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. Author manuscript; available in PMC: 2022 Jul 6.
Published in final edited form as: Ibis (Lond 1859). 2021 Feb 5;163(3):977–989. doi: 10.1111/ibi.12935

Sex ratio of Western Bluebirds Sialia mexicana is mediated by phenology and clutch size

ANDREW W BARTLOW 1,*, MARK D JANKOWSKI 2, CHARLES D HATHCOCK 3, RANDALL T RYTI 4, STEVEN L RENEAU 5, JEANNE M FAIR 1
PMCID: PMC9257600  NIHMSID: NIHMS1820450  PMID: 35801167

Abstract

Mothers may produce more of one sex to maximize their fitness if there are differences in the cost of producing each sex or there are differences in their relative reproductive value. Breeding date and clutch size are known to influence offspring sex ratios in birds through sex differences in dispersal, social behaviours, differential mortality, and available food resources. We tested if breeding date, clutch size and drought conditions influenced offspring sex ratios in a sexually size-monomorphic species, the Western Bluebird, by interrogating a 21-year dataset. After controlling for differential mortality, we found that hatch dates late in the breeding season were associated with the production of more females, suggesting that the value of producing males declines as the breeding season progresses. When clutch size was taken into account, small clutches yielded significantly more females late in the breeding season compared to the early and middle parts of the breeding season that produced significantly more males. Large clutches early in the season tended to produce more females, although this was not significant. Drought severity was not correlated with sex ratio adjustment. We propose and discuss several explanations for these patterns, including male offspring, but not female offspring, acting as helpers, increased female nestling provisioning late in the breeding season, differences in food abundance, and egg-laying order. Future work will help to uncover the mechanisms leading to these patterns. Identifying patterns and mechanisms of sex ratio skew from long-term datasets is important for informing predictions regarding life-history trade-offs in wildlife populations.

Keywords: breeding date, long-term study, parental investment, sex allocation

Variation in offspring sex ratio in wildlife populations has been of great interest for understanding parental investment and sex allocation (Mayr 1939, Trivers & Willard 1973, Sheldon 1997, Nager et al. 1999). If the costs and benefits of producing sons and daughters are equal, then even (i.e. 50:50) sex ratios should be expected. However, often the costs and benefits of producing different sexes are not equal, and mothers should adjust sex ratios according to factors that influence the relative reproductive value of each sex. The advantage of producing sons or daughters may vary when there are differences in the cost of producing different sexes or there are differences in their relative fitness (Wright et al. 1988). Therefore, mothers may modify sex ratios to maximize their own fitness by producing more offspring of one sex (Trivers & Willard 1973, Nager et al. 1999).

One set of factors used to test and explain adaptively skewed sex ratios are differences in parental quality, which includes maternal body condition (Trivers & Willard 1973, Nager et al. 1999) and paternal attractiveness (Ellegren et al. 1996). A second set of factors known to cause skewed sex ratios is ecological. These include differences in dispersal between sexes (Gowaty 1993), differences in social behaviours (e.g. helping behaviours; Emlen et al. 1986, Komdeur et al. 1997), differences in breeding opportunities (Clutton-Brock 1986, Dijkstra et al. 1990, Krebs et al. 2002), and food availability (Myers 1978). For example, when sexes differ in dispersal from the natal area, sex ratios should be biased towards the non-philopatric (dispersing) sex to reduce competition with parents (Clark 1978, Gowaty 1993). This idea has been termed the local resource competition hypothesis (LRC; Clark, 1978). Under periods of unfavorable conditions, such as drought, LRC predicts the non-philopatric sex will be favored due to diminished food resources (Gaughwin et al. 2020). In cooperatively breeding species in which some helpers help at their parents’ nests, there should be a bias towards the helping sex (e.g. helping behaviours; Emlen et al. 1986). This would make the reproductive value of the helping sex higher than the non-helping sex because they ‘repay’ the cost of their production (Emlen et al. 1986). This is called the repayment hypothesis (reviewed in Khwaja et al. 2017) or local resource enhancement (LRE; Gowaty, 1993).

The time of breeding in the breeding season is known to influence offspring sex ratios (Clutton-Brock 1986, Dijkstra et al. 1990, Smallwood & Smallwood 1998, Krebs et al. 2002, Velando et al. 2002, Eraud et al. 2006). For example, mothers may overproduce the more costly sex (in sexually size dimorphic species) during periods of high food availability (Myers 1978, Dijkstra et al. 1990, Appleby et al. 1997). Mothers may also adjust offspring sex ratios throughout the breeding season because of helping behaviours (LRE) and differential dispersal (LRC) (Stamps 1990, Gowaty 1993, Koenig & Dickinson 1996). The helping sex may be overproduced early in the breeding season, especially if they can help their parents with a second breeding attempt during the same season. In periods of high food abundance (which can change throughout the breeding season and with environmental conditions, such as drought), the philopatric sex should be favored (Clark 1978, Eraud et al. 2006). Alternatively, Koenig and Dickinson (1996) proposed that more of the non-philopatric sex should be produced later in the breeding season if food availability improves and parental provisioning increases the body condition of nestlings for dispersal (Stamps 1990).

Clutch size has been shown to be correlated with sex ratio adjustment in some species. Large and small clutch sizes can show different responses in the proportion of male and female offspring produced as the breeding season progresses (Saino et al. 2008). Saino et al. (2008) found an interaction between clutch size and hatch date of Barn Swallows Hirundo rustica, such that in large clutches, males increased throughout the breeding season. In small clutch sizes, there were more females as the season progressed. Body condition of females may explain these patterns, especially if body condition decreases throughout the breeding season (Velando et al. 2002) or if females manipulate the position of males and females in the egg-laying order (Krebs et al. 2002, Moreno-Rueda et al. 2016, Navara 2018).

Most studies on sex ratio adjustment deal with sexually size-dimorphic species, in which one of the sexes is larger and more costly to produce. Fewer studies have addressed sex ratio skew in sexually size-monomorphic species, especially in the context of sex ratio skew throughout the breeding season. Studies addressing breeding date (i.e. laying date or hatch date) in species with little to no sexual size dimorphism have shown mixed results. For example, Cepková et al. (2020) and Que et al. (2019) found no variation in sex ratios throughout the breeding season. In contrast, two studies examining seasonal variation in sex ratios showed opposite results of sex ratio skew, one showing more females in Spotless Starling Sturnus unicolor broods (Cordero et al. 2001) and the other showing more males in Eurasian Skylark Alauda arvensis broods produced early in the breeding season (Eraud et al. 2006). Furthermore, most studies on sex ratio adjustment record sex ratios over one or a few breeding seasons and suffer from small sample sizes, making more broadly applicable conclusions difficult to reach (Koenig & Dickinson 1996, West & Sheldon 2002). Here, we determine if the timing of breeding, clutch size, and/or drought stress affect the sex ratios of Western Bluebirds Sialia mexicana by interrogating a 21-year dataset. We also document the variation in offspring sex ratios and look for sex ratio differences among years.

Western Bluebirds are sexually dimorphic in plumage colouration, but monomorphic in body size in our population both as 5-day old nestlings (mean ± SD) (males: 12.24g ± 2.30, n = 108; females: 12.11g ± 2.25, n = 133; t = −0.45, P = 0.66] and as adults (males: 24.7g ± 3.18, n = 59; females: 24.1g ± 3.76, n = 86; t = −1.01, P = 0.31; J.M. Fair unpubl. data). Males are the philopatric sex and breed near their natal area, while females disperse to new populations (Koenig & Dickinson 1996). Males are also helpers at their parents’ nests, even as juveniles in a second brood of the same year (Dickinson et al. 1996, Dickinson & Akre 1998, Dickinson 2004, Jacobs et al. 2015). A small percentage of juvenile helpers are females, but the majority (> 85%) have been shown to be males (Dickinson et al. 1996). This may give males a higher reproductive value since the cost of producing males may be offset by them helping to rear their siblings (Emlen et al. 1986). Additionally, drought stress is known to decrease the body condition of adult and nestling bluebirds in our study area, most likely through a reduction in food availability (Fair & Whitaker 2008). We hypothesize that male-biased sex ratios will be produced early in the breeding season because they can be helpers later in the same breeding season. We also hypothesize that clutch size will be important in determining sex ratio bias throughout the breeding season, such that small and large clutches will show different patterns. Specifically, we predict large clutches should consist of more males throughout the breeding season and in small clutch sizes, we predict more females as the season progresses. We also test the hypothesis that drought conditions should result in more of the non-philopatric sex (females), potentially due to reduced food availability. We test these hypotheses by analyzing a dataset from 1997 to 2017 (inclusive) in which 2965 Western Bluebird nestlings from 735 broods were sexed.

METHODS

Study site and study species

This study was conducted on Los Alamos National Laboratory (LANL) and surrounding areas located in north-central New Mexico. The 111 km2 LANL property is located on the Pajarito Plateau. Narrow mesas separated by deep, steep-sided canyons decline from the Jemez Mountains to the Rio Grande River and include both canyon and mesa-top habitats. The Pajarito Plateau is comprised of larger canyon systems that originate on U.S. Forest Service land in the Jemez Mountains. Smaller canyon systems originate within LANL boundaries and extend eastward to the Rio Grande or to confluences with the larger canyon systems. The canyon systems are separated geographically from each other and result in 12 different watersheds. The canyon floors are typically flat and the sides of the canyons are rocky and partially covered by trees.

Juniper Juniperus monosperma-savanna community is found along the Rio Grande on the eastern border of the plateau and extends upward on the south-facing sides of canyons at elevations between 1700 and 1900 m. Piñon-juniper habitat, made up of Piñon Pine Pinus edulis and Juniper Juniperus monosperma is generally between 1900 to 2100 m in elevation, covering large portions of the mesa tops and south-facing slopes at lower elevations. Ponderosa Pine Pinus ponderosa communities are found in the western portion of the plateau between 2100 and 2300 m in elevation. The majority of the nestboxes were located in the piñon-juniper, Ponderosa Pine, mixed conifer habitats, and riparian habitats.

The Western Bluebird is a widely distributed, sexually dimorphic (in plumage colouration) and a monogamous species that nests in secondary nest cavities (Jacobs et al. 2015). It is insectivorous primarily during the breeding season (Guinan et al. 2020). In this study area, they are facultative migrants, with some individuals remaining in the area during winter months, especially during warmer or less severe winters (Fair & Myers 2002). The Western Bluebirds on the Los Alamos study area have a relatively small home range of approximately 6000 m2 delineated within a watershed (Colestock 2007).

Field methods

During the winter of 1997, 450 nestboxes were placed on LANL property. Nestboxes were added in new watersheds over the years through 2017, resulting in over 800 nestboxes (see Musgrave et al. 2019 for a map of study site and nestbox locations). Nestboxes were placed approximately 2 m off the ground on Ponderosa Pine and Piñon Pine trees and spaced approximately 50 to 75 m apart, spanning an elevation gradient from 1890 to 2305 m.

Starting in April of each year, nestboxes were visited and nests with eggs were considered active and consequently visited weekly until the first eggs hatched (day = 0) and nestlings fledged (day = 17–21). Hatch date and clutch size (i.e. number of eggs laid) were recorded for each nest. Data were collected for each breeding season (April to August) from 1997 through 2017 (inclusive). Only nests with clutch sizes of three or more eggs were included in the current analysis. The modal clutch size of Western Bluebirds is five eggs (With & Balda 1990, Guinan et al. 2020). Nests with one or two eggs are outliers and are likely the result of partial predation or are non-viable eggs, which mostly occurs very early or very late in the breeding season. We discarded two broods that had a clutch size of two eggs.

Nestling sex was determined by plumage colour identification of nestlings that were 12 days or older by the amount of blue on the wing and tail (Pyle 1987, Koenig & Dickinson 1996, Dickinson 2004). This technique was verified as a reliable method of sexing in our population (J.M. Fair unpubl. data). Here, sex ratios most closely match tertiary sex ratios, which is the sex ratio when nestlings are no longer dependent on their parents (Gowaty 1993), since bluebird nestlings begin fledging around day 17. Some nestlings died, were depredated, or fledged before they could be sexed. Only the first breeding attempts in nestboxes were used because only approximately 5% of the nests in the nestboxes have double broods (Jacobs et al. 2013). In this study, 15 (2.0%) broods were considered a second brood by the same female and were removed from this analysis. Sex ratios of broods were calculated as the percentage of nestlings that were male.

Palmer Drought Severity Index

The Palmer Drought Severity Index (PDSI) is a measure of the relative moisture content in the environment (Palmer 1965). It is based on temperature and precipitation in an area and takes the previous month’s conditions into account. High values are considered moist years, while low values indicate greater drought severity. We obtained monthly PDSI values specific to the Northern Mountains (Climate Division 2) in New Mexico from NOAA National Centers for Environmental Information (https://www.ncdc.noaa.gov/cag/divisional/). For each brood, we used the monthly PDSI value for the month in which eggs hatched.

Data analysis

The following analyses were carried out using the software R ver. 3.6.1 (R Core Development Team 2019). Generalized linear mixed models (GLMMs) were used throughout and completed using the lme4 ver. 1.1.21 (Bates et al. 2015) and lmerTest ver. 3.1.0 (Kuznetsova et al. 2017) packages. Because we were interested in sex ratios at the parental and population levels, analyses were performed on broods and individual nestlings. Only broods with complete data on hatch date and clutch size were included in these analyses. We discarded data for 58 nestlings from 17 broods over the 21-year period because of incomplete data.

We tested for differences in offspring sex ratios among years using a GLMM with a binomial distribution and a logit link (Krackow & Tkadlec 2001). This approach was followed by completing a Wald test to test the significance of the main effect for this multilevel factor variable. The binomial response variable was a matrix of two vectors: the number of male and of female offspring within a brood (Wilson & Hardy 2002). Year was the fixed effect and watershed was set as the random effect to control for slight uncontrolled variation in sex ratio among watersheds. To assess the offspring sex ratio of the population each year, two-tailed binomial tests were run on each year separately. We compared P-values to both a Bonferroni corrected alpha level of 0.002 due to multiple tests and an alpha level of 0.05, as has been recently suggested (VanderWeele & Mathur 2019).

We used GLMMs with binomial distributions and logit links to test if hatch date, clutch size, and/or PDSI predicted offspring sex ratio. Brood was the unit of analysis. Hatch date was a continuous variable in these models. Our first analysis used all nestlings sexed (n = 2965) from 735 broods. There were 526 nestlings (15.1%) out of a possible 3491 (based on clutch size) that were not sexed either because they did not hatch, died, or fledged before they could be sexed. To test whether the missing nestlings and therefore differential mortality, could explain our results, we re-ran the analysis using only broods in which all nestlings were sexed (n = 391 broods and 1839 nestlings) to see if our results remained the same. In these broods, clutch size was equal to the number of nestlings sexed. The model selection procedure, described below, was used for both analyses.

Model selection was performed using the dredge function in the MuMIn package ver. 1.43.6 (Barton 2019) using the data described above. The binomial response variable was the number of male offspring and the binomial denominator was the number of nestlings that were sexed. Year was included as the only random effect (watershed and box identity explained very little variation and were not included as random effects). Each global model included hatch date (continuous variable), clutch size, the interaction between hatch date and clutch size, and PDSI. We included the interaction between hatch date and clutch size in these models because it has been shown to be important in sex ratio skew in Barn Swallows Hirundo rustica (Saino et al. 2008). These predictor variables were standardized using the standardize function in the arm package ver. 1.10.1 (Gelman & Su 2018) to make parameter estimates easier to interpret and to help with model convergence. The best model was determined by ranking candidate models by corrected Akaike Information Criteria (AICc). Models with delta AICc values greater than two were considered significantly different models (Burnham & Anderson 2002). Model weights, taking into account all candidate models are also reported along with the results of the top model. The fixed effects with 95% confidence intervals not crossing zero were considered important.

To further investigate the best predictor variables (hatch date and clutch size), we used binomial GLMMs with the same specifications as above. We ran GLMMs between sex ratios and hatch date in three different groups based on clutch size: small clutches (3 and 4 eggs), medium clutches (5 eggs) and large clutches (6 and 7 eggs). For these analyses, we evaluated significance at an alpha level of 0.05.

We also split broods into three groups based on when they hatched in order to account for non-linear changes throughout the breeding season. For these additional binomial GLMMs, the hatch date variable was categorical. Broods were generally split by the month in which they hatched. Broods that hatched in April (n = 4) were included in May and one brood that hatched in August was included in July. We used all nestlings sexed (n = 2965) from the 735 broods. In addition to analyses at the brood level, we analyzed the sex ratio of individual nestlings using binomial tests. Specifically, we determined whether the ratios of nestlings produced during a given time period and/or clutch size group significantly differed from a 50:50 ratio. For these analyses, we evaluated significance at an alpha level of 0.05.

RESULTS

We analyzed sex ratios of 2965 nestlings from 735 broods and 383 nestboxes from 1997 to 2017 (inclusive). The mean nest offspring sex ratio over the whole 21-year period was 50.3% (male). The frequency of sex ratios throughout the entire time period is shown in Figure 1a. The sex ratio of broods significantly differed among years (Wald test: X2 = 34.82, df = 20, P = 0.02; Fig. 1b). There were no significant deviations in the sex ratio of individual nestlings during any year after comparing P-values to a Bonferroni corrected alpha level of 0.002. However, two years were significant when compared to an alpha level of 0.05 (2008: P = 0.004; 2009: P = 0.014). These years were both male-biased (2008: 61.0% males, n = 42 broods; 2009: 58.7% males, n = 53 broods).

Figure 1.

Figure 1.

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(a) Histogram of Western Bluebird sex ratios throughout the study period (1997 to 2017) in northern New Mexico, USA. (b) Mean proportion (± 1 SE) of males in bluebird broods each year from 1997 to 2017. Numbers above the bars are the number of broods sampled each year. The dotted red line indicates a 50% sex ratio. Sex ratios greater than 50% have more males, while less than 50% have more females. There were 2965 nestlings from 735 total broods. None of the years deviated from 50:50 based on two-tailed binomial tests and a Bonferroni corrected alpha of 0.002.

The top model predicting sex ratio included hatch date, clutch size, and their interaction (Table 1). The other models were greater than 2 delta AIC units from the top model. Each term was important based on the 95% confidence intervals not crossing zero (Table 2). The Palmer Drought Severity Index was not in the top model, but it was in the second ranked model. However, in this model, PDSI was not important (GLMM: estimate = 0.009, SE ± 0.099, z = 0.089, P = 0.93 [95% CI: −0.19 – 0.21]). Hatch date and clutch size both had negative estimates. Fewer eggs laid was correlated with a greater proportion of males being produced; larger numbers of hatched eggs were more even in terms of sex ratio or produced a greater proportion of females. In terms of hatch date, birds breeding and hatching earlier had a higher proportion of male offspring compared to birds that bred and hatched later in the breeding season. The interaction between hatch date and clutch size was also important and had a positive estimate. As hatch date increased (i.e. later hatch dates), the coefficient of clutch size on sex ratio increased. We found that large clutch sizes are not associated with comparatively more females later in the breeding season.

Table 1.

The top five models ranked by AICc for predicting offspring sex ratios of Western Bluebirds using binomial GLMMs in northern New Mexico, USA from 1997 to 2017. Hatch date was a continuous variable and year was the random effect in these models.

Parameters in model AICc delta AICc Model weight
Hatch date * clutch size 2032.3 0.00 0.70
Hatch date * clutch size + PDSI 2034.3 2.03 0.26
Hatch date + clutch size 2039.4 7.12 0.02
Hatch date + clutch size + PDSI 2041.4 9.14 0.01
Clutch size 2041.8 9.49 0.01
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Table 2.

Parameter estimates of the top ranked GLMM from Table 1 predicting offspring sex ratio of Western Bluebirds in northern New Mexico, USA from 1997 to 2017. C.I. stands for confidence interval. Year was the random effect and hatch date was a continuous variable. The fixed effects with 95% confidence intervals not crossing zero were considered important.

GLMM with a binomial distribution for brood sex ratio
Random effect Variance Standard deviation
Year 0.024 0.15
Fixed effects Estimate Standard value z-value 95% C.I.
Intercept 0.065 0.05 1.20 − 0.04 – 0.18
Hatch date − 0.17 0.08 − 2.19 − 0.33 – − 0.02
Clutch size − 0.18 0.08 − 2.38 − 0.34 – − 0.03
Hatch date * clutch size 0.37 0.12 2.98 0.13 – 0.62
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To untangle and illustrate these interaction results between clutch size and hatch date, we analyzed sex ratios throughout the breeding season separately in three different clutch size groups. We found that in small clutches (3 and 4 eggs), males significantly decreased as hatch date increased (Binomial GLMM: coefficient = −0.21 ± 0.08, z = −2.64, P = 0.008; Fig. 2a). Medium clutches (5 eggs) did not significantly differ throughout the breeding season (Binomial GLMM: coefficient = −0.073 ± 0.05, z = −1.53, P = 0.13; Fig. 2b). Large clutches (6 and 7 eggs) increased in the number of males throughout the breeding season, but not significantly (Binomial GLMM: coefficient = 0.26 ± 0.15, z = 1.77, P = 0.076; Fig. 2c).

Figure 2.

Figure 2.

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Mean proportion of male offspring according to hatch date for (a) small clutch sizes, (b) medium clutch sizes, and (c) large clutch sizes. Means were calculated after broods were aggregated by hatch date. Regression lines are from a linear model between hatch date and mean proportion of males. The dotted red lines indicates a 50% sex ratio. Sex ratios greater than 50% are male-biased and those less than 50% are female-biased. Small clutch sizes became significantly less male throughout the breeding season.

For the broods where all nestlings were sexed (n = 391 broods and 1839 nestlings), we largely found the same results. The top model was the interaction between hatch date and clutch size. Hatch date and the interaction between hatch date and clutch size were important based on the 95% confidence intervals of the estimates (hatch date: [−0.42 to −0.02]; hatch date*clutch size: [0.12 to 0.72]). Clutch size was not important in the top model (95% C.I.s [−0.39, 0.007]). Similar results were found with PDSI; PDSI was not in the top model and was not important in the second ranked model.

To further examine hatch date to account for non-linear changes throughout the breeding season, we split broods (n = 735) into three groups based on when they hatched (28 April to 31 May; 1 June to 30 June; and 1 July to 3 August), which was approximately at monthly intervals (hereafter, groups will be referred to as ‘May’, ‘June’, and ‘July’). We found a significant difference among these groups (Wald test: X2 = 6.12, df = 2, P = 0.047; Fig. 3a). We found that broods that hatched in July produced significantly more females than broods hatching in May (GLMM: estimate = 0.35, SE ± 0.15, z = 2.31, P = 0.02) and June (GLMM: estimate = 0.35, SE = ± 0.15, z = 2.42, P = 0.02). Broods hatching in May and June were not significantly different (GLMM: estimate = −0.002, SE = ± 0.09, z = −0.025, P = 0.98; Fig. 3a). Sample sizes shown in Figure 2 are number of broods.

Figure 3.

Figure 3.

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(a) Mean proportion of Western Bluebird males (± 1 SE) in broods according to the month of hatching in northern New Mexico, USA from 1997 to 2017. There was a significant difference among groups (different letters indicate significance at a significance level of P = 0.05). Sample sizes (n) are the number of broods. Dotted red line indicates 50% sex ratio. Sex ratios greater than 50% are male-biased and those less than 50% are female-biased. (b) Mean proportion of bluebird males (± 1 SE) in broods according to the month of hatching separated according to clutch size. Numbers next to boxes are the number of broods in each clutch size group. Dotted red line indicates 50% sex ratio. Sex ratios greater than 50% are male-biased and those less than 50% are female-biased.

The sex ratio of the individual nestlings that came from broods that hatched in May was 51.4% male (465/905). This did not significantly differ from 50:50 (two-tailed binomial test: P = 0.43). The sex ratio of the individual nestlings that came from broods that hatched in June was 50.7% male (932/1838), which also did not significantly differ from 50:50 (two-tailed binomial test: P = 0.56). The sex ratio of the individual nestlings that came from broods that hatched in July was 42.8% male (95/222). This was significantly different from 50:50 (two-tailed binomial test: P = 0.037).

The interaction between hatch date and clutch size in the original GLMM (with hatch date as a continuous variable) suggested that the pattern of sex ratio throughout the breeding season depends on the number of eggs laid. We split broods according to the clutch size (3- and 4-egg clutches, 5-egg clutches, and 6- and 7-egg clutches). The 3- and 4-egg clutch group and the 5-egg clutch group showed similar patterns with hatch date; broods hatching in July had more females than the other two hatch date groups (Fig. 3b). However, this pattern did not hold for birds that produced clutches with 6 or more eggs (Fig. 3b). For these large clutches, comparatively more females were produced early in the breeding season. Switching from producing more males to more females was most pronounced in clutches containing 3 and 4 eggs. In these small broods that hatched in May and June, nestlings were 56.0% male (350/625), which was significantly different from 50:50 (two-tailed binomial test: P = 0.003). In June alone, small broods were significantly male-biased (252/444; two-tailed binomial test: P = 0.005). However, in July, nestlings from small broods were only 40% male (44/110), which also significantly differed from 50:50 (two-tailed binomial test: P = 0.04).

DISCUSSION

Offspring sex ratios can be adaptively skewed by mothers in response to a variety of factors, such as parental quality (i.e. body condition), ecological and environmental factors and social behaviours (Ankney 1982, Wright et al. 1988, Cockburn & Double 2008, Saino et al. 2008, Darolová et al. 2009). Our goal was to determine if offspring sex ratios of a sexually size-monomorphic species are influenced by breeding date, clutch size, and/or drought severity. Using a large, long-term dataset of Western Bluebird broods, we found that hatch date and clutch size were significant in explaining variation in offspring sex ratios.

There was a positive interaction between hatch date and clutch size. Large clutches did not follow the pattern of the fewest males being produced later in the breeding season. Large clutches in May tended to produce female nestlings, although this did not significantly differ from 50:50. A larger sample size of large clutch size sex ratios in May could provide more evidence of this pattern. We only had 14 broods with six or seven eggs in May, which makes interpretation of this pattern difficult. Switching from producing more males to more females was most pronounced in clutches containing three or four eggs. In these clutches, offspring were male-biased in the early and middle of the breeding season and female-biased late in the breeding season, similar to another study on Barn Swallows Hirundo rustica (Saino et al. 2008). It is unclear why small and large clutches showed different patterns. Differences may include diet quality (Arnold et al. 2003), egg investment (English et al. 2014), and egg-laying order (Ankney 1982, Dijkstra et al. 1990, 2010, Krebs et al. 2002, Song et al. 2019, Tschumi et al. 2019).

Although nestling mortality cannot explain the interaction between hatch date and clutch size, it may explain the negative effect of clutch size on sex ratios. Clutch size did not have an effect on sex ratios in the truncated dataset in which all nestlings were sexed (n = 391 broods). Early mortality of female nestlings may explain the correlation that was found using the full dataset between fewer eggs laid and a higher proportion of males. Ruling out differential mortality, based on similar results between the full and truncated datasets, egg-laying order and female manipulation of the sex of first laid chicks could explain the interaction results (Moreno-Rueda et al. 2016, Tschumi et al. 2019). This manipulation would be more pronounced in small clutches than in large clutches, which is what our results show. If males are laid first in the early part, but not the later part of the breeding season, then this would align with our results of more females in small clutches at the end of the breeding season and more males in small clutches at the beginning of the breeding season. At the end of the season, males would only be produced in larger clutches the majority of the time. Similar to our results, Velando et al. (2002) showed that broods of European Shags Phalacrocorax aristotelis were also male-biased in the early part of the breeding season and female-biased late in the season. Chicks from first-laid eggs were male in early broods, but female in later broods. Following up on which sex is laid first at different times of the breeding season will allow us to determine whether manipulation of sexes in the laying order plays a role in the patterns of sex ratio skew observed here.

The timing of reproduction during a breeding season has been shown to cause deviations from 50:50 sex ratios in other bird species (Dijkstra et al. 1990 [Common Kestrel Falco tinnunculus], Smallwood & Smallwood 1998 [American Kestrel Falco sparverius], Krebs et al. 2002 [Crimson Rosella Platycercus elegans], Husby et al. 2006 [House Sparrow Passer domesticus]). In a similar study, Koenig and Dickinson (1996) found that offspring sex ratios of Western Bluebirds in California did not change throughout the breeding season, opposite of our results. Using a larger dataset, we found that sex ratios were slightly skewed toward males in the early and middle parts of the breeding season, although this was not significant, and females during the end of the breeding season. Producing fewer males towards the end of the breeding season suggests that the profitability of males declines as the breeding season progresses. Both male and female bluebirds breed during their second year, but males can act as helpers in the nests of their parents (supporting LRE) in our population (Jacobs et al. 2015). Males are also known to help their parents with a second brood during the same year (Dickinson et al. 1996, Dickinson & Akre 1998). Therefore, males would be less desirable late in the breeding season since they would not be able to be helpers in the same breeding season. Producing females may be more profitable late in the breeding season, especially if food is limited. Even though this is not a widespread pattern in birds (Khwaja et al. 2017), several species overproduce the sex that acts as helpers (Eguchi et al. 2009, Koenig & Dickinson 2016, Preston et al. 2016). However, recent data from a different study system in California show that, in Western Bluebirds, the fitness of nonbreeding helper males and their parents is lower than that of breeding males, suggesting that producing more helper males is not beneficial (Dickinson 2004, Dickinson et al. 2016).

In our population, little information is known regarding natal dispersal and philopatry. However, data from the same study site may provide some insight. As nestboxes were checked, some parents were captured opportunistically, either by obtaining them from the nest or by setting up mist-nets near the focal box. Of 87 birds that were originally ringed as nestlings and returned to the same general area, 70 (80.4%) were male (E.J. Abeyta unpubl. data), suggesting that males are more philopatric than females. An outstanding question in our system that still remains is: do returning males help their parents or do they seek their own territories the following year, either on their own or by inheriting them from their parents or relatives? Knowing this will help narrow down which hypotheses (e.g. LRE, LRC, or nest-site/territory availability) pertain to this study system and which is more likely to explain the observed sex ratio patterns.

Resource availability and LRC may better explain our results of more males early compared to late in the breeding season. If more food is available in the early and middle parts of the breeding season, it is hypothesized to lead to the production of the philopatric sex because resources are not limited and competition with parents would be low. We have no data on food availability throughout the season. Drought severity is a proxy for food availability, but was not correlated with sex ratios. Drought conditions may only be relevant during extreme cases. Food likely decreases throughout the summer regardless of whether an area is wetter or moderately dryer than normal.

Similarly, nest-site/territory availability is hypothesized to lead to more early males. The Early Bird Hypothesis proposes that males produced early in the breeding season have a competitive advantage when choosing nest-sites and territories for the next breeding season (Smallwood & Smallwood 1998). Extending this argument, if nest-sites/territories are more abundant early in the breeding season, mothers should produce a male-biased sex ratio, which would decrease throughout the breeding season as breeding sites diminish in number. Western Bluebirds are able to mate the year after they hatch. Secondary cavity-nesting species, like the Western Bluebird, are limited by the number of available cavities in a given area and may therefore suffer from limited breeding opportunities (Wiebe 2011). Song et al. (2016) found that offspring sex ratios of a secondary cavity-nesting species were male-biased in areas with more nest-sites. However, we doubt that our population is nest-site-limited, since there is a large nestbox network (> 800 nestboxes) in our study area and a low percentage are occupied in any given year. More information regarding resource availability, in the form of food and nest-sites, and whether returning males act as helpers in our study area will help to distinguish among these possible explanations (LRE vs. LRC vs. Early Bird Hypothesis) regarding more males early in the breeding season.

An explanation for more females late in the breeding season is that nestlings in later nests are in higher body condition pre-dispersal (Stamps 1990). This has been hypothesized to lead to more of the non-philopatric sex later in the breeding season (Koenig & Dickinson 1996), which in the case of Western Bluebirds, is females. This could occur if food availability increases throughout the breeding season (Stamps, 1990). This hypothesis seems implausible because food availability most likely diminishes throughout the summer. In the same population of bluebirds (with a much larger number of broods), clutch size decreased throughout the breeding season (Wysner et al. 2019). These patterns may be due to lack of food (Decker et al. 2012), although we have no data on food availability. Future work is needed to quantify food availability at various times of the year to rule out this explanation. This can be achieved by trapping insects, the main summer food source of bluebirds, at various times throughout the summer to quantify their relative abundance (Dunn et al. 2011). Alternatively, supplemental feeding can be used to examine food abundance and sex ratio skew throughout the breeding season by providing food to nestboxes (Récapet et al. 2017).

The pattern of fewer bluebird males late in the breeding season may also occur by male nestlings having higher mortality later in the breeding season rather than the result of mothers adaptively skewing offspring sex ratios. There are two reasons why we do not think differential mortality plays a role in sex ratio adjustment documented here. First, the missing nestlings only constituted 15% of the number of eggs laid. Some of these missing nestlings were most likely depredated, which would occur in equal proportions. Secondly, we found similar results when we analyzed broods in which the clutch size was equal to the number of nestlings sexed (n = 391 broods; 1839 nestlings). In this analysis, the brood sex ratios close to fledging (tertiary sex ratio) were the same as the sex ratio at both hatching (secondary sex ratio) and egg production (primary sex ratio). Therefore, differential mortality cannot explain the patterns observed.

The sex ratio over the whole study period was 50.3% male. Thus, there was no overall sex bias in our population. Years differed significantly, but only two years (2008 and 2009) were significantly male-biased if compared to an alpha level of 0.05 (P = 0.004 and P = 0.014, respectively). We are not sure why these two years were slightly male-biased. Perhaps food was more abundant or environmental conditions were favorable leading to males, the more philopatric sex, being overproduced. In these two years, environmental conditions were normal in terms of drought and moisture availability. Moreover, drought severity did not correlate with sex ratios in our system and did not help to explain any variation as hypothesized. The measure of drought used here, PDSI, was not in the top model that predicted brood sex ratios. This variable was in the second best model, but it was not important. Therefore, we reject our hypothesis that drought stress results in more of the non-philopatric sex (females).

To summarize, hatch date and clutch size were important factors regarding offspring sex ratio adjustment of Western Bluebirds that may have gone unnoticed with a smaller sample size. To our knowledge, this is the longest running dataset on sex ratios in a passerine. Bluebirds offer a highly tractable model system to study natural sex ratio adjustment according to timing of breeding, clutch size, and resource availability. Future work will help to uncover the mechanisms leading to these patterns and will aid in making predictions regarding life-history trade-offs in wildlife populations.

Supplementary Material

Supplemental Material

FUNDING

We thank the following people for assistance in the field: A. Jacobs, K. Burnett, K. Colestock, J. Foxx, D. Keller, L. Maestas, M. Musgrave, E. Phillips, E. Powell, L. Reader, R. Robinson, M. Salazar, A. Sanchez, S. Sherwood, B. Thompson, and S. Whitaker. We are grateful to O. Myers for establishing the avian nest box monitoring network. We also would like to thank the Associate Editor and two anonymous reviewers for their help in improving the manuscript. This research was funded by the Environmental Restoration Program. Los Alamos National Security, LLC, operator of the Los Alamos National Laboratory under Contract No. DE-AC52-06NA25396 with the U.S. Department of Energy and Triad National Security, LLC, current operator of Los Alamos National Laboratory, under Contract No. 89233218CNA000001.

Footnotes

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest. This research does not reflect the official positions and policies of the US EPA. Mention of products/trade names does not constitute recommendation for use by US EPA.

ETHICAL APPROVAL

All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (Animal Care and Use Committee, Los Alamos National Laboratory Institutional #16-70). All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

DATA AVAILABILITY

The data that support the findings of this study are openly available on Dryad at https://doi.org/10.5061/dryad.xwdbrv1ck.

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Supplementary Materials

Supplemental Material
NIHMS1820450-supplement-Supplemental_Material.xlsx (125.7KB, xlsx)

Data Availability Statement

The data that support the findings of this study are openly available on Dryad at https://doi.org/10.5061/dryad.xwdbrv1ck.

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