Sex Allocation - Developments

Developments

Our understanding of selfish sex ratio distorters was revolutionised in the 1980s and 1990s. Relatively little was known about distorters at the time of Charnov’s (1982) monograph; they were assumed to be rare aberrations. Appreciation of their importance started to emerge, however, with Werren and Skinner’s discovery that three different sex ratio distorters occurred in the parasitoid wasp Nasonia vitripennis (Werren et al. 1981; Skinner 1982, 1985). This discovery was shocking because Nasonia had been intensively studied as a model species for understanding LMC and had provided some of the best evidence that individuals adjust offspring sex ratios in response to environmental conditions. The next major jump into the sex allocation limelight for sex ratio distorters was the discovery that endosymbiotic bacteria such as Wolbachia and Cardinium were responsible for many cases of sex ratio distortion, and that these endosymbionts were extremely widespread. There is now an extensive literature on sex ratio distorters, with recent work by G. Hurst and colleagues demonstrating how we can even follow their spread and suppression in natural populations.

The other major development of the 1980s was an understanding of the population level consequences of individual level sex ratio adjustment. Frank (Frank 1987) showed that Trivers & Willard type sex ratio adjustment can lead to a bias in the population sex ratio or the overall population investment ratio. He also showed that the direction and magnitude of this bias could be hard to predict, depending upon biological details that could be hard or impossible to assess. A consequence of this, which is still rarely appreciated, is that population level patterns will often be useless for testing whether sex allocation is being adjusted facultatively in response to local conditions. Frank, Charnov and Bull also showed that an important exception to this is in sex changing organism, where we can make and test predictions about the population sex ratio.

Research on sex allocation conflict between individuals really took off in the 1990s. Trivers & Hare’s (1976) paper had attracted much interest, but there are limitations on the testability of their predictions, using population level data. Boomsma & Grafen (Boomsma and Grafen 1990; Boomsma 1991; Boomsma and Grafen 1991) solved this, by showing that a range of more specific predictions could be made for how sex allocation should vary between colonies, within a population. In particular, they predicted that if workers were in control of sex ratio in a colony, we should observe split sex ratios, with some colonies producing predominantly male reproductives, and others predominantly female. Stunning support for their predictions rapidly followed from both observational and experimental studies on bees and ants. Since then, an impressive level of understanding has been obtained in this area by looking at: the underlying mechanisms; finer levels of within colony adjustment; mistakes; situations where the workers do not win. A new area of research on conflict was also opened up by the work of Strand and colleagues, showing the potential for sex allocation conflict in polyembryonic wasps, and how this might lead to the evolution of a sterile worker caste.

The 1990s saw the conventional wisdom on sex ratio adjustment in vertebrates overturned. It had long been assumed that chromosomal (genetic) sex determination (CSD) in vertebrates such as birds and mammals would prevent adaptive control of offspring sex ratios. This conception was clearly blown out of the water by a number of studies, primarily on birds. Komdeur and colleagues showed that Seychelles warblers were capable of adjusting the proportion of males in a clutch from between 10% and 90%, depending upon environmental conditions ( Komdeur et al. 1997). Sex allocation is adjusted in the Seychelles warbler in response to cooperation and competition with offspring. Another area of sex ratio adjustment in birds was opened up by Sheldon and colleagues, who showed that females, in species such as collared flycathers and blue tits, can adjust the sex of their offspring in response to mate quality, with females producing a higher proportion of sons when they mated more attractive males. This work was built upon previous findings by Burley (1981), that were so revolutionary in their time, that they had been effectively ignored for 15 years. The patterns of sex ratio adjustment in response to helping and male attractiveness have since been shown to be repeatable within and across species, proving clear evidence for control of offspring sex ratios in species with CSD ( West and Sheldon 2002).

The final major development of the 1990s was Frank’s (1998) reunification of sex allocation theory, in his mongraph Foundations of social evolution. Our understanding of sex allocation theory increased enormously during the 1980s and 1990s, thanks largely to the work of Taylor and Frank. They clarified the underling reasons for adjustment of sex allocation, linked different areas of research, and developed new methods for constructing theory, that were both simpler to apply and more general. Frank brought all this together in his 1998 monograph, which provided a guide on how to model sex allocation, as well as a unification of existing work. Taylor and Frank’s work was part of a more general programme on how to model inclusive fitness and social evolution, in which sex allocation theory has played a pivotal role.

The major development this millennium has been the attempt to explain broad taxonomic variation in the extent of sex ratio adjustment. This has united work in different conceptual areas on different taxa. One consequence has been to determine when vertebrates, with supposedly constraining CSD, really do show consistent patterns of sex ratio adjustment in the predicted direction. For example, birds adjust their offspring sex ratios in response to mate quality and the number of helpers on their patch (West and Sheldon 2002), but primates show no consistent pattern with maternal quality (Brown and Silk 2002). The other consequence of this work has been to show how variation in the extent of sex ratio adjustment across species can be explained by variation in the strength of selection. For example, birds show greater shifts of sex ratio in response to the number of helpers on their patch, when helpers provide greater benefits (Griffin et al. 2005), and wasps show greater shifts of sex ratio in response to host size, when host size better correlates with the resources that will be available for their offspring (West and Sheldon 2002). This work has emphasised that cases in which vertebrates show little or no sex ratio adjustment may just reflect a lack of selection, rather than the constraints of CSD, but also how sex allocation can be used to address very general issues on how adaptation may be limited.