Reversed sex change by widowed males in polygynous and protogynous fishes: female removal experiments in the field

Abstract

Sex change, either protogyny (female to male) or protandry (male to female), is well known among fishes, but evidence of bidirectional sex change or reversed sex change in natural populations is still very limited. This is the first report on female removal experiments for polygnous and protogynous fish species to induce reversed sex change in the widowed males in the field. We removed all of the females and juveniles from the territories of dominant males in the cleaner wrasse Labroides dimidiatus (Labridae) and the rusty angelfish Centropyge ferrugata (Pomacanthidae) on the coral reefs of Okinawa. In both species, if new females or juveniles did not immigrate into the territories of the widowed males, some of them emigrated to form male-male pairs. When a male-male pair formed, the smaller, subordinate partner began to perform female sexual behaviours (n = 4 in L. dimidiatus; n = 2 in C. ferrugata) and, finally, released eggs (n = 1, respectively). Thus, the reversed sex change occurred in the widowed males according to the change of their social status. These results suggest that such female removal experiments will contribute to the discovery of reversed sex change in the field also in other polygnous and protogynous species.

Bending Genders: The Biology of Natural Sex Change in Fish

“…Field evidence for bidirectional hermaphroditism is limited to 10 species in 5 families [Manabe et al, 2013;Kuwamura et al, 2015], and most reports are for species formerly thought to be protogynous. For example, in some socially polygamous and primarily protogynous species where social structure is highly unstable, sexchanged males may revert back to female should they find themselves competing with a larger male (e.g., Okinawa pygmy goby, Trimma okinawae, Manabe et al [2007]; cleaner wrasse, Labroides dimidiatus, Kuwamura et al [2011]). Natural bidirectional sex change has not been reported for any otherwise protandrous species.…”

Testing the Low-density Hypothesis for Reversed Sex Change in Polygynous Fish: Experiments in Labroides dimidiatus

“…The widowed males were expected to choose nearby individuals for new mates to avoid the cost of farther movement; reducing movement costs has been suggested as an important factor for the evolution of bidirectional sex change920. The results of this study also suggest that male-male competition for females affects mate choice.…”

“…These results support two of the above predictions (P2 and P4). It was also suggested that the widowed males tended to choose the nearby male20, as is predicted in P3, but it has not been confirmed whether a widowed male would choose to pair with another widowed male even in the presence of females, since we removed all females in the previous study.…”

“…Therefore, we have previously proposed that the reversed sex change should be favoured in low-density populations of polygynous species1920. In low-density populations in which facultative monogamy occurs, males may sometimes become single as a result of accidental mate loss.…”

“…In previous field experiments, we removed all females from the study area in two polygynous coral reef fish, the cleaner wrasse Labroides dimidiatus and the rusty angelfish Centropyge ferrugata 20. When no immigration occurred, a portion of widowed males moved to pair with other widowed males, and the smaller in the male-male pair changed sex.…”