Phenotypic differences between the sexes in the sexually plastic mangrove rivulus fish (Kryptolebias marmoratus)

Abstract

To maximize reproductive success, many animal species have evolved functional sex change. Theory predicts that transitions between sexes should occur when the fitness payoff of the current sex is exceeded by the fitness payoff of the opposite sex. We examined phenotypic differences between the sexes in a sexchanging vertebrate, the mangrove rivulus fish (Kryptolebias marmoratus), to elucidate potential factors that might drive the 'decision' to switch sex. Rivulus populations consist of self-fertilizing hermaphrodites and males. Hermaphrodites transition into males under certain environmental conditions, affording us the opportunity to generate 40 hermaphrodite-male pairs where, within a pair, individuals possessed identical genotypes despite being different sexes. We quantified steroid hormone levels, behavior (aggression and risk taking), metabolism and morphology (organ masses). We found that hermaphrodites were more aggressive and risk averse, and had higher maximum metabolic rates and larger gonadosomatic indices. Males had higher steroid hormone levels and showed correlations among hormones that hermaphrodites lacked. Males also had greater total mass and somatic body mass and possessed considerable fat stores. Our findings suggest that there are major differences between the sexes in energy allocation, with hermaphrodites exhibiting elevated maximum metabolic rates, and showing evidence of favoring investments in reproductive tissues over somatic growth. Our study serves as the foundation for future research investigating how environmental challenges affect both physiology and reproductive investment and, ultimately, how these changes dictate the transition between sexes.

The Genome of the Self-Fertilizing Mangrove Rivulus Fish,Kryptolebias marmoratus: A Model for Studying Phenotypic Plasticity and Adaptations to Extreme Environments

“…These species are distributed in close association with red mangrove forests ( Rhizophora mangle ) along the coastal regions of central and south Florida, the Caribbean and the eastern coasts of Central and South America ( Costa 2006 ). Mangrove rivulus exist primarily as hermaphrodites with preferential internal self-fertilization ( Harrington 1961 ), but the species exhibits environmental sex determination, with primary males developing from embryos incubated at low temperatures (18–20 °C; [ Harrington 1967 ; Harrington and Kallman 1968 ; Ellison et al 2015 ]), and remains sexually labile throughout adulthood ( Harrington 1971 , 1975 ; Turner et al 2006 ; Garcia et al 2016 ) ( fig. 1 ).…”

Relationships between external sexually dimorphic characteristics and internal gonadal morphology in a sex‐changing fish

“…There are a number of other characteristics found in males (e.g., black margin on anal and caudal fins) but these characteristics typically appear, sometimes prominently, later in male development and thus, cannot be used as a diagnostic tool for identifying young primary males or secondary males during periods immediately following complete sex change. Of all characteristics observed in the laboratory colony animals, the presence of orange and the loss of an ocellus occurs most reliably, which is why they were assessed in this study, and other investigations of phenotypic differences between the sexes (Soto & Noakes, ; Garcia et al ., ).…”

“…Garcia et al . () found that males have a significantly greater fat stores than hermaphrodites, while hermaphrodites committed their energy primarily to the gonad. It is possible that lower body condition in males showing a ‘transitional’ external phenotype might result from these individuals allocating energy into restructuring their gonad tissue instead of storing it as fat.…”

Sexual phenotype drives variation in endocrine responses to social challenge in a quasi-clonal animal

“…However, genotypic differences (e.g. heterotypic chromosomes and their associated genes) per se are not necessary to drive dramatic sex differences, as evidenced by pronounced phenotypic differences between males and females in animals with environmental sex determination [ 31 , 32 ] and in animals that undergo sex change during adulthood [ 33 , 34 ].…”

“…in Atlantic croaker ( Micropogonias undulatus ), [ 47 ]). Rivulus hermaphrodites are significantly more aggressive than males towards model conspecifics [ 34 ]; however, whether hermaphrodites and males behave differently during, and exhibit different hormonal responses after, dyadic contests remains unclear. To test this hypothesis, we first measured pre-contest (baseline) steroid hormones (testosterone (T), cortisol (F), oestradiol (E2) and 11-ketotestosterone (11-KT)).…”