Behavioral Ecology Advance Access originally published online on May 25, 2005
Behavioral Ecology 2005 16(4):763-769; doi:10.1093/beheco/ari052
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Sex allocation in response to paternal attractiveness in the zebra finch
a School of Biology, University of St. Andrews, Fife KY16 9TS, UK, and b Department of Environmental and Evolutionary Biology, University of Glasgow, Glasgow, UK
Address correspondence to A.N. Rutstein, who is now at the University of New South Wales, Sydney, NSW 2031, Australia. E-mail: a.rutstein{at}unsw.edu.au.
Received 7 September 2004; revised 14 March 2005; accepted 28 March 2005.
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ABSTRACT |
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Females mated to attractive males are predicted to produce male-biased broods. Previous studies on zebra finches, Taeniopygia guttata, in which colored leg rings were used to alter male attractiveness, support this hypothesis. However, because molecular sexing techniques were not available, it was not known when during development this bias arose. Also, because both attractive (red-ringed) and unattractive (green-ringed) males were within the same aviary, assortative mating between treatments may have confounded the results. Using two different experimental designs, we tested whether the sex ratio of zebra finch eggs and chicks differed in response to paternal ring color whilst controlling for assortative mating between treatments. In the aviary experiment, birds could interact socially, but all males in an aviary had the same leg ring color. In the cage experiment, each female was randomly assigned a red- or green-ringed mate, thus also eliminating assortative mating within treatments. Offspring were sexed based on plumage or using a molecular method. The sex ratio at laying did not differ between treatments in either the aviary (n = 313 eggs) or cage (n = 151 eggs) experiments, suggesting that female zebra finches do not manipulate the primary sex ratio in response to their mate's ring color. However, in the cage experiment we found greater male embryonic mortality in the attractive group, which resulted in a female-biased sex ratio at sexual maturity, that is, in the opposite direction to that found in previous studies. Possible explanations for the disparity between our results and those of previous studies are considered.
Key words: attractiveness, differential mortality, sex ratio, Taeniopygia guttata, zebra finch.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sex allocation theory predicts that parents should bias investment towards offspring of the sex that confers higher relative fitness on the parents (Charnov, 1982
; Trivers and Willard, 1973). The value of such offspring may depend on a range of environmental and social factors. For example, parents with poorer prospects for investment in their offspring are predicted to invest preferentially in the sex with the lower variance in reproductive success (Trivers and Willard, 1973). More recently, research has started to focus on how an individual's attractiveness influences sex allocation decisions by its mate (Burley, 1981, 1986a, 1988; Sheldon, 2000). Females benefit from mating with an attractive male because attractiveness has been suggested to signal male genetic quality (Andersson, 1986; Hamilton and Zuk, 1982; Jennions and Petrie, 2000; Zahavi, 1975). It is also thought to display that he is a high-quality, well-nourished individual capable of providing superior parental care (Hoelzer, 1989; Norris, 1990). If sons inherit some of these attractive traits from their father, then they in turn will enjoy greater reproductive success as adults (the sexy son hypothesis; Weatherhead and Robertson, 1979). Therefore, it will be advantageous for a female mated to an attractive male to bias her offspring sex ratio in favor of sons.
The earliest studies investigating sex ratio manipulation in relation to paternal attractiveness were carried out by Nancy Burley on the zebra finch, Taeniopygia guttata (Burley, 1981, 1986a). This is a nonterritorial, socially monogamous species that exhibits considerable sexual dimorphism in plumage. Attractive males have higher display rates (Collins et al., 1994; Houtman, 1992; Ratcliffe and Boag, 1987; Ten Cate and Mug, 1984) and redder bills (Burley and Coopersmith, 1987; de Kogel and Prijs, 1996), both of which are heritable, condition-dependent traits (Houtman, 1992; Price, 1996; Price and Burley, 1993). A great advantage of this species for the purposes of experimental design is that attractiveness can be artificially manipulated using colored leg rings. In mate choice trials females have consistently demonstrated strong preferences for males with red leg rings over males with green leg rings (Burley, 1988; Burley et al., 1982; Hunt et al., 1997). The reason for this is thought to be because red leg rings act as a super stimulus, enhancing the red bill color, which is a carotenoid-based, condition-dependent secondary sexual trait (Blount et al., 2003).
In now classic experiments carried out on captive populations in aviaries, Burley found that, when attractiveness was manipulated with colored leg rings, the offspring sex ratio was biased towards the sex of the more attractive parent. Females mated to red-ringed (attractive) males produced a more male-biased sex ratio at sexual maturity (61.3% males) compared with females mated to green-ringed (unattractive) males (50.2% males) (Burley, 1986a). Burley argued that this was adaptive because she found that red-ringed males had significantly higher long-term reproductive success compared with their green-ringed counterparts; red-ringed males reared more and higher quality young (Burley, 1986b) and they were more likely to be polygynous (Burley, 1985, 1988). In addition, red-ringed males were more likely to obtain extrapair copulations (EPCs), and their mates were less likely to participate in EPCs compared with mates of green-ringed males (Burley et al., 1994, 1996).
Burley (1986a) proposed that this sex ratio skew was brought about by differential mortality of chicks soon after hatching. However, because offspring were sexed from plumage characteristics at sexual maturity (8 weeks of age), the sex of unhatched eggs and dead chicks was not known. Thus, the stage at which the skew arose could not be determined. Skewed sex ratios among birds can result from sex ratio adjustment prior to laying (primary level) and/or after laying (secondary level). The latter occurs through differential mortality of one sex before hatching (Blank and Nolan, 1983) or after hatching (Howe, 1976; Oddie, 2000; Teather and Weatherhead, 1989) and may result either from direct parental manipulation (Nishiumi et al., 1996; Stamps et al., 1987; Yasukawa et al., 1990) or may be a nonadaptive consequence of one sex being more susceptible to suboptimal developmental conditions (Martins, 2004). The precise physiological mechanisms responsible for primary sex ratio adjustment remain elusive (for review see Pike and Petrie, 2003), but this early manipulation is more energetically efficient because fewer resources are wasted (Komdeur and Pen, 2002).
In addition, assortative mating between treatments could have confounded Burley's results because aviaries contained both red- and green-ringed males. Therefore, if higher quality females preferentially mated with attractive, red-ringed males and vice versa, female body condition and not paternal attractiveness could have determined a mother's sex allocation strategy. This would have profound implications for the interpretation of the results (Rintamaki et al., 1998). Indeed, disentangling other confounding variables such as territory quality has also been problematic in correlational field studies on sex allocation (Ellegren et al., 1996; Kölliker et al., 1999; Yamaguchi et al., 2004).
In this paper we report on two experiments designed to test whether and at what stage sex ratio adjustment occurs in relation to mate attractiveness in zebra finches, while controlling for assortative mating between treatments. In the first experiment we used aviaries to replicate the original aviary study of Burley (1981, 1986a) in which birds could interact socially but with one important difference: we housed red- and green-ringed males in separate aviaries to avoid assortative mating between the color treatments. In the second experiment we completely eliminated assortative mating within treatments by using single pairs of birds in individual cages. We predicted that if sex ratio adjustment was advantageous in relation to paternal attractiveness, then in both experiments we would find a male bias among offspring of red-ringed male pairs at laying. The advantage of using both types of design is that in the aviary experiment we could simulate a more realistic social context. However, assortative mating within treatments might still occur and, also, sample size is limited because individuals within an aviary may not be independent. These problems are resolved using the cage experiment in which we could completely eliminate any possible confounding effect of assortative mating and therefore of female quality. In addition, we could increase the sample size and therefore the statistical power.
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METHODS |
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Subjects
All birds were of wild-type phenotype, between 1 and 2 years of age, and were either bred in captivity in our laboratories or came from other UK universities or private breeders. Because naive females breed poorly, all females had undergone at least one reproductive attempt, but not with a red- or green-ringed male and not within 6 months prior to the experiment. In the current experiments females were in cages or aviaries with males with whom they had not previously bred.
Experimental setup
In both experiments male attractiveness was manipulated with plastic, colored, leg rings supplied by A. C. Hughes, Middlesex, U.K. Males in the "attractive" group were given red leg rings, and males in the "unattractive" group were given green leg rings. These preferences have been confirmed in mate choice tests with females in the St. Andrews zebra finch population (Munro KM, unpublished honors thesis). Females were given sexually neutral colored (orange), numbered plastic leg rings for identification (Burley et al., 1982).
All birds were fed on a diet of mixed seed (foreign finch mix supplied by Haith's, Cleethorpes, Lincolnshire, U.K.), supplemented twice a week with a protein supplement (Haith's egg biscuit) and greens. Fresh drinking water, oystershell grit, and cuttlebone were available ad libitum.
Sexing
Chicks that survived to maturity were sexed from plumage characteristics. Any chicks that died prior to maturity and any fertile eggs (Arnold et al., 2003a) that failed to hatch were sexed using molecular techniques. DNA was extracted from chick/embryonic tissue using the Puregene DNA extraction kit (Gentra Systems, Minneapolis, USA). The cage experiment used molecular sexing methodology and primers modified from Griffiths et al. (1998), described by Rutstein et al. (2004b). In the aviary experiment, sex was identified using primers P2 and P17 according to the protocol in Arnold et al. (2003b), again modified from Griffiths et al. (1998).
Aviary experiment
Twenty males and 21 females were released into each of four outdoor aviaries (measuring 2.8 x 5.5 x 2.5 m) during the months of August and September 2001 at the Garscube Estate campus of the University of Glasgow. The experiment was repeated from May to August 2002 with different individuals.
Half the males were given green leg rings and half were given red leg rings. Importantly, the treatment groups were kept separate, so aviaries contained either all red-ringed males or all green-ringed males in order to control for assortative mating between treatments. After 2 weeks acclimation, aviaries were provided with a surplus of nest-boxes and nesting material. Eggs were collected and replaced with dummy eggs after 4 days of incubation or when candling revealed signs of development. In two aviaries in 2001 only, eggs were allowed to hatch and chick survival was monitored daily.
Cage experiment
Fifty male zebra finches were randomly assigned to either the attractive or unattractive group. Fifty females were weighed, measured (tarsus length), and randomly assigned a male from one of these groups. Pairs were kept in individual breeding cages measuring 75 x 40 x 40 cm, within the animal house in the University of St. Andrews. Cages were fitted with open nest-boxes, and birds were maintained on a 16:8 h light:dark lighting schedule under full-spectrum lights (Hunt et al., 1997). Cages were arranged so that they could view other cages for comparison of ring color.
We checked nest-boxes daily between 0900 and 1000 h. We removed the second egg of each clutch for androgen analysis (as part of a separate experiment to investigate the effects of androgen deposition on offspring development) and replaced it with a dummy egg. Second eggs were placed in an incubator at 37.5°C for 72 h so that the embryo would be large enough for sexing. Eggs were stored at –20°C for later dissection and removal of embryonic tissue for DNA extraction. The remaining eggs were left in the nest to hatch. Chick survival was monitored daily.
Once the chicks had reached independence (35 days of age), pairs were separated and transferred to single-sex groups for 1 month. All females that laid fertile eggs were given a month's break. These females were then reweighed and paired with a different mate from the other treatment group. Females paired with red-ringed males in the first round of breeding were now given green-ringed males and viceversa. The above experimental procedure was repeated.
Statistical analyses
The overall sex ratio for each treatment was analyzed using G tests. Because chicks within the brood may not be independent, brood sex ratios (sons/number sexed) and mortality data were also analyzed at the brood level by fitting a generalized linear mixed model (GLMM) using the GLIMMIX macro in SAS (SAS Institute, 1998). The error distribution was binomial with a logit link, weighted by brood size. Paternal ring color was entered as a fixed factor and female as a random factor. In the aviary experiment, only the first clutch per pair was included, and colony was also entered as a random factor to control for any aviary effects. As an indicator of female condition, we used residual of body mass on tarsus length in the cage experiment and latency to laying in the aviary experiment. Nonsignificant factors were excluded in a backwards stepwise fashion with nonsignificant interactions excluded first. All models used a Satterthwaite correction for degrees of freedom. Standard errors (SE) are presented for all means.
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RESULTS |
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Aviary experiment
Analyses were carried out on first clutches from 36 green-ringed male pairs (mean clutch size ± SE: 4.33 ± 1.43 eggs) and 44 red-ringed male pairs (4.34 ± 1.57 eggs). Sex identification was successful for 78% of eggs (122/156) laid by females paired to green-ringed males and 76% of eggs (145/191) laid by those with red-ringed mates (Gadj1 = 0.35, p > .5). Molecular sexing failed in a few cases because eggs were infertile or DNA could not be extracted as it was too degraded. In the majority of cases, eggs could not be sexed because they had been broken or disappeared before collection. There was no effect of year on the clutch sex ratio at laying (F1,77 = 0.0, p = .99) and so data were pooled for both years.
Overall, the number of male and female offspring did not differ significantly from parity at laying (Table 1). In a GLMM (Table 2), the mean clutch sex ratio at laying did not vary with paternal ring color (mean clutch sex ratio: red-ringed male pairs, 0.54 ± 0.31; green-ringed male pairs, 0.49 ± 0.29), clutch size or female quality. Aviary identity was entered into the model as a random factor to control for the potential nonindependence of nests within the same aviary but was nonsignificant in this analysis. In the two aviaries in which eggs were allowed to hatch, neither was there a significant difference in the clutch sex ratio at laying for red- ringed (0.43 ± 0.28) and green-ringed male pairs (0.55 ± 0.19, F1,21 = 2.39, p = .14) nor was there a significant difference at hatching (red-ringed male pairs, 0.45 ± 0.34; green-ringed male pairs, 0.58 ± 0.18; Table 2) or at fledging (red-ringed male pairs, 0.39 ± 0.31; green-ringed male pairs, 0.58 ± 0.18; Table 2). By adulthood (approximately 4 months of age), however, the mean brood sex ratio was significantly more male-biased among green-ringed male pairs (0.57 ± 0.22) compared with red-ringed male pairs (0.28 ± 0.34, Table 2).
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This difference at adulthood was due to differential mortality after fledging. Mortality was significantly higher among offspring of red-ringed male pairs (F1,23 = 11.55, p = .003) and among male offspring (F1,60 = 12.06, p = .001).
Cage experiment
In the first breeding round, fertile clutches (i.e., clutches comprising at least one fertile egg) were laid by 17 females mated to red-ringed males (mean clutch size ± SE: 4.77 ± 0.33 eggs) and 15 females mated to green-ringed males (mean clutch size: 4.77 ± 0.43 eggs). Sex identification was successful for 90% of eggs (81/90) from red-ringed male pairs and for 85% of eggs (70/82) from green-ringed male pairs (Gadj1 = 0.84, p > .7). The remainder of the eggs either showed no sign of embryonic development, so were presumed to be infertile, or were broken by the birds soon after laying.
Overall, an equal proportion of male and female eggs was produced in both treatments (Table 1), and in a GLMM the mean clutch sex ratio per female also did not differ between treatments (mean clutch sex ratio ± SE: red-ringed male pairs, 0.43 ± 0.05; green-ringed male pairs, 0.50 ± 0.06; Table 2). There was also no effect of female quality or clutch size on the mean clutch sex ratio (Table 2).
Twenty-seven pairs hatched young in round one (14 red-ringed male pairs and 13 green-ringed male pairs). More female chicks hatched in the red-ringed treatment, whereas an equal proportion of males and females hatched in the green-ringed treatment (Table 1). However, the mean brood sex ratio was not significantly different between the two treatments (mean brood sex ratio ± SE: red-ringed male pairs, 0.31 ± 0.08; green-ringed male pairs, 0.50 ± 0.08; Table 2).
Twenty-two pairs fledged young in round one (11 in each treatment). Again, significantly more female chicks fledged in the red-ringed treatment, whereas an equal proportion of males and females fledged in the green-ringed treatment (Table 1). The mean fledged brood sex ratio was significantly more female biased among red-ringed male pairs (0.19 ± 0.06) than among green-ringed male pairs (0.54 ± 0.08, Table 2). At adulthood, there remained a female-bias among offspring of red-ringed male pairs (Table 1), and again the mean brood sex ratio was significantly more female biased among red-ringed male pairs (0.21 ± 0.07) compared with green-ringed male pairs (0.52 ± 0.08, Table 2).
This change in the sex ratio between treatments was due to differential embryonic mortality. In a GLMM, male embryo mortality was significantly higher than female embryo mortality (Table 3), and markedly so among red-ringed male pairs (red-ringed male pairs: 63% [17/27] of male embryos died compared with 17.9% [7/39] of female embryos, F1,47 = 8.46, p = .006; green-ringed male pairs: 31% [9/29] of male embryos died compared with 20% [6/30] of female embryos, F1,42 = 0.26, p = .61; interaction between ring color and embryo sex: F1,91 = 3.07, p = .08). There was no effect of ring color, hatchling sex, or brood size on posthatching mortality, but the offspring of mothers in poorer condition had lower survival rates (Table 3). Postfledging, there was no effect of ring color, fledgling sex, brood size, or female quality on mortality (Table 3).
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Within-female analyses of the primary sex ratio
In the cage experiment, 24 females that laid fertile clutches in round one also laid fertile clutches in their second breeding attempt with a new male. In a paired GLMM analysis for these 24 females, there was no effect of ring color on the sex ratio at laying (mean clutch sex ratio ± SE: red-ringed male pairs, 0.42 ± 0.06; green-ringed male pairs, 0.46 ± 0.06, F1,23 = 0.35, p = .56) and there was no effect of order of treatment, that is, whether females were paired with a red- or a green-ringed male first (F1,22 = 0.79, p = .38).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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In the light of Burley's widely cited studies, we examined whether and at what stage zebra finches adjusted their sex ratio in relation to paternal attractiveness. We predicted that any sex ratio skew would be observed at laying because sex ratio adjustment is more efficient at this early stage, compared with later mechanisms of sex ratio adjustment (Komdeur and Pen, 2002
). However, using two different experimental designs we found no significant differences in the primary sex ratio between attractiveness treatments. This remained true for the paired analysis of the cage experiment, which was designed to provide a more powerful test of the ability of individual females to adjust their sex ratio (Oddie and Reim, 2002).
A failure to detect a sex ratio skew at laying suggests that either females are incapable of adjusting their sex ratio at this stage or that it is not advantageous to do so under these conditions. We would expect sex ratio adjustment to be advantageous in zebra finches because attractive males benefit from increased reproductive success (Burley, 1985, 1986b, 1988; Burley et al., 1994, 1996), and extrapair paternity has been found both in the wild, albeit at a low frequency (Birkhead et al., 1990), and in captivity (Birkhead et al., 1989). Therefore, sexual selection would act more strongly in males, and this is reflected by the high degree of plumage dimorphism between the sexes.
In studies with similar sample sizes, female zebra finches have been shown to facultatively adjust their sex ratio at laying (Rutkowska and Cichon, 2002; Rutstein et al., 2004b; but see Arnold et al., 2003b) and at hatching (Bradbury and Blakey, 1998; Kilner, 1998) in response to the experimental diet they received. There may be several reasons for this apparent discrepancy. Under poor dietary conditions female chicks reared under restricted food conditions have lower rates of growth and survival compared with male chicks (Bradbury and Blakey, 1998; de Kogel, 1997; Kilner, 1998; Martins, 2004), and female reproductive success is more dependent on early developmental condition than that of males (Gorman and Nager, 2004; Haywood and Perrins, 1992). Therefore, rearing conditions would exert a particularly strong selection pressure on females to skew the sex ratio. Furthermore, it could be that high-quality genes from attractive fathers benefit not only sons but equally benefit daughters (good genes hypothesis; Zahavi, 1975), especially if extrapair paternity rates are relatively low, as suggested by the only study carried out in the wild to date (Birkhead et al., 1990). As a result, the net benefit from being fathered by an attractive male might not differ substantially between the sexes.
Existing data in other species also suggest that sex ratio adjustment is more likely to occur in response to condition-determining (rather than attractiveness) cues. In great reed warblers, Acrocephalus arundinaceous, male nestling provisioning was correlated with the sex ratio at hatching but male attractiveness was not (Westerdahl et al., 1997, 2000). Similarly, in blue tits, Parus caeruleus, female age and nest-box location had stronger effects on primary sex ratio bias than did male ultraviolet plumage ornaments (Sheldon et al., 1999). Therefore, lower selection pressure on sex ratio manipulation in response to paternal attractiveness traits may be generally true among birds.
A second possibility is that male quality is harder for females to assess compared with environmental quality and their own condition (West and Sheldon, 2002). Therefore, it would not be advantageous for females to adjust the primary sex ratio after only a week or so within pairing with a new male. This may be especially true of nonterritorial species such as the zebra finch (and in territorial species it is hard to tease apart territory quality from male quality). By the time that the chicks have hatched, the female may be better able to assess a male's quality, in which case, a later mechanism of brood sex ratio adjustment could be implemented.
If females do not or cannot adjust their primary sex ratio in relation to mate attractiveness, then a sex ratio skew at hatching or fledging may be brought about by differential mortality, either due to direct parental manipulation, as proposed by Burley (1986a), or by nonadaptive differential vulnerability of one sex (Martins, 2004). There was a higher postfledging mortality among offspring of red-ringed male pairs in the aviary experiment. However, this needs to be interpreted cautiously because broods within the same aviary might not be independent, although we found no aviary effect in the analysis of the larger data set. The cage experiment found clear evidence of differential mortality, with greater male embryonic mortality among red-ringed male pairs compared with green-ringed male pairs. Consequently, the sex ratio at maturity was more female biased among red-ringed male pairs, which is the opposite result to that found by Burley (1981, 1986a).
One possible cause of this differential embryo mortality is that females mated to attractive males deposited higher concentrations of yolk androgens in their eggs. This was found to be the case in a study by Gil et al. (1999), conducted on zebra finches at St. Andrews University, in which yolk androgens were assayed in whole clutches of freshly laid eggs. Although we did not find any difference in androgen concentrations between attractiveness treatments (for results see Rutstein et al., 2004a), we removed only the second egg, which may not give a full picture for the whole clutch, and allowed an embryo to develop, which may affect yolk androgen levels (Elf and Fivizzani, 2002; Rutstein et al., 2005), and so may not represent initial maternal allocation. While the majority of avian studies suggest that androgens may be beneficial to offspring (Eising and Groothuis, 2003; Eising et al., 2001; Lipar and Ketterson, 2000; Schwabl, 1993, 1996), elevated concentrations of androgens may also be harmful to offspring and reduce hatching success (Sockman and Schwabl, 2000). Gil et al. (1999) proposed that females increased their allocation of androgens to eggs fathered by attractive males because these (presumed higher quality) offspring would be worth or could withstand the elevated costs of high androgen concentrations. Because male attractiveness was artificially altered in our experiment, and therefore offspring would not have been of higher genetic quality, the embryos may not have been able to withstand any elevation in yolk androgens. Male eggs may have been more susceptible to maternal hormones (von Engelhardt et al., 2004), or females may have deposited higher concentrations of androgens in male eggs (Müller et al., 2002; Petrie et al., 2001). If this were the case, then the secondary sex ratio skew observed in our study would have been a nonadaptive by-product of heavy investment in eggs fathered by more attractive males. The assortative mating that may have occurred in Burley's aviary experiments between attractive males and high-quality females would have resulted in offspring that were of higher quality than the average for the aviary. These offspring may not have been adversely affected by elevated yolk androgen levels and, elevated androgen levels in these high-quality eggs may have benefited sons.
Could differences in experimental design have led to such contrasting results between ours and Burley's study for other reasons? The female zebra finches in Burley's study were exposed to both attractive and unattractive males in the aviary. It is possible, therefore, that this comparison is necessary for females to gauge the attractiveness of their mate. However, several factors make this explanation unlikely. First, all females had bred before, and therefore would possess some "bench mark" of male attractiveness. Second, in the cage experiment, females could view other males with different ring colors. Finally, in the study of Gil et al. (1999), there was a clear effect of male attractiveness using a similar cage design, in which females could not compare between males. One possibility that cannot, however, be ruled out is that sex ratio manipulation in relation to male attractiveness may only be beneficial in a "population" comprising both attractive and unattractive individuals. Only in such a population are there large perceived benefits of producing sons when mated to an attractive male because attractive sons will obtain superior mates and greater opportunities for EPCs.
In conclusion, we found no support for the prediction from the sexy son hypothesis that females should produce male-biased clutches when mated with an attractive male. There was no sex ratio skew at laying, and we unexpectedly found a female bias among red-ringed male pairs at sexual maturity. Assortative mating in the studies of Burley (1981, 1986a) may have confounded her results because female quality would not be independent of male quality. This requires further testing, first to look at mate choice within aviaries containing both attractive and unattractive males, and, in addition, we need a more detailed study of primary sex allocation, offspring sex ratios, and survival rates in relation to both male and female quality. Finally, our data add to a considerable body of evidence that has failed to find an adaptive sex ratio skew in relation to paternal attractiveness (Saino et al., 1999; Westerdahl et al., 1997, but see Grindstaff et al., 2001; Leech et al., 2001; Radford and Blakey, 2000; Saino et al., 2002; Westneat et al., 2002; Zann and Runciman, 2003). This may be because, compared with other factors such as rearing environment, male attractiveness does not represent as strong a selection pressure on maternal sex allocation as previously believed.
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ACKNOWLEDGEMENTS |
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At Glasgow, we thank G. Adam, A. Kirk, J. Laurie, and G. Law for help with bird husbandry. At St. Andrews, we thank I. Maynard and A. Oliver for help with husbandry. We also thank the Biotechnology and Biological Sciences Research Council for funding A.N.R. and L.G. and the Natural Environment Research Council for providing a studentship for H.E.G. K.E.A. is supported by a Royal Society University Research Fellowship.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Andersson S, 1986. Evolution of condition-dependent sex ornaments and mating preferences: sexual selection based on viability differences. Evolution 40:804–816.[CrossRef][ISI]
Arnold KE, Orr KJ, Griffiths R, 2003a. Primary sex ratios in birds: problems with molecular sex identification of undeveloped eggs. Mol Ecol 12:3451–3458.[CrossRef][Medline]
Arnold KE, Griffiths R, Stevens DJ, Orr KJ, Adam A, Houston DC, 2003b. Subtle manipulation of egg sex ratio in birds. Proc R Soc B 2:216–219.
Birkhead T, Burke T, Zann R, Hunter FM, Krupa AP, 1990. Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata, revealed by DNA fingerprinting. Behav Ecol Sociobiol 27:315–324.[CrossRef]
Birkhead TR, Hunter FM, Pellatt EJ, 1989. Sperm competition in the zebra finch Taeniopygia guttata. Anim Behav 38:935–950.[CrossRef]
Blank JL, Nolan VJ, 1983. Offspring sex ratio in red-winged blackbirds is dependent on maternal age. Proc Natl Acad Sci USA 80:6141–6145.
Blount JD, Metcalfe NB, Birkhead TR, Surai PF, 2003. Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science 300:125–127.
Bradbury RR, Blakey JK, 1998. Diet, maternal condition, and offspring sex ratio the zebra finch, Poephila guttata. Proc R Soc B 265:895–899.[CrossRef]
Burley N, 1981. Sex-ratio manipulation and selection for attractiveness. Science 211:721–722.
Burley N, 1985. Leg-band color and mortality patterns in captive breeding populations of zebra finches. Auk 102:647–651.
Burley N, 1986a. Sex-ratio manipulation in color-banded populations of zebra finches. Evolution 40:1191–1206.[CrossRef][ISI]
Burley N, 1986b. Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445.[CrossRef][ISI]
Burley N, 1988. The differential-allocation hypothesis—an experimental test. Am Nat 132:611–628.[CrossRef][ISI]
Burley N, Coopersmith CB, 1987. Bill color preferences of zebra finches. Ethology 76:133–151.
Burley N, Krantzberg G, Radman P, 1982. Influence of color-banding on the conspecific preferences of zebra finches. Anim Behav 30:444–455.[CrossRef]
Burley NT, Enstrom DA, Chitwood L, 1994. Extra-pair relations in zebra finches—differential male success results from female tactics. Anim Behav 48:1031–1041.[CrossRef]
Burley NT, Parker PG, Lundy K, 1996. Sexual selection and extrapair fertilisation in a socially monogamous passerine, the zebra finch Taeniopygia guttata. Behav Ecol 7:218–226.
Charnov EL, 1982. The theory of sex allocation. Princeton, New Jersey: Princeton University Press.
Collins SA, Hubbard C, Houtman AM, 1994. Female mate choice in the zebra finch—the effect of male beak color and male song. Behav Ecol Sociobiol 35:21–25.[CrossRef][ISI]
de Kogel CH, 1997. Long-term effects of brood size manipulation on morphological development and sex-specific mortality of offspring. J Anim Ecol 66:167–178.[CrossRef]
de Kogel CH, Prijs HJ, 1996. Effects of brood size manipulations on sexual attractiveness of offspring in the zebra finch. Anim Behav 51:699–708.[CrossRef]
Eising CM, Eikenaar C, Schwabl H, Groothuis TGG, 2001. Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc B 268:839–846.[Medline]
Eising CM, Groothuis TG, 2003. Yolk androgens and begging behaviour in black-headed gull chicks: an experimental study. Anim Behav 66:1027–1034.[CrossRef]
Elf PK, Fivizzani AJ, 2002. Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool 293:594–600.[CrossRef][ISI][Medline]
Ellegren H, Gustafsson L, Sheldon BC, 1996. Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc Natl Acad Sci USA 93:11723–11728.
Gil D, Graves J, Hazon N, Wells A, 1999. Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128.
Gorman HE, Nager RG, 2004. Prenatal developmental conditions have long-term effects on offspring fitness. Proc R Soc B 271:1923–1928.[CrossRef]
Griffiths R, Double MC, Orr K, Dawson RJG, 1998. A DNA test to sex most birds. Mol Ecol 7:1071–1075.[CrossRef][Medline]
Grindstaff JL, Buerkle CA, Casto JM, Nolan V, Ketterson ED, 2001. Offspring sex ratio is unrelated to male attractiveness in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 50:312–316.[CrossRef]
Hamilton WD, Zuk M, 1982. Heritable true fitness and bright birds: a role for parasites? Science 218:384–387.
Haywood S, Perrins CM, 1992. Is clutch size in birds affected by environmental conditions during growth. Proc R Soc B 249:195–197.[Medline]
Hoelzer GA, 1989. The good parent process of sexual selection. Anim Behav 38:1067–1978.[CrossRef]
Houtman AM, 1992. Female zebra finches choose extra-pair copulations with genetically attractive males. Proc R Soc B 249:3–6.[CrossRef]
Howe HF, 1976. Egg size, hatching asynchrony, sex and brood reduction in the common grackle. Ecology 57:1195–1207.[CrossRef][ISI]
Hunt S, Cuthill IC, Swaddle JP, Bennett ATD, 1997. Ultraviolet vision and band-colour preferences in female zebra finches Taeniopygia guttata. Anim Behav 54:1369–1382.[CrossRef][ISI][Medline]
Jennions MD, Petrie M, 2000. Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64.[Medline]
Kilner R, 1998. Primary and secondary sex ratio manipulation by zebra finches. Anim Behav 56:155–164.[CrossRef][ISI][Medline]
Kölliker M, Heeb P, Werner I, Mateman AC, Lessells CM, Richner H, 1999. Offspring sex ratio is related to male body size in the great tit (Parus major). Behav Ecol 10:68–72.
Komdeur J, Pen I, 2002. Adaptive sex allocation in birds: the complexities of linking theory and practice. Phil Trans R Soc B 357:373–380.
Leech DI, Hartley IR, Stewart IRK, Griffith SC, Burke T, 2001. No effect of parental quality or extrapair paternity on brood sex ratio in the blue tit (Parus caeruleus). Behav Ecol 12:674–680.
Lipar JL, Ketterson ED, 2000. Maternally-derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird. Proc R Soc B 267:2005–2010.[Medline]
Martins TLF, 2004. Sex-specific growth in zebra finch nestlings: a possible mechanism for sex ratio adjustment. Behav Ecol 15:174–180.
Müller W, Eising CM, Dijkstra C, Groothuis TGG, 2002. Sex differences in yolk hormones depend on maternal social status in Leghorn chickens (Gallus gallus domesticus). Proc R Soc B 269:2249–2255.[Medline]
Nishiumi I, Yamagishi S, Maekawa H, Shimoda C, 1996. Paternal expenditure is related to brood sex ratio in polygynous great reed warblers. Behav Ecol Sociobiol 39:211–217.[CrossRef][ISI]
Norris KJ, 1990. Female choice and the quality of parental care in the great tit Parus major. Behav Ecol Sociobiol 27:275–281.
Oddie KR, 2000. Size matters: competition between male and female great tit offspring. J Anim Ecol 69:903–912.[CrossRef]
Oddie KR, Reim C, 2002. Egg sex ratio and paternal traits: using within-individual comparisons. Behav Ecol 13:503–510.
Petrie M, Schwabl H, Brande-Lavridsen N, Burke T, 2001. Maternal investment—sex differences in avian yolk hormone levels. Nature 412:498–498.[Medline]
Pike TW, Petrie M, 2003. Potential mechanisms of avian sex manipulation. Biol Rev 78:553–574.[Medline]
Price DK, 1996. Sexual selection, selection load and quantitative genetics of zebra finch bill colour. Proc R Soc B 263:217–221.
Price DK, Burley NT, 1993. Constraints on the evolution of attractive traits: genetic (co)variance of zebra finch bill colour. Heredity 71:405–412.
Radford AN, Blakey JK, 2000. Is variation in brood sex ratios adaptive in the great tit (Parus major)? Behav Ecol 11:294–298.
Ratcliffe LM, Boag PT, 1987. Effects of color bands on male competition and sexual attractiveness in zebra finches (Poephila guttata). Can J Zool 65:333–338.
Rintamaki PT, Lundberg A, Alatalo RV, Hoglund J, 1998. Assortative mating and female clutch investment in black grouse. Anim Behav 56:1399–1403.[CrossRef][ISI][Medline]
Rutkowska J, Cichon M, 2002. Maternal investment during egg laying and offspring sex: an experimental study of zebra finches. Anim Behav 64:817–822.[CrossRef]
Rutstein AN, Gilbert L, Slater PJB, Graves JA, 2004a. Mate attractiveness and primary resource investment in the zebra finch. Anim Behav 68:1087–1094.[CrossRef]
Rutstein AN, Gilbert L, Slater PJB, Graves JA, 2005. Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch. Behav Ecol 16:62–69.
Rutstein AN, Slater PJB, Graves JA, 2004b. Diet quality and resource allocation in the zebra finch. Biol Lett 271:S286–S289.[CrossRef]
Saino N, Ellegren H, Møller AP, 1999. No evidence for adjustment of sex allocation in relation to paternal ornamentation and paternity in barn swallows. Mol Ecol 8:399–406.[CrossRef]
Saino N, Ferrari R, Martinelli R, Romano M, Rubolini D, Møller AP, 2002. Early maternal effects mediated by immunity depend on sexual ornamentation of the father in the barn swallow (Hirundo rustica). Proc R Soc B 269:1005–1009.[Medline]
SAS Institute, 1998. SAS/STAT user's guide, v. 8. Cary, North Carolina: SAS Institute.
Schwabl H, 1993. Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450.
Schwabl H, 1996. Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Physiol A Mol Integr Physiol 114:271–276.
Sheldon BC, 2000. Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402.[CrossRef][Medline]
Sheldon BC, Andersson S, Griffith SC, Ornborg J, Sendecka J, 1999. Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877.[CrossRef]
Sockman KW, Schwabl H, 2000. Yolk androgens reduce offspring survival. Proc R Soc B 267:1451–1456.[Medline]
Stamps J, Clark A, Kus B, Arrowood P, 1987. The effects of parent and offspring gender on food allocation in budgerigars. Behaviour 101:177–199.
Teather KL, Weatherhead PJ, 1989. Sex-specific mortality in nestling great-tailed grackles. Ecology 70:1485–1493.[CrossRef]
Ten Cate C, Mug G, 1984. The development of mate choice in zebra finch females. Behaviour 90:125–150.
Trivers RL, Willard DE, 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–91.
von Engelhardt N, Dijkstra C, Daan S, Groothuis TGG, 2004. Effects of 17-ß-estradiol treatment of female zebra finches on offspring sex ratio and survival. Horm Behav 45:306–313.[CrossRef][Medline]
Weatherhead PJ, Robertson RJ, 1979. Offspring quality and the polygyny threshold: ‘the sexy son hypothesis’. Am Nat 113:201–208.[CrossRef][ISI]
West SA, Sheldon BC, 2002. Constraints in the evolution of sex ratio adjustment. Science 295:1685–1688.
Westneat DF, Stewart IRK, Woeste EH, Gipson J, Abdulkadir L, Poston JP, 2002. Patterns of sex ratio variation in house sparrows. Condor 104:598–609.[CrossRef]
Westerdahl H, Bensch S, Hansson B, Hasselquist D, von Schantz T, 1997. Sex ratio variation among broods of great reed warblers Acrocephalus arundinaceus. Mol Ecol 6:543–548.[CrossRef]
Westerdahl H, Bensch S, Hansson B, Hasselquist D, von Schantz T, 2000. Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler (Acrocephalus arundinaceus). Behav Ecol Sociobiol 47:312–318.[CrossRef]
Yamaguchi N, Kawano KK, Eguchi K, Yahara T, 2004. Facultative sex ratio adjustment in response to male tarsus length in the varied tit Parus varius. Ibis 126:108–113.
Yasukawa K, McClure JL, Boley RA, Zanocco J, 1990. Provisioning of nestling by male and female red-winged blackbirds, Agelaius phoeniceus. Anim Behav 40:153–166.[CrossRef]
Zahavi A, 1975. Mate Selection - Selection for a Handicap. J Theor Biol 53:205–214.[CrossRef][ISI][Medline]
Zann R, Runciman D, 2003. Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations. Behav Ecol Sociobiol 54:294–302.[CrossRef]
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  T. W. Fawcett, B. Kuijper, I. Pen, and F. J. Weissing Should attractive males have more sons? Behav. Ecol., January 1, 2007; 18(1): 71 - 80. [Abstract] [Full Text] [PDF]
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