Sex in an Evolutionary Perspective: Just Another Reaction Norm

Abstract

It is common to refer to all sorts of clear-cut differences between the sexes as something that is biologically almost inevitable. Although this does not reflect the status of evolutionary theory on sex determination and sexual dimorphism, it is probably a common view among evolutionary biologists as well, because of the impact of sexual selection theory. To get away from thinking about biological sex and traits associated with a particular sex as something static, it should be recognized that in an evolutionary perspective sex can be viewed as a reaction norm, with sex attributes being phenotypically plastic. Sex determination itself is fundamentally plastic, even when it is termed "genetic". The phenotypic expression of traits that are statistically associated with a particular sex always has a plastic component. This plasticity allows for much more variation in the expression of traits according to sex and more overlap between the sexes than is typically acknowledged. Here we review the variation and frequency of evolutionary changes in sex, sex determination and sex roles and conclude that sex in an evolutionary time-frame is extremely variable. We draw on recent findings in sex determination mechanisms, empirical findings of morphology and behaviour as well as genetic and developmental models to explore the concept of sex as a reaction norm. From this point of view, sexual differences are not expected to generally fall into neat, discrete, pre-determined classes. It is important to acknowledge this variability in order to increase objectivity in evolutionary research.

Fig. 1

Response in sex ratio to incubation temperature in crocodiles. Females are produced at low and high temperatures while intermediate temperatures result in male offspring

Fig. 2

Phylogeny of changes in sex determination mode. Sex determination is immensly variable, this phylogeny is an attempt to illustrate this diversity. Taxa has been chosen to illustrate transitions between sex determination systems. We used phylogenies on amphibians from Hillis and Green (1990), on lizards and snakes from de Queiros and Martin (1996a, b), on fishes from Mank et al. (2006) the overall topology is derived from the Tree of life project (Maddison and Schulz –2006). Data on reptiles was compiled from Bull (1980), on amphibians from Hillis and Green (1990), on Bassiana duperreyi from Shine et al. (2002), on birds from Ellegren (2000), on fishes from Mank et al. (2006)

Fig. 3

The genetic sex determination cascade in Drosophila. Sexual development in Drosophila is determined by the ratio of X-chromosomes to autosomes which decides whether the Sxl-gene is turned on, leading to the female pathway, or turned off, leading to male sexual development. Redrawn and simplified from Pomiankowski et al. (2004) and Gilbert (2000)

Fig. 4

Phylogeny of sex role-reversals. This phylogeny illustrates the variation in sex roles over evolutionary time. It is not representative for the whole tree of animal life as we have included only some examples of species with sex role reversal. Female butterflies (Acraea encedon) show sex role reversed swarming behaviour in Wolbachia-infected populations (Jiggins et al. 2000). Two groups are known for multiple origins of sex-role reversals, namely the pipefishes and their relatives and shorebirds. There are also a number of species that show flexible sex roles, such as two-spotted gobies and katydid insects. Black lineages indicate reversed sex roles, white lineages “conventional” sex roles and hatched branches show equivocal ancestral states. Phylogeny and sex role reversals in pipefishes are referred from Wilson et al. (2003). For shorebirds we used the phylogeny from Liker et al. (2001) and references on sex-role reversal from Zuk (2002) and Owens (2002)