Sex-specific metamorphosis of cypris larvae in the androdioecious barnacle Scalpellum scalpellum (Crustacea: Cirripedia: Thoracica) and its implications for the adaptive evolution of dwarf males.

Niklas Dreyer,Jørgen Olesen,Rikke Beckmann Dahl,Benny Kwok Kan Chan,Jens Thorvald Høeg

doi:10.1371/journal.pone.0191963

Abstract

Androdioecy (co-existence of hermaphrodites and dwarf males) is a fascinating yet poorly understood phenomenon. The pedunculated barnacle Scalpellum scalpellum is an emerging model species for the system. In S. scalpellum, dwarf males and hermaphrodites are very different in adult morphology (e.g., in feeding structures and reproductive organs), but they share the same larval development with nauplii followed by cypris larvae. Recently, it was found that S. scalpellum cypris larvae display both genetic and environmental sex determination, but no detailed morphological study has yet investigated how the settled cypris larvae differ subsequent to settlement. This study investigates the morphological aspects of the onset of sex determination in the cyprids of S. scalpellum by examining their metamorphosis into either dwarf males or hermaphrodites under laboratory conditions. This study emphasizes morphological differences, such as size and shape of primordial shell plates, development of a flexible peduncle and of thoracopods. It was shown that the cypris larvae start to differ already one day after settlement on either a hydroid (leading to hermaphrodites) or an adult hermaphrodite (leading to dwarf males). Dwarf males gradually developed an ovoid body shape and two pairs of circular scutal and tergal primordia. Such cyprids developed neither a carina nor any peduncle or cirri for feeding. The study concludes that the dwarf males of S. scalpellum are not just hermaphrodites arrested early in development. This entails that dwarf males constitute their own separate developmental pathways and points to S. scalpellum dwarf males being more specialized than previously stated. Finally, the study compares differences in dwarf male morphology between S. scalpellum with two other androdioecious species with less specialized dwarf males and use this to discuss evolutionary implications for the adaptive evolution of dwarf males across the Cirripedia.

Highlights

In his seminal papers on the Cirripedia, Charles Darwin wrote that ‘the diversity in sexual relations appears to me eminently curious (. . .)’ but ‘regarding the final cause of separation of the sexes and of the existence of complemental males, I can throw no light’ [1]
S1–S4 Videos provide an overview of the entire sequence of events in the metamorphosis into hermaphrodites and dwarf males
Metamorphosis of cypris larvae in Scalpellum scalpellum scutal primordium (G) 7–9 days; cypris carapace shed, peduncle has developed so the specimen is raised to near vertical stance. (H) 10–12 days; full armament of shell plates including three latus plates

Summary

Introduction

In his seminal papers on the Cirripedia, Charles Darwin wrote that ‘the diversity in sexual relations appears to me eminently curious (. . .)’ but ‘regarding the final cause of separation of the sexes and of the existence of complemental males, I can throw no light’ [1]. Cirripede males are always small (called dwarf males) compared to their female or hermaphrodite partner to which they are permanently attached. Dwarf males have evolved independently in several lineages and are likely to be advantageous in being located adjacently to the ovipore. They reach maturity faster than their larger partners and survive at higher rates to this stage [5, 6, 7, 8, 9, 10, 11, 12]. Detailed studies of dwarf male structure and function, and especially their development from the settled cypris larva, exist only for a handful of cirripede species [13, 14]

Methods

Results

Conclusion