Sex Control in Fish: Approaches, Challenges and Opportunities for Aquaculture

J. Mar. Sci. Eng. 2015, 3, 329-355; doi:10.3390/jmse3020329 OPEN ACCESS Journal of Marine Science and Engineering ISSN 2077-1312 www.mdpi.com/journal/jmse Review Sex Control in Fish: Approaches, Challenges and Opportunities for Aquaculture Alyssa M. Budd *, Quyen Q. Banh, Jose A. Domingos and Dean R. Jerry Centre for Sustainable Tropical Fisheries and Aquaculture, James Cook University, Townsville, Queensland 4810, Australia; E-Mails: (Q.Q.B.); (J.A.D.); (D.R.J.) * Author to whom correspondence should be addressed; E-Mail: ; Tel.: +61-7-4781-4880. Academic Editor: Kerstin Johannesson Received: 20 April 2015 / Accepted: 20 May 2015 / Published: 28 May 2015 Abstract: At present, aquaculture is the fastest growing sector of animal food production and holds great potential as a sustainable solution for world food security. The ability to control sex is one of the most important factors for the commercialisation and efficient propagation of fish species, due to influences on reproduction, growth and product quality. Accordingly, there is a large body of research that targets sexual development in commercially important species in an attempt to understand and control fish sex and reproductive function. In this review, we provide an introduction to sex determination and differentiation in fish, including the genetic, epigenetic and environmental factors that can influence fish sex ratios. We also summarise the major approaches used to control sex in fish and discuss their application in commercially important species. Specifically, we discuss the use of exogenous steroid hormones, chromosome ploidy, environmental manipulations, sexlinked genetic markers, selection for altered sex ratios, and transgenics and comment on the challenges associated with controlling sex in a commercial environment. Keywords: sex ratio; reproductive control; triploidy; hormonal manipulation; epigenetics; environment; QTL J. Mar. Sci. Eng. 2015, 3 330 1. Introduction Sex control is one of the most important and highly targeted areas of aquaculture research due to influences on husbandry management, productivity and economics. Without the ability to regulate sexual differentiation, maturation, and reproduction, farmers have little control over breeding processes, both in the hatchery and throughout grow-out. Arguably, in aquaculture species that have become global commodities, control over sex and reproduction has been the primary facilitator for large-scale industrial production. In species that are yet to reach industrial scale production, elucidation of sex differentiation and improved reliability of reproduction remains a key area of applied research. The Need for Sex Control Several broad goals in aquaculture can be reached through a better understanding of sex control. These include: (i) prevention of precocious maturation and uncontrolled reproduction (e.g., in tilapia); (ii) the desire to farm monosex populations due to differences in growth rate and economic value of the sexes (e.g., tilapia, shrimp); (iii) reducing the impact of phenotypic sex on product quality (e.g., Atlantic salmon, oysters); (iv) increasing stability of mating systems (e.g., sex change in groupers) and (v)) environmental and/or intellectual property protection (e.g., non-indigenous species, or genetically improved strains). The relative importance of each of these goals depends upon the reproductive biology and culture system of the species concerned. Precocious maturation occurs in several farmed species including Nile tilapia (Oreochromis niloticus) [1], freshwater crayfish (Cherax destructor) [2] and Atlantic salmon (Salmo salar), which have a tendency to sexually mature and reproduce before attaining a body size that is suitable for harvest. This precocious maturation leads to slow growth as energy is diverted into reproduction, creates large variance in product size at harvest and results in overpopulation of ponds and, therefore, an inability to control animal densities and feeding rates. Furthermore, deterioration in flesh quality is often observed in female Atlantic salmon as they reach sexual maturity through the diversion of energy (e.g., lipids) towards reproductive processes resulting in differences in economic value between males and females [3]. The desire to farm monosex populations may also be provoked by sex-specific growth rates. Male Nile tilapia, for example, grow faster and have lower feed conversion rates than females [4], while female Kuruma prawns (Penaeus japonicus) are generally larger than males at the time of harvest [5]. As a result, farmers have adopted both manual (e.g., hand sexing and selective removal) and/or various technological (e.g., exogenous hormone treatment, chromosome ploidy manipulation, molecular tools, or hybridisation) approaches to produce monosex populations for culture (Table 1). J. Mar. Sci. Eng. 2015, 3 331 Table 1. Common approaches used to manipulate sex in aquaculture fishes. Approach Hormonal manipulation Technique Administration of exogenous hormones (e.g., 17β-estradiol, 11-α-methyltestosterone) Administration of aromatase inhibitor (e.g., Fadrozole) Purpose Representative example species Monosex Atlantic cod, Gadus morhua [6] Nile tilapia (Oreochromis niloticus) [7] Monosex Hybridisation Cross breeding Monosex Chromosome Ploidy Gynogenetics Triploidy Envionmental manipulation Manipulation of social factors Monosex Sterility Production of male broodstock Selection Nile tilapia (Oreochromis niloticus) [8] Honeycomb grouper (Epinephelus merra) [9] Tilapia (O. aurea x O. niloticus) [10] Bass (Morone saxatilis x M. mississippiensis) [11] Rainbow trout (Oncorhynchus mykiss) [12] Atlantic salmon (Salmo salar) [13,14] Orange-spotted grouper (Epinephelus coioides) [15] Temperature treatment during gonadal differentiation Monosex populations European Seabass (Dicentrarchus labrax) [16–18] Marker assisted selection (MAS) Monosex populations Nile tilapia (Oreochromis niloticus) [19,20] Turbot (Scophthalmus maximus) [21] J. Mar. Sci. Eng. 2015, 3 332 An ability to control sex and breeding is also important for hatcheries in order to produce seedstock, particularly if the purpose is reliable production of specific family combinations for selective breeding. Many fishes such as Atlantic salmon, rainbow trout (Oncorhynchus mykiss) and channel catfish (Ictalurus punctatus) can be reliably dry stripped to obtain eggs and sperm, which are subsequently mixed in buckets to produce fertilized eggs. This ability to strip spawn fish allows for easy creation of large numbers of either half- or full-sib families, depending on the mating design. However, in many other aquaculture species, strip spawning is inadequate for industrial scale production, and accordingly, natural reproduction is relied upon. Barramundi (Lates calcarifer) (also known as Asian seabass), for example, is a mass-spawning, sequential protandrous (male to female sex-changing) h (...truncated)