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Foundation species provide critical resources to ecological community members and are major determinants of biodiversity. The barnacle Balanus glandula is one such species and dominates space among the higher reaches on wave-swept shores. Here, we show that B. glandula produces a 199.6-kDa glycoprotein (named "MULTIFUNCin"), and following secretion, a 390-kDa homodimer in its native state. MULTIFUNCin expression is localized in the epidermis, cuticle, and new shell material. Consequently, this molecule can specify upon contact the immediate presence of a live barnacle. Shared, conserved domains place MULTIFUNCin in the α2-macroglobulin (A2M) subgroup of the thioester-containing protein family. Although previously undescribed, MULTIFUNCin shares 78% nucleotide sequence homology with a settlement-inducing pheromone (SIP) of the barnacle, Amphibalanus amphitrite Based on this and further evidence, we propose that the two proteins are orthologues and evolved ancestrally in structural and immunological roles. More recently, they became exploited as chemical cues for con- and heterospecific organisms, alike. MULTIFUNCin and SIP both induce habitat selection (settlement) by conspecific barnacle larvae. In addition, MULTIFUNCin acts as a potent feeding stimulant to major barnacle predators (sea stars and several whelk species). Promoting immigration via settlement on the one hand, and death via predation on the other, MULTIFUNCin simultaneously mediates opposing demographic processes toward structuring both predator and prey populations. As a multifunctional protein cue, MULTIFUNCin provides valuable sensory information, conveys different messages to different species, and drives complex biotic interactions.

Foundation species provide critical resources to ecological community members and are key determinants of biodiversity. The barnacle Balanus glandula is one such species and dominates space among the higher reaches of wave-swept shores (Northeastern Pacific Ocean). This animal produces a cuticular glycoprotein (named "MULTIFUNCin") of 199.6 kDa, and following secretion, a 390 kDa homodimer in native form. From field and lab experiments, we found that MULTIFUNCin significantly induces habitat selection by conspecific larvae, while simultaneously acting as a potent feeding stimulant to a major barnacle predator (whelk, Acanthinucella spirata). Promoting immigration via settlement on the one hand, and death via predation on the other, MULTIFUNCin drives opposing demographic processes toward structuring predator and prey populations. As shown here, a single compound is not restricted to a lone species interaction or sole ecological function. Complex biotic interactions therefore can be shaped by simple chemosensory systems and depend on the multifunctional properties of select bioactive proteins.

Sensory systems provide critical filters that enable organisms to detect and recognize valuable resources. Trophic cascades, structuring populations and communities, are determined to a large degree by trait-mediated interactions that rely on sensory inputs. Certain molecules serve as chemosensory stimuli and play keystone roles in determining outcomes of predator-prey dynamics at multiple trophic levels. Here, a surface-adsorbed glycoprotein signal molecule, MULTIFUNCin, is fully identified and its role in waveswept rocky intertidal community dynamics investigated. Barnacles (Balanus glandula), are constrained to produce MULTIFUNCin for cuticle/shell formation. This compound evoked settlement by conspecifics larvae in field assays, and thus, operates as seminal cue for recruitment. Moreover, the same substances triggered predation by a numerically dominant whelk species (Acanthinucella spirata) on barnacle juveniles and adults in lab and field experiments. This glycoprotein, therefore, balances simultaneous demographic processes that enhance, and diminish, barnacle populations. As dominant competitors for space, the relative equilibrium between barnacle recruitment and predation mortality has strong, cascading direct and indirect effects on community dynamics. Hence, MULTIFUNCin plays a keystone role within rocky intertidal habitats.