Within-female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens.

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J Evol Biol. Author manuscript; available in PMC 2016 March 09. Published in final edited form as: J Evol Biol. 2016 March ; 29(3): 602–616. doi:10.1111/jeb.12810.

Within-female plasticity in sex allocation is associated with a behavioral polyphenism in house wrens E. Keith Bowers, Charles F. Thompson, and Scott K. Sakaluk Behavior, Ecology, Evolution, and Systematics Section, School of Biological Sciences, Illinois State University, Normal, IL 61790-4120, USA

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Abstract

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Sex-allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within-individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioral polyphenism in females, and its expression varies with seasonal changes in the environment. Between-nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over-represented in earlier-laid eggs, were in better condition than daughters, which are over-represented in later-laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within-female changes in offspring sex and not by sex-biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.

Keywords

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maternal effect; sex allocation; sibling rivalry; Trivers-Willard; Troglodytes aedon

Introduction Environmental heterogeneity early in life often has a profound effect on fitness in wild populations (Lindström, 1999; Monaghan, 2008; Wilkin & Sheldon, 2009; but see also Drummond & Ancona, 2015). Although environmental conditions outside the nest often

Correspondence: E. Keith Bowers; Behavior, Ecology, Evolution, and Systematics Section, School of Biological Sciences; Campus Box 4120, Illinois State University, Normal, IL 61790-4120, USA. [email protected]; tel: +1 309 438 7804; fax: +1 309 438 3722.

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play a critical role in development, the within-nest environment and interactions among family members can also create phenotypic variation among closely related individuals. In altricial animals, for example, competition among siblings for parental resources affects their morphological development, immune activity, and survival prior to independence, with consequences for subsequent life-history trajectories (Mock & Parker, 1997, 1998; Saino et al., 1997; Stockley & Parker, 2002; Müller et al., 2003; Forbes, 2011).

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Sibling rivalry has probably been best studied in the context of asynchronous hatching of eggs, in which offspring are born into pronounced competitive hierarchies (Mock & Ploger, 1987; Ricklefs, 1993; Mock & Parker, 1997; Smiseth et al., 2007a,b). Hatching asynchrony is common among avian taxa and occurs when several days elapse between hatching of the first and last eggs of a clutch, creating distinct differences in size among siblings after hatching and giving earlier-hatching offspring a pronounced size advantage over their younger siblings (Forbes & Glassey, 2000; Johnson et al., 2009). Not surprisingly, the initial size hierarchy affects the subsequent growth and survival of offspring, with earlier-hatching offspring generally attaining a larger size than their younger siblings (Slagsvold, 1986; Nilsson & Svensson, 1996; Badyaev et al., 2003a,b; Maddox & Weatherhead, 2008; Kontiainen et al., 2010; Merkling et al., 2014). This can favor a bias in parental reproductive allocation toward older offspring with higher reproductive value (Jeon, 2008). In contrast, synchronous hatching also occurs in many species, and occurs when all the eggs of a clutch hatch within a shorter period of time, generally within a day (Clark & Wilson, 1981; Slagsvold & Lifjeld, 1989; Pennock, 1990; Hébert & Sealy, 1992). As a result, siblings within synchronously hatched broods tend to be similar in age, size, and competitive ability. For example, Mock & Ploger (1987) manipulated variation in hatching spans in nests of cattle egrets (Bubulcus ibis) and found that, although mortality of younger nestlings was more common in broods with pronounced hatching asynchrony (hatching spans of 3 days), the intensity of sibling competition was actually greater within synchronously hatched broods as evidenced by increased aggression and reduced growth rates among nestlings (see also Hahn, 1981; Mock & Schwagmeyer, 1990; Stoleson & Beissinger, 1997; Viñuela, 2000; Smiseth & Morgan, 2009). Thus, parental manipulation of hatching spans (i.e., variation in the degree of hatching synchrony of eggs) has important consequences for the social environment and degree of sibling rivalry experienced by their offspring (Forbes, 1993; Carranza, 2004; Jeon, 2008; Bowers et al., 2013b). An important insight that has emerged is that, even if asynchronous hatching produces fewer fledglings than synchronous hatching, hatching asynchrony may still be adaptive if the older siblings have increased post-fledging survival or reproductive success later in life (Amundson & Slagsvold, 1998).

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Recent work suggests that effects of sibling competition on developing offspring can be sexspecific, with one sex being more sensitive than the other to variation in sibling rivalry and the amount of parental resources obtained (Uller, 2006; Bogdanova & Nager, 2008; Rosivall et al., 2010; Bonisoli-Alquati et al., 2011; Komdeur, 2012). Such a situation occurs in the house wren (Troglodytes aedon), as the mass and size of sons is more variable than that of daughters with respect to their position in the age-related competitive hierarchy established by asynchronous hatching (Bowers et al., 2011, 2015a). This increased sensitivity of sons relative to daughters has important consequences for sex-allocation strategies if it is

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associated with sex-differences in survival and future reproduction. For example, if sons are more sensitive to food restriction, then mothers in resource-poor environments may maximize the number of surviving offspring by over-producing daughters (Myers, 1978; Merkling et al., 2012, 2015). Alternatively, if the reproductive success of sons is more variable than that of daughters and more strongly influenced by body condition or the quality of the rearing environment (e.g., Sheldon, 1998; Krist, 2006), then mothers able to produce high-quality offspring might preferentially invest in sons to produce males with high reproductive potential, but invest more heavily in producing daughters when unable to produce high-quality offspring because even low-quality daughters will have higher fitness than low-quality sons (Trivers & Willard, 1973; Clutton-Brock et al., 1984; Cockburn et al., 2002; Bowers et al., 2013a; Booksmythe et al. 2015; but see Leimar, 1996; Hewison & Gaillard, 1999). Indeed, female house wrens hatching their eggs asynchronously, thus creating a competitive advantage for older offspring, over-produce sons among earlier-laid eggs and daughters, which are less sensitive to sibling competition than sons, among laterlaid eggs within clutches (Bowers et al., 2011, 2014a).


Sex-allocation theory assumes a degree of individual plasticity in maternal strategies, allowing females to adjust the sex ratio in relation to varying environmental conditions. However, few studies have investigated how an individual’s strategy changes across different environments and social contexts (but see Martin & Festa-Bianchet, 2011; Baeta et al., 2012; Pryke et al., 2011; Pryke & Rollins, 2012). Here, we examine within-individual, seasonal variation in sex allocation by female house wrens in relation to the degree of hatching synchrony of eggs, and its consequences for offspring condition, recruitment, and reproductive success. First, we explored whether females hatching their eggs synchronously or asynchronously differed in components of investment in young, including clutch size and egg size, and whether offspring condition varied with the timing of breeding and hatching asynchrony. We then determined whether sex ratios changed across reproductive attempts and in relation to hatching asynchrony. Parental investment strategies often vary with the seasonal abundance of arthropod prey (Finke et al., 1987; Pennock, 1990; Styrsky et al., 1999; Barnett et al., 2011). In temperate habitats, prey availability typically declines over the course of summer, with high-quality prey, primarily lepidopteran larvae, most abundant early and least abundant toward the end (Perrins, 1965; Kendeigh, 1979). Thus, we predicted that seasonal variation in hatching asynchrony would be associated with seasonal changes in the sex ratio. Specifically, we predicted that synchronously hatched broods would become progressively female-biased as breeding seasons progressed, but that asynchronously hatched broods would not become as strongly female-biased because they generally contain sons among earlier-laid eggs and daughters among later-laid eggs within clutches (Bowers et al., 2011). Finally, we tested whether differences in offspring condition and synchronous vs. asynchronous hatching influenced their subsequent recruitment and reproductive success, predicting that adults reared in asynchronously hatched broods, particularly males that had a sibling-competitive advantage early in life, would have increased size and reproductive success relative to males reared without a competitive advantage in synchronously hatched broods.


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Materials and methods Study site and species

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We studied a population of house wrens breeding in Illinois, USA (40.665°N, 88.89°W) from 2009-2015. House wrens are secondary-cavity-nesting songbirds with a widespread distribution in the New World (Johnson, 2014), and readily accept nestboxes. Nestboxes (N = 820; see Lambrechts et al., 2010 for details on nestbox construction and dimensions) were distributed at a density of 5.4 boxes/ha in secondary deciduous forest. Clutch sizes typically range from four to eight eggs. Only females incubate the eggs and brood nestlings, but both parents feed young after hatching, and fledging occurs 14-16 d post-hatching (Bowers et al., 2013b; 2014b). Males are highly territorial, with heavier, larger, and more attractive males typically out-competing others for breeding territories and mates and having increased reproductive success (Johnson & Kermott, 1990; DeMory et al., 2010; Bowers et al., 2015a,b). General procedures From May-August, we checked nestboxes at least twice weekly for evidence of female settlement. After egg laying was complete and females commenced full incubation (eggs warm to the touch), we captured, measured, and banded females with a numbered, aluminum U. S. Geological Survey leg band. We captured females and males mid-way through the incubation period either by capturing them inside their nestbox or using mist nets outside the nestbox. Males received three additional colored leg bands arranged in a unique combination so they could be identified visually without being recaptured (males are more difficult to capture than females).


In 2009, we visited nests multiple times daily during hatching to document the span of time that elapsed between hatching of the first and last eggs of a clutch, which shows a strongly bimodal distribution (Bowers et al., 2011). In subsequent years (2010-2013), we visited nests once daily when hatching was expected to classify broods as synchronous or asynchronous based on the number of days required for all viable eggs in a nest to hatch; nests were deemed to have hatched synchronously when all eggs hatched within a day and asynchronously when two or more days were required for all eggs to hatch. We visited a subset of nests during egg laying (N = 52 nests) in the 2010 breeding season to weigh eggs (±0.001 g) on the morning each was laid to determine whether eggs that hatch synchronously or asynchronously differ in mass. We visited another subset of nests (N = 40 nests) daily during egg laying in the 2012 breeding season to document whether the onset of full incubation during egg laying predicted hatching asynchrony; here, we documented the onset of “full,” diurnal incubation (Kendeigh, 1952) as determined by eggs being noticeably warm to the touch in the early morning. In 15 of these 40 nests, females initiated full incubation on or before laying the penultimate egg of the clutch; the eggs within seven of these clutches eventually hatched asynchronously and the remaining eight clutches hatched synchronously. However, in 25 of the 40 nests, females delayed the onset of full incubation until the day the last egg of the clutch was laid, and these eggs eventually hatched synchronously in 23 of the 25 nests. Although we have no data on partial heat applied nocturnally to eggs prior to the onset of diurnal incubation, the onset of incubation as we


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assessed it here significantly predicted whether eggs eventually hatched synchronously or asynchronously (Fisher’s exact test: P = 0.008).

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In all years (2009-2013), we weighed nestlings (±0.1 g) 11 days after hatching began within a nest, measured the length of their tarsus (±0.1 mm) with dial calipers, and drew a blood sample (ca. 10-50 μL) from the brachial vein with heparinized capillary tubes for molecular sexing (details in Bowers et al., 2011). We subsequently visited nests daily thereafter to determine when fledging occurred. In sum, out of 2,396 viable eggs produced, we determined the sex of 2,016 offspring (i.e., 15.9% were unsexed because of mortality prior to sampling). Although sampling blood from nestlings at this age introduces the possibility that female and male nestlings died in the nest at an unequal rate prior to sampling, we have previously found no evidence of this (Bowers et al., 2015a). Moreover, in our analyses of sex ratios, we obtain similar qualitative results when analyzing modified forms of our dataset assuming that all unsexed offspring were either (i) entirely female (all nests: hatching asynchrony × date interaction: F1, 383 = 4.43, P = 0.036; repeated measures of paired nests: hatching asynchrony × clutch interaction: F1, 230.9 = 7.86, P = 0.006) or (ii) entirely male (all nests: hatching asynchrony × date interaction: F1, 383.5 = 6.98, P = 0.009; repeated measures of paired nests: hatching asynchrony × clutch interaction: F1, 231.3 = 14.97, P < 0.001). Thus, mortality within the nest prior to blood sampling should introduce only noise, not a bias, to our results.


The subset of available nestboxes used in the present study (N = 258) has been in place since the 1982 breeding season in a nature preserve that has been subject to minimal human disturbance. Thus, we used the productivity of these nesting sites in previous years as a measure of territory quality to determine whether this influences hatching asynchrony. We obtained two independent proxies for territory quality quantified as (i) the number of clutches initiated within a given nestbox over the ten years preceding this study, and (ii) the mean body mass of nestlings fledged from a nestbox over the same span of time. Each variable positively predicted the mean mass of nestlings produced at a given territory in the current study (number of clutches: estimate ± SE = 0.114 ± 0.050, F1, 363 = 5.29, P = 0.022; mean nestling mass: estimate ± SE = 0.118 ± 0.050, F1, 348 = 5.70, P = 0.018), but these two metrics were not correlated with each other (r404 = 0.068, P = 0.170). Territory quality assessed using this approach is also associated with the female production of extra-pair young, where females paired with males on putatively higher-quality territories tend to produce fewer extra-pair young within their broods (Bowers et al., 2015b). Thus, these are reliable indicators of territory quality that reflect both site attractiveness and the productivity of birds that use the site (see also Janiszewski et al., 2013), which we used to predict whether females would hatch their eggs synchronously or asynchronously. We attempted to catch all adults in each year preceding, during, and following the current study. Among the 2,047 offspring (N = 380 broods) that survived to leave the nest, 95 (4.6 %) recruited to the breeding population; this recruitment rate is typical for our study population and is similar to that reported for other populations of house wrens (Kendeigh, 1941; Poirier et al., 2004). Long-term data from the study population suggest that variation in recruitment is largely driven by variation in survival; although some offspring surviving to adulthood likely settle elsewhere, our data suggest that this is unrelated to environmental J Evol Biol. Author manuscript; available in PMC 2016 March 09.

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or phenotypic variation (Bowers et al., 2014c). Thus, a lack of data on dispersers should not introduce a bias to our results for recruits. Data analysis All analyses were performed using SAS (version SAS 9.3), all tests are two-tailed (α = 0.05), and we centered and standardized variables prior to analysis following Schielzeth (2010). We included year and maternal identity as random effects in all analyses, and we included nest identity as an additional random effect in analyses of offspring condition, recruitment, and reproductive success to account for non-independence of young produced within the same brood. Investigating residual variation and parameters indicative of model fit or overdispersion revealed that the models we used fit the data well.

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We first analyzed seasonal variation in clutch sizes using a linear mixed model with clutchinitiation date, maternal body condition (i.e., size-adjusted body mass), and hatching asynchrony (synchronous vs. asynchronous) as main effects, and we included brood number (first or second of the season) as a within-female effect. To analyze size-adjusted body mass, we included tarsus length as a covariate in analyses with body mass, thus representing body mass adjusted for differences in skeletal size (e.g., Garcáa-Berthou, 2001). We then analyzed egg mass using a similar model with relative egg-laying order (egg number divided by clutch size) and clutch size as covariates, and nest as a random effect instead of maternal identity and year, as each nest in this analysis was produced by a different female. We analyzed the frequency of hatching asynchrony in relation to time of year (hatching date), maternal body condition, year, and territory quality (using both the average pre-fledging mass of nestlings and the number of clutches produced on a given territory as measures of territory quality) using a generalized linear mixed model (GLMM) with a binary response (synchronous or asynchronous hatching). We recently found that modal-sized broods have a longer nestling period when hatched asynchronously than when hatched synchronously (Bowers et al., 2013b); however, because females hatching their eggs asynchronously tend to initiate incubation at an earlier stage during egg laying than synchronous females, the entire length of the breeding cycle from clutch initiation to fledging may actually be shorter for asynchronously hatched broods. Thus, we analyzed the length of breeding attempts in relation to hatching asynchrony using survival analysis (PROC PHREG) with broods that failed prior to fledging as censored values. We accounted for non-independence among years and among nests produced by the same female following Allison (2010), utilizing the robust variance estimator in PROC PHREG, which accounts for non-independent observations similar to a mixed model. We then analyzed variation in nestling body condition (body mass while controlling for variation in tarsus length) using a linear mixed model that included hatching date, hatching asynchrony, nestling sex, and an interaction between hatching asynchrony and sex as main effects, and we included brood number (first or second of the season) as a within-female effect. We analyzed the number of young fledged using hatching asynchrony, hatching date, and an interaction between the two effects. We used these same predictors to analyze brood sex ratios (N = 2,016 offspring from 392 broods produced from 2009-2013) using a GLMM with the number of male offspring in a nest as the dependent variable and the number of sexed offspring as the binomial denominator (i.e., events/trials syntax), and we used a repeated-measures approach,


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including brood number as a within-female effect. Williams (1979) argued that, if clutches are biased more strongly toward sons or daughters than expected by chance, sensu the Trivers-Willard Model, then variance in sex ratios should be greater than expected under null Mendelian segregation. Thus, we tested this by analyzing variation in sex ratios using a randomization test in R version 3.1.0 that compared the observed variance in sex ratios with a distribution of 10,000 simulated datasets with randomly reshuffled sex ratios given the clutch sizes and total number of males and females observed in the real population (Postma et al., 2011).

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We analyzed offspring recruitment in relation to body condition, hatching asynchrony, hatching date, and offspring sex using a GLMM with a binary response. We then analyzed variation in the body condition of yearling offspring using hatching asynchrony in their natal nest as a main effect. The mass of adult females changes predictably during the nesting cycle, declining from incubation through the nestling period (Cavitt & Thompson, 1997). Therefore, we analyzed females and males separately, testing for differences within the sexes attributable to hatching asynchrony in their natal brood. Finally, we analyzed variation in mating success (i.e., an individual’s probability of producing multiple broods in its first breeding season) and lifetime reproductive success (total number of fledglings produced) in relation to hatching asynchrony, sex, and the interaction between the two.

Results Nest productivity, hatching asynchrony, and brood sex ratios

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There was a consistent, seasonal decline in clutch size (estimate ± SE = −0.606 ± 0.043, F1, 104.7 = 203.00, P < 0.001) while controlling for maternal condition (effect of body condition on clutch size: estimate ± SE = 0.105 ± 0.045, F1, 293.8 = 5.50, P = 0.020; random effect of maternal identity, estimate ± SE = 0.090 ± 0.051). Clutches that eventually hatched synchronously or asynchronously did not differ in clutch size (estimate ± SE = 0.070 ± 0.094, F1, 394 = 0.56, P = 0.456) or in egg mass (Table 1a). There was also an increase in the frequency of asynchronous hatching over the course of the breeding season (Table 1b; Fig. 1a); no other variables, other than the onset of incubation during egg laying (see Methods), predicted whether eggs hatched synchronously or asynchronously (Table 1b). There was also a slight trend for asynchronous breeding attempts to take less overall time from clutch initiation to fledging, but the difference was marginal (mean days ± SE, excluding depredated nests: synchronous = 33.6 ± 0.1 d, asynchronous = 33.3 ± 0.2 d; survival analysis

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= 3.486, P = 0.062). Within-female plasticity in the degree of hatching synchrony was high, as females hatching their eggs synchronously early within breeding seasons were equally as likely to hatch their eggs asynchronously as they were synchronously during their second brood (Fig. 1b); 46.1% of females in the current study produced a second brood after fledging their first within the same year. Females were more likely to switch from synchronous hatching early to asynchronous hatching later within seasons than they were to switch from asynchronous to synchronous hatching (Fig. 1b; = 7.68; P = 0.007). Thus, the increase in asynchronous hatching of eggs over the course of the breeding season (Fig. 1a) was not caused simply by between-individual differences. Among females that were double-brooded (i.e., those that initiated a second clutch after having successfully fledged a


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brood earlier in the year), the frequency of synchronous hatching during the first brood of

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the season was greater than that of asynchronous hatching (

= 17.6, P < 0.001; Fig. 1b).


The body condition of nestlings (i.e., body mass adjusted for variation in skeletal size) prior to fledging generally declined over the course of the breeding season (Table 1c; Fig. 1c), and this decline was independent of year (hatching date × year: F1, 343 = 0.22, P = 0.639), nestling sex (hatching date × sex: F1, 1681 = 0.09, P = 0.769), and the degree of hatching synchrony (hatching date × synchrony: F1, 352 = 0.04, P = 0.844). Nestling body condition was also influenced by an interaction between hatching asynchrony and nestling sex (Table 1c). Males hatched in synchronous and asynchronous broods did not differ in pre-fledging body condition, on average (size-adjusted body mass: synchronous males = 10.19 ± 0.06 g, asynchronous males = 10.16 ± 0.07 g, least-squares means ± SE), whereas females in asynchronously hatched broods (10.02 ± 0.07 g) were slightly, but significantly, lighter than their brothers (F1, 1643 = 9.38, P = 0.002), and were also lighter than females in synchronously hatched broods (synchronous females = 10.20 ± 0.06 g; F1, 479 = 5.76, P = 0.017). Analyzing raw values for nestling body mass (i.e., while not adjusting for skeletal size) yields a qualitatively similar result (hatching asynchrony × sex interaction: F1, 1696 = 6.24, P = 0.013). The number of young successfully fledged from nests also declined as the breeding season progressed (Fig. 1d,e); however, there was an interaction between time of season and hatching asynchrony in their effect on fledging success (Table 1d), as the magnitude of the effect of time differed between synchronous (estimate ± SE = −0.513 ± 0.069, F1, 150 = 54.51, P < 0.001) and asynchronous broods (estimate ± SE = −0.293 ± 0.073, F1, 110 = 16.17, P = 0.001). Thus, asynchronously hatched broods fledged slightly more young from later-season nests than did synchronously hatched broods (Fig. 1d,e). Posthatching nestling mortality was not affected by variation in hatching date (estimate ± SE = 0.002 ± 0.073, F1, 219 = 0.12, P = 0.729), hatching asynchrony (estimate ± SE = −0.047 ± 0.106, F1, 373 = 0.20, P = 0.656), nor an interaction between the two (estimate ± SE = −0.044 ± 0.103, F1, 373 = 0.18, P = 0.668).

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Offspring sex ratios also varied seasonally, depending upon whether females hatched their eggs synchronously or asynchronously (Table 1e; Fig. 2). Although synchronous and asynchronous broods did not differ in sex ratios early in the breeding season, females hatching their eggs synchronously in their later-season broods produced relatively more daughters (effect of clutch-initiation date: estimate ± SE = −0.136 ± 0.061, F1, 59.01 = 5.01, P = 0.029; Fig. 2b), whereas the proportion of sons increased for asynchronously hatched nests over the course of the breeding season (estimate ± SE = 0.139 ± 0.069, F1, 58.29 = 4.04, P = 0.049; Fig. 2c). We also analyzed this pattern with the absolute number of sons within broods as the dependent variable, as opposed to the sex ratio (i.e., proportion of offspring that were male). This revealed a similar interaction between clutch-initiation date and hatching asynchrony (interaction estimate ± SE = 0.321 ± 0.140, F1, 384 = 5.28, P = 0.022). While the absolute number of sons declined over the course of the breeding season within synchronously hatched broods (follow-up test: estimate ± SE = −0.385 ± 0.095, F1, 52.3 = 46.46, P < 0.001), asynchronously hatched broods contained a similar absolute number of sons regardless of clutch-initiation date (follow-up test: estimate ± SE = −0.046 ± 0.100, F1, 142 = 0.021, P = 0.648).


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We followed this analysis by exploring within-female changes in the sex ratio of their offspring from first to second broods within seasons for double-brooded females. These sex ratios (Fig. 2d,e) closely reflected those found at the level of the larger population (Fig. 2b,c), and there was an interaction between hatching asynchrony and clutch number (first or second clutch of the season) in their effect on offspring sex (repeated-measures GLMM with clutch number as a within-female effect: interaction term estimate ± SE = −0.924 ± 0.219, F1, 231.6 = 17.81, P < 0.001). Specifically, there was a reduction in the proportion of sons produced by females hatching their later-season clutches synchronously relative to what these females had produced earlier within breeding seasons (F1, 203.2 = 29.98, P < 0.001; Fig. 2d). However, for females hatching their later-season clutches asynchronously, the sex ratios they produced at this time were no different from those they had produced earlier within the season (F1, 223.4 = 0.46, P = 0.497; Fig. 2e). We also analyzed paired sex ratios according to whether females hatched their eggs synchronously or asynchronously for both clutches of the season or whether they switched between the two. This also revealed female plasticity in sex allocation with respect to hatching asynchrony and the timing of breeding (interaction effect: F3, 124 = 3.83, P = 0.012; Fig. 2f), as females hatching their second clutch of the season synchronously increased the production of daughters whether their first clutch of the season hatched synchronously (F1, 124 = 10.86, P = 0.001) or asynchronously (F1, 124 = 4.38, P = 0.038). However, females hatching their second clutch asynchronously did not change the sex ratio from first to second clutches (synchronous-to-asynchronous: F1, 124 = 0.00, P = 0.948; asynchronous for both clutches: F1, 124 = 1.00, P = 0.320).

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Finally, we used a simulation-based approach to test for extra-binomial variation in sex ratios. Given the non-random patterns of sex allocation observed, extreme sex ratios (i.e., heavily male- and female-biased broods) might be expected to be more common than expected by chance, but this was not the case (Fig. 3). Generating 10,000 simulated populations with a randomly reshuffled sex ratio for each clutch (given the total number of males and females observed in the real dataset) produced an expected variance of 0.0619 with a 95% confidence interval ranging from 0.0558-0.0684. The observed variance (0.0576) falls within this 95% CI, and 90.7% of the simulations had a sex-ratio variance greater than that observed in the real data. Thus, although not statistically significant, the observed sex-ratio variation was actually slightly lower (i.e., 1:1 sex ratios more common) than that expected by chance (Fig. 3). Offspring recruitment and reproductive success

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There was an interaction between nestling body mass and hatching asynchrony in their effect on the likelihood that a nestling would recruit as an adult in the breeding population (Table 2a). There was no difference between the overall number of recruits produced by synchronous and asynchronous broods, but, at the level of the individual, heavy offspring from asynchronous broods had the highest overall recruitment (Fig. 4a,b). Hatching asynchrony also affected the size-adjusted body mass of adult offspring, and in a sexspecific manner (Table 2b; Fig. 4c); adult males that were reared in asynchronous broods were in better condition than those reared in synchronously hatched broods in their first breeding season, whereas females did not differ with respect to the degree of hatching synchrony in their natal brood (Fig. 4c). Consistent with the sex-difference in body


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condition of males reared in synchronous vs. asynchronous broods, there was a sex-specific effect of hatching asynchrony on the probability that these adult offspring would be multibrooded within their first breeding season (Table 2c; Fig. 4d). Specifically, males reared in asynchronously hatched broods were more likely to pair multiply (either through polygyny or sequential monogamy) than males that were reared within synchronously hatched broods (F1, 76 = 4.90, P = 0.030; Fig. 4d), and males reared in asynchronous broods were also more likely to produce multiple broods than their sisters (F1, 76 = 5.14, P = 0.026). However, there was no difference in the probability that females would be multi-brooded on the basis of their having been reared in a synchronous or asynchronous brood (F1, 76 = 0.64, P = 0.425). Overall, offspring reared in asynchronously hatched broods produced more fledglings in their lifetime in the study population than those reared in synchronous broods, an effect that was similar in both males and females (Table 2d; Fig. 4e).

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Discussion


We observed pronounced seasonal variation in brood-level productivity, with seasonal declines in clutch size, the condition of offspring, and the number of young fledged. Consistent with these findings, we found an increase in the frequency of asynchronous hatching, an increase that was largely attributable to within-female changes over the course of the breeding season, as approximately half of the females that produced a second brood switched hatching patterns between their first and second broods of the season (Fig. 1b). Although observational, our data show that the increase in asynchronous hatching over the course of the breeding season did not cause the seasonal decline in fledging success, because asynchronously hatched broods actually fledged more young, on average, later within seasons than did synchronously hatched broods (Fig. 1d,e). Contrary to our expectations, territory quality did not predict whether females would hatch their eggs synchronously or asynchronously, despite the fact that our measures of territory quality are generally predictive of nestling condition and that studies of other species suggest that hatching asynchrony is associated with female quality and environmental conditions (Slagsvold & Lifjeld, 1989; Wiebe & Bortolotti, 1994; Wiebe, 1995; Wiehn et al., 2000). Notwithstanding the lack of an effect of territory quality on hatching asynchrony, hatching patterns did vary seasonally and in a manner consistent with changes in resource availability. We suggest that, when food is abundant, synchronous vs. asynchronous hatching is less consequential for offspring development and survival than when food is more strongly limited later within breeding seasons. For example, in a population of house wrens in Utah, synchronously hatched broods, in which nestlings were of similar age and size, were associated with increased parental workloads and reduced per-capita prey availability relative to asynchronous hatching as the breeding season progressed (Pennock, 1990). Indeed, in the current study, differences in hatching asynchrony were associated with differences in offspring sex ratios later, but not earlier, within breeding seasons, with synchronous broods producing more daughters and asynchronous broods producing more sons. We, therefore, propose that the hatching patterns observed reflect a behavioral polyphenism representing sharply distinct strategies for allocating offspring within broods. For example, although the probability of individual recruitment is skewed within asynchronous broods, being particularly biased against those in below-average condition (below ca. 10 g), the above-


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average offspring within these broods have the highest probability of recruitment to future breeding populations and have greater reproductive success than synchronously hatched young (see also Amundsen & Slagsvold, 1998).

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Only nestlings in the best condition within asynchronous broods were likely to return as adults in subsequent years, whereas recruitment occurred nearly randomly with respect to body condition for young reared in synchronous broods. Thus, the persistence of hatching synchrony and asynchrony within populations may be explained, in part, by a classic tradeoff between offspring number and quality. For example, asynchronous hatching could potentially invade a population comprised exclusively of synchronous hatching because asynchronous broods produce sons that have an advantage over those produced in synchronous broods, whereas synchronous hatching could potentially invade a population that is exclusively asynchronous because synchronous hatching results in all offspring within the brood having similar chances of survival, and the daughters produced in these broods do not require as high of a level of resources as sons to become successful breeders.

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Although the onset of full incubation relative to clutch completion predicted whether eggs hatched synchronously or asynchronously, we do not yet have a complete understanding of the factors that contribute to this variation within and among populations at both proximate and ultimate levels (see also Harper et al., 1992, 1994; Ellis et al., 2001a). We do know that the maternal onset of incubation and synchronous vs. asynchronous hatching are not associated with differences in the amounts of maternally derived androgens in egg yolks (Ellis et al., 2001b), or in the porosity of eggshells, which could otherwise contribute to differences in the rate of gas exchange across the shell and the rate of embryonic development (Bowers et al., 2015c). However, we recently found that broods hatching synchronously tend to fledge at slightly younger ages than those hatching asynchronously, and that females fledging their first broods sufficiently early are more likely to produce a second brood. Females fledging their first broods earlier within a season also take less time to initiate their second brood within the same year, and fledging earlier in the year greatly increases the recruitment of these second-brood offspring (Bowers et al., 2013b). Thus, females might not initiate incubation as a response to variation in resource abundance or territory quality, but, rather, hatch their eggs synchronously early within seasons as a form of individual optimization to reduce their time spent provisioning young so they can produce a second brood.

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In a previous study of this population, Janota et al. (2002) investigated seasonal variation in sex ratios, predicting a decline in the production of sons from early- to late-season broods. Consistent with their predictions, broods were male-biased early in the breeding season, when the conditions for rearing young are typically at their peak; Janota et al. (2002) also predicted that brood sex ratios would shift toward daughters as the breeding season progressed, but did not detect such a pattern. We also found a slight male-bias among earlyseason broods, consistent with that earlier study; however, the inclusion of hatching asynchrony in our analysis revealed divergent sex-allocation strategies as the breeding season progressed. On one hand, we found a seasonal increase in the production of daughters within synchronously hatched broods (Fig. 2b), consistent with predictions given a seasonal decline in environmental conditions for rearing nestlings, and this increase was J Evol Biol. Author manuscript; available in PMC 2016 March 09.

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marked by within-female changes in offspring sex ratios (Fig. 2d,f). On the other hand, there was a seasonal increase in the proportion of sons within asynchronously hatched broods (Fig. 2c). Male house wrens experience intense intrasexual competition as adults, and compete vigorously over limiting nest cavities used to attract females (e.g., Kendeigh, 1941; Belles-Isles & Picman, 1987); in the current study, those reared in asynchronous broods and enjoying a size advantage over their sisters while in the nest were heavier and had greater success in acquiring mates than males reared in synchronous broods without a siblingcompetitive advantage early in life.


We did not expect the seasonal increase in the proportion of male offspring within asynchronously hatched broods, given that this is a time of the season at which conditions for rearing offspring are generally suboptimal. However, it is important to note that variation in the proportion of male offspring within clutches or broods may not necessarily reflect the absolute number of sons that are produced (Frank, 1990). In contrast with synchronously hatched broods, in which the absolute number of sons declined seasonally, the absolute number of sons remained constant within asynchronously hatched broods over the course of the breeding season (note that synchronous and asynchronous broods did not differ in posthatching mortality of nestlings). Given that males are over-produced primarily among earlier-laid eggs and daughters among later-laid eggs within asynchronously hatching clutches (Bowers et al., 2011), the seasonal increase in the proportion of males within asynchronous broods is likely attributable to a seasonal reduction in clutch size with no change in the number of sons per se (see also Figure 3 in Frank, 1990). Thus, the seasonal change in offspring sex ratios within asynchronously hatching clutches may not reflect direct or adaptive adjustment of offspring sex, but, rather, a byproduct of the seasonal decline in clutch size. The males reared in asynchronously hatched broods were more likely to produce multiple broods of young in their first breeding season than those from synchronous broods. Whether through polygyny or sequential monogamy, the number of broods a male produces has a much greater effect on his reproductive success than do gains and losses in paternity within broods (Poirier et al., 2004). Thus, producing sons later within breeding seasons may not be maladaptive in itself, even though conditions are harsher than they are earlier in the season, if these males benefit from a sibling-competitive advantage within broods (see also Carranza, 2004). Indeed, a benefit of asynchronous hatching may be that, by providing certain individuals within broods a competitive advantage and preferential allocation, these individuals are buffered from environmental conditions outside the nest, albeit at a cost to their younger, lighter siblings (Mock & Parker, 1997).

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The decline in the production of sons within synchronously hatched broods fit with our predictions. However, given that the reproductive success of sons from synchronously hatched broods was lower than those from asynchronously hatched broods, it is worth asking why synchronously hatched broods were not more female-biased than they were, or why they were not markedly female-biased at all times and not just later within breeding seasons. A number of hypotheses might explain why synchronously hatched broods were not more female-biased than we observed. For example, selection for equal sex ratios at the level of the clutch or brood is likely to be strong (Fisher 1930), and it may be that this selection for equal sex ratios within synchronously hatched broods is overcome later, but not


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earlier, within breeding seasons for reasons that we could not detect in the current study. It is also possible that variation in offspring sex ratios per se is not heritable (e.g., Postma et al., 2011), and, therefore, does not change evolutionarily, even when between-female differences in offspring reproductive success arise. We recently proposed that, even in the absence of any potential constraints to sex allocation imposed through Mendelian segregation of sex chromosomes, if the condition and future reproductive success of sons is more strongly affected by variation in the rearing environment than that of daughters, then increases in the proportion of males within broods in multiparous species should actually depress the average quality and survival of these offspring as sons suffer increased costs of sibling competition (Bowers et al., 2015a). This should especially be the case in birds, as over-producing males within clutches would necessarily place some of them later within the laying and hatching sequence, and, therefore, at a competitive disadvantage (see also Bortolotti, 1986; Bogdanova & Nager, 2008; Bonisoli-Alquati et al., 2011). Thus, sexspecific sibling rivalry likely imposes a limit on the extent to which sons are over-produced within broods. Williams (1979) proposed that variation in sex ratios among nests should exhibit extra-binomial variation if clutches are biased more strongly toward sons or daughters than expected by chance, and concluded that, in the absence of extra-binomial variation, mothers are unable to influence the sex of their offspring. We detected evidence of non-random sex allocation, yet sex-ratio variation was, if anything, lower than expected by chance (Fig. 3). Thus, a lack of extra-binomial variation in sex ratios does not necessarily mean that mothers are unable to influence offspring sex.


When seasonal variation in resource abundance and timing of breeding affect offspring fitness, parents are predicted to adjust offspring sex ratios accordingly (e.g., Dijkstra et al., 1990; Daan et al., 1996; Pen et al., 1999; Freed et al., 2009; Baeta et al., 2012). However, whether offspring sex ratios actually affect parental fitness in this context has remained largely unexplored to date, and is widely regarded as a major gap in the field (e.g., West, 2009). In the current study, females hatching their eggs synchronously later within breeding seasons reduced their production of sons relative to what they had produced earlier. This shift toward daughters within synchronously hatched broods, during a time in the season at which conditions for rearing offspring are generally suboptimal, resulted in mothers producing more of the sex less likely to suffer a reproductive disadvantage in adulthood. At the same time, the number of sons produced within asynchronous broods remained the same. These distinct hatching patterns were also associated with differential effects on offspring recruitment in relation to pre-fledging condition. Therefore, we propose that female incubation and hatching patterns represent distinct behavioral strategies for allocating offspring within broods, and that these are associated with plasticity in sex-allocation, allowing mothers to allocate sons and daughters according to environmental conditions.

Acknowledgments We thank the 2009-2015 Wren Crews for field assistance and the ParkLands Foundation, the Illinois Great Rivers Conference of the United Methodist Church, and the Sears and Butler families for the use of their properties. We also thank two anonymous reviewers for helpful comments that improved the manuscript, and Erik Postma for supplying the randomization test in R. Financial support was provided by the School of Biological Sciences, Illinois State University; the National Science Foundation (grants IBN-0316580, IOS-0718140, IOS-1118160); the National Institutes of Health (grant R15HD076308-01); the Sigma Xi Society; the Animal Behavior Society; the American Ornithologists’ Union; the American Museum of Natural History’s Frank M. Chapman Memorial Fund;


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Research Internships in Science and Engineering (RISE) from the Deutscher Akademischer Austauschdienst; the Champaign County Audubon Society; and the Beta Lambda Chapter of the Phi Sigma Society. All research activities were performed in accordance with (1) Illinois State University Institutional Animal Care and Use Committee Numbers 10-2009, 05-2010, 04-2013, (2) United States Geological Survey banding permit 09211, and (3) United States Fish and Wildlife Service collecting permit MB692148-0.

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Fig. 1.

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(a) Seasonal variation in the occurrence of asynchronous hatching (relative frequency). (b) Relative frequency of synchronous and asynchronous hatching among double-brooded females; within second broods, solid blocks represent females that maintained the same hatching pattern as their previous brood, whereas speckled blocks represent females that switched hatching patterns between broods (e.g., the majority of females hatching their eggs asynchronously in their second brood hatched their eggs synchronously in their first brood). (c) The body mass of nestlings prior to leaving the nest (brood means). (d,e) the number of young fledged from broods hatched synchronously and asynchronously, including three nests that failed because of parental abandonment. Lines in (a,d,e) are predictions from generalized linear mixed models ± 95 % confidence limits. Hatching dates are based on the ordinal calendar (day 130 = 10 May in non-leap years).

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Fig. 2.

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Variation in offspring sex ratios (proportion male) in relation to clutch-initiation date (a; all nests) and hatching asynchrony (b,c); lines are predictions from a generalized linear mixed model ± 95 % confidence limits. (d,e) Within-female changes in sex ratios across broods in relation to the degree of hatching synchrony of her second brood of the season; lines represent individual reaction norms (line width reflects the number of overlapping observations), and dots represent LS means ± S.E. (f) Sex ratios across paired broods for females that hatched their eggs synchronously (Sync) or asynchronously (Async) for both clutches of the season and those that switched between the two (LS means ± S.E.); dashed lines depict females that produced significantly different sex ratios between first and second broods (P < 0.05, see text).


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Relative frequency of sex ratios observed among nests compared with the null frequency of sex-ratios expected from 10,000 randomly reshuffled datasets.

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Bowers et al.

Page 22


Fig. 4.

Author Manuscript

(a,b) Recruitment of offspring as breeders into the local population in relation to the degree of hatching synchrony and pre-fledging body mass. Lines are predictions from a generalized linear mixed model ± 95 % confidence limits. (c) Body mass of recruited female and male offspring as breeding adults (LS means ± SE). (d) Probability that recruits would produce multiple broods of offspring in their first breeding season in relation to their sex and hatching asynchrony in their natal nest (LS means ± SE). (e) The number of fledglings produced by recruits during their lifetime breeding in the study population in relation to their sex and hatching asynchrony in their natal nest (LS means ± SE). Numbers in (c-e) are sample sizes; some recruits had to be omitted from the analysis of reproductive success because their nests were included in experiments that manipulated this variable.


Author Manuscript

Author Manuscript

Author Manuscript 0.109 ± 0.143 0.618 ± 0.137

Nest identity

J Evol Biol. Author manuscript; available in PMC 2016 March 09. 0.188 ± 0.414 −0.612 ± 0.435 0.005 ± 0.435

‡ ‡

‡

§

0.019 ± 0.248 0.086 ± 0.516

Year

Hatching asynchrony

(c) Nestling body condition

−0.370 ± 0.348

Maternal identity

0.030 ± 0.122

−0.007 ± 0.119

Intercept

Territory quality (clutches)

Territory quality (mass)

§

2013 (40.9 %, N = 50)

2012 (41.1 %, N = 66)

2011 (27.3 %, N = 114)

--

−0.225 ± 0.530

2010 (45.6 %, N = 124)

2009 (35.6 %, N = 48)

Year ‡

0.084 ± 0.122

†

Female tarsus length

0.308 ± 0.144 −0.127 ± 0.126

Female body mass

Hatching date

(b) Frequency of asynchronous hatching

0.369 ± 0.120

Intercept

−0.270 ± 0.113

0.265 ± 0.025

−0.043 ± 0.122

−0.306 ± 0.241

Female body mass

Clutch size

Egg-laying order

Clutch-initiation date

Asynchronous

*

Hatching asynchrony

(a) Egg mass

Estimate ± S.E.

2.36

0.06

0.00

1.68

0.47

1.01

4.60

9.40

5.65

109.20

0.12

1.62

F

1

1

1

4

1

1

1

1

1

1

1

1

ndf

343.0

317.0

317.0

317.0

221.0

217.0

317.0

45.1

45.9

278

44.9

45.1

ddf

0.126

0.805

0.956

0.155

0.492

0.316

0.033

0.004

0.022

< 0.001

0.729

0.21

P

Effects on nest productivity, hatching asynchrony, and sex ratios. Random effects in italics.

Author Manuscript

Table 1 Bowers et al. Page 23

Author Manuscript

¶

0.418 ± 0.070 0.006 ± 0.010

Nest

Maternal identity

J Evol Biol. Author manuscript; available in PMC 2016 March 09. 0.010 ± 0.066 0.000 ± 0.000 0.006 ± 0.011

Maternal identity

Year

8.96

0.00

2.93

4.00

60.33

4.11

228.42

6.47

5.00

37.92

1

1

1

1

1

1

1

1

1

1

74.3

384.0

73.7

383.1

371.0

240.0

376.0

1693.0

1641.0

1655

0.003

0.968

0.088

0.046

< 0.001

0.043

< 0.001

0.011

0.025

< 0.001

P

relative to 2013 breeding season (values in parentheses represent the relative frequency of asynchronous nests, sample sizes reflect total nests);

‡

included as both a fixed and random effect;

†

relative to synchronously hatched nests;

*

Note: ndf = numerator degrees of freedom, ddf = denominator degrees of freedom;

0.266 ± 0.089

Intercept

−0.135 ± 0.060

Clutch-initation date

Hatching asynchrony × Date

0.149 ± 0.087

Asynchronous*

Hatching asynchrony

(e) Offspring sex ratios

0.006 ± 0.012

0.040 ± 0.030

Year

−0.067 ± 0.190

Maternal identity

0.186 ± 0.093

−0.488 ± 0.063

0.193 ± 0.095

Intercept

Hatching asynchrony × Date

Hatching date

Asynchronous*

Hatching asynchrony

(d) Number of young fledged

0.044 ± 0.062

0.083 ± 0.066

Year

0.212 ± 0.014

Intercept

−0.174 ± 0.068

0.010 ± 0.043

−0.237 ± 0.038

−0.036 ± 0.087

Tarsus length

Hatching asynchrony × Sex

Female

Sex

Hatching date

Asynchronous*

ddf

Author Manuscript ndf

Author Manuscript

F

Author Manuscript

Estimate ± S.E.

Bowers et al. Page 24

Author Manuscript ¶ relative to male offspring.

based on productivity of a nesting site over the ten years preceding this study (see Methods);

Author Manuscript

§


Author Manuscript

Author Manuscript


Author Manuscript

Author Manuscript

Author Manuscript

*

†

‡

−3.273 ± 0.513

0.380 ± 0.138 0.749 ± 0.157

Adult tarsus length

Intercept

J Evol Biol. Author manuscript; available in PMC 2016 March 09. 0.158 ± 0.098

†


Female

Sex

Asynchronous*

Hatching asynchrony

(c) Probability of multiple mating

−2.281 ± 1.120

0.012 ± 0.750

1.592 ± 0.719

−0.700 ± 0.131

Adult tarsus length

Intercept

0.410 ± 0.195

Asynchronous*

Hatching asynchrony

Males

−0.042 ± 0.320

Asynchronous*

Synchrony

Females

(b) Body mass of adult offspring

−0.735 ± 0.463

Intercept

0.108 ± 0.268

0.491 ± 0.245

Sex × Hatching asynchrony

Female

Sex

Mass × Hatching asynchrony

Asynchronous

0.160 ± 0.301

0.084 ± 0.106

Tarsus length

Hatching asynchrony

−0.073 ± 0.152

Body mass

(a) Offspring recruitment

Estimate ± S.E.

4.14

2.72

0.65

2.60

4.42

7.54

0.02

2.52

1.25

4.01

0.73

0.62

1.74

F

1

1

1

1

1

1

1

1

1

1

1

1

1

ndf

76

76

58.1

50.0

50.0

34.0

34.0

1934.0

1934.0

1871.0

598.9

1934.0

1626.0

ddf

0.045

0.103

0.423

0.113

0.041

0.010

0.897

0.112

0.264

0.045

0.393

0.430

0.188

P

Effects on offspring recruitment, adult body mass, and reproductive success.

Author Manuscript

Table 2 Bowers et al. Page 26

†

−0.399 ± 0.184

Intercept

0.31

1.81

5.88

0.69

0.01

1

1

1

1

1

83.9

84.0

82.0

76

76

analyzed separately for females and males (see Methods).

relative to male offspring;

‡

†

relative to synchronously hatched nests;

*

Note: ndf = numerator degrees of freedom, ddf = denominator degrees of freedom;

−0.249 ± 0.451

0.428 ± 0.259

0.671 ± 0.276

−0.119 ± 0.464


Female

Sex

Asynchronous*

Hatching asynchrony

(d) Offspring reproductive success

Intercept

0.025 ± 0.333 −0.230 ± 0.278

Adult tarsus length

Author Manuscript

Adult body mass

ddf

Author Manuscript ndf

0.582

0.182

0.018

0.409

0.942

P

Author Manuscript

F

Author Manuscript

Estimate ± S.E.



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