Sponge symbiosis is facilitated by adaptive evolution of larval sensory and attachment structures in barnacles.

Meng-Chen Yu,Niklas Dreyer,Gregory Aleksandrovich Kolbasov,Benny Kwok Kan Chan,Jens Thorvald Høeg

doi:10.1098/rspb.2020.0300

Abstract

Symbiotic relations and range of host usage are prominent in coral reefs and crucial to the stability of such systems. In order to explain how symbiotic relations are established and evolve, we used sponge-associated barnacles to ask three questions. (1) Does larval settlement on sponge hosts require novel adaptations facilitating symbiosis? (2) How do larvae settle and start life on their hosts? (3) How has this remarkable symbiotic lifestyle involving many barnacle species evolved? We found that the larvae (cyprids) of sponge-associated barnacles show a remarkably high level of interspecific variation compared with other barnacles. We document that variation in larval attachment devices are specifically related to properties of the surface on which they attach and metamorphose. Mapping of the larval and sponge surface features onto a molecular-based phylogeny showed that sponge symbiosis evolved separately at least three times within barnacles, with the same adaptive features being found in all larvae irrespective of phylogenetic relatedness. Furthermore, the metamorphosis of two species proceeded very differently, with one species remaining superficially on the host and developing a set of white calcareous structures, the other embedding itself into the live host tissue almost immediately after settlement. We argue that such a high degree of evolutionary flexibility of barnacle larvae played an important role in the successful evolution of complex symbiotic relationships in both coral reefs and other marine systems.

Highlights

Marine sponges (Porifera) are key players in coral reef ecology and can support a high diversity of symbiotic life [1,2,3]
(1) Does larval settlement on sponge hosts require novel adaptations facilitating symbiosis? (2) How do larvae settle and start life on their hosts? (3) How has this remarkable symbiotic lifestyle involving many barnacle species evolved? We found that the larvae of sponge-associated barnacles show a remarkably high level of interspecific variation compared with other barnacles
We argue that such a high degree of evolutionary flexibility of barnacle larvae played an important role in the successful evolution of complex symbiotic relationships in both coral reefs and other marine systems

Summary

Introduction

Marine sponges (Porifera) are key players in coral reef ecology and can support a high diversity of symbiotic life (mutualism, parasitism and commensalism) [1,2,3]. The relationship between microbes and their sponge hosts has been widely explored [4,5,6]. Symbiotic lifestyles with sponges are widespread in invertebrate animals and can exhibit an array of remarkable specializations. This is seen in, for example, the sponge-dwelling shrimps, which have evolved novel mating strategies and eusocialism [7]. Little is known about the biology of sessile sponge-associated invertebrates. The larvae of these organisms must first attach and successfully metamorphose into a permanently sessile form embedded within the live tissue of their sponge host, but the severe difficulties in culturing and maintaining the royalsocietypublishing.org/journal/rspb Proc.

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