Sex Differentiation in an All-Female (XX) Rainbow Trout Population with a Genetically Governed Masculinization Phenotype

Abstract

Sex determination is known to be male heterogametic in the rainbow trout, Oncorhynchus mykiss; however, scattered observations that deviate from this rather strict genetic control have been reported. Here, we provide a detailed morphological and histological characterization of the gonadal differentiation and development (from 43 days postfertilization to 11 months of age) in an all-female (XX) population with a genetically governed masculinization phenotype. In comparison with control males and females, the gonadal differentiation in these animals was characterized by many perturbations, including significantly fewer germ cells. This decrease in germ cells was confirmed by the significantly decreased expression of 2 germ cell maker genes (vasa and sycp3) in the masculinized XX populations as compared with the control females and control males. Although only a proportion of the total adult population was partially or fully masculinized, this early differentiating phenotype affected nearly all the sampled animals. This suggests that the adult masculinization phenotype is the consequence of an early functional imbalance in ovarian differentiation in the entire population. We hypothesize that the lower number of germ cells that we observed in this population could be one cause of their masculinization.

High Temperature Increases the Masculinization Rate of the All-Female (XX) Rainbow Trout “Mal” Population

“…In agreement with previous studies performed with mal -carrying animals [20] – [22] , we confirmed that the masculinization rates at the reference temperature of 12°C were variable among half-sib progeny (experiment A) and independent progeny (experiment B) depending on the breeding pair, respectively. This result was clearly demonstrated in our common garden experiment, controlled for possible tank effects, in which different progeny exhibited different masculinization rates independent from the temperature effects.…”

“…Despite a strict male heterogamety in rainbow trout, spontaneous masculinization has been found in some XX fish belonging to a population of gynogenetic doubled haploid individuals [20] . Analysis of the transmission of this male phenotype in a three generation pedigree supported the hypothesis that a recessive mutation in one putative minor sex determination factor (termed mal ), together with other sex modifier loci, was responsible for the partial or full masculinization of some of these XX individuals [20] – [22] . Preliminary observations also suggested that this expression of maleness was influenced by environmental factors; low temperature during the first stages of development reduced the frequency of masculinized individuals [Quillet et al, unpublished data].…”

“…Fish gonadal phenotypes were analyzed and classified as described in Valdivia et al [22] (see S2 Figure ). Briefly, the fish were scored as “normal female” when no sign of masculinization could be detected by histological analysis on either gonad and when no delay in gametogenesis could be observed compared to the control females (XX all-female population).…”

Genetic determinism of spontaneous masculinisation in XX female rainbow trout: new insights using medium throughput genotyping and whole-genome sequencing

“…Within those intersex individuals, whatever the rearing temperature of fry, the right gonad was very often more masculinised than the left gonad. This particularity was first described by Quillet et al (2004) 40 and confirmed by Valdivia et al (2013Valdivia et al ( , 2014 12,15 , in families originating from the INRA XXmal carrying line. Under normal rearing condition, the left-right asymmetry (LR) is almost undetectable as intersex fish remain rare and poorly described.…”

“…However, despite a strict sex-linkage of the sdY locus in many salmonid species 8 , spontaneous masculinisation of XX females have been reported in rainbow trout, first in experimental groups 11 , but also in commercial populations (unpublished data). These spontaneous masculinisation and their transmission across generations have been characterized in gynogenetic families, where the role of minor genetic factors acting in addition to the major sdY sex determination system has been suspected 11,12 . Later, Guyomard et al 13 (2014) detected QTLs associated to masculinisation in two doubled haploid gynogenetic trout families.…”