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

Abstract

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.Electronic supplementary materialThe online version of this article (doi:10.1007/s00114-017-1434-z) contains supplementary material, which is available to authorized users.

Hermaphroditism in fish: incidence, distribution and associations with abiotic environmental factors

“…Following these criteria, and after an extensive review of the literature, functional hermaphroditism was confirmed in 7 orders, 27 families (6% of all fish families) and 94 genera, but without estimation of actual number of species for each type of hermaphroditism (Sadovy de Mitcheson and Liu 2008). More recent studies have investigated the incidence of hermaphroditism in specific groups, e.g., gobies (Cole 2010;Manabe et al 2013;Sunobe et al 2017), serranids (Erisman and Hastings 2011), polynemids (Shihab et al 2017;Butler et al 2018) and sparids (Pla et al 2020) to name some examples, but a global picture, based on current phylogenetic relationships, and with number of species for each major type of hermaphroditism taking into account only confirmed cases is missing. These last points, i.e., based on currently accepted phylogeny and only on confirmed species are very important.…”

Life‐history constraints, short adult life span and reproductive strategies in coral reef gobies of the genus Trimma

“…Sex change strategies can be inferred by gonad structure (Lowe et al ., 2021 ; Sunobe et al ., 2017 ). The high number of individuals with gonads in a transitional state indicates that sex change may occur frequently in the three species examined here.…”

“…Sex change can occur in as little as 4 days (female to male) and 6 days (male to female) in T. okinawae (Sunobe & Nakazono, 1993 ; Yamaguchi, 2016 ). Bisexual gonads in both male and female phases are seen in other small fishes with short reproductive life spans and high mortality, such as the genera Eviota (Maxfield & Cole, 2019a ; Schemmel & Cole, 2016 ), Lythrypnus (Maxfield & Cole, 2019b ; Muñoz‐Arroyo et al ., 2019 ), Bryaninops (Munday et al ., 2002 ), Priolepis (Manabe et al ., 2013 ) and multiple other Trimma species (Sunobe et al ., 2017 ). High and unpredictable mortality can mean that an individual's social circumstances can quickly change.…”

Rapid turnover and evolution of sex-determining regions amongSebastesrockfishes

“…Among vertebrates, teleost fishes exhibit the most variability in sex-determination mechanisms (Bachtrog, 2014). Among these are ESD, as in many flatfishes (Luckenbach et al, 2009), socially or environmentally driven sequential hermaphroditism in gobies (Sunobe et al, 2017), variable MSD in several clades including salmonids, halibut, and tuna (McKinney et al, 2020; Chiba et al, 2021; Edvardsen et al, 2022).…”