Sex change and the size-advantage model

doi:10.1016/0169-5347(88)90176-0

Trends in Ecology & Evolution

Volume 3, Issue 6, June 1988, Pages 133-136

https://doi.org/10.1016/0169-5347(88)90176-0 Get rights and content

Abstract

At the intraspecific level, the size-advantage model attempts to explain why some species change sex and others do not. Generally, sex change is favored if the relation between reproductive success and size or age differ between the sexes. Differential costs of reproduction and the mating system appear to be among the major factors producing differences in reproductive expectations between the sexes. On the intraspecific level, tests of the model consist of predicting the optimal size or age of sex change. In general, an individual should change sex if it can increase its reproductive value (future expected reproduction) by doing so. Reproductive values are often dependent on the local environment, local population demography, and the individual's own status, and labile sex change appears to be common. Many of the objections to the size-advantage model arise from confusion between the intraspecific and intraspecific versions.

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Sex differences in cell number in the preoptic area of the hypothalamus (POA) are documented across all major vertebrate lineages and contribute to differential regulation of the hypothalamic-pituitary-gonad axis and reproductive behavior between the sexes. Sex-changing fishes provide a unique opportunity to study mechanisms underlying sexual differentiation of the POA. In anemonefish (clownfish), which change sex from male to female, females have approximately twice the number of medium-sized cells in the anterior POA compared to males. This sex difference transitions from male-like to female-like during sex change. However, it is not known how this sex difference in POA cell number is established. This study tests the hypothesis that new cell addition plays a role. We initiated adult male-to-female sex change in 30 anemonefish (Amphiprion ocellaris) and administered BrdU to label new cells added to the POA at regular intervals throughout sex change. Sex-changing fish added more new cells to the anterior POA than non-changing fish, supporting the hypothesis. The observed effects could be accounted for by differences in POA volume, but they are also consistent with a steady trickle of new cells being gradually accumulated in the anterior POA before vitellogenic oocytes develop in the gonads. These results provide insight into the unique characteristics of protandrous sex change in anemonefish relative to other modes of sex change, and support the potential for future research in sex-changing fishes to provide a richer understanding of the mechanisms for sexual differentiation of the brain.
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In recent years, observations of distinct organisms have linked the quality of the environment experienced by a given individual and the sex it will develop. In most described cases, facing relatively harsh conditions resulted in masculinization, while thriving in favorable conditions promoted the development of an ovary. This was shown indistinctively in some species presenting a genetic sex determination (GSD), which were able to sex-reverse, and in species with an environmental sex determination (ESD) system. However, this pattern strongly depends on evolutionary constrains and is detected only when females need more energy for reproduction. Here, I describe the mechanisms involved in this environmentally driven sex allocation (EDSA), which involves two main energy pathways, lipid and carbohydrate metabolism. These pathways act through various enzymes and are not necessarily independent of the previously known transducers of environmental signals in species with ESD: calcium–redox, epigenetic, and stress regulation pathways. Overall, there is evidence of a link between energy level and the sexual fate of individuals of various species, including reptiles, fish, amphibians, insects, and nematodes. As energy pathways are evolutionarily conserved, this knowledge opens new avenues to advance our understanding of the mechanisms that allow animals to adapt their sex according to the local environment.
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Citation Excerpt :
These data suggest that sexual fate is not changed by exogenous chemicals and it is tightly regulated by the endogenous cues (such as a certain body size and age) in the hermaphroditic fish. Therefore, even if the “size-advantage hypothesis” is widely used to explain the timing of sex change in hermaphroditic fish (Warner, 1988; Ghiselin, 2006), the molecular and cellular mechanisms that regulate the timing of the sex change in nonsocial cue-influenced hermaphroditic fish remain unclear. Molecular and cellular regulation of secondary sex differentiation and reversible sex change are interesting research areas.
In teleost fish, sex can be determined by genetic factors, environmental factors, or both. Unlike in gonochoristic fish, in which sex is fixed in adults, sex can change in adults of hermaphroditic fish species. Thus, sex is generated during the initial gonadal differentiation stage (primary sex differentiation) and later during sexual fate alternation (secondary sex differentiation) in hermaphroditic fish species. Depending on the species, sex phase alternation can be induced by endogenous cues (such as individual age and body size) or by social cues (such as sex ratio or relative body size within the population). In general, the fluctuation in plasma estradiol-17β (E2) levels is correlated with the sexual fate alternation in hermaphroditic fish. Hormonal treatments can artificially induce sexual phase alternation in sequential hermaphroditic fishes, but in a transient and reversible manner. This is the case for the E2-induced female phase in protandrous black porgy and the methyltestosterone (MT)- or aromatase inhibitor (AI)-induced male phase in protogynous grouper. Recent reviews have focused on the different forms of sex change in fish who undergo sequential sex change, especially in terms of gene expression and the role of hormones. In this review, we use the protandrous black porgy, a nonsocial cue-influenced hermaphroditic species, with digonic gonads (ovarian and testis separated by a connective tissue), as a model to describe our findings and discuss the molecular and cellular regulation of sexual fate determination in hermaphroditic fish.
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Trends in Ecology & Evolution

ReviewSex change and the size-advantage model

Abstract

J. Theor Biol.

Trends Ecol. Evol.

The Theory of Sex Allocation

Annu. Rev. Ecol. Syst.

Rev. Biol.

The Economy of Nature and the Evolution of Sex

Am. Nat.

Science

Am. Nat.

Am. Nat.

Evolution

Oecologia

Bioscience

Evol. Biol.

Bioscience

Mar. Biol. Lett.

Am. Nat.

Review
Sex change and the size-advantage model