Frank, S. A. 1990. Sex allocation theory for birds and mammals. Annual Review of Ecology and Systematics 21:13-55.

Parents divide their reproductive effort into the production of sons and daughters. Darwin (1871) was intrigued by the fact that parents usually split their effort so that approximately equal numbers of sons and daughters are raised. He believed that this male:female ratio had been adjusted by natural selection because he understood that the number of females set a limit on reproductive capacity. He could not, however, clearly specify how natural selection shaped the sex ratio. Fisher (1930, 1958) provided the explanation by noting that frequency-dependent selection stabilizes the sex ratio near equality.

Since Fisher presented his explanation, many examples of biased sex ratios have been observed in nature. For example, Hamilton (1967) observed very female-biased sex ratios in parasitic wasps that mate in small groups. Hamilton explained this bias by showing that in these wasps the mating competition among brothers violates a latent assumption in Fisher's argument.

In other examples of observed biases, the explanations put forth provided new dimensions to Fisher's central theory rather than direct exceptions. The most important of these new dimensions for birds and mammals was observed by Trivers and Willard (1973). They noted that, in some mammals, healthy mothers tended to produce a relatively higher proportion of sons than unhealthy mothers. They explained this pattern of variation among families by suggesting that a healthy son is reproductively more valuable than a healthy daughter and that a mother's health partly determines her offspring's vigor.

The point of these examples is to show how sex allocation theory has grown by a series of interesting observations, single-cause explanations, exceptions and new explanations. This is a natural way for a theory to grow. One problem, however, is that logical flaws slip easily into such a haphazard structure. For example, the Trivers-Willard (1973) model about variation in sex ratio among families is nearly always applied simultaneously with Fisher's model for equal sex ratio at the population level. Actually, the assumptions required for the Trivers-Willard model imply that Fisher's theory cannot apply (Frank 1987). The fact that these two theories are about different types of sex ratio pattern has led to the mistaken belief that the ideas can be applied independently.

The vast literature on sex allocation theory has been reviewed several times recently (Bull 1983; Bull and Charnov 1988; Charnov 1982; Karlin and Lessard 1986). Several reviews of observed sex allocation patterns in birds and mammals are also available (Clutton-Brock 1986; Clutton-Brock and Iason 1986; Hrdy 1987). I believe, however, that the logical structure of sex allocation theory has not been adequately reconciled with the natural history of birds and mammals. The main ideas of the theory were developed for organisms with little or no parental care, with mechanisms of sex ratio adjustment such as haplodiploidy or environmental sex determination, with no trade-offs between the sex ratio of a current brood and future reproduction, and often for simultaneous or sequential hermaphrodites.

By contrast with the types of natural history that sex allocation theory has attempted to explain, birds and mammals are characterized by extensive parental care, a sex determination mechanism that to some extent constrains sex ratio, complex mechanisms for adjusting parental investment in the sexes, variation in these mechanisms at all taxonomic levels, and a trade-off between current sex ratio and future reproduction. A complete theory for birds and mammals must show how various aspects of life history may interact in determining the patterns of selection on sex allocation. The theory viewed in total will expose some flaws in the simple single-cause explanations that typify application of sex allocation theory to birds and mammals.

Overview

Two different perspectives on the theory must be summarized in order to provide an accurate description of its current state. The first is the series of observations and single-cause explanations that defines the history of the field. The second is the set of logical relationships among these single-cause explanations that define the structure of the theory and the interactions that must be considered when applying the theory to real cases. For these reasons I will review the theory in a loosely chronological way but will use hindsight to explain ideas and provide commentary. This approach will allow me to highlight the logical structure of the theory from a modern perspective and to show how some logical flaws have slipped into common usage.

In the first section of this review I will recount the major single-cause forces that shape sex allocation biases. In the second section I will describe how the theory has expanded and become more realistic as the ideas were first applied and authors critically evaluated the structure of the theory in light of these applications.

Early theoretical and empirical studies of sex allocation focused mainly on adaptive significance, with less attention paid to mechanism, genetics, ontogeny and phylogeny. To some authors this has been irksome, since in an ideal world knowledge of phylogenetic history and of the genetic and phenotypic bases of variation must precede analyses of adaptive significance. I have delayed discussion of the bases of variation until the third section because these issues were not central to the early development of the field, which was guided by the patterns most easily observed in nature and by the simplest explanations available. I will briefly summarize a few of the many fascinating discoveries about mechanism that have been made recently. Here as in other sections of the paper I will cite empirical studies only to the extent that they help to understand the theory.

Up to now I have been lax about the distinction between the numbers of sons and daughters that a family produces and the relative amount of resource that is devoted to sons and daughters. From this point I will use sex ratio for the relative number of sons and daughters and sex allocation for the relative amounts of energy and resource devoted to sons and daughters.