American Society of Naturalists

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“Correlated evolution of sex allocation and mating system in wrasses and parrotfishes”

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Jennifer R. Hodge, Francesco Santini, and Peter C. Wainwright (July 2020)

Size advantage drives the evolution of sex change in an iconic group of sex changing fishes (Labridae)

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Male size advantage promotes the evolution of sex change from female to male

An organism that changes functional sex during the course of its reproductive life is known as a sequential hermaphrodite. This type of sex change occurs in a variety of animals and plants, but among vertebrate animals it is only found in some fishes. Theory predicts that sequential hermaphroditism should evolve in animals when, for a given sex, reproduction is more effective at a certain size (the size-advantage model). For example, when large males maintain social status by monopolizing access to resources or females, the reproductive success of small males is suppressed, and sex change from female to male is predicted. This is the theory, but until now we lacked empirical evidence that sex change evolves as a consequence of size advantage.

Working at the University of California, Davis, Jennifer Hodge and colleagues analyzed the different forms of sex allocation and mating expressed by wrasses and parrotfishes – the second largest family of marine fishes and a model system for studies of sequential hermaphroditism. Accounting for evolutionary history, they find that female-to-male sex change has evolved in response to mating systems characterized by male size advantage. They also find that the mating system with the strongest male size advantage favors the most pronounced expression of hermaphroditism in which all males are derived via sex change. Once evolved, this combination of mating and sex allocation is rarely lost. The authors suggest the reason that male size advantage is able to alter selection in favor of sex change in fishes is likely because their gonads develop from a single type of tissue, rather than from two as in most vertebrates, resulting in plastic sex determination.

This study provides important insight into why sex change evolves and the mechanisms that are required to sustain it.


Abstract

In accordance with predictions of the size-advantage model, comparative evidence confirms that protogynous sex change is lost when mating behavior is characterized by weak size advantage. However, we lack comparative evidence supporting the adaptive significance of sex change. Specifically, it remains unclear whether increasing male size advantage induces transitions to protogynous sex change across species, as it can within species. We show that in wrasses and parrotfishes (Labridae), the evolution of protogynous sex change is correlated with polygynous mating, and that the degree of male size advantage expressed by polygynous species influences transitions between different types of protogynous sex change. Phylogenetic reconstructions reveal strikingly similar patterns of sex allocation and mating system evolution with comparable lability. Despite the plasticity of sex determination mechanisms in labrids, transitions trend towards monandry (all males derived from sex-changed females), with all observed losses of protogyny accounted for by shifts in the timing of sex change to prematuration. Likewise, transitions in mating system trend from the ancestral condition of lek-like polygyny toward greater male size advantage, characteristic of haremic polygyny. The results of our comparative analyses are among the first to confirm the adaptive significance of sex change as described by the size-advantage model.