Trade-offs in life-history evolution

Trade-offs represent the costs paid in the currency of fitness when a beneficial change in one trait is linked to a detrimental change in another. If there were no trade-offs, then selection would drive all traits correlated with fitness to limits imposed by history and design. However, we find that many life-history traits are maintained well within those limits. Therefore, trade-offs must exist. Trade-offs have played a central role in the development of life-history theory, from Gadgil & Bossert (1970), Charnov & Krebs (1973), Schaffer (1972, 1974a, b) and Bell (1980) on to the present. They have been measured through field observations (e.g. Clutton-Brock, Guinness & Albon, 1982, 1983), through experimental manipulations in laboratory (e.g. Partridge & Farquhar, 1981) and field (e.g. Askenmo, 1979), through -phenotypic correlations in the laboratory (e.g. Bell, 1984a, b) and through genetic correlations (e.g. Rose & Charlesworth, 1981a, b), to mention only a few of the more prominent studies. They have been reviewed by Stearns (1976, 1977), Bell (1980), Charlesworth (1980), Warner (1984), Reznick (1985), Partridge & Harvey (1985, 1988) and most thoroughly by Bell & Koufopanou (1986). In addition, the methods used to measure trade-offs have been the subject of criticism (Tuomi, Hakala & Haukioja, 1983; Partridge, 1987) and controversy (Reznick, Perry & Travis, 1986; Bell, 1986). The most prominent life-history trade-off involves the cost of reproduction. It has two major components, costs paid in survival and costs paid in future reproduction. Two approaches to analysing those costs were suggested by Williams: genetic costs represented by antagonistic pleiotropy (Williams, 1957) and phenotypic costs represented by negative correlations between current reproductive effort and future survival and reproduction (Williams, 1966a, b). A third, physiological approach to trade-offs has been developed by Hirshfield & Tinkle (1974) and Calow (1979), among many others (cf. Townsend & Calow, 1981). In this extensive discussion, a few points have not always received the attention they deserve: (1) That trade-offs can be measured and analysed at the level of the genotype, the phenotype and what lies between (intermediate structure) is well known and uncontroversial but it has not always been emphasized that each of those levels makes an essential contribution to our understanding. It is not a question of either genetic correlations or phenotypic correlations or physiological trade-offs but of how such measurements combine to deliver information about potential evolutionary responses. A study conducted at just one of these levels is likely to be of as little use as the information on the nature of the elephant delivered by one blind man holding its tail. (2) One can draw a useful distinction between intraindividual trade-offs for example, between the reproductive effort made by a female in one season and the probability that she will survive to the next season and intergenerational trade-offs for example, between a female's reproductive effort and the probability that her offspring will survive to the next season. Intraindividual tradeoffs (and only some of them) have received most attention but intergenerational trade-offs, which are arguably just as important, have been relatively ignored. They deserve more attention. (3) The genetic structure of a population, in particular the genetic variance-covariance matrix for a set of important life-history traits, reflects the very recent past, describes the present and predicts the near-term future. There is no logical or direct way to use the current genetic structure of a population to infer the trade-offs that constrained the past approach to the current state even if they occurred as recently as a few tens of generations ago (J. Travis, personal communication). (4) Our understanding of a trade-off can be described as first order (slope known), second order (curvature known) or third order (all details, including interaction effects, known). In a few cases we have reliable information about firstorder effects. In no case known to me do we have reliable information on second-order effects, which are important in the theory (e.g. Schaffer, 1974a). Measurement of third-order effects, however desirable (Pease & Bull, 1988), remains a matter for future research.