Temperature preference of Nile tilapia (Oreochromis niloticus) juveniles induces spontaneous sex reversal

Abstract

Nile tilapia ( Oreochromis niloticus ) is an African freshwater fish that displays a genetic sex determination system (XX|XY) where high temperatures (above 32°C to 36.5°C) induce masculinization. In Nile tilapia, the thermosensitive period was reported from 10 to 30 days post fertilization. In their natural environment, juveniles may encounter high temperatures that are above the optimal temperature for growth (27–30°C). The relevance of the thermal sex reversal mechanism in a natural context remains unclear. The main objective of our study is to determine whether sexually undifferentiated juveniles spontaneously prefer higher, unfavorable temperatures and whether this choice skews the sex ratio toward males. Five full-sib progenies (from 100% XX crosses) were subjected to (1) a horizontal three-compartment thermal step gradient (thermal continuum 28°C– 32°C– 36.5°C) during the thermosensitive period, (2) a control continuum (28°C– 28°C– 28°C) and (3) a thermal control tank (36.5°C). During the first days of the treatment, up to an average of 20% of the population preferred the masculinizing compartment of the thermal continuum (36.5°C) compared to the control continuum. During the second part of the treatment, juveniles preferred the lower, nonmasculinizing 32°C temperature. This short exposure to higher temperatures was sufficient to significantly skew the sex ratio toward males, compared to congeners raised at 28°C (from 5.0 ± 6.7% to 15.6 ± 16.5% of males). The proportion of males was significantly different in the thermal continuum, thermal control tank and control continuum, and it was positively correlated among populations. Our study shows for the first time that Nile tilapia juveniles can choose a masculinizing temperature during a short period of time. This preference is sufficient to induce sex reversal to males within a population. For the first time, behavior is reported as a potential player in the sex determination mechanism of this species.

Phenotypic plasticity and epigenetics of fish: embryo temperature affects later-developing life-history traits

“…According to Ospina-Álvarez & Piferrer (2008), temperature-influenced sex differentiation occurs in 33 cichlids and several other species. Furthermore, larvae of genetically female flatfishes of the genus Paralichthys can change sex when exposed to warm water (Montalvo et al 2012a,b), and Nile tilapia Oreochromis niloticus exhibit sex reversal in some lakes (Nivelle et al 2019).…”

Effects of global warming on sex ratios in fishes

“…The patterns are often not very strong [see, for example, the Supplementary Table S1 of Ospina‐Álvarez and Piferrer (2008)]. Moreover, there is often significant variation among families, as in D. rerio (Ribas et al ., 2017), C. gariepinus (Santi et al ., 2016) and O. niloticus (Baroiller & D'Cotta, 2001; Nivelle et al ., 2019), and there can be significant variation among experimental runs, as observed in European sea bass (Vandeputte & Piferrer, 2018). Some of this variation could, however, be due to sex‐specific mortality at very early stages (see discussion below).…”

“…Species with genetic sex determination (GSD) can have their phenotypic sex modulated by temperature as, for example, medaka Oryzias latipes (Temminck & Schlegel 1846) (Kitano et al ., 2012), sockeye salmon Oncorhynchus nerka (Walbaum 1792) (Azuma et al ., 2004; Craig et al ., 1996), rainbow trout Oncorhynchus mykiss (Walbaum 1792)(Valdivia et al ., 2014) and sablefish Anoplopoma fimbria (Pallas 1814) (Huynh et al ., 2019). An interesting observation in this context is that juveniles of O. niloticus or C. gariepinus (both species with GSD) sometimes seem actively to seek warmer temperatures around the time of sex differentiation in order to develop into males (Nivelle et al ., 2019; Santi et al ., 2017). Such temperature‐induced genotype–phenotype mismatches can produce interesting long‐term effects on demography, as discussed below.…”

Hematological response of Tilapia (Oreochromis niloticus) in Laundry wastewater

“…An increase in water temperature also causes a reduction in DO levels in the water. The optimal temperature for tilapia growth is range 22-30°C (Zuhrawati, 2014;Nivelle et al, 2019). pH values of water at various treatments increase with the high detergent concentration due to bases chemical of detergent.…”