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

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.

Independent and adaptive evolution of phenotypic novelties driven by coral symbiosis in barnacle larvae

“…Scleractinian corals comprise some of the most extreme habitats permanently colonized by other animals as they possess nematocyst cells and complex biochemical defense mechanisms that in concert deter symbiont invasion (Stella et al 2010;Baeza 2015;Bruno and Witman 1996;Yu et al 2020). On the one hand, this challenge is exacerbated in animals that permanently invade live corals as they face being overgrown and engulfed by the hosts (Baeza 2015;Chan et al 2020a).…”

“…On the other hand, they gain shelter from predators and may enjoy increased longevity compared to free-living relatives. A remarkable range of symbiotic invertebrate taxa take residency in or on corals, and these play crucial roles in the maintenance and stability of reef systems (Stella et al 2010;Baeza 2015;Chan et al 2020a,b;Yu et al 2020). Yet, despite the significance of symbiotic relationships on coral reefs, the underlying mechanisms of how such intimate relationships are functionally established remain poorly understood.…”

“…1A-I; Baeza 2015; Chan et al 2020a). A series of recent studies have documented remarkable convergent and adaptive evolution of larval form and function in invertebrates (Nielsen 2012;Hart 1996;Carrier et al 2018;McEdward 2000;Yu et al 2020). However, a significant knowledge gap concerns whether the features that enable localization, exploration, invasion, and establishment are adaptively selected for by niche requirements in invertebrate larvae.…”

“…The functional and structural biologies of barnacle cypris antennules have recently attracted much attention as they are critical in understanding how and why barnacles are found in such an astounding variety of niches, which range the surfaces of whales, sea snakes, sharks, polychaetes, bryozoans, hydroids, crustaceans, mollusks, rocky shores, deep-sea hydrothermal vents, sea-spiders, sponges, and corals (Fig. 1; Al-Yahya et al 2016;Yu et al 2020;Martin et al 2014;Høeg et al 2015;.…”

“…Here, we test whether similar ecological niches entail adaptive evolution of key larval phenotypic traits related to permanent host invasion. Stimulated by the discoveries that sponge and rocky shore barnacles sport adaptive larval antennular traits (Yu et al 2020), we investigate the antennular biomechanics and structure, mode of host invasion and exploration, and larval development of three coral-dwelling barnacles: the burrowing barnacles Berndtia utinomii and B. purpurea (Cirripedia: Acrothoracica) and the epibiotic balanomorphan barnacle Darwiniella angularis (Cirripedia: Thoracicalcarea: Pyrgomatidae). These species are separated by more than 100 my of barnacle evolution, are distantly related, yet all live surrounded by the soft tissues and skeleton of corals (Utinomi 1961;Pérez-Losada et al 2009;Tsang et al 2009;Chan et al 2014;Malay and Michonneau 2014;Pérez-Losada et al 2014;Tsang et al 2014;Lin et al 2016;Liu et al 2016;Ewers-Saucedo et al 2019).…”