Latitudinal Variation of a Defensive Symbiosis in the Bugula neritina (Bryozoa) Sibling Species Complex

Abstract

Mutualistic relationships are beneficial for both partners and are often studied within a single environment. However, when the range of the partners is large, geographical differences in selective pressure may shift the relationship outcome from positive to negative. The marine bryozoan Bugula neritina is a colonial invertebrate common in temperate waters worldwide. It is the source of bioactive polyketide metabolites, the bryostatins. Evidence suggests that an uncultured vertically transmitted symbiont, “Candidatus Endobugula sertula”, hosted by B. neritina produces the bryostatins, which protect the vulnerable larvae from predation. Studies of B. neritina along the North American Atlantic coast revealed a complex of two morphologically similar sibling species separated by an apparent biogeographic barrier: the Type S sibling species was found below Cape Hatteras, North Carolina, while Type N was found above. Interestingly, the Type N colonies lack “Ca. Endobugula sertula” and, subsequently, defensive bryostatins; their documented northern distribution was consistent with traditional biogeographical paradigms of latitudinal variation in predation pressure. Upon further sampling of B. neritina populations, we found that both host types occur in wider distribution, with Type N colonies living south of Cape Hatteras, and Type S to the north. Distribution of the symbiont, however, was not restricted to Type S hosts. Genetic and microscopic evidence demonstrates the presence of the symbiont in some Type N colonies, and larvae from these colonies are endowed with defensive bryostatins and contain “Ca. Endobugula sertula”. Molecular analysis of the symbiont from Type N colonies suggests an evolutionarily recent acquisition, which is remarkable for a symbiont thought to be transmitted only vertically. Furthermore, most Type S colonies found at higher latitudes lack the symbiont, suggesting that this host-symbiont relationship is more flexible than previously thought. Our data suggest that the symbiont, but not the host, is restricted by biogeographical boundaries.

Lack of Overt Genome Reduction in the Bryostatin-Producing Bryozoan Symbiont “Candidatus Endobugula sertula”

“…Endobugula sertula" (7), which is a pattern of distribution consistent with a vertical mode of symbiont transmission, where respective populations have been genetically isolated since host divergence. However, we previously found evidence that horizontal transmission is likely also possible (19). We found that two sibling species of B. neritina, northern (N) and shallow (S), previously thought to be allopatrically distributed, actually coexist along the Western Atlantic.…”

“…Although "Ca. Endobugula sertula" has proven difficult to isolate and culture, the lack of extensive genome reduction suggests that a transient host-free existence may be possible, a plausible explanation for the symbiont acquisition by type N hosts found alongside symbiotic type S hosts at low latitudes (19) PCR amplicons observed PCR amplicons not observed…”

“…Collection of samples AB1_ovicells and MHD_larvae has been described elsewhere (76 (19) and found to be the "shallow" (S) genotype. Both samples were preserved in RNAlater and stored at Ϫ80°C.…”

“…However, we recently found that under some circumstances, "Ca. Endobugula sertula" may be horizontally transferred between B. neritina individuals (19), which is not consistent with strict host dependency that is associated with extreme genome reduction (18).…”

Some Bryozoa species recently introduced into the Azores: reproductive strategies as a proxy for further spread

“…Recent molecular evidence suggests that B. neritina consists of at least three genetically distinct types of colonies along the coasts of the USA [41,46] [27]. Type S colonies have an invasive behaviour, are globally distributed, including genetic confirmation of colonies from Galicia-in the north-eastern Atlantic [27], and are considered to have undergone widespread introduction as a fouling organism [74].…”