Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture

Abstract

Controlling the sex ratio is essential in finfish farming. A balanced sex ratio is usually good for broodstock management, since it enables to develop appropriate breeding schemes. However, in some species the production of monosex populations is desirable because the existence of sexual dimorphism, primarily in growth or first time of sexual maturation, but also in color or shape, can render one sex more valuable. The knowledge of the genetic architecture of sex determination (SD) is convenient for controlling sex ratio and for the implementation of breeding programs. Unlike mammals and birds, which show highly conserved master genes that control a conserved genetic network responsible for gonad differentiation (GD), a huge diversity of SD mechanisms has been reported in fish. Despite theory predictions, more than one gene is in many cases involved in fish SD and genetic differences have been observed in the GD network. Environmental factors also play a relevant role and epigenetic mechanisms are becoming increasingly recognized for the establishment and maintenance of the GD pathways. Although major genetic factors are frequently involved in fish SD, these observations strongly suggest that SD in this group resembles a complex trait. Accordingly, the application of quantitative genetics combined with genomic tools is desirable to address its study and in fact, when applied, it has frequently demonstrated a multigene trait interacting with environmental factors in model and cultured fish species. This scenario has notable implications for aquaculture and, depending upon the species, from chromosome manipulation or environmental control techniques up to classical selection or marker assisted selection programs, are being applied. In this review, we selected four relevant species or fish groups to illustrate this diversity and hence the technologies that can be used by the industry for the control of sex ratio: turbot and European sea bass, two reference species of the European aquaculture, and salmonids and tilapia, representing the fish for which there are well established breeding programs.

Keywords: aquaculture; fish; genetic architecture; sex determination; sex ratio.

FIGURE 1

Major events leading to ovarian vs. testicular differentiation in fish. The first event, sex determination – the establishment of gender – can be triggered by the action of a major sex determining master gene, several sex-associated loci, an environmental factor (e.g., temperature) in an ecologically relevant context (i.e., occurring normally in the habitat of the species) or a combination of them, typically when the gonads are still sexually undifferentiated or even before they are formed at the most rudimentary stage (pre-gonadal stage). Successive events are connected by horizontal arrows and include differences in the proliferative rate of germ cells (females > males), which can be one of the first effects of the sex determining factor, whether genetic or environmental. During this period, the germ cell-somatic cell crosstalk is very important, but still largely uncharacterized. Also, during these early events, biotic and abiotic factors (e.g., stress, abnormally high temperature, etc.) can change the course of subsequent sex differentiation, usually in the female → male direction (diagonal dashed arrow). Finally, also at the beginning of gonad differentiation – the transformation of an undifferentiated gonad into a testis or ovary – the accidental (i.e., contamination) or deliberate (e.g., sex control treatment) incorporation of sex steroids, androgens or estrogens can result in female → male (vertical blue dotted arrow) or male → female (vertical red dotted arrow) sex-reversal, i.e., in that genotypic females and males develop into phenotypic males and females, respectively.

FIGURE 2

Model on the origin and evolution of the SD region-bearing chromosome from studies in mammals, birds and Drosophila. This model, although has been demonstrated in some fish, shows a large variation on its progression, which is reflected on the degree of differentiation between the chromosomes of the sexual pair. The origin of a new sexual pair is related to the origin of genes (A,B) with antagonistic alleles favorable to females (Af, Bf) or to males (Am, Bm) associated with a new SDg. Subsequent steps involve accumulation of repetitive elements (rep) and the degeneration of the Y chromosome because of its permanent heterozygotic state at the differential region (d: recessive non functional variant of a sex-linked gene).

FIGURE 3

Scheme of crosses aimed at obtaining all-female populations of turbot. I, II, and III represent the three generations required for the full process. Neomales (ZW) are obtained in generation I by applying methyltestosterone in the diet in undifferentiated fry. Identification of neomales (I) and superfemales (II) is usually done by individual progeny testing, so parents producing 50:50 f/m in cross I and II are culled because they are not neomales and superfemales, respectively. Crossing normal males (ZZ) with superfemales (WW) would produce 100% females (ZW) assuming a single full penetrant SDg.