LINDQUIST LAB RESEARCH

The conceptual underpinning for much of the Lindquist group research is the impact of bioactive secondary metabolites on ecological interactions and evolutionary processes.

• Defensive strategies of marine cnidarians

Jellyfish and gorgonians (Fig. A) possess different defensive strategies: nematocysts and distasteful secondary metabolites, respectively. With Jay Stachowicz (UC Davis), we have discovered that, among hydroids, nematocysts and distasteful lipophilic compounds occur (inset) as alternative defenses that are equally effective against fish. Urchins readily consume nematocyst-defended hydroids but not chemically-defended species and were shown to strongly influence the diversity and abundance of hydroids in NC and FL. Our research has also identified an intriguing biogeographic pattern with the Atlantic and Pacific being rich and depauperate, respectively, in chemically defended hydroid species.

• Symbioses

The vast majority of described symbioses are associations of macroorganisms with microorganisms, the later providing novel biochemical services that increase host fitness. Results of two projects, one recently published and one under review, represent the 1st and 2nd examples from the marine environment of symbiotic microbes producing chemical defenses that protect the host from predators. The first study found that larvae of the bryozoan, Bugula neritina, are defended from predators by secondary metabolites called bryostatins and confirmed that these compounds are produced by a bacterial symbiont. The 2nd example involves unique symbioses between a complex of related coral-reef isopods and microbial episymbiont communities dominated by unicellular cyanobacteria (Fig. B). The isopods consume their photosymbionts and “cultivate” them by inhabiting exposed sunlit substrates, a behavior made possible by symbiont production of a chemical defense repulsive to fishes. Defensive symbioses are possibly quite common and important in marine environments but largely unrecognized.

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• Sponge impacts on coral reefs

Sponges (Fig. C) are another group of marine invertebrates that can host abundant communities of microbes (TEM inset) known to produce some of the bioactive secondary metabolites isolated from sponges and to possibly mediate important N transformations, such N2 fixation. Sponges may substantially influence levels and speciation of N in reef water because of their great abundance and unparalleled ability to filter seawater. In situ measurements of sponge pumping rates by video techniques and with ADVs (with Jim Hench, Fig. D) found some species filtering up to 50,000 L of seawater per L of tissue per d. Sponge abundance on Caribbean reefs has likely been increasing as important spongviores, such as turtles and urchins, have been decimated by overfishing and disease, respectively. Sponges can harm reef corals through direct contact, by the release of allelochemicals and possibly indirectly, for example, by remineralization of PON/DON to DIN that stimulates the growth of macroalgae and coral pathogens. Studies with Martens (UNC), Hench (Stanford) and Hentchel (U. Würzburg) are focused on: (i) the flux of nutrients, oxygen, and bioactive metabolites from sponges; (ii) the breadth of N conversion mediated by sponges and associated microbes, (iii) identifying microbes involved in important N transformations, and (iv) coral-sponge-urchin interactions.

• Larval dispersal and life history evolution

Long-distance larval dispersal vs. philopatry (i.e., remaining near the maternal adult) is an important life-history dichotomy that has substantial implications for levels of genetic exchange among populations. Thus, a better understanding of the factors affecting life-history evolution among marine species has utility for developing management and conservation strategies. Numerous hypotheses have been proposed regarding the selective forces, trade-offs, and constraints leading to the evolution of these different reproductive/dispersal strategies and their suites of associated traits. Research by the Lindquist group has shown that unpalatable secondary metabolites effectively protect larvae of diverse taxa of sessile marine invertebrates against predators. Regardless of their taxonomic affiliation (from sponges to tunicates), chemically defended larvae exhibit a combination of traits suggesting that their risk of predation is low: large size, bright coloration, daytime spawning, vulnerable morphology, and virtually no ability to elude predators. Further, chemically defended larvae tend to occur among brooding species and settle only minutes to hours after their release, although their large size would suggest they have energy reserves sufficient for a lengthy planktonic existence. Because their predation risk has been minimized, chemically defended larvae likely exhibit traits not associated with predator avoidance but that have a distinct selective advantage at other life stages. As examples, (i) large larvae become large juveniles and size is directly correlated with survival; (ii) daytime spawning allows chemically defended larvae to use strong photic cues to direct their settlement to refuges against grazers and UV exposure, typically shaded cracks and crevices in the substrate; and (iii) quick larval settlement places juvenile in a habitat that proved favorable for growth and reproduction.

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