Sex Allocation - Modern Research

Modern Research

Modern research on sex allocation began with Hamilton (1967), which made five pivotal contributions to the field of sex allocation, and evolutionary biology more generally. First, he showed how competition between relatives can select for biased sex allocation. When populations are structured such that brothers compete for mates, this leads to selection for a female biased sex allocation by a process that Hamilton termed local mate competition (LMC). This insight has led to one of the most productive areas of evolutionary biology. Second, Hamilton showed how the sex ratio can be modelled using game theory. His approach for determining the ‘unbeatable strategy’ was very similar to, and laid the ground-stones for the technically superior evolutionarily stable strategy (ESS) approach that was later formalised by Maynard Smith & Price (1973). Third, he showed that simple mathematical models could be used to make comparative predictions that could be easily tested. His specific example was to show that selection favours more female biased sex ratios when fewer females lay eggs on a patch, and that this could be tested either by comparing across species or by looking at how individuals vary their behaviour under different conditions. The use of comparative predictions is taken for granted today, because they form the daily bread of evolutionary and behavioural ecology research programmes. However, it should be remembered just how astounding it was at the time, to suggest that a few lines of simple maths could make testable predictions about how organisms should behave. Fourth, he showed how different genes within a genome can be selected to pursue their own selfish interests, to the detriment of other member of the genome, and the way in which meiotic drive fitted into this framework. Fifth, by emphasising the costliness of male production, and the evolution of parthenogenesis, it helped to initiate the debate over the adaptive function of sex.

The next major step was made by Trivers & Willard (1973) who showed that individuals could be selected to adjust the sex of their offspring in response to environmental conditions. They discussed their prediction in the context of mammals such as caribou, and why offspring sex ratios might be adjusted in response to maternal condition. Charnov and colleagues built upon this work by showing how the same principal could be applied more widely to a huge range of issues in both dioecious and hermaphroditic species. For example, whether host size should influence offspring sex ratios in parasitoid wasps, the age and direction of sex change in sequential hermaphrodites and when different breeding systems such as simultaneous hermaphroditism or environmental sex determination (ESD) should be favoured (Charnov 1982). Importantly, these predictions clearly lend themselves to empirical testing, which has helped make the Trivers & Willard hypothesis and its various extensions, one of the two most productive areas of sex allocation, alongside LMC theory.

Another major strand of sex allocation research was initiated when Trivers & Hare (1976) examined conflict over sex allocation in the social hymenoptera (ants, bees & wasps). This paper made two key contributions. First, it combined Fishers (1930) theory of equal investment with Hamilton’s (1964) inclusive fitness theory, to show how the ES sex allocation differed from the point of view of the queen and their workers. Research on sex allocation conflict within the social hymenoptera has since become the third most productive area in the field of sex allocation (chapter 9). Second, they showed how parent-offspring conflict and inclusive fitness (kin selection) theory could generate predictions that could be tested with empirical data. This was at a time when these topics were still contentious, and to this day, sex allocation still provides some of the clearest support for inclusive fitness theory.

Charnov’s (1982) monograph, The theory of sex allocation, brought all this together, providing a masterly synthesis of theoretical and empirical work. He unified the different areas of sex allocation research into a single field. From a theoretical perspective, Charnov showed how the same underlying concepts and similar mathematical models could be applied to all of the problems of sex allocation. From an empirical perspective, Charnov’s monograph showed the power of ‘selection thinking’ and simple models to make predictions that could be tested with empirical data, and led to a surge of interest in sex allocation that continues to this day. The increase in interest in this area is demonstrated by the increasing number of citations per year – comparing 2007 with 1982, the number of citations produced by a search on the phrase “sex allocation” has increased 50 fold, and the number of citations produced by a search on the phrases “sex allocation” or “sex ratio” has doubled (Web of Knowledge; subject areas: zoology, genetics & heredity, evolutionary biology, behavioural sciences, plant biology). Charnov’s monograph also contained a wealth of leads to potentially useful biological systems, that remain underexploited to this day.

In the 1980s, our theoretical understanding of LMC leaped forward. At a very general level, the reasons for the female biased sex ratio were clarified, disentangling the separate effects of competition between males, the availability of mates for those males, and inbreeeding (Taylor 1981; Frank 1985; Herre 1985; Frank 1986). In addition to settling a long running controversy, this work solved the debate over the level at which selection operates (Frank 1986), which sadly still persists in other areas. At a more specific level, a number of workers began extending LMC theory to fit the biology of specific systems. This generated a slew of new predictions, which allowed for some of the most elegant tests of LMC theory, in a wide range of organisms, and such work is still extremely active today.

Following Charnov’s monograph, there was a profusion of empirical studies testing the various forms of Trivers & Willard’s (1973) hypothesis. The most famous of these was Clutton-Brock and colleagues work on red deer, which provided support for both the assumptions and predictions of Trivers & Willard’s hypothesis, in response to maternal quality (Clutton-Brock et al. 1984). This work has inspired many researchers over the years and an extensive literature on sex allocation in ungulates has accumulated (Sheldon and West 2004). Equally impressive, were two long-term studies on species with environmental sex determination (ESD), by Conover and colleagues on a fish and by Adams and colleagues on a shrimp. These studies showed the pattern of ESD, the fitness consequences, and why the pattern of ESD should vary across populations.