Hermaphrodites and parasitism: size-specific female reproduction drives infection by an ephemeral parasitic castrator

Caitlin R Fong,Armand M Kuris,Ryan F Hechinger

doi:10.1038/s41598-019-55167-x

Abstract

Sex can influence patterns of parasitism because males and females can differ in encounter with, and susceptibility to, parasites. We investigate an isopod parasite (Hemioniscus balani) that consumes ovarian fluid, blocking female function of its barnacle host, a simultaneous hermaphrodite. As a hermaphrodite, sex is fluid, and individuals may allocate energy differentially to male versus female reproduction. We predicted the relationship between barnacle size and female reproductive function influences the distribution of parasites within barnacle populations. We surveyed 12 populations spanning ~400 km of coastline of southern California and found intermediate-sized barnacles where most likely to be actively functioning as females. While it is unclear why larger individuals are less likely to be actively reproducing as females, we suggest this reduced likelihood is driven by increased investment in male reproductive effort at larger sizes. The female function-size relationship was mirrored by the relationship between size and parasitism. We suggest parasitism by Hemioniscus balani imposes a cost to female function, reinforcing the lack of investment in female function by the largest individuals. Within the subset of suitable (=female) hosts, infection probability increased with size. Hence, the distribution of female function, combined with selection for larger hosts, primarily dictated patterns of infection.

Highlights

Sex can influence patterns of parasitism because males and females can differ in encounter with, and susceptibility to, parasites
Hemioniscus balani is a parasitic isopod that specialises on barnacle ovarian fluid and blocks female reproduction[6,7,8]
We consistently detected that parasitism tracked the distribution of female function, consistent with the known biology of H. balani, which specialises on female function of the host and has an active searching stage that should permit it to find preferred barnacle hosts

Summary

Introduction

Sex can influence patterns of parasitism because males and females can differ in encounter with, and susceptibility to, parasites. Hemioniscus balani is a parasitic isopod that specialises on barnacle ovarian fluid and blocks female reproduction[6,7,8] This protandrous isopod infects at least 14 species of hermaphroditic barnacles and has a cosmopolitan distribution[6,7,8,9]. C. fissus is a protandrous hermaphrodite—individuals begin their lives as males and, with increasing age and size, allocate more energy to female function to become simultaneous hermaphrodites[5,15,16,17,18]. Parasites might prefer, and actively infect, larger hosts with more resources (e.g.13,19–21) To test these hypotheses, we surveyed barnacles for size, female reproductive function, and parasitism by H. balani from 12 populations at 6 localities along the Southern California Bight

Methods

Results

Conclusion