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Keywords:

  • brood sex ratio;
  • cooperative breeding;
  • local resource competition;
  • long-tailed tit;
  • repayment;
  • sex allocation

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

In cooperatively breeding species, the fitness consequences of producing sons or daughters depend upon the fitness impacts of positive (repayment hypothesis) and negative (local competition hypothesis) social interactions among relatives. In this study, we examine brood sex allocation in relation to the predictions of both the repayment and the local competition hypotheses in the cooperatively breeding long-tailed tit Aegithalos caudatus. At the population level, we found that annual brood sex ratio was negatively related to the number of male survivors across years, as predicted by the local competition hypothesis. At an individual level, in contrast to predictions of the repayment hypothesis, there was no evidence for facultative control of brood sex ratio. However, immigrant females produced a greater proportion of sons than resident females, a result consistent with both hypotheses. We conclude that female long-tailed tits make adaptive decisions about brood sex allocation.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Classical sex allocation theory suggests that the fitness effects of producing sons and daughters are the same for each parent, resulting in all parents producing the same ratio of sons and daughters, so frequency-dependent selection will tend to stabilize the sex ratio at equilibrium at the population level (Fisher, 1930). However, the ideal sex ratio for individual breeders will depend on the fitness advantages of producing their own sons vs. daughters, which will not necessarily be the same as the ideal sex ratio for the population. Therefore, when the relative fitness of male and female offspring differs with environmental, individual or social conditions, breeders should adjust the sex ratio accordingly to maximize their fitness (Trivers & Willard, 1973; Charnov, 1982; Frank, 1990).

Many studies have investigated patterns of sex ratio variation in relation to the predictions of theoretical models, demonstrating that sex ratio variation can be related to multiple factors, including maternal traits (Heg et al., 2000; Whittingham & Dunn, 2000; Rosenfeld & Roberts, 2004; Rubenstein, 2007), paternal traits (Ellegren et al., 1996; Griffith et al., 2003), social status of females (Nishiumi, 1998; Westerdahl et al., 2000), time of breeding (Andersson et al., 2003; Husby et al., 2006; Cockburn & Double, 2008), laying or hatching sequence (Heinsohn et al., 1997; Legge et al., 2001; Woxvold & Magrath, 2007), clutch size (Lessells et al., 1996), territory quality (Komdeur, 1996; Komdeur et al., 1997; Byholm et al., 2002; Ewen et al., 2003; Forsman et al., 2008) and the presence of helpers (Gowaty & Lennartz, 1985; Ligon & Ligon, 1990; Clarke et al., 2002; Dickinson, 2004; Griffin et al., 2005). If these factors work simultaneously within populations, formulation of clear predictions about an optimal sex ratio will be difficult (Hardy, 2002; West & Sheldon, 2002; Wild & West, 2007).

In the cooperative breeding literature, research on adaptive offspring sex ratios has focused on testing Fisherian and individual sex allocation hypotheses at both the population and individual levels. In social species, the fitness of the sexes partly depends upon the fitness impacts of positive and negative social interactions among relatives (Clark, 1978; Emlen et al., 1986; West et al., 2005; Wild, 2006). For this reason, theoretical models predict that when members of one sex help their parents to control critical resources (local resource enhancement model; Emlen, 1997), or if offspring of one sex repay part of the cost of their parents’ investment and therefore become less costly to produce (repayment model; Emlen et al., 1986; Pen & Weissing, 2000), parents are predicted to bias the sex ratio in favour of the more helpful sex, usually the philopatric sex. In contrast, when offspring of one sex differentially competes either with each other or with their parents for food, mates or other resources, and this competition decreases their value to their parents, the sex ratio of offspring should be biased towards the noncompeting sex, usually the dispersing sex (local mate or resource competition model; Hamilton, 1967; Clark, 1978).

Sex allocation has been investigated in relation to the predictions from these theoretical models in several cooperatively breeding species (e.g. Griffin et al., 2005; Rathburn & Montgomerie, 2005; Woxvold & Magrath, 2007; Rubenstein, 2007; Cockburn & Double, 2008). However, the results of some studies are either inconsistent (e.g. Clarke et al., 2002; Ewen et al., 2003) or, in other cases, may not match the predictions of either the repayment or local resource competition models (e.g. Koenig & Dickinson, 1996; Koenig et al., 2001; Berg, 2004; Cockburn & Double, 2008); in such cases, both repayment and local resource competition models may be acting simultaneously (Komdeur, 1996; Komdeur et al., 1997; Hasselquist & Kempenaers, 2002; Ewen et al., 2003; West et al., 2005). Moreover, multiple selective factors, such as life history traits and demographic and environmental conditions, may potentially influence sex allocation decisions of female breeders at an individual level but may not be apparent at a population level (Cockburn et al., 2002; Hardy, 2002; Wild & West, 2007).

In this study, we use long-term data to describe the brood sex allocation pattern in the cooperatively breeding long-tailed tit Aegithalos caudatus, in relation to the predictions of the repayment and local resource competition hypotheses. If helpers have positive effects on the fitness of breeders, parents are predicted to invest differentially in the helping sex, leading to a biased sex ratio at the population level. At an individual level, female breeders without helpers may produce more of the helping sex to generate helpers (Emlen et al., 1986; Pen & Weissing, 2000), as reported in several studies (Gowaty & Lennartz, 1985; Komdeur et al., 1997; Ligon & Ligon, 1990; Ewen et al., 2003; Dickinson, 2004; Griffin et al., 2005). In long-tailed tits, helpers are usually male, the philopatric sex, and all helpers are failed breeders who switch from breeding to helping at the end of a temporally constrained season (MacColl & Hatchwell, 2002). Helpers exhibit strong kin-biased helping behaviour (Russell & Hatchwell, 2001; Nam et al., 2010) and by increasing recruitment from helped broods, gain substantial kin-selected fitness benefits from cooperation (MacColl & Hatchwell, 2004). In addition to increased productivity, male breeders obtain fitness benefits from receiving help by reducing their own reproductive costs by working less hard to provision broods (MacColl & Hatchwell, 2003; Meade et al., 2010). Therefore, males should be the more valuable sex in the cooperative breeding system of long-tailed tits, and the brood sex ratio at the population level should be biased towards the philopatric helping sex. The long-tailed tit is well suited to this investigation because sex allocation is unlikely to be influenced by territory quality, as found in other studies (Komdeur, 1996; Julliard, 2000; Hasselquist & Kempenaers, 2002), because breeders do not defend exclusive territories and resources (Hatchwell et al., 2001). Moreover, there is no evidence that nest predation, the level of investment by parents and helpers or survival rate varies in relation to habitat within our study site (MacColl & Hatchwell, 2003). Thus, there is no correlation between the location of a nest and the likelihood of a breeding attempt succeeding or the breeders at the nest receiving help (Hatchwell et al., 2004). Consequently, habitat or territory quality should not affect sex allocation decisions by female breeders in our population across years, simplifying the predictions of theoretical models of sex allocation.

We address two questions linked by the predictions from models in our population. First, we examine whether brood sex ratios are consistent with the repayment (local resource enhancement) model or the local resource competition model at both the population and individual levels. Secondly, to consider potentially confounding influences on brood sex ratios, we investigate the effect of maternal traits and ecologically relevant factors on sex allocation in individual broods.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Study species and data collection

A population of 17–72 pairs of long-tailed tits was studied from 1994 to 2009 in the Rivelin Valley, Sheffield, UK (55°23′N, 1°34′W). Long-tailed tits spend the winter in flocks of 6–30 birds, including overlapping generations of kin from one or more families and also unrelated male and female immigrants (Hatchwell et al., 2001; Sharp et al., 2008). All birds start each season by breeding independently in monogamous pairs, occupying nonexclusive breeding ranges. Long-tailed tits are single-brooded, raising a maximum of one brood per year, but they often have several breeding attempts because of nest failures; these are usually caused by predation, which occurs at all stages of the breeding cycle (Hatchwell et al., 1999). Breeders whose nests fail early in the season usually re-nest, but if failure occurs later in the season, breeders abandon independent breeding until the following year rather than re-nest, and some of these failed breeders become helpers at the nest of another pair (MacColl & Hatchwell, 2002). Most helpers are male and provide care at the nest of close relatives (Russell & Hatchwell, 2001; Nam et al., 2010), helping to provision nestlings and fledglings (MacColl & Hatchwell, 2003). In our study population, extra-pair paternity (EPP) and intraspecific brood parasitism are infrequent (< 10% for EPP and 0% for brood parasitism, M. Simeoni & B.J. Hatchwell, unpublished; Hatchwell et al., 2002). For further details of the study species and system, see Hatchwell & Sharp (2006).

Adults were captured in mist-nets and ringed with unique colour combinations prior to breeding (mean proportion of adult population ringed > 95%). At each capture of an adult, body mass (to 0.1 g), wing length and tarsus length (to 0.1 mm) were measured. Nestlings in accessible nests (> 95% of all nests; B.J. Hatchwell, unpublished) were also uniquely colour-ringed, and their body mass (to 0.1 g) and tarsus length (to 0.1 mm) were recorded on day 9–13 of the nestling period (86% on day 11, day of hatching = day 0). In 2001, access to some areas of the site was prohibited owing to an outbreak of foot and mouth disease and fewer nests were found, so data from 2001 to 2002 were not used for analysis of brood sex allocation at the population level and data from 2001 were excluded from analysis at the individual level. Throughout the breeding season (March–June), the nests of all pairs were located and closely monitored until fledging or failure. All accessible nests were observed, usually every second day, to record breeding events, including timing of laying, clutch size, hatch date, brood size and fledge date, and to identify parents and helpers (if present). We took blood samples from all adults and nestlings (under UK Home Office licence) and determined the gender of each individual using molecular techniques (Griffiths et al., 1998).

Brood sex ratio

In this study, brood sex ratio was calculated as the proportion of male nestlings in relation to the total number of male and female nestlings produced in a brood. Brood size was recorded on day 11 of the nestling period when nestlings were ringed and blood samples taken. In our long-tailed tit population, most eggs hatch and there is little brood reduction. In the sample used here, the mean (±SE) clutch size was 9.7 ± 0.95 (= 160 clutches) eggs, and the mean brood size was 8.9 ± 1.22 (= 160 broods) chicks. The proportion of eggs that failed to hatch was 0.08 (83 cases in 160 broods), and the proportion of hatched chicks that did not survive until fledging was 0.09 (35 cases in 194 broods; N.B. the sample of fledged brood sizes is larger than the sample of clutch sizes because clutch size could not be determined for all breeding attempts). There was no difference in the sex ratio of complete broods where all the eggs hatched (= 77) and incomplete broods containing unhatched eggs (= 83; inline image = 0.457, = 0.499). Furthermore, there was no difference in the sex ratio of broods where brood size at sampling matched initial clutch size (= 77) and those where brood size was lower than initial clutch size (= 131; inline image = 0.071, = 0.789). Therefore, we have no evidence for sex-biased mortality of embryos or nestlings, and hence, the sex ratio of broods at the time of the sampling should be close to the primary sex ratio in our population.

Data analyses

We recorded the brood sex ratio of 195 broods during 16 breeding seasons and used data from 160 of these broods to examine brood sex allocation in this study. The data set was reduced because where there were data points for the same female breeder from multiple years, one data point for each female breeder was randomly selected to analyse brood sex ratio allocation and any broods that were reduced in size by partial predation during the nestling stage were removed from the data set. Sample sizes in each model differed because all the information about brood sex ratio had to be available for each explanatory variable. All statistical analyses were performed in the R environment, version 2.7.0 (R Development Core Team, 2008).

We first tested for an overall sex ratio bias across years and for any brood sex ratio bias in each given year using the normal approximation of the binomial test. In these cases, we calculated the overall brood sex ratio as the proportion of male nestlings of the total number of nestlings produced in the population. We investigated the effect of demographic factors on annual brood sex ratio at the population level in relation to the predictions of the local competition hypothesis. We used the brood sex ratio of 153 broods for this analysis, because data from the 2001 and 2002 breeding seasons were excluded. We fitted generalized linear models with a logit link function and a quasibinomial error to account for underdispersion. In these models, the P-values came from F tests instead of chi-squared tests. The response variable was the total number of male nestlings produced per year, with the total number of male and female nestlings produced each year as the binomial denominator. We used the number of male survivors, female survivors, immigrant males, immigrant females and the total number of male and female breeders in the population as explanatory variables. Any breeders that were unringed at the beginning of each breeding season (except in 1994 when the study began) were classed as immigrant breeders (MacColl & Hatchwell, 2004). Any breeders that had spent at least 1 year in the study population were classed as resident breeders. ‘Male survivors’ means both male breeders and philopatric male recruits from the previous breeding season that were seen in the breeding population in subsequent years. ‘Female survivors’ refers to female breeders who had been seen in the breeding population in previous years and philopatric recruits from previous years. For ‘immigrant males and females’, we calculated the number of immigrant breeders in the population in each given year. ‘All male and female breeders’ was defined as the total number of all breeders (resident and immigrant) in the population in each given year. We tested the effect of demographic factors on annual brood sex ratios of ‘resident pairs’ (= 126) and ‘immigrant pairs’ (= 22) using this model. In this analysis, if at least one of the breeders in a brood was a resident breeder, this pair was classed as a ‘resident pair’; ‘immigrant pair’ described pairs in which both breeders were immigrants.

To investigate brood sex ratio variation within broods of individual female breeders in relation to the predictions of the repayment hypothesis, we used the presence of helpers at the previous breeding attempt and the number of potential helpers for either or both male and female breeders in the current attempt as explanatory variables to explain brood sex ratio variation. We fitted generalized linear models with a binomial error and a logit link function. The response variable was the number of male nestlings, with the total number of nestlings in the brood as the binomial denominator. For the presence of helpers, we used a binary variable set to 1 if female breeders received help at the previous breeding attempt; otherwise set to 0. This explanatory variable is referred to as ‘Helped?’. ‘Number of potential helpers’ is defined as the number of known first-order relatives present in each given year, determined by pedigree information. In this analysis, we counted only numbers of first-order relatives (e.g. parents, offspring and siblings), referred to as potential helpers, because long-tailed tits show strongly kin-biased helping behaviour (Russell & Hatchwell, 2001; Nam et al., 2010).

To analyse the effect of ecologically relevant factors on brood sex ratio variation, we also fitted generalized linear models with a binomial error and a logit link function. The number of male nestlings was used as the response variable, with brood size as the binomial denominator. The explanatory variables were year, lay date (date when female laid the first egg), hatching date, brood size, female age, the origin of breeders and tarsus length of the female breeder. ‘Brood size’ was the number of chicks present in the nest on day 11; this is a good indicator of brood size from hatching because nestling starvation is rare (Hatchwell et al., 2004). ‘Female age’ was the age in years of female breeders in a given year. Age is known precisely for resident females ringed as chicks in our study site. Immigrant females are assumed to be 1 year old at the time of ringing, because most immigrant females are yearlings that have dispersed from their natal site before the breeding season. This is a reasonable assumption, because there is no evidence that any significant dispersal occurs after a bird’s first winter (McGowan et al., 2003). For the origin of breeders, we used a binary variable set to 1 if the individual breeder was an immigrant; otherwise set to 0. This explanatory variable is referred to as ‘Resident?’. All interaction terms between predictor variables were tested and were not significant (> 0.05).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Population brood sex ratio

The overall brood sex ratio was slightly male biased in our study population, although not significantly different from parity (males = 748, females = 676; sex ratio = 0.53, 95% CI = 0.50–0.55; binomial test: = 0.060). Brood sex ratio did not differ significantly from parity in any given year, and there was no significant difference in brood sex ratio between years (inline image = 12.32, = 0.655).

Females tended to produce fewer sons as the number of male breeders present in the study site each year increased, although this effect was not significant (F1,11 = 4.57, = 0.056; Table 1). However, there was a significant negative relationship between brood sex ratio and the total number of male survivors (the number of resident male breeders plus the philopatric male recruits from the previous year) (F1,11 = 15.25, P = 0.002; Table 1; Fig. 1). The other factors included in the model were not significantly related to population brood sex ratio (Table 1). When breeding pairs were categorized as either ‘resident pairs’ or ‘immigrant pairs’ and analysed separately, the negative relationship between brood sex ratio and the number of male survivors was still apparent for resident pairs (F1,11 = 8.98, = 0.012; Table 1) but not for immigrant pairs (F1,11 = 1.29, = 0.289; Table 1). Other factors included in the model did not significantly affect brood sex ratio in either resident or immigrant breeding pairs (Table 1).

Table 1.   Results of generalized linear models analysing brood sex ratio (proportion of male nestlings) in relation to demographic factors at the population level.
VariablesAll breeding pairsResident breeding pairsImmigrant breeding pairs
Estimate ± SEd.f.FPEstimate ± SEd.f.FPEstimate ± SEd.f.FP
  1. We refitted the model using quasibinomial error to account for the underdispersion. In the analyses, the P-values came from F tests instead of chi-squared tests. Significant P-values are shown in bold.

Total no. of male breeders−0.007 ± 0.00314.5730.056−0.007 ± 0.00413.6510.082−0.007 ± 0.01210.3080.594
 No. of male survivors−0.016 ± 0.004115.2510.002−0.016 ± 0.00518.9820.012−0.026 ± 0.02211.2910.289
 No. of male immigrants−0.003 ± 0.00610.1950.667−0.003 ± 0.00610.2420.632−0.001 ± 0.01910.0020.964
Total no. of female breeders−0.006 ± 0.00313.2130.100−0.006 ± 0.00412.9360.114−0.007 ± 0.01210.3240.585
 No. of female immigrants−0.008 ± 0.00811.1380.309−0.013 ± 0.00812.3770.151−0.015 ± 0.03010.2670.620
 No. of female survivors−0.008 ± 0.00413.5830.085−0.007 ± 0.00511.6540.225−0.014 ± 0.01411.0220.342
image

Figure 1.  The relationship between the number of male survivors and brood sex ratio at the population level in 13 years from 1995 to 2009, excluding 2001 and 2002. The solid line shows the predicted values from the model (Table 1). The vertical dotted lines show the mean number of male survivors across years, and the horizontal line indicates parity for sex ratio.

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Effect of helping on brood sex ratio

The sex ratio in broods belonging to female breeders that received help during the previous breeding season (sex ratio ± SE = 0.51 ± 0.04, = 24 broods) was not significantly different to that of female breeders that did not receive help in the previous year (sex ratio ± SE = 0.53 ± 0.016, = 109 broods; inline image = 0.338, = 0.553; Table 2). An alternative way of examining the effect of helpers on brood sex ratio is to use the number of potential helpers for the current brood for both members of a pair or for each individual breeder (Table 2). This analysis allows for the fact that the presence of helpers relies on the potential helper failing in its own breeding attempt and the potential recipient having a brood to care for. However, again there was no evidence of a relationship between the number of potential helpers and brood sex ratio for either male breeders (mean number of potential helpers = 1.4, range = 0–6; inline image = 0.040, = 0.818; Table 2), female breeders (mean number of potential helpers = 1.5, range = 0–6; inline image = 0.429, = 0.513; Table 2) or both breeders combined (mean number of potential helpers = 1.9, range = 0–7; inline image = 0.418, = 0.518; Table 2).

Table 2.   Results of generalized linear models analysing the effects of the presence of helpers and number of potential helpers on brood sex ratios.
Predictor variablesSample sizeEstimate ± SEd.f.χ2P
Helped?1330.087 ± 0.14710.3380.553
No. of potential helpers (both breeders)125−0.022 ± 0.03310.4180.518
No. of potential helpers (male breeder)1020.008 ± 0.03510.0400.818
No. of potential helpers (female breeder)81−0.030 ± 0.04510.4290.513

Maternal traits and ecological factors

We investigated the effect of maternal traits and ecologically relevant factors on sex allocation at the level of individual broods (Table 3). First, we examined whether the origin of male and female breeders (resident or immigrant) was related to brood sex ratio. In females, there was a significant difference in brood sex ratio between residents and immigrants (inline image = 3.934, = 0.047; Table 3; Fig. 2). Overall, the sex ratio was biased towards males in broods of immigrant female breeders (sex ratio ± SE = 0.55 ± 0.01, 95% CI = 0.50–0.59, = 75 broods; binomial test: = 0.015), but not in broods produced by resident female breeders (sex ratio ± SE = 0.50 ± 0.01, 95% CI = 0.46–0.53, = 79 broods; binomial test: = 0.940). In the case of males, however, the sex ratio did not differ between broods of resident (sex ratio ± SE = 0.54 ± 0.01, = 108 broods) and immigrant male breeders (sex ratio ± SE = 0.50 ± 0.03, = 46 broods; inline image = 1.227, = 0.268; Table 3). There was no significant interaction between the origin of male and female breeders (inline image = 1.775, = 0.183; Table 3). Secondly, we found no evidence that nestling sex ratio varied with brood size, female age or tarsus length (Table 3). Finally, there was no relationship between brood sex ratio and either lay date or hatch date (Table 3). There were no significant interaction terms between all factors (> 0.05 in all cases).

Table 3.   Summary of generalized linear models examining brood sex ratio variation in relation to ecologically relevant factors and maternal traits.
Predictor variablesSample sizeEstimate ± SEd.f.χ2P
  1. All interaction terms between origin of breeders and predictor variables were tested and were not significant (> 0.05). Sample size was included in analyses. Significant P-values are shown in bold.

Year1601512.3200.655
Lay date141−0.002 ± 0.00610.0800.777
Hatch date150−0.005 ± 0.00710.4300.512
Brood size (continuous)1600.001 ± 0.04510.0010.978
Brood size (categorical)16050.8430.974
Female age (continuous)157−0.066 ± 0.06011.2230.269
Female age (categorical)15743.9320.415
Maternal tarsus length84−0.011 ± 0.15010.0050.943
Origin of breeders
 Resident? (male breeder)151−0.142 ± 0.11911.2270.268
 Resident? (female breeder)1510.201 ± 0.10813.9340.047
 Resident? (male : female)1510.319 ± 0.24011.7750.183
image

Figure 2.  Mean brood sex ratio in relation to the origin of both breeders (sample size = 56, 22, 49 and 24 broods from left). The horizontal dotted line indicates sex ratio parity.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

In this study, we have described brood sex allocation in relation to predictions of the repayment and local competition hypotheses. The results show that at the population level, offspring sex ratio is not significantly biased towards either sex. However, the proportion of sons produced did decrease as survivorship of males from the previous season increased. This effect was driven by variation in sex allocation by resident breeders rather than by immigrant breeders. We found no relationship between individual brood sex ratio and the presence of either helpers at the previous breeding attempt or the potential helpers for the current brood, but immigrant females produced a higher proportion of sons than resident females. We now discuss these results in the context of the repayment and local competition models.

At the population level, the absence of an overall bias in sex allocation towards males is contrary to the predictions of the repayment hypothesis (Emlen et al., 1986) but makes adaptive sense given the unusual nature of the long-tailed tit’s cooperative breeding system. In typical cooperative breeders, helping occurs within families and helpers are normally offspring that delay dispersal and remain on their natal territory before eventually dispersing to breed independently, providing that they survive long enough and the opportunity to breed arises (Hatchwell, 2009). Therefore, philopatric offspring are likely to be helpers initially, with a lower probability of eventually becoming independent breeders, so there is likely to be a fitness benefit to breeders from biasing the sex ratio towards the helping sex. By contrast, in the long-tailed tit, all surviving offspring initially attempt to breed independently in monogamous pairs, with a proportion redirecting their care to become helpers only in the event of breeding failure and the availability of kin with active nests nearby. Therefore, the probability of becoming a breeder is much higher than that of becoming a helper, so the population sex ratio would be expected to approximate a Fisherian equilibrium of parity, as observed. Moreover, the variance in lifetime reproductive success of male and female long-tailed tits is very similar (MacColl & Hatchwell, 2004), again suggesting that a population sex ratio of parity is likely to be adaptive.

Several studies of other cooperatively breeding species have found no evidence of a sex ratio bias towards the helping sex at the population level (Koenig & Dickinson, 1996; Legge et al., 2001; Arnold et al., 2001; Rathburn & Montgomerie, 2005; Cockburn & Double, 2008). However, in some cases, a facultative offspring sex ratio adjustment matching the predictions of the repayment model is apparent at an individual level, despite the lack of sex ratio bias at the population level (Koenig & Dickinson, 1996; Komdeur et al., 1997; Legge et al., 2001). Therefore, although the overall brood sex ratio was not significantly different from parity in our population, biasing offspring production towards the helping sex could increase the fitness of some breeders, resulting in a sex ratio bias at the individual level. However, we found no evidence for facultative control of brood sex ratios in relation to the presence of helpers at previous breeding attempts or potential helpers for the current breeding attempt (Table 2). This absence of facultative sex ratio adjustment according to the predictions of the repayment model contrasts with studies of other cooperatively breeding species, but again this finding may make adaptive sense in the context of the long-tailed tit’s unusual cooperative breeding system where helping is less predictable than in typical cooperative systems. Long-tailed tit’s helping decisions are driven by the kinship of potential helpers to available recipients in the population, most helpers being siblings of one breeder (Russell & Hatchwell, 2001; Nam et al., 2010), and also by the lottery of predation creating failed breeders, i.e. potential helpers (Hatchwell et al., 2004). Moreover, long-tailed tits have a low annual survival rate (McGowan et al., 2003; Meade & Hatchwell, 2010), and the divorce rate is high among surviving pairs of long-tailed tits (Hatchwell et al., 2000). Consequently, the opportunity to obtain fitness benefits by receiving help from offspring will be less predictable than in typical cooperative breeders, in which helpers are mostly nonbreeding philopatric offspring from previous breeding attempts living in stable family groups (Hatchwell, 2009). Thus, long-tailed tit breeders cannot guarantee to obtain help from their relatives, especially not from their offspring from earlier breeding attempts. Furthermore, females determine the sex ratio of a clutch of eggs, whereas most helpers are relatives of male breeders (Nam et al., 2010), so females may not have good information about potential helpers in the population. For these various reasons, it is plausible that unpredictable future benefits of receiving help are insufficient to cause facultative adjustments in brood sex ratios by female long-tailed tits. This conclusion highlights the importance of the predictability of interacting with kin (positively or negatively) when testing hypotheses about adaptive sex allocation.

On the other hand, we did find evidence for a facultative adjustment of brood sex ratio by females in relation to their origin (Table 3; Fig. 2); the sex ratio in immigrant females’ broods was biased towards males, whereas brood sex ratio did not differ from parity for resident female breeders. Immigrant female breeders are likely to have fewer kin in the population than resident females (Sharp et al., 2008), so it may be important to bias production towards males to generate clusters of philopatric males who may help each other in future seasons. In the case of resident females, some will have already produced a brood in a previous year, or, if they are philopatric, may already have male relatives in the population. This is consistent with studies of other cooperative breeders, where female breeders who already have helpers produced a balanced sex ratio (e.g. Gowaty & Lennartz, 1985; Legge et al., 2001; Ewen et al., 2003). Therefore, although the presence of helpers did not affect sex allocation in female breeders, there might be a differential strategy for brood sex ratio allocation between resident and immigrant female breeders. An alternative explanation is that offspring sex adjustment in relation to the origin of female breeders is consistent with the local competition hypothesis. Resident females should favour a female-biased sex ratio (i.e. favour the dispersing sex) relative to immigrant females because the philopatric offspring of resident females are more likely to interact, and hence compete, with relatives (Taylor & Crespi, 1994; El Mouden & Gardner, 2008). It is difficult to differentiate between these two interpretations because it is not clear whether the difference in brood sex ratios of resident and immigrant females is driven by increased production of males by immigrants or increased production of females by residents, relative to the population mean (Fig. 2).

At the population level, we found a negative relationship between annual brood sex ratio and male survivorship across years (Fig. 1). In years when more males survived from year n to year + 1, brood sex ratio was skewed more towards the dispersing sex (females) than in years with relatively few male survivors in the population. The local competition hypothesis (Clark, 1978) proposes that when offspring of one sex differentially competes either with each other or with their parents for local resources or mating opportunities in a population, and this competition decreases their value to their parents, parents should produce offspring sex ratios that minimize competition among relatives in a population by biasing production towards the dispersing sex. Thus, this result is consistent with the local competition hypothesis.

Studies of western bluebirds Silalia mexicana (Dickinson, 2004) and red-backed fairy-wrens Malurus melanocephalus (Varian-Ramos et al., 2010) found a negative relationship between the proportion of the philopatric sex in a brood and annual group size. Both studies suggest that local competition among relatives affected brood sex ratio in a population, and group size was a predictor of competition among relatives in a population. In our analyses, we considered several factors linked to population density that might influence brood sex allocation (Table 1), but only the number of male survivors was significant. Male survivorship should be an important factor in long-tailed tit sex allocation, because local recruitment is male biased (Sharp et al., 2008). For this reason, the number of male survivors should be a good predictor of local competition among current breeders who are related to each other and therefore an important factor when females make brood sex allocation decisions. We would also expect this effect to be more likely for residents than immigrants, as observed, because of the timing of dispersal. Long-tailed tits spend the nonbreeding season in fluid winter flocks, composed mainly of relatives (often from more than one family), but also including immigrants of both sexes (Hatchwell et al., 2001; Sharp et al., 2008). These immigrants disperse into winter flocks throughout the winter and long after they first form during the post-fledging period (Russell, 1999). Therefore, residents would have much better information about flock composition than immigrants, allowing residents (but perhaps not immigrants) to bias the sex ratio in response to male survivorship among flocks.

Theoretical studies suggest that multiple selective factors such as life history traits, demographic factors and environmental conditions may influence sex allocation by female breeders at an individual level, because these factors can also influence the costs and benefits of producing male and female offspring (Trivers & Willard, 1973; Cockburn et al., 2002; Hardy, 2002; Wild & West, 2007). To examine potentially confounding influences of maternal traits and ecologically relevant factors, we investigated the effect of multiple factors on sex ratio allocation in a brood. We found no evidence for facultative sex allocation in relation to maternal traits and ecologically relevant factors (Table 3). The age and physical condition of female breeders did not affect the brood sex ratio in the current breeding attempt. In addition, there was no effect of either brood size and lay date, or hatch date on sex allocation decision by females. These findings are similar to other studies showing weak or nonexistent facultative adjustment of sex ratio in relation to the predictions of the Trivers–Willard hypothesis in birds (Ewen et al., 2004; Cassey et al., 2007; Cockburn & Double, 2008).

In conclusion, in this study, we failed to find either a brood sex ratio bias towards the helping sex at the population level or facultative adjustment of brood sex ratio by individual females according to either the presence or absence of helpers or potential helpers. However, two results suggest that long-tailed tits may facultatively adjust the sex ratio of their broods. Firstly, although the potential benefit of repayment by helpers might not be a sufficiently strong selective pressure to cause a sex ratio bias, immigrant females produced a greater proportion of sons than resident female breeders, as predicted by this hypothesis. On the other hand, this result could also be interpreted as supportive of the local competition hypothesis, because resident females produced a correspondingly greater proportion of females, the dispersing sex. Secondly, we found that annual brood sex ratio was related to the number of male survivors in the population, as predicted by the local competition hypothesis. These results suggest that the local competition hypothesis may explain brood sex ratio allocation at the population level, whereas sex allocation decisions by immigrant females are consistent with both the repayment and local competition hypotheses.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

We thank A. Bamford, M. K. Fowlie, N. Green, J.-W. Lee, A. MacColl, A. McGowan, D. Richardson, S. P. Sharp, M. Simeoni, D. J. Ross and A. F. Russell for their invaluable assistance with data collection in the field. We are grateful to D. Gillespie for statistical advice and two anonymous reviewers for their useful discussions and comments on the manuscript. We also thank the Sheffield Molecular Genetics Facility for their assistance with genetic analysis and Sheffield City Council, Yorkshire Water and Hallamshire Golf Club for permission to research on their land. This work was partly funded by the University of Sheffield and the Natural Environment Research Council, for which we are most grateful.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References