Ecological and evolutionary consequences of alternative sex-change pathways in fish

Benvenuto, Chiara; Coscia, Ilaria; Chopelet, Julien; Sala-Bozano, Maria; Mariani, Stefano

doi:10.1038/s41598-017-09298-8

Cited by 37 publications

(46 citation statements)

References 64 publications

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“…Indeed, we often tend to oversimplify the complexity of sequential hermaphroditism: not all protogynous species are haremic, as not all protandrous species mate in pairs. A recent study 28,85 has revealed a broader variation in effective population size in protogynous species that differs from the more limited expectations obtained when all protogynous species were considered haremic by default. Instead, some protogynous species were found to be group spawners, altering the expectations that all protogynous species should have low effective population size due to their supposed haremic system.…”

Section: Discussionmentioning

confidence: 82%

“…The prediction column summarizes the overall expectation on sperm competition (and thus GSI) for the sexual system, based on the most common mating and spawning mode, according to the SAM 23,24 . *Protogynous group spawners should be favoured as large males can produce more sperm 28 . **Promiscuous large groups are not common, but still present in protandrous species (see text for examples).…”

Section: Methodsmentioning

confidence: 99%

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

Pla

Benvenuto

Capellini

et al. 2020

Sci Rep

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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...

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Section: Discussionmentioning

confidence: 82%

Section: Methodsmentioning

confidence: 99%

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

Pla

Benvenuto

Capellini

et al. 2020

Sci Rep

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“…The above model assumes a single, knife-edge age at which all surviving individuals change sex. In real populations, the distribution of sex ratio over time is typically sigmoidal [7]:…”

Section: (A) Ess Theorymentioning

confidence: 99%

“…Sex reversal is found in over a dozen invertebrate phyla, including corals, sponges, molluscs, annelids, echinoderms and (alone among arthropods) crustaceans; in plants, simultaneous hermaphrodites are more common, but species that change sex occur in all major groups [1][2][3]. Among vertebrates, this strategy is restricted to teleost fishes, but within that group it occurs in at least 27 families [4][5][6][7][8].…”

Section: Introductionmentioning

confidence: 99%

“…A well-known consequence of skewed sex ratio is a reduction of effective population size, N e [16], which in turn reduces the effectiveness of natural selection, and leads to higher rates of genetic drift, inbreeding and loss of genetic variability [17]. Although some potential consequences of sex reversal for N e have been noted [7,18,19], costs have not been evaluated quantitatively in the ESS context. Is it possible that evolutionary drag, in terms of increased genetic drift, has limited the number of species that can support viable sex-changing populations?…”

Section: Introductionmentioning

confidence: 99%

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Consequences of sex change for effective population size

2018

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Sequential hermaphroditism, where males change to females (protandry) or the reverse (protogyny), is widespread in animals and plants, and can be an evolutionarily stable strategy (ESS) if fecundity rises faster with age in the second sex. Sequential hermaphrodites also generally have sex ratios skewed towards the initial sex, and standard theory based on fixed sexes indicates that this should reduce effective population size (N e ) and increase the deleterious effects of genetic drift. We show that despite having skewed sex ratios, populations that change sex at the ESS age do not have reduced N e compared with fixed-sex populations with an even sex ratio. This implies that the ability of individuals to operate as both male and female allows the population to avoid some evolutionary constraints imposed by fixed sexes. Furthermore, N e would be maximized if sex change occurred at a different (generally earlier) age than is selected for at the individual level, which suggests a potential conflict between individual and group selection. We also develop a novel method to quantify the strength of selection for sex reversal.

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Epigenetics underpins phenotypic plasticity of protandrous sex change in fish

Budd

Robins

Whybird³

et al. 2022

Ecology and Evolution

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Phenotypic plasticity is an important driver of species resilience. Often mediated by epigenetic changes, phenotypic plasticity enables individual genotypes to express variable phenotypes in response to environmental change. Barramundi (Lates calcarifer) are a protandrous (male‐first) sequential hermaphrodite that exhibits plasticity in length‐at‐sex change between geographic regions. This plasticity is likely to be mediated by changes in DNA methylation (DNAm), a well‐studied epigenetic modification. To investigate the relationships between length, sex, and DNAm in a sequential hermaphrodite, here, we compare DNAm in four conserved vertebrate sex‐determining genes in male and female barramundi of differing lengths from three geographic regions of northern Australia. Barramundi first mature as male and later sex change to female upon the attainment of a larger body size; however, a general pattern of increasing female‐specific DNAm markers with increasing length was not observed. Significant differences in DNAm between males and females of similar lengths suggest that female‐specific DNAm arises rapidly during sex change, rather than gradually with fish growth. The findings also reveal that region‐specific differences in length‐at‐sex change are accompanied by differences in DNAm and are consistent with variability in remotely sensed sea temperature and salinity. Together, these findings provide the first in situ evidence for epigenetically and environmentally mediated sex change in a protandrous hermaphrodite and offer significant insight into the molecular and ecological processes governing the marked and unique plasticity of sex in fish.

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Ecological and evolutionary consequences of alternative sex-change pathways in fish

Cited by 37 publications

References 64 publications

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

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

Consequences of sex change for effective population size

Epigenetics underpins phenotypic plasticity of protandrous sex change in fish

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