the first-hatched nestlings within a brood that achieve higher LRS than their later hatched siblings (Martínez-Padilla et al., 2017; Song et al., 2019). We recognize that tree swallow clutches hatch asynchronously (Bitton et al., 2006), but do not have long-term data on hatching sequence to explore this possibility further.

Previous studies in tree swallows have shown that nestlings hatched from early-season nests and/or those that are heavier prior to fledging are more likely to recruit locally (Shutler et al., 2006; Harriman, 2014; Lombardo et al., 2020). Thus, it is possible that we did not detect carry-over effects of these variables on LRS_a because our sample of birds are mainly those early hatched and/or heavier nestlings, as reported in Shutler et al. (2006) and Harriman (2014), and are of relatively higher quality compared to non-recruiting offspring. In other species, higher quality individuals attain better breeding territories (van de Pol et al., 2006), and so lower quality individuals may have been outcompeted (e.g., Mumme et al., 2015), at least in SK where competition for nest boxes is high (Shutler et al., 2012). Alternatively, this pattern may also arise because of the selective disappearance of lower quality offspring prior to becoming a breeder (Nevoux et al., 2010; Payo-Payo et al., 2016). While the underlying mechanism is unknown, that local recruits may be relatively high quality is supported by two lines of evidence. First, a decrease in the proportion of local recruits with advancing hatching date suggests that more high-quality individuals were hatched earlier than later in the season ( Supplementary Figure S5 ). Second, the reported negative effects of later hatching date (SK/BC), lower pond abundance (SK), and lower temperature (SK/BC) on pre-fledging body mass of nestlings (Berzins et al., 2021) are no longer detected on body mass of local recruits as adults ( Supplementary Tables S8 , S9 ; Supplementary Figures S6 , S7 ). While a positive association between maternal body condition and nestling body mass at the SK site (Harriman et al., 2017) persisted in adulthood ( Supplementary Table S8 ; Supplementary Figure S6 ), models including these variables were not supported. Such a finding, however, does align with previous work in female tree swallows (Berzins et al., 2020), great tits (Parus major, Verhulst et al., 1995), and northern wheatears (Oenanthe Oenanthe, Pärt et al., 2017) showing that individual traits are less influential for achieving high LRS_a than environmental factors.

Effects of the natal environment on LRS_a were context-specific, depending largely on the locally varying temperature and moisture conditions. At the SK site, local recruits that developed in warmer temperatures were heavier prior to fledging (Berzins et al., 2021) and achieved higher LRS_a as adults, consistent with positive silver-spoon effects. Contrary to our hypothesis, however, we found a negative trend of warmer temperature on LRS_a at the BC site. Dawson et al. (2005) demonstrated that nestlings may have benefited from being reared in experimentally heated nests at the BC site as they were heavier prior to fledging. The contrasting results between studies in the same study population may be explained by the magnitude in temperature increase that nestlings were exposed to during development. For instance, Dawson et al. (2005) experimental study elevated the temperature of nests within the range of normal variation, whereas in our study, the highest temperatures experienced by local recruits during development overlapped with record-breaking heat waves (The Canadian Press, 2013). The temperatures local recruits experienced while growing during the heat waves in June of 2004 and 2013, were ~1.5 to 3.5°C greater than the mean T_max for the month of June and during the period of nestling growth for all nests in those years ( Supplementary Figure S8 ). It is therefore possible that at the BC site, where temperature is generally cooler during the breeding season than the more arid SK site in the prairies ( Table 1 ), high temperature extremes may instead reflect unfavorable environmental conditions. A positive relationship between the pre-fledging body mass of local recruits and temperature during development ( Supplementary Table S8 ; Supplementary Figure S7 ) may suggest that only local recruits that were relatively high-quality (i.e., heavier as nestlings) were able to buffer the effects of developing in such high temperatures in the short-term but still incurred fitness costs as adults, consistent with the silver-spoon hypothesis. Although suggestive, our results add to the increasing number of studies reporting negative effects of extreme heat-related events on fitness prospects of offspring (Eastwood et al., 2022; Lv et al., 2023).

Moisture conditions, such as pond abundance and PDSI, are driven largely by precipitation and have contrasting effects on the local population dynamics of tree swallows across their range (Weegman et al., 2017). At the more arid SK site, wetter conditions are generally favorable, reflecting abundant ponds (Weegman et al., 2017; Berzins et al., 2020), and by association increased abundance of aerial insects with aquatic larval stages (Berzins et al., 2022). Since ponds in the prairies of North America unequivocally benefit breeding birds (Bartzen et al., 2010; Zhao et al., 2019; Devries et al., 2023), including tree swallows (Michelson et al., 2018; Berzins et al., 2021), it is unclear why local recruits reared when pond abundance was high did not achieve the highest LRS_a as adults. One possibility is that the nutritional environment under higher pond abundance may actually be inferior to intermediate pond conditions due to extensive flooding and lower productivity of ponds. For instance, larger ponds can become deeper, permanent, lake-like systems during extensive flooding events (Cressey et al., 2016; Hayashi et al., 2016), which have less diverse invertebrate communities and lower nutrient turnover than smaller seasonal and temporary ponds (McLean et al., 2020; Fritz and Whiles, 2021). A study in tree swallows recently invoked this reasoning, i.e., sites with more pond area, but containing a few large lake-like ponds, may provide less aquatic insect food during growth, to explain why the observed increase in nestling quality and predicted survival leveled off when the surface area of ponds in a region was at intermediate levels (Berzins et al., 2022). While the SK site experienced an extended wet period from 2011 to 2017, with expansion of several larger ponds, ponds of varying sizes, depths, and permanence still existed within this wetland complex. We do not, however, have additional data on pond area and aquatic insect availability to further explore these relationships over the SK time series. Nevertheless, how the type and surface area of ponds in the landscape influence the nutritional environment experienced by aerial insectivores on the breeding grounds warrants further investigation.

Our study focused on testing for silver-spoon effects of natal conditions on LRS_a, which predict fitness benefits to individuals developing in a good environment, independent of the adult environment (Monaghan, 2008). However, we recognize that LRS_a may also be influenced by current environmental conditions experienced by local recruits during breeding. Previous studies at the SK site have shown that LRS_a and apparent survival of tree swallows were higher when breeders experienced relatively high pond abundance (Clark et al., 2018; Berzins et al., 2020). Therefore, our results may also be explained by local recruits reared when pond abundance was highest being more likely to encounter poorer pond conditions as breeders due to cycling in pond abundance during wet-dry periods ( Supplementary Figure S9 ). This reasoning would also explain the fewer breeding attempts made by local recruits reared in high versus intermediate pond abundance ( Supplementary Table S10 ; Supplementary Figure S10 ). In other species, such as tawny owls (Strix aluco), the phase of the vole cycle (i.e., increasing or decreasing) that local recruits experience as first-time breeders was more influential for LRS than natal conditions (Millon et al., 2010). For tree swallows at the SK site, females generally begin breeding at 2 years old or older (Berzins et al., 2020), in contrast to males ( Supplementary Figure S1 ). Age of first breeding does not appear to vary with natal pond abundance for females, but it does for males ( Supplementary Figure S10 ). This points to the possibility that males hatched in years of differing natal pond abundance may encounter different competitive environments at recruitment that affects their opportunity for breeding (i.e., mismatched natal and adult environments; Monaghan, 2008). When natal pond numbers are relatively low and few males recruit to the breeding population, competition for nest boxes may be reduced which allows males to breed at younger ages and have more lifetime breeding attempts ( Supplementary Figure S10 ). In contrast, when natal ponds are abundant and more males recruit, competition for breeding sites, particularly in SK where occupancy of nest boxes is high, becomes more intense, resulting in a concomitant delay in age at first breeding and a decrease in the number of lifetime breeding attempts ( Supplementary Figure S10 ). While outside the scope of our present study, that LRS_a of local recruits could potentially be influenced by complex interactions with pond conditions across life stages, depending on whether ponds are increasing or decreasing during wet-dry periods, is an idea that warrants further investigation.

In contrast to the more arid SK site, wetter conditions in BC are generally unfavorable (Berzins et al., 2020), as is also evident in other parts of the range of tree swallows (Weegman et al., 2017). For instance, in Ontario and Quebec, Canada, prolonged precipitation reduces the availability of insects, and so negatively affects the quality and fledging success of nestlings (Cox et al., 2019; Garrett et al., 2022). Our results at the BC site indicate that the negative effects for nestlings reared in wetter natal conditions may also carry-over to affect their fitness as adults, in accordance with the silver-spoon hypothesis. Breeding at earlier ages may enhance fitness by increasing the number of lifetime breeding attempts (Blums and Clark, 2004), especially in short-lived species (Gustafsson and Pärt, 1990). We suspect that local recruits experiencing wetter PDSI conditions had lower LRS_a because they delayed breeding to 2 years old or older, and tended to breed fewer times than recruits hatched when PDSI conditions were intermediate ( Supplementary Table S10 ; Supplementary Figure S11 ).

Our results have important conservation implications as climate change is predicted to increase local weather variability, and the frequency and severity of temperature extremes and drought. In the interior of BC, wetter and warmer natal conditions that resulted in reduced LRS_a suggest that potential increases in precipitation and heat waves with climate change (IPCC, 2021) could have adverse demographic consequences in the future. Indeed, the number of extreme heat-related events is already increasing (Parisien et al., 2023), with the highest ever recorded temperatures in 2021 exceeding >35°C during nestling development. While warmer temperatures at the SK site had positive carry-over effects on LRS_a, suggesting tree swallows may benefit from increasingly warm temperatures associated with climate change (Mantyka-Pringle et al., 2019), results from the BC population caution that higher than average temperatures as predicted for the prairies (IPCC, 2021) could led to reductions in fitness of tree swallows in the future. For instance, higher temperatures may not only increase the evaporation of ponded water, but also the susceptibility to drought (Douville et al., 2021). Recent evidence at the SK site highlights the importance of abundant ponds for promoting the population stability of tree swallows (Clark et al., 2018; Berzins et al., 2020, 2021). However, ongoing losses of ponds to agricultural drainage and infilling (Bartzen et al., 2010), combined with the predicted drying of ponds in parts of the prairies (Johnson et al., 2010; Londe et al., 2023) may lead to population declines via lower recruitment and LRS_a. Conserving and restoring prairie ponds may therefore be critical for sustaining tree swallow populations in a changing climate.

Aerial insectivores have experienced steep population declines in North America (Rosenberg et al., 2019), but within species there is high spatiotemporal variability in population trends across their ranges (Michel et al., 2016). By evaluating two distinct populations of tree swallows, we show locally varying natal environments had carry-over effects on adult LRS_a. Consequently, natal environmental conditions that generate differences in fitness may explain trends in population-level demographics. Unveiling population responses to environmental variability on the breeding grounds is important as offspring will be increasingly exposed to modified natal environments as climate and land use changes intensify across the globe.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The animal study was approved by University Animal Care Committee, University of Saskatchewan; Animal Care and Use Committee, University of Northern British Columbia. The study was conducted in accordance with the local legislation and institutional requirements.

LB: Conceptualization, Formal analysis, Investigation, Visualization, Writing – original draft, Writing – review & editing. RD: Conceptualization, Funding acquisition, Investigation, Writing – review & editing, Resources. RC: Conceptualization, Funding acquisition, Investigation, Writing – review & editing, Resources.