Sperm competition and sex change: a comparative analysis across fishes

Current theory to explain the adaptive significance of sex change over gonochorism predicts that female-first sex change could be adaptive when relative reproductive success increases at a faster rate with body size for males than for females. A faster rate of reproductive gain with body size can occur if larger males are more effective in controlling females and excluding competitors from fertilizations. The most simple consequence of this theoretical scenario, based on sexual allocation theory, is that natural breeding sex ratios are expected to be female biased in female-first sex changers, because average male fecundity will exceed that of females. A second prediction is that the intensity of sperm competition is expected to be lower in female-first sex-changing species because larger males should be able to more completely monopolize females and therefore reduce male-male competition during spawning. Relative testis size has been shown to be an indicator of the level of sperm competition, so we use this metric to examine evolutionary responses to selection from postcopulatory male-male competition. We used data from 116 comparable female-first sex-changing and nonhermaphroditic (gonochoristic) fish species to test these two predictions. In addition to cross-species analyses we also controlled for potential phylogenetic nonindependence by analyzing independent contrasts. As expected, breeding sex ratios were significantly more female biased in female-first sex-changing than nonhermaphroditic taxa. In addition, males in female-first sex changers had significantly smaller relative testis sizes that were one-fifth the size of those of nonhermaphroditic species, revealing a new evolutionary correlate of female-first sex change. These results, which are based on data from a wide range of taxa and across the same body-size range for either mode of reproduction, provide direct empirical support for current evolutionary theories regarding the benefits of female-first sex change.