A new experimental model for the investigation of sequential hermaphroditism

Abstract

The stunning sexual transformation commonly triggered by age, size or social context in some fishes is one of the best examples of phenotypic plasticity thus far described. To date our understanding of this process is dominated by studies on a handful of subtropical and tropical teleosts, often in wild settings. Here we have established the protogynous New Zealand spotty wrasse, Notolabruscelidotus, as a temperate model for the experimental investigation of sex change. Captive fish were induced to change sex using aromatase inhibition or manipulation of social groups. Complete female-to-male transition occurred over 60 days in both cases and time-series sampling was used to quantify changes in hormone production, gene expression and gonadal cellular anatomy. Early-stage decreases in plasma 17β-estradiol (E2) concentrations or gonadal aromatase (cyp19a1a) expression were not detected in spotty wrasse, despite these being commonly associated with the onset of sex change in subtropical and tropical protogynous (female-to-male) hermaphrodites. In contrast, expression of the masculinising factor amh (anti-Müllerian hormone) increased during early sex change, implying a potential role as a proximate trigger for masculinisation. Collectively, these data provide a foundation for the spotty wrasse as a temperate teleost model to study sex change and cell fate in vertebrates.

Effects of cortisol on female-to-male sex change in a wrasse

“…The effect of stress as a potential trigger for sex change in spotty wrasse was investigated by implanting cortisol pellets into IP spotty wrasse individuals under socially inhibitory conditions between the months of June–September 2017. This is during the breeding season, which lasts from late July until November, but outside of the optimal window for natural sex change, which occurs between November–May (i.e., outside the breeding season) [ 49 ]. Fish were captured around high tide by hook and line off the coast of Tauranga, Bay of Plenty, New Zealand (37.6878° S, 176.1651° E) and kept at the Aquaculture Centre at Toi Ohomai Institute of Technology, Tauranga.…”

“…Fish were fed frozen green-lipped mussels ( Perna canaliculus ) three times a week for the duration of the experiment (ten weeks) (standard practice for this species). The duration of the experiment and the sampling times were estimated based on previous data on the completion of sex change in captive spotty wrasse using an aromatase inhibitor (60 days) or social inhibition (66 days) [ 49 ].…”

“…Sections were cut at 3 μm and stained with Mayer’s haematoxylin and eosin. Gonadal sections were examined under light microscope and subsequently classified into a series of stages (i.e., female (breeding or non-breeding), early transitioning, mid-transitioning, late transitioning, IP male, and TP male) based on key histological events observed during sex change in socially controlled spotty wrasses [ 48 , 49 ].…”

“…For the gonads, a nanoString nCounter TM CodeSet probe array of 19 candidate genes was designed for spotty wrasse as described in Goikoetxea et al [ 49 ] and was used to examine gene expression (S3 Table in S1 File ). NanoString gene expression quantification nCounter TM CodeSet was performed at the Otago Genomics Facility, University of Otago, New Zealand.…”

Protogynous functional hermaphroditism in the North American annual killifish, Millerichthys robustus

“…Consequently, there is clear behavioural control over sex change, where social or mating systems confer differential advantages for each sex under particular social and ecological conditions 1 . We now have a solid mechanistic understanding of sex change, including hormonal, histological and molecular mechanisms of the process 12 , especially in sparid, gobiid and serranid fishes where sequential hermaphroditism is common 13 . These fishes are typically marine, long-lived and may form relatively compact social groups.…”