A social basis for the development of primary males in a sex-changing fish

Abstract

An example of alternative male strategies is seen in diandric protogynous (female first) hermaphrodites, where individuals either mature directly as male (primary males) or first reproduce as female and then change sex to male (secondary males). In some sex-changing fishes, the testes of primary males appear anatomically similar to those of non-sex-changing species, whereas the testes of secondary males have anatomical evidence of their former ovarian function. Here, we provide evidence that in the bluehead wrasse, Thalassoma bifasciatum , these strikingly different male phenotypes arise from differences in the ontogenetic timing of environmental sex determination, timing that can be experimentally altered through changes in the social circumstances. Juveniles differentiated almost exclusively as females when reared in isolation, regardless of whether they were collected from a reef with a high proportion of primary males or from a reef with a low proportion of primary males. In contrast, one individual usually differentiated as a primary male when reared in groups of three. Our results indicate that primary males of the bluehead wrasse are an environmentally sensitive developmental strategy that has probably evolved in response to variation in the reproductive success of primary males in populations of different sizes.