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

Abstract

Hermaphroditism is ubiquitous among plants and widespread in the animal kingdom. It is an unsolved problem why reversed sex change has evolved in polygynous and protogynous reef fish. We have previously suggested that facultative monogamy occurs in low-density populations of polygynous species and that males that become single as a result of accidental mate loss may change sex when they meet larger males. In this study, to test this ‘low-density hypothesis', we conducted field experiments with the coral reef fish Labroides dimidiatus in which a portion of females were removed to create a low-density situation. The ‘widowed' males moved to search for a new mate when no male, female or juvenile fish migrated into their territories and paired with nearby single fish, whether male or female. Alternatively, males expanded their territories to take over the nearest pair whose male was much smaller. These results support our low-density hypothesis.

Evolution of bidirectional sex change and gonochorism in fishes of the gobiid genera Trimma, Priolepis, and Trimmatom

“…Male-to-female sex change occurs by establishing a pair between the nearest or second-nearest males after experimental removal or natural disappearance of females. The reverse sex change condition seems to correspond with low density (Kuwamura et al 2011 , 2014 , 2015 ; Kadota et al 2012 ). As territorial males rarely lose their mates, such a low-density condition could occur near the edge of the distribution (Kuwamura et al 2011 ).…”

“…Labroides dimidiatus (Labridae) , Centropyge ferrugata (Pomacanthidae), Dascyllus aruanus (Pomacentridae), and Cirrhitichthys falco (Cirrhitidae) are harem polygynous species that change sex from female to male when a dominant male disappears, as in protogynous fishes. However, sex change from male to female takes place in the smaller male of male–male pair under low-density conditions induced by experimental removing a female (Kuwamura et al 2011 , 2014 , 2015 ) or natural disappearance of females (Kadota et al 2012 ). In the monogamous coral dwelling gobiid fish Paragobiodon echinocephalus and Gobiodon histrio , bidirectional sex change takes place in male–male and female–female pairs.…”

Timing reproduction in teleost fish: cues and mechanisms

“…As males and females have different reproductive potentials across life stages and environments, there is an advantage to change to the sex most advantageous for a given stage of life [23]. The social environment is the main determinant of whether a fish will change sex.…”

On the proper rearing density in domesticated zebrafish to avoid unwanted masculinization. Links with the stress response

“…The influence of stocking density on fish sex ratios has only been documented in a few fish species, e.g. paradise fish, Macropodus opercularus (Francis, 1984), some coral reef fish species (Kuwamura et al, 2014;Lutnesky, 1994), European eel, Anguilla anguilla (Huertas and Cerdà, 2006;Krueger and Oliveira, 1999;Roncarati et al, 1997), European sea bass, Dicentrarchus labrax (Saillant et al, 2003) and zebrafish (Hazlerigg et al, 2012). However, as for any confined animal, a rearing density beyond a certain threshold has evident detrimental consequences in fish, including lower survival, decreased growth, higher incidence of deformities, increased susceptibility to diseases, and altered reproduction (e.g.…”