Title: Identity of a Tilapia Pheromone Released by Dominant Males that Primes Females for Reproduction
Abstract: Knowledge of the chemical identity and role of urinary pheromones in fish is scarce, yet it is necessary in order to understand the integration of multiple senses in adaptive responses and the evolution of chemical communication [1Stacey N. Hormonally derived sex pheromones in fishes.in: Norris D.O. Lopez K.H. Hormones and Reproduction of Vertebrates. Academic Press, London2011: 169-192Google Scholar]. In nature, Mozambique tilapia (Oreochromis mossambicus) males form hierarchies, and females mate preferentially with dominant territorial males, which they visit in aggregations or leks [2Bruton M.N. Boltt R.E. Aspects of the biology of Tilapia mossambica Peters (Pisces: Cichlidae) in a natural freshwater lake (Lake Sibaya, South Africa).J. Fish Biol. 1975; 7: 423-445Crossref Scopus (123) Google Scholar]. Dominant males have thicker urinary bladder muscular walls than subordinates or females and store large volumes of urine, which they release at increased frequency in the presence of subordinate males or preovulatory, but not postspawned, females [3Keller-Costa T. Lopes O.S. Lima M. Hubbard P.C. Iacovella A. Canário A.V.M. Almeida O. Barata E.N. Muscular hypertrophy of urinary bladders in dominant tilapia facilitates the control of aggression through urinary signals.Behaviour. 2012; 149: 953-975Crossref Google Scholar, 4Barata E.N. Hubbard P.C. Almeida O.G. Miranda A. Canário A.V. Male urine signals social rank in the Mozambique tilapia (Oreochromis mossambicus).BMC Biol. 2007; 5: 54Crossref PubMed Scopus (99) Google Scholar, 5Barata E.N. Fine J.M. Hubbard P.C. Almeida O.G. Frade P. Sorensen P.W. Canário A.V. A sterol-like odorant in the urine of Mozambique tilapia males likely signals social dominance to females.J. Chem. Ecol. 2008; 34: 438-449Crossref PubMed Scopus (63) Google Scholar]. Females exposed to dominant-male urine augment their release of the oocyte maturation-inducing steroid 17α,20β-dihydroxypregn-4-en-3-one (17,20β-P) [6Huertas M. Almeida O.G. Canário A.V.M. Hubbard P.C. Tilapia male urinary pheromone stimulates female reproductive axis.Gen. Comp. Endocrinol. 2014; 196: 106-111Crossref PubMed Scopus (24) Google Scholar]. Here we isolate and identify a male Mozambique tilapia urinary sex pheromone as two epimeric (20α- and 20β-) pregnanetriol 3-glucuronates. We show that both males and females have high olfactory sensitivity to the two steroids, which cross-adapt upon stimulation. Females exposed to both steroids show a rapid, 10-fold increase in production of 17,20β-P. Thus, the identified urinary steroids prime the female endocrine system to accelerate oocyte maturation and possibly promote spawning synchrony. Tilapia are globally important as a food source but are also invasive species, with devastating impact on local freshwater ecosystems [7Morgan D.L. Gill H.S. Maddern M.G. Beatty S.J. Distribution and impacts of introduced freshwater fishes in Western Australia.N. Z. J. Mar. Freshw. Res. 2004; 38: 511-523Crossref Scopus (101) Google Scholar, 8Canonico G.C. Arthington A. McCrary J.K. Thieme M.L. The effects of introduced tilapias on native biodiversity.Aquat. Conserv. Mar. Freshw. Ecosyst. 2005; 15: 463-483Crossref Scopus (313) Google Scholar]. Identifying the chemical cues that mediate reproduction may lead to the development of tools for population control [9Corkum L.D. Belanger R.M. Use of chemical communication in the management of freshwater aquatic species that are vectors of human diseases or are invasive.Gen. Comp. Endocrinol. 2007; 153: 401-417Crossref PubMed Scopus (21) Google Scholar, 10Madliger C. Towards improved conservation management: a consideration of sensory ecology.Biodivers. Conserv. 2012; 21: 3277-3286Crossref Scopus (21) Google Scholar, 11Sorensen P.W. Stacey N.E. Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes.N. Z. J. Mar. Freshw. Res. 2004; 38: 399-417Crossref Scopus (131) Google Scholar].