Contrasting variation within and covariation between gender-related traits in autogamous versus outcrossing species: Alternative evolutionary predictions

We present several predictions concerning the expression of genetic variation in, and covariation among, gender-related traits in perfect-flowered plant taxa with different breeding systems. We start with the inference that the pollen:ovule (P/O) ratio in obligately autogamous species (in which the ovules in a flower are fertilized only by the pollen it produces) should be under much stronger stabilizing selection than in outcrossing taxa. Consequently, we predict that obligately autogamous taxa should exhibit lower genetic coefficients of variation in the P/O ratio. Nevertheless, genetic variation in both pollen and ovule production per flower might persist within autogamous as well as outcrossing populations. In autogamous taxa, genotypes with relatively few pollen grains and ovules per flower (but producing relatively high numbers of flowers) and genotypes with comparatively high numbers of gametes per flower (but producing relatively few flowers) could co-exist if lifetime flower production is selectively neutral. In contrast, in outcrossers, the maintenance of genetic variation in ovule and pollen production per flower might result predominantly from their ability to maintain variation in phenotypic and functional gender. Given genetic variation in primary sexual traits, we predict that the genetic correlation between investment in male and female gametes per flower should qualitatively differ between selfers and outcrossers. We predict a positive genetic correlation between pollen and ovule production per flower in obligately autogamous taxa, primarily because strong stabilizing selection on the P/O ratio should select against the gender specialists that would be necessary to effect a negative genetic correlation between mean pollen and ovule production per flower. Moreover, the fact that autogamous individuals are 50% female and 50% male means that gender-biased phenotypes cannot be functionally gender-biased, preventing selection from favouring phenotypic extremes. In contrast, in outcrossing taxa, in which functionally male- and female-biased genotypes may co-exist, the maintenance of contrasting genders could contribute to the expression of negative genetic correlations between pollen and ovule production per flower. We discuss these and a number of corollary predictions, and we provide a preliminary empirical test of the first prediction. This revised version was published online in July 2006 with corrections to the Cover Date.