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Published in final edited form as: Gen Comp Endocrinol. 2022 Nov 17;333:114166. doi: 10.1016/j.ygcen.2022.114166

Urbanization and maternal hormone transfer: Endocrine and morphological phenotypes across ontogenetic stages

Jennifer J Heppner 1,*, Jesse S Krause 1, Jenny Q Ouyang 1
PMCID: PMC10978011  NIHMSID: NIHMS1972362  PMID: 36402244

Abstract

The phenotypes observed in urban and rural environments are often distinct; however, it remains unclear how these novel urban phenotypes arise. Hormone-mediated maternal effects likely play a key role in shaping developmental trajectories of offspring in different environments. Thus, we measured corticosterone (Cort) and testosterone (T) concentrations in eggs across the laying sequence in addition to Cort concentrations in nestling and adult female house wrens (Troglodytes aedon) at one urban and one rural site. We found that egg T concentrations were not different between birds from urban and rural sites. However, across all life stages (egg, nestling, and adult female), Cort concentrations were higher at the urban site. Additionally, urban nestling Cort concentrations, but not rural, correlated with fine-scale urban density scores. Furthermore, rural egg volume increased over the laying sequence, but urban egg volume leveled off mid-sequence, suggesting either that urban mothers are resource limited or that they are employing a different brood development strategy than rural mothers. Our study is one of the first to show that egg hormone concentrations differ in an urban environment with differences persisting in chick development and adult life stages. We suggest that maternal endocrine programing may shape offspring phenotypes in urban environments and are an overlooked yet important aspect underlying mechanisms of urban evolution.

Keywords: Maternal effects, Corticosterone, Testosterone, Phenotypic plasticity, House wren, Egg yolk

1. Introduction

Urban land cover has increased exponentially in the past decade with projections of more than two-thirds of the world’s populations living in urban areas by 2050 (United Nations, 2018). Research has shown that urban and non-urban animal phenotypes differ in morphological and physiological traits (Birnie-Gauvin et al., 2017; Giraudeau et al., 2014; Madliger and Love, 2015; Meillère et al., 2015; Putman et al., 2019). For example, urban exploiters have different hormone levels than their rural counterparts (Bonier, 2012). However, it remains unclear how these different phenotypes arise. While both genetic and plastic mechanisms play a role in the development of the urban phenotype (Bonier et al., 2007; Miles et al., 2021; Ouyang et al., 2019; Rivkin et al., 2019; Santangelo et al., 2018), studies have often overlooked the role of prenatal and parental effects.

Maternal effects adaptively modulate offspring developmental courses and have been proposed as a mechanism to help organisms cope with environmental change (von Engelhardt and Groothuis, 2011). Since developing offspring have limited to no knowledge of the environment they will be exposed to, hormone-mediated effects could program offspring phenotypes as means to increase fitness (Coslovsky and Richner, 2011; Groothuis and Schwabl, 2008; Marshall and Uller, 2007). Due to the immediate and long-term impacts of maternal effects on offspring phenotype (Groothuis et al., 2005), they likely play a role in assisting organisms in colonizing novel environments and coping with anthropogenic conditions (Räsänen and Kruuk, 2007). As urban ecology and evolution research increases its focus on abiotic conditions altering endocrine phenotypes, it is becoming more important to understand how maternal hormones differ across human-modified landscapes (Groothuis et al., 2019).

Adult hormone phenotypes change across urbanization gradients (Bonier, 2012; Davies et al., 2017; Davies and Sewall, 2016). However, hormone concentrations vary depending on the city, the species, and the sex (Davies et al., 2018; Injaian et al., 2020; Partecke et al., 2005). For example, most studies show that testosterone (T) concentrations are lower in urban environments possibly due to lower competition or increased investment in survival versus reproduction (Atwell et al., 2014; Davies et al., 2018; Davies and Sewall, 2016; Partecke et al., 2005). While research shows that glucocorticoids can correlate with urbanization and other human-related factors, the direction of its effects varies depending on many abiotic and biotic conditions (Dantzer et al., 2014; Dickens and Romero, 2013; Injaian et al., 2020). For example, in Reno, NV, USA, a fine-scale measure of urban density positively correlated with house sparrow (Passer domesticus) glucocorticoid levels (White et al., 2022). In our study system of house wrens (Troglodytes aedon) across an urbanization gradient, we found that urban adults have higher corticosterone (Cort) concentrations (Davies et al., 2017) with nestlings also exhibiting higher concentrations at hatching (Ouyang et al., 2019). Offspring phenotypes are the result of genetic and environmentally mediated mechanisms, such as phenotypic plasticity, but in our previous study, we did not investigate the possibility of prenatal parental effects on this offspring phenotype. To our knowledge, only one study has investigated egg yolk hormone concentrations in an urban environmental context in birds, in which they found that androgens were lower in urban compared to forest dwelling populations (Partecke et al., 2020). This study highlights that the maternal transfer of hormones is a likely but understudied mechanism of phenotypic adaptation to anthropogenic change.

To investigate the differences that could initiate the development of endocrine phenotypes in an urban environment, we used a long-term study of two free-living populations of house wrens. We measured egg, nestling, and adult female morphologies and hormone concentrations. Due to our previous research and organismal exposure to urban challenges, we predicted that urban eggs would have higher Cort and lower T concentrations, possibly due to Cort’s negative effect on circulating androgens (Tsutsui et al., 2010). Furthermore, we predicted that endocrine phenotypes would be consistent across life stages of birds, in which urban eggs, nestlings, and adults would have higher Cort concentrations compared to rural counterparts (Almasi et al., 2012; Hayward and Wingfield, 2004; Love and Wynne-Edwards, 2005; Saino et al., 2005), due to our previous findings in nestling and adult house wrens (Davies et al., 2017; Ouyang et al., 2019). Alternatively, offspring phenotype may not be affected by maternal hormones if the hormones are metabolized during early embryonic development (Vassallo et al., 2019; von Engelhardt et al., 2009). However, if differences in Cort and T exist across ontogenetic development and between urban and rural wrens, these endocrine phenotypes may result in morphological differences with slower offspring growth in urban environments, which we have observed previously in our study species (Baldan and Ouyang, 2020). Overall, we predicted that urban phenotypic differences could result from hormone-mediated maternal effects.

2. Methods

2.1. Field sites and protocol

This study was conducted between May and August of 2019 at two sites that differ in urbanization scores in the Reno-Washoe area (Baldan and Ouyang, 2020). The urban site was a city park in Reno, NV (39°30′3″N, 119°50′ 00″W) and the rural site was the University of Nevada, Reno Agricultural Experimental Station, a university owned agricultural farm (39°30′ 50″N, 119°51′ 43″W). Following the validated methods of Seress et al., 2014, this urban site had a higher urbanization score with a lower abundance of insectivorous food in which rural wrens fed their nestlings a majority of caterpillars while urban parents fed nestlings alternative food items of lower quality (Baldan and Ouyang, 2020).

House wrens are small cavity nesters that readily use nest boxes across an urbanized gradient (Heppner and Ouyang, 2021; Ouyang et al., 2019) and lay one egg per day for a total of 5–8 eggs per clutch. We monitored nest boxes every 3 to 4 days for activity of nest building. Once a female began laying, we removed 1 to 3 eggs per nest across the laying sequence on the day they were laid to measure egg hormone concentrations across the laying order. While house wrens can lay up to 8 eggs, we only collected eggs 1 through 6 (either combinations of eggs 1, 3 and 5 or 2, 4 and 6) to ensure samples sizes were even across the laying sequence. We replaced eggs taken with dummy eggs, which females readily accepted and incubated. Eggs were then stored at −20 °C until analysis. We measured egg morphology (mass, length, and width) on the day it was laid. Eggs not collected developed naturally in the nest.

We closely monitored nests to identify the first day eggs hatched (day 0). We measured offspring body mass and tarsus length to calculate body condition (estimated as a scaled mass index (Peig and Green, 2009)) on days 1, 4, 8, and 12 post hatching to monitor growth of nestlings between environments. On day 12 post hatching, we took a blood sample from the brachial vein of nestlings (<20 μl) between 09:00 and 11:00 to measure plasma hormone concentrations (average time to sample = 170 s; s.d. = 58). Between days 9–11 post hatching, we captured adult females in the nest boxes to collect a blood sample from the brachial vein between 10:30 and 14:30 to measure plasma Cort concentrations (average time to sample = 234 s; s.d = 74). We released adults after taking body mass and tarsus measurements for calculating body condition. Time for blood collection of young and adult samples did not affect Cort concentrations (p > 0.05). Samples were immediately stored on ice and then centrifuged at 9950g for 10 min. We removed the plasma and stored samples at −80 °C until analysis. This study was carried out in accordance with recommendations of the Institutional Animal Care and Use Committee of the University of Nevada, Reno.

2.2. Egg hormone extraction and assay

We extracted hormones from eggs following the protocol from Taves et al., 2011 and validated for house wrens (see Supplemental Material; Figure S1). First, eggshells were removed and all egg components including yolk and albumen were homogenized. Immediately after, we added four times the volume of methanol. Samples were then sonicated for 15 min and centrifuged at 2 °C and 3000g for 10 min. Egg steroids were extracted using solid phase extraction of C18 columns (Agilent Bond Elut LRC-C18 OH, #12113045) under vacuum filtration. We eluted egg steroids with 90 % methanol, dried the samples with a centrifugal evaporator (GeneVac EZ-2), and reconstituted the samples in 195 ul of kit assay buffer for both Cort and T. Both hormones were extracted from every egg collected.

The concentration of egg hormones (Cort and T) in each egg was subsequently measured using enzyme-linked immunoassays (EIA) (Arbor Assays DetectX Corticosterone EIA Kit Improved Sensitivity, Product # K014; Arbor Assays DetectX Testosterone EIA Kit, Product # K032). We randomized samples across plates (3 plates per hormone). Three internal controls (water blank, non-spiked egg control pool (NSC), and high spiked egg control pool (HSC)) were used for each hormone to calculate intra- and inter-plate variations (CV). Both assays were validated by assessing parallelism and recovery (see Supplemental Materials) with all samples falling within the detectable range of the standard curves. All samples were assayed in triplicate across three plates for each hormone. Cross reactivity with progesterone was 0.24 % for the Cort and < 0.02 % for the T Kits (for cross reactivity of other hormones see Supplementary Materials). Intra- and inter-plate CVs were calculated from CVs of samples, non-spiked, and spiked controls across all three plates. Intra-and inter-plate CVs were 6.5 % and 17.8 % for Cort and 6.6 % and 15.1 % for T, respectively.

2.3. Adult female and nestling plasma Cort assay

To measure the concentration of Cort in adult females and nestlings, we used an enzyme-linked immunosorbent assay kit (Enzo Life Sciences; Farmingdale, NY, USA) previously validated for house wrens (Davies et al., 2017). We diluted plasma 1:40 in assay buffer with 0.5 % steroid displacement reagent and randomized samples across the plate. To calculate intra-assay variation (CV), we included a pool of the kit standard 3 and assayed in triplicate. The intra-plate CV was 6.79 %.

2.4. Urban nestling plasma Cort and urban density metric

Due to the bimodal distribution of urban Cort values, we modeled whether urbanization at a finer scale varied with hormone values. We used published urban density values from White et al. (2022). Briefly, White et al. modeled urban density by combining four metrics at the building level: the number of residents and employees, building footprint and height estimates, resulting in a 2 m2 rasterized surface (White et al., 2018). Therefore, this model is a three-dimensional representation of where humans spend most of their time.

2.5. Statistical analysis

All models were run in R version 4.1.2 (R Core Team, 2019). We used the lme4 package (Bates et al., 2015) to perform linear mixed models (LMM) and the lmerTest package (Kuznetsova et al., 2017) to report all p-values. All final models met assumptions of normality and homoscedasticity of residual errors. Significance was taken at α = 0.05. For all models, we included nest ID as a random effect. We used LMMs to test the effects of site, lay order, the interaction of site and lay order, date, and clutch size on egg mass and volume. To test the difference of egg hormone concentrations between sites, we standardized each egg Cort and T concentrations by their original whole egg mass (hormone concentration/mass). We used LMMs to test effects of site, lay order, date, and clutch size on mass standardized egg Cort and mass standardized egg T concentrations. We ran all models with the interaction of site and lay order and when the interaction was not significant, we removed it from the model. For the egg Cort model, we removed two statistical outliers that were more than two standard errors away from the mean. We note that our results remain the same even if we include these outliers. To test the correlation between egg T and Cort, we ran a LMM with nest as a random effect.

We used a LMM to test effects of site, date, and body condition (on day 12) on nestling plasma Cort concentrations. We removed two statistical outliers to ensure the statistical assumption of normality of residuals. We note that our results remain the same whether or not we include these outliers. Next, we used a LMM to test the effects of site, age, and date on offspring body condition with nest and nestling ID as random effects. We used a generalized linear model to predict offspring Cort concentrations with the interaction of site and urban density as fixed effects and nest as a random effect. Lastly, we used linear models to test urbanizations effects on adult female Cort and body condition.

3. Results

We monitored 10 urban and 10 rural nests (25 urban eggs, 25 rural eggs). For both urban and rural nests, egg size increased with lay order (Table 1). Egg mass and volume models also showed a significant interaction between site and lay over. As lay order increased, urban eggs had lower mass and volume than rural ones (Fig. 1A, Table 1). The model for egg Cort concentrations showed that urban eggs had higher Cort concentrations compared to rural eggs. Additionally, Cort concentrations decreased over the laying sequence for both urban and rural nests (Fig. 1B, Table 1). While egg T did not differ between sites, it decreased across the laying sequence for both urban and rural eggs. Additionally, there was an effect of date, in which eggs laid later in the season had higher T concentrations (Fig. 1C, Table 1). There was no correlation between egg Cort and egg T concentrations (p > 0.05).

Table 1.

Results from linear mixed models measuring differences in egg mass, egg volume, egg Cort, egg T, nestling Cort, and nestling body condition between urban and rural house wren nests. Fixed effects that were significant (p < 0.05) are highlighted in bold. Nest ID and offspring ID (in the case of offspring growth) were included as a random effect to correct for repeated measures.

Coefficient SE t p
Egg Mass:
Site −0.04 0.04 −1.2 0.25
Lay Order 0.03 0.00 8.8 0.00
Date 0.00 0.00 1.1 0.27
Clutch Size −0.00 0.01 −0.31 0.76
Site:Lay Order −0.01 0.00 −2.88 0.005
Egg Volume:
Site −0.04 0.04 −1.18 0.25
Lay Order 0.03 0.00 8.84 0.00
Date 0.00 0.00 1.14 0.27
Clutch Size −0.00 0.01 −0.31 0.76
Site:Lay Order −0.01 0.01 −2.88 0.005
Egg Cort:
Site 0.05 0.02 3.06 0.01
Lay Order −0.01 0.00 −3.31 0.00
Date −0.00 0.00 −1.63 0.12
Clutch Size −0.01 0.01 −0.85 0.41
Egg T:
Site 0.04 0.06 0.61 0.55
Lay Order −0.03 0.01 −3.25 0.00
Date 0.00 0.00 2.56 0.02
Clutch Size 0.03 0.03 1.18 0.26
Nestling Cort:
Site 12.49 4.66 2.68 0.02
Date 0.14 0.13 1.06 0.31
Body Condition 1.04 2.25 0.46 0.65
Nestling Body Condition:
Site −0.05 0.12 0.45 0.66
Age −0.02 0.01 −1.71 0.09
Date −0.01 0.00 −2.24 0.05
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Fig. 1.

Fig. 1.

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(A) Egg morphology depicted as egg volume and egg (B) Cort and (C) T concentrations across the laying sequence between urban and rural eggs. All egg hormones are standardized by the egg mass. Solid green lines represent rural individuals and broken grey lines represent urban individuals. Circles plotted are means with standard error bars.

Due to predation and nest failure, we monitored 9 urban and 7 rural nests to fledgling (26 urban chicks, 19 rural chicks). Urban nestlings had on average higher Cort concentrations compared to rural ones (Fig. 2A, Table 1). Nestling growth (body condition) did not differ between urban and rural sites as nestlings aged but body condition did decrease over the breeding season (Table 1). We found that there was a significant interaction of site and urban density (coef: 71.2, SE = 30.6, t = 2.3, p = 0.02) in which urban density did not correlate with rural offspring Cort concentrations but did correlate with urban offspring Cort concentrations (Fig. 2C). Lastly, we measured adult female plasma Cort concentrations between 7 urban and 5 rural females to show that during chick rearing, urban females had higher plasma Cort concentrations compared to rural females (Fig. 2B; coef = 4.1, SE = 1.6, t = 2.7, p = 0.02). Body conditions of adult house wrens did not differ between sites (p = 0.7).

Fig. 2.

Fig. 2.

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(A) Nestling plasma and (B) adult female plasma Cort concentrations between urban and rural nests. Shown are boxplots with raw data of each individual. Green represents rural individuals and grey represent urban individuals. (C) Plasma Cort levels of nestlings across urban density scores of each nest location at a fine scale of 2 m2. The solid green line represents rural nests, and the broken grey line represents urban nests. Note that we plot average corticosterone values of each nest to avoid non-independence.

4. Discussion

To our knowledge, our study is one of the first to look at egg hormone concentrations in an urban environment and record parallel phenotypes across ontogenetic stages. We found that urban eggs had higher Cort concentrations, even though urban eggs were smaller than rural ones. Likewise, Cort concentrations were higher in urban nestlings and adult females compared to rural birds. However, we found no differences in nestling growth rates, likely because we alleviated parental effort by removing three eggs from the nest. We note that we only had two sites and our results could be site-related rather than urbanization per se. However, we find similar within-site relationships when measuring urbanization as a continuous variable, in which urban nestling Cort concentrations, but not rural, correlated with urban density score.

4.1. Corticosterone concentrations across ontogenetic stages

We found that urban eggs had higher Cort concentrations across the laying sequence compared to rural eggs. To our knowledge, this is the first study that has investigated Cort concentrations in eggs in response to urbanization. Empirical and correlative studies have shown that maternal Cort concentrations correlate with egg concentrations (Almasi et al., 2012; Groothuis and Schwabl, 2008; Hayward and Wingfield, 2004; Love and Wynne-Edwards, 2005; Saino et al., 2005). Here, as in our previous work, we found that adult urban females had higher Cort than rural ones (Davies et al., 2017). Thus, higher circulating concentrations in urban adult females likely results in greater Cort transfer to the egg. We note that to prevent nest desertion, we waited to catch females until after nestlings hatched and that Cort concentrations may be different during egg-laying. As Cort responds to elevated allostatic load, environmental challenges (including urban-related) can increase circulating Cort concentrations (Davies et al., 2017; French et al., 2010; Hau et al., 2016; White et al., 2022). Thus, whether through a passive inevitable transfer from high circulating concentrations or an adaptive strategy to shape offspring phenotype, urban females pass higher Cort concentrations to developing embryos (Groothuis et al., 2005). This maternal Cort has been shown to affect offspring phenotype across taxa, resulting in smaller offspring at hatching, slower growth, altered physiological stress responses, higher anxiety, reduced immunity, and altered behavior (De Fraipont et al., 2000; Ensminger et al., 2021, 2018; Haussmann et al., 2012; Hayward and Wingfield, 2004; Henriksen et al., 2011; Love and Wynne-Edwards, 2005; Rubolini et al., 2005; Sheriff et al., 2009; Stead et al., 2022; Zimmer et al., 2013). Additionally, females in lower condition and in lower quality habitats transfer more Cort to their offspring leading to offspring of lower body condition (Bonier et al., 2009; Love et al., 2008; Sheriff et al., 2010) with some studies suggesting this as an adaptive mechanism “matching” phenotypes with the environment (Love and Williams, 2008). Therefore, due to the low quality of food resources in the urban habitat, urban females that have higher circulating Cort concentrations may pass those hormones to their eggs (Love and Williams, 2008). Whether this strategy is adaptive to match urban offspring to their environment cannot be tested in our study but is a promising avenue of future research.

We also found that both urban and rural egg Cort concentrations decreased across the laying sequence. Elevation of egg Cort can alter offspring morphology, physiology and behavior, including lowering mass at hatching, slowing growth, and increasing nestling begging (Bowers et al., 2016; Hayward and Wingfield, 2004; Loiseau et al., 2008; Love and Wynne-Edwards, 2005). Therefore, differences in the hormones deposited in eggs across the laying sequence may affect the disparity of phenotypes and offspring quality based on laying order (Henriksen et al., 2013; Love and Wynne-Edwards, 2005; Saino et al., 2005). Most studies that have investigated Cort concentrations of nestlings do not consider the effect of lay order on hormone concentrations (Hayward and Wingfield, 2004; Ouyang et al., 2019). One other study found that Cort increased across the laying order in European starlings (Sturnus vulgaris), suggesting a brood-reduction strategy (Love et al., 2008), in which later laid eggs exposed to higher maternal Cort may be smaller at hatching and outcompeted by siblings (Love and Wynne-Edwards, 2005). However, in our study, egg size and volume increased with laying order, yet mass-corrected Cort concentrations still decreased. This intra-clutch variation in maternal Cort suggests that house wren females may be physiologically adopting the brood-survival strategy.

This difference in egg Cort parallels the differences observed in offspring Cort levels between urban and rural sites and follows the pattern of the maternal Cort phenotypes of each location. Across multiple ontogenetic stages (adult, egg, and nestling), urban individuals had higher Cort than their rural counterparts (Figure S2). Specifically at day 12, urban nestlings had higher Cort, suggesting their phenotype may be related to the maternal phenotype and investment (Hayward and Wingfield, 2004; Sheriff et al., 2010). Previously, we found that hormone levels already differ at day 0 for nestling house wrens (Ouyang et al., 2019) which may be attributed to hormone-mediated maternal effects. This elevation of glucocorticoids can have significant influences on offspring phenotype and may aid them in unpredictable environments. For example, pre-hatching Cort treatment increased risk-taking behavior in a novel environment, resulting in higher food acquisition in Japanese quail (Coturnix japonica) (Zimmer et al., 2013). Additionally, house wren offspring hatched from mothers with experimentally elevated Cort, had increased recruitment probability when reared by experimental mothers compared with control mothers, showing environmental/maternal matching (Weber et al., 2018). Therefore, urban mothers may be depositing more Cort (either passively or actively) that may increase offspring fitness in an urban, food-limited environment.

Moreover, variation in offspring Cort levels were higher at the urban site than at the rural site. When including a continuous urbanization index (urban density), we find that urban individual Cort levels were positively correlated with urban density. This shows that urban areas are more heterogeneous than rural sites with more variation in environmental urban indices and may be the reason why we do not see a correlation in rural offspring. Furthermore, this finding contributes evidence for the hypothesis that urban areas may increase phenotypic variation due to environmental heterogeneity (Thompson et al., 2021).

4.2. Testosterone concentrations across the laying sequence

We did not find a difference in T levels between urban and rural eggs. In the one other study that investigated egg hormone concentrations in response to urbanization, they found that urban eggs had lower T concentrations compared to forest eggs, but only in female embryos (Partecke et al., 2020). Our study is limited in that we did not sex our embryos so this trend may likely have been missed. As we have not measured T in adults in our study, we cannot draw conclusions about maternal transfer of this hormone. However, we observed a decrease in egg T across the laying sequence, which suggests a decrease in maternal deposition of this hormone over the laying order. As maternal T has been shown to enhance offspring fitness through increasing growth and competitive abilities (Groothuis et al., 2005; Groothuis and Schwabl, 2008) with increasing levels across the laying sequence benefiting later laid eggs (Hsu et al., 2016; Reed and Vleck, 2001; Schwabl, 1993), this trend may suggest a reduction of T across the laying sequence leads to brood reduction (Schwabl et al., 1997). We did find an increase in T levels as the breeding season progressed, which suggests that females may be investing more in young during times of lower food abundance to ensure the survival of their offspring. As egg T and Cort levels were not correlated in eggs, it could be that the brood strategy differs based on the hormone and its effects (Groothuis et al., 2005; Love et al., 2008; Schwabl, 1993).

4.3. Egg and nestling morphology

Like other studies before, we found that egg mass and volume increased over the laying sequence (Ardia et al., 2006; Soma et al., 2007; Styrsky et al., 2002). As house wrens are altricial, hole-nesting species, they likely adopt a “brood-survival strategy” when it comes to laying, offering higher investment for later-laid eggs so that they can compete with first-born offspring (Slagsvold et al., 1984). In our study, we found a significant interaction between site and lay order, suggesting that the strategy might differ for urban vs rural parents. Rural mothers seem to be following the brood-survival strategy as their eggs continued to increase in size and mass over the lay sequence. However, urban mothers started the laying-sequence with increasing egg size and mass, but this effect leveled out by egg four. This change in urban mothers could represent a resource constraint, physiological consequence, or a shift to an adaptive strategy. Urban mothers could be food limited as insect biomass is lower at urban sites (Baldan and Ouyang, 2020; Seress et al., 2018) and unable to add more substance to their later laid eggs. Additionally, elevated Cort of urban mothers could be reallocating resources in the eggs, leading to lighter egg masses and ultimately, reduced nestling masses (Henriksen et al., 2013). Alternatively, but not mutually exclusive, this pattern could be an adaptive strategy towards brood-reduction in resource-limited urban environments, such that only the most competitive offspring survive (D’Alba and Torres, 2007; Forbes and Mock, 2016).

We had expected that differences in maternal investment would relate to offspring fitness in terms of growth (Hayward and Wingfield, 2004; Love and Wynne-Edwards, 2005). For example, Strange et al found that in house wren nestlings hatched from corticosterone-injected eggs were lighter than controls (2016). However, we found no differences between urban and rural nestlings. As we removed up to 3 eggs from each nest, the parental effort to raise the brood was reduced. Therefore, it is likely that all parents, even in food-limited urban areas, were able to raise their offspring such that offspring growth and morphology did not differ between sites. We note that when broods are not experimentally reduced, we found that urban nestlings do have lower mass at fledgling, perhaps due to the smaller egg sizes and/or increase in maternal Cort levels at urban sites (Baldan and Ouyang, 2020) which are mirrored in other species and cities (Meillère et al., 2015). Additionally, we found that across both urban and rural environments nestling body condition decreased throughout the season matching the decline of food abundance as the breeding season progresses in both environments (Baldan and Ouyang, 2020; Seress et al., 2018).

4.4. Conclusion

Our study helps open the investigation of maternal investment strategies between urban and rural parents. We showed that across egg, offspring, and adult female glucocorticoid phenotypes, Cort was elevated in the urban environment. Whether these phenotypes are matched to their environment is the next step in evolutionary physiology. As we show that urbanization can have profound effects on offspring development, hormone-mediated maternal effects likely play a key role in adaptively shaping urban phenotypes.

Supplementary Material

supplementary materials

Acknowledgements

We thank Ryan Fung, Valentina Alaasam, and Avery Grant for valuable field assistance. We thank the Caughlin Ranch HOA for use of the land for nest boxes. We are grateful to Lora Richards for the use of her lab and equipment for egg hormone extractions.

Funding

JQO is funded by the National Science Foundation (OIA-1738594) and the National Institute of Health (P20 GM103650).

Footnotes

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Appendix A. Supplementary material

Supplementary data to this article can be found online at http://doi.org/10.1016/j.ygcen.2022.114166.

Data availability

All scripts and data used for this manuscript are available on GitHub at: https://github.com/JenniferJHeppner/Urban_maternal_hormone_transfer. Inquiries can be directed to the corresponding author.

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Associated Data

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

Supplementary Materials

supplementary materials
NIHMS1972362-supplement-supplementary_materials.pdf (387KB, pdf)

Data Availability Statement

All scripts and data used for this manuscript are available on GitHub at: https://github.com/JenniferJHeppner/Urban_maternal_hormone_transfer. Inquiries can be directed to the corresponding author.

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