A phylogenetic comparative analysis on the evolution of sequential hermaphroditism in seabreams (Teleostei: Sparidae)

Abstract

systems, particularly for both types of sequential hermaphroditism, given that it contains many gonochoristic, protogynous and protandrous species, with differences in sexual systems even between species belonging to the same genus. The main theoretical framework to explain the evolutionary advantage of sequential hermaphroditism based on sex allocation theory is the size-advantage model (SAM) 9,19-21. The SAM proposes that individuals should switch sex when the second sex achieves a greater fitness at a larger body size than the first sex, thus increasing lifetime fitness 22. When larger males have higher reproductive success than smaller males and similar sized females, fish should reproduce initially as female and change later to male (protogyny) 19,23,24. Conversely, protandry is expected when large females have greater fitness than smaller females and similar sized males 19,20. Empirical studies support this model in several fish families, explaining quantitatively the size or age at which an individual should change sex, as well as the overall population sex ratio 25,26. Typically, male-biased sex ratios are observed in populations of protandrous species, while female-biased sex ratios are observed in populations of protogynous species, especially in haremic groups 19,26,27. Mating systems (the number and social dominance of mates involved) and spawning mode (i.e., group spawning, where several males spawn with one or several females, or pair-mating, where a single male spawns with a single female), determine the fitness that a fish of a given size can achieve as a female or as a male 23,28. Fish mating systems range from monogamy or pair-mating, to harem polygyny (one dominant male controls access to multiple females 29), lek-type polygyny (temporary harems 25), and large polygamous or promiscuous aggregations (where group spawning occurs 30). Sperm competition is particularly intense in large aggregations with multiple males 31,32 while it is absent in monogamy and pair-mating, and low in polygynous mating systems. Sperm competition and spawning modes have been used to infer mating systems 33-35 , which are relevant when testing the predictions of SAM since they can generate sex-specific differences in reproductive expectations 23,24,36,37. Thus, the first study that tested the predictions of SAM incorporating the mating system in a phylogenetic context focused on the evolution of protogynous groupers according to pair spawning mode 35. Indeed, protandry should be favored when sperm competition is low (mating occurs between members of monogamous or random pairs 19,22-24), and mate monopolization by large males should occur in protogynous species 23. Even though sperm competition was not included in the original formulation of the model 9,19 , it was subsequently mentioned as absent in protogyny 21,23,24,38 , limited in protandry (considered typical of random pairing and small groups) 22,23 and high in gonochorism (when mating occurs in large groups) 21,23,35,39. The influence of sperm competition on sex c...

Switches, stability and reversals: the evolutionary history of sexual systems in fish

“…Conversely, the longer life in protogynous species maximises the fitness of 419 the large successful males (second sex) that can monopolize females in harems or in spawning 420 grounds. In addition, male investment in gonad tissue (as quantified by the gonadosomatic 421 index) is lower in protogyny, as expected by theory 48,54 , since large males can better monopolize mating opportunities and face low levels of sperm competition in harems and spawning aggregations (Table 2). Small-sized protandrous males in spawning aggregations instead need to boost their investment in the gonads but even in the absence of sperm competition (monogamy) they require large gonads to fertilize highly fecund females larger than themselves 54 .…”

“…The intensity of sperm competition has been incorporated in the size advantage model 50 as it can play a significant role in the advantage of protogyny: changing sex from female to male should be more advantageous when paternity assurance is high due to reduced sperm competition 51 . Consistent with these predictions, the gonadosomatic index (GSI), defined as the percentage of body mass devoted to the gonads 52 and a reliable indicator 173 of the intensity of sperm competition 53 , is significantly lower in protogynous teleost species than in gonochoristic congeners 47,48,54 . However, protandrous teleost fish do not always conform to theoretical expectations, exhibiting higher GSI as males than expected 48 .…”

“…However, protandrous teleost fish do not always conform to theoretical expectations, exhibiting higher GSI as males than expected 48 . We have recently proposed that, at least in the family Sparidae, high male GSI in protandrous fish can be explained not only by spawning aggregations and high sperm competition in some species, but also because high investment in the gonads represents a compensatory mechanism that allows small males to fertilize highly fecund females much larger than themselves 54 . ♂ ↔ ♀ 1:1 ♂ = ♀ ♂♀ Individuals produce gametes of both sexes at the same time or in a short period of time 186…”

Stress and sex determination in fish: from brain to gonads

“…They can be grouped into biotic and abiotic parameters. Among biotic parameters, are density and social interactions, which have been well characterized in Anguilliformes and hermaphroditic fish, respectively (Geffroy and Bardonnet, 2016;Gemmell et al, 2019;Pla et al, 2020). Abiotic parameters may be chemical or physical.…”

Evolution of Sex Determination in Amniotes: Did Stress and Sequential Hermaphroditism Produce Environmental Determination?

“…The other aspect shared between ESD species and sequential hermaphrodites is the frequently biased sex ratio. [ 46,101 ] Charnov and Bull [ 102 ] already proposed a uniting model for ESD and sequential hermaphrodites showing that skewed sex ratios are stable evolutionary strategies under certain conditions. ESD species and sequential hermaphrodites could also share the proximate mechanism of sex determination—the stress‐related pathway.…”