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Heredity 80 (1998) 397–402 Received 17 November 1997 Short Review Recent studies of avian sex ratios BEN C. SHELDON Department of Zoology, Uppsala University, Villav¨agen 9, S-752 36 Uppsala, Sweden Sex allocation theory, and its success in predicting sex ratios demonstrations of sex ratio biases consistent with sex alloca- in such taxa as parasitoid wasps, is often cited as one of the tion theory in wild bird populations. Solution of the second crowning achievements of theoretical evolutionary biology. problem may come with the incorporation of realistic life Its success in some vertebrate taxa, particularly birds, has history data into models and the use of experimental manip- been more modest. I discuss two reasons for this. First, it is ulations to reveal the fitness consequences of allocation strat- difficult to obtain avian sex ratio data before substantial egies. Further data concerning sex ratio variation in taxa such offspring mortality has occurred. Second, the theory and data as birds, with chromosomal sex determination, are valuable required to predict sex allocation patterns (let alone sex ratio because they allow the investigation of the role of constraint patterns) in vertebrates are complex and hard to obtain. vs. adaptation in evolution. Recently developed molecular genetic techniques allowing Keywords: natural selection, sex allocation, sex identifica- sex identification from DNA samples have largely solved the tion, sex ratio, sexual selection. first problem and there have been several striking empirical Separate sexes are associated with sex-differences in life paucity of studies showing even minor skews in sex ratio in histories. A consequence of this is that selection acts differ- directions consistent with expectations from theory. Williams ently in the two sexes, which can change the relative repro- (1979) concluded famously, that the best data from birds ductive value of each sex of offspring. As a result individuals ‘give no support to any theory of adaptive sex ratio evolution’ are selected to vary their allocation of resources between the and suggested that this reflected a constraint imposed by the sexes. Major contributions to sex allocation theory were Mendelian process of meiosis. Although evidence to support made by Fisher (1930), Hamilton (1967) and Charnov (1982). the existence of adaptive sex ratio skews has since been Three broad classes of process can be expected to influence obtained from outcrossed bird and mammal populations, the optimal sex allocation by parents: differential costs, such patterns do not seem to be very common. In this review conditional sex allocation and structured populations I describe some recent studies of sex ratio variation in birds, (recently reviewed by Hardy, 1997). The success of sex alloca- and discuss some ways in which this field may develop. tion theory in predicting patterns of sex allocation in nature Although this review describes data that are relevant to the has, in some cases, been extraordinary. Thus, sex allocation theory of sex allocation, most of the studies described here theory is able to predict with considerable accuracy the have addressed the sex ratio. Sex allocation is the quantity on proportion of female eggs that a female parasitoid wasp which selection acts, whereas the sex ratio merely describes should lay, dependent on both host size and the number of the relative numbers of sons and daughters; the two need not females that have already laid in a given host (reviewed by be equivalent. Unfortunately, the sex ratio is far easier to Godfray, 1994); the rate of outcrossing of malarial parasites measure than is sex allocation. For the remainder of this from the sex ratio of gametocytes measured from blood review I assume, as have most studies, that the sex ratio smears of infected hosts (Read et al., 1995); and the timing of reflects sex allocation. Further, I address only studies relating sex reversal in marine shrimps on the basis of changes in to adaptive sex allocation at the level of the individual family. population structure (Charnov, 1982). It is not surprising that Population level patterns of sex allocation are interesting in sex allocation theory is often cited in textbooks as one of the their own right (Clutton-Brock, 1986), but most recent most successful areas of theoretical evolutionary biology (e.g. studies have not been concerned with the population sex Ridley, 1993). ratio, and few have involved samples large enough to detect If one were to restrict an assessment of the predictive any but the largest deviations from equality with much success of sex allocation theory to vertebrate taxa with power. chromosomal sex determination, particularly birds, the I have nothing to say about the genetics of sex ratio varia- verdict would be less favourable. Few studies have been able tion in birds in this review, other than to repeat the often- to make and test quantitative predictions and there is also a noted conclusion (based on selection experiments with poultry) that there is no evidence for any such variation, nor Correspondence. Tel.:+46/ 18 4712655; Fax:+46/ 18 559888; any evidence for the operation of non-Mendelian sex ratio E-mail: [email protected] distorters as found more often in invertebrates (Hardy, ©1998 The Genetical Society of Great Britain. 397 398 B. C. SHELDON 1997). The theories of adaptive sex allocation described tion. First, if there is selection for biased sex allocation at the below are silent about whether genetic variation for the sex family level, then equal allocation at the population level is ratio should be present in contemporary populations. no longer evolutionarily stable. Second, it is unlikely that studying just the variance in family sex ratios will reveal anything of interest about adaptation. New techniques for sex identification Some specific characteristics of avian life histories have Although the adults of many bird species show conspicuous consequences for predicting sex allocation. For example, the sexual dimorphism in either size or colour, this dimorphism is simplest model of sex allocation when fitness varies assumes often reduced or absent among juveniles. For most birds, the that the degree of bias in sex allocation is independent of the proportion of marked juveniles which are recaptured as reproductive value of the clutch (Bull, 1981; Charnov, 1982). adults is less than 10 per cent, so that it is usually hopeless to If this is the case, the optimum sex ratio is a step function expect sex ratios measured among adults to reveal biases in with a threshold at which a switch from production of one sex sex ratio among families. Although some species of birds to the other should occur (Fig. 1). While this assumption may which exhibit marked sexual size dimorphism (e.g. members be broadly true for hymenoptera where a female can poten- of the family Icteridae) can be readily sexed as nestlings on tially ‘determine’ offspring sex by deciding whether to fertil- the basis of body size before fledging, these species cannot ize each egg, it may not be true for birds. If birds are easily be used to test theories of adaptive sex allocation constrained by meiosis to produce an equal sex ratio, sex because sexual size dimorphism is probably correlated with allocation could only be modified by selectively favouring one sex differences in mortality (Clutton-Brock et al., 1985). Thus, sex of offspring over the other, and the sex ratio could only environmentally caused sex-biased mortality can generate a be altered by killing more offspring of one sex. Since such correlation between environmental quality and sex ratio of actions would reduce the reproductive value of the clutch, the same sign as that expected were parents to adjust sex the optimal sex allocation pattern will show a gradual ratios adaptively. Also, sex cannot be determined for very response to variation in the variable with differential effects small nestlings, or nestlings which die before hatching, so that on fitness. The costs of sex allocation in organisms with it is difficult to know whether a biased sex ratio reflects chromosomal sex determination (CSD) may therefore be one biased production or mortality. A reliable means to identify explanation of why sex ratio biases tend to be weaker than in sex at all developmental stages is required in order for sex organisms with more labile sex determination mechanisms. ratio variation to be described accurately. The assumption that CSD is a constraint tends to be made Birds, like mammals, have separate sex chromosomes more by default than in response to evidence to this effect. (females ZW, males ZZ), and this makes the isolation of Determining the mechanism(s) by which sex allocation occurs sex-specific genetic markers possible. Although sex-specific in birds is important because this information suggests how genetic markers have occasionally been discovered fortui- sex allocation theory should be applied. tously (for example while probing southern blots of genomic One further factor with potential influence on sex alloca- DNA with minisatellite sequences), a major step in the tion strategies concerns the extent to which parents are able development of simple molecular identification techniques to estimate the value of any variable with sex-specific effects was taken with Griffiths & Tiwari’s (1993) description of a on offspring fitness at the time when offspring sex is deter- method, based on randomly primed PCR, for isolating sex-linked markers. Recent developments have involved the characterization of a pair of highly conserved Z and W-linked genes (CHD1-Z and CHD1-W), for which locus-specific primers are now available, that can determine sex for almost all birds (Griffiths & Tiwari, 1995; Griffiths et al., 1996; Elleg- ren & Sheldon, 1997). Markers of this type have been used in a growing number of studies of avian sex ratios, often involv- ing retrospective analysis of sex ratio variation in samples originally collected for other purposes (e.g.

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