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

C Benvenuto,J Chopelet,I Coscia,S Mariani,M Sala-Bozano

doi:10.1038/s41598-017-09298-8

C Benvenuto, J Chopelet + Show 3 more

Open Access

https://doi.org/10.1038/s41598-017-09298-8

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Abstract

Sequentially hermaphroditic fish change sex from male to female (protandry) or vice versa (protogyny), increasing their fitness by becoming highly fecund females or large dominant males, respectively. These life-history strategies present different social organizations and reproductive modes, from near-random mating in protandry, to aggregate- and harem-spawning in protogyny. Using a combination of theoretical and molecular approaches, we compared variance in reproductive success (Vk*) and effective population sizes (Ne) in several species of sex-changing fish. We observed that, regardless of the direction of sex change, individuals conform to the same overall strategy, producing more offspring and exhibiting greater Vk* in the second sex. However, protogynous species show greater Vk*, especially pronounced in haremic species, resulting in an overall reduction of Ne compared to protandrous species. Collectively and independently, our results demonstrate that the direction of sex change is a pivotal variable in predicting demographic changes and resilience in sex-changing fish, many of which sustain highly valued and vulnerable fisheries worldwide.

Highlights

Unique among vertebrates[1], sex-changing fish develop and reproduce as males first and grow into highly fecund females, or reproduce initially as females to later change into large dominant males
In reproductive success and skewed sex ratios are the two most powerful forces that shape a parameter of crucial significance in population genetics, ecology and conservation: the effective population size (Ne), which offers a view of the intensity of genetic drift and the changes in genetic variability in a population and its potential for persistence and resilience[16, 17]
Hermaphroditic fish are an intriguing group of animals

Summary

Introduction

Unique among vertebrates[1], sex-changing fish develop and reproduce as males first and grow into highly fecund females (protandry), or reproduce initially as females to later change into large dominant males (protogyny). The main theoretical model proposed to explain its adaptive value, the size advantage model[6,7,8], predicts that sex change should occur when the reproductive success of an individual depends on its size, but more so for one sex than the other In this scenario, protandry is favoured over fixed separate sexes (gonochorism) when larger females have higher reproductive value than smaller ones (they can produce more eggs), while protogyny is favoured in situations where size allows dominant males to control the reproductive access to females. As a result of such changes over an individual’s lifetime, sequentially hermaphroditic species typically exhibit sex ratios that depart from the balanced ≈ 0.5 observed in gonochoristic species, and are generally skewed towards the ‘first sex’ Such a bias is more pronounced in protogynous species than protandrous ones[15]. Wright[18] was the first to realize that the “effective population number” should refer only to the “breeding population and not to the total number of individuals of all ages”; the effective population number in natural populations is generally smaller than the census size of the same population, sometimes by one or more orders of magnitude

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