Where the Ends Meet: An Overview of Sex Determination in Atheriniform Fishes

Abstract

Atheriniform fishes have recently emerged as attractive models for evolutionary, ecological, and molecular/physiological studies on sex determination. Many species in this group have marked temperature-dependent sex determination (TSD) and yet many species also have a sex determinant gene that provides a strong drive for male differentiation. Thus, in these species the 2 forms of sex determination that were once considered to be mutually exclusive, environmental (ESD) and genotypic (GSD) sex determination, can coexist at environmentally relevant conditions. Here, we review the current knowledge on sex determination in atheriniform fishes with emphasis on the molecular and physiological mechanisms of ESD and GSD, the coexistence and cross-talk between these 2 mechanisms, the possibility of extragonadal transduction of environmental information and/or extragonadal onset of sex determination, and the results of field studies applying novel tools such as otolith increment analysis and molecular markers of genetic sex developed for selected New World and Old World atheriniform species. We also discuss the existence of molecular and histological mechanisms to prevent the discrepant differentiation in parts of the gonads because of ambiguous or conflicting environmental and genetic signals and particularly the possibility that the female is the default state in these species.

Sex reversal of pejerrey (Odontesthes bonariensis), a species with temperature‐dependent sex determination, in a seminatural environment

“…In fact, a more recent view is that GSD and ESD are part of a continuum of sex determination mechanisms that can actually coexist in an individual (Geffroy et al ., 2021), as was also demonstrated in the target of this study, Odontesthes bonariensi s (Yamamoto et al ., 2014, 2019). Water temperature effects on sex determination, or temperature‐dependent sex determination (TSD), seem to be by far the most common form of ESD in fish, particularly amongst Pleuronectiformes, Cichliformes and Atheriniformes (Luckenbach et al ., 2009; Ser et al ., 2010; Strüssmann et al ., 2021). So far, TSD has been described in over 60 species belonging to 13 families of fish and the sex ratio appears to follow three types of response to environmental temperature: (a) more males at high temperatures, (b) more females at high temperatures or (c) more males at extreme (high or low) temperatures (Ospina‐Álvarez & Piferrer, 2008).…”

“…So far, TSD has been described in over 60 species belonging to 13 families of fish and the sex ratio appears to follow three types of response to environmental temperature: (a) more males at high temperatures, (b) more females at high temperatures or (c) more males at extreme (high or low) temperatures (Ospina‐Álvarez & Piferrer, 2008). However, there are also reports of alternative forms of ESD such as the effects of pH, photoperiod, hypoxia and density, amongst other factors, in several fish taxa (Baroiller & D'Cotta, 2016; Devlin & Nagahama, 2002; Strüssmann et al ., 2021; Valenzuela & Lance, 2004; Yamamoto et al ., 2019). Knowledge on various forms of ESD is essential for the study of the evolution of sex‐determining mechanisms, since deductions about the distribution and predominance of a particular type of mechanism may be biased (Mank et al ., 2006; Ospina‐Álvarez & Piferrer, 2008; Strüssmann et al ., 2021; Valenzuela & Lance, 2004).…”

“…However, there are also reports of alternative forms of ESD such as the effects of pH, photoperiod, hypoxia and density, amongst other factors, in several fish taxa (Baroiller & D'Cotta, 2016; Devlin & Nagahama, 2002; Strüssmann et al ., 2021; Valenzuela & Lance, 2004; Yamamoto et al ., 2019). Knowledge on various forms of ESD is essential for the study of the evolution of sex‐determining mechanisms, since deductions about the distribution and predominance of a particular type of mechanism may be biased (Mank et al ., 2006; Ospina‐Álvarez & Piferrer, 2008; Strüssmann et al ., 2021; Valenzuela & Lance, 2004). More importantly, detailed information on how genetic and environmental factors interact to affect the sex ratios in the wild is relevant to assess the potential threats of global warming and climate change to fish populations (Ospina‐Álvarez & Piferrer, 2008; Strüssmann et al ., 2010, 2021; Honeycutt et al ., 2019; Geffroy et al ., 2021).…”

Sex Determination and Differentiation in Teleost: Roles of Genetics, Environment, and Brain

“…At the molecular level, both density and hypoxia activate the stress axis, or the hypothalamus-pituitary-adrenal axis, and upregulates the expression of cortisone. The conversion of cortisone is mediated by the 11β-HSD enzyme, which participates in androgen pathways specifically in the final step of 11-oxygenated androgens synthesis [76]. Thus, an increased level of cortisol results in an increased level of 11-ketotestosterone (11-KT), which induces male sex development.…”

Gonadal Transcriptome Analysis and Sequence Characterization of Sex-Related Genes in Cranoglanis bouderius

“…Generally, there are two kinds of biological sex determination: genetic sex determination (GSD) and environmental sex determination (ESD) [ 1 , 2 , 3 ]. GSD refers to sex determination by the organism’s chromosomes, whereas ESD refers to sex determination by environmental factors such as hormones [ 4 ], temperature [ 5 ], light intensity [ 6 ], pH [ 7 ], and so on.…”