Evolution of bidirectional sex change and gonochorism in fishes of the gobiid genera Trimma, Priolepis, and Trimmatom

• Published in: Die Naturwissenschaften Vol. 104; no. 3-4; pp. 15 - 11
• Main Authors: Sunobe, Tomoki, Sado, Tetsuya, Hagiwara, Kiyoshi, Manabe, Hisaya, Suzuki, Toshiyuki, Kobayashi, Yasuhisa, Sakurai, Makoto, Dewa, Shin-ichi, Matsuoka, Midori, Shinomiya, Akihiko, Fukuda, Kazuya, Miya, Masaki
• Format: Journal Article
• Language: English
• Published: Berlin/Heidelberg Springer Berlin Heidelberg 01.04.2017; Springer Nature B.V
• Subjects: Animals; Biomedical and Life Sciences; Ecological conditions; Environment; Evolution; Evolutionary genetics; Female; Fish; Fish behavior; Fishes - anatomy & histology; Fishes - classification; Fishes - genetics; Fishes - physiology; Genes, Mitochondrial - genetics; Gonads; Hermaphroditism; Histology; Life Sciences; Male; Mating; Mitochondria; Monogamy; Original Paper; Phylogeny; Priolepis; Reproduction - immunology; Sex; Sex Determination Processes - genetics; Sex Determination Processes - physiology; Sexual Behavior, Animal - physiology; Sexuality; Species; Trimma; Trimmatom; Phylogenetic analysis; Mating system; Bidirectional sex change; Low-density model; Size-advantage model; Gobiidae
• ISSN: 0028-1042; 1432-1904
• DOI: 10.1007/s00114-017-1434-z

Size-advantage and low-density models have been used to explain how mating systems favor hermaphroditism or gonochorism. However, these models do not indicate historical transitions in sexuality. Here, we investigate the evolution of bidirectional sex change and gonochorism by phylogenetic analysis using the mitochondrial gene of the gobiids Trimma (31 species), Priolepis (eight species), and Trimmatom (two species). Trimma and Priolepis formed a clade within the sister group Trimmatom . Gonadal histology and rearing experiments revealed that Trimma marinae , Trimma nasa , and Trimmatom spp. were gonochoric, whereas all other Trimma and Priolepis spp. were bidirectional sex changers or inferred ones. A maximum-likelihood reconstruction analysis demonstrated that the common ancestor of the three genera was gonochoristic. Bidirectional sex change probably evolved from gonochorism in a common ancestor of Trimma and Priolepis. As the gonads of bidirectional sex changers simultaneously contain mature ovarian and immature testicular components or vice versa, individuals are always potentially capable of functioning as females or males, respectively. Monogamy under low-density conditions may have been the ecological condition for the evolution of bidirectional sex change in a common ancestor. As T. marinae and T. nasa are a monophyletic group, gonochorism should have evolved from bidirectional sex change in a common ancestor.