Chemical Signaling in Ecology and Evolution

 

I am generally interested in the chemical ecology of aquatic organisms, including the chemical basis for habitat choice by larvae, sperm navigation, foraging by scavengers, and defense from predation. Currently, we are performing comparative tests of how algal chemical defenses have influenced diversification of consumers using a molecular phylogeny of the Sacoglossa. Other on-going studies explore the chemical ecology of defense in the sea slug genus Alderia, and coevolution of secondary metabolites and photosynthesis.

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Habitat Choice in the Sea: Chemical Settlement Cues

 

Most marine invertebrates spend their adult life on the sea floor. Dispersal, which permits gene flow between populations, is accomplished by tiny larvae that spend anywhere from minutes to months in the plankton. Eventually, larvae face the challenge of locating a suitable adult habitat before settling to the bottom. Finding a good area is critical for species that depend on one host or prey species; if the adult host is not found soon after the larva completes its metamorphosis, the juvenile will starve. We have studied how chemical cues mediate settlement in laboratory and field experiments. Research focused on larvae of the sea slug Alderia willowi, which settle in response to carbohydrates produced by the adult host alga Vaucheria. This work employed chemical techniques such as NMR and GC/MS to characterize bioactive oligosaccharides, and video motion analysis to quantify changes in larval swimming and settlement behavior in response to dissolved cues of habitat suitability. More recent work showed that the NO signalling pathway underlies the initial decision to metamorphose without habitat cues, or the subsequent sensitivity to cues in larvae that delay settlement.

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Romero*, M.R., Phuong*, M., Bishop, C.D., and P.J. Krug. 2013. Differential function of nitric oxide signaling during habitat choice by two larval morphs of the sea slug Alderia willowi: mechanistic insight into evolutionary transitions in dispersal strategies. Journal of Experimental Biology, 216: 1114-1125.

(doi: 10.1242/jeb.080747) PDF

 

Botello*, G. and P.J. Krug. 2006. Desperate larvae revisited: Age, energy and experience affect sensitivity to settlement cues in larvae of the gastropod Alderia sp. Marine Ecology Progress Series 312: 149-159. PDF

 

Krug, P.J. 2006. “Defense of benthic invertebrates against surface colonization by larvae: A chemical arms race.”  Pp. 1-53 in: Clare A. and Fusetani N. (eds) Marine Molecular Biotechnology, vol 2. Springer, Berlin. PDF

 

Krug, P.J. and R.K. Zimmer. 2004. Developmental dimorphism: Consequences for larval behavior and dispersal potential in a marine gastropod.  Biological Bulletin 207: 233-246. PDF

 

Krug, P.J.  2001.  Bet-hedging dispersal strategy of a specialist marine herbivore: A settlement dimorphism among sibling larvae of Alderia modesta.  Marine Ecology Progress Series 213: 177-192. PDF

 

Krug, P.J. and R.K. Zimmer. 2000. Developmental dimorphism and expression of chemosensory-mediated behavior: Habitat selection by a specialist marine herbivore. Journal of Experimental Biology 203: 1741-1754. PDF

 

Krug, P.J. and R.K. Zimmer. 2000. Larval settlement: chemical markers for tracing production, transport, and distribution of a waterborne cue. Marine Ecology Progress Series 207: 283-296. PDF

 

Krug, P.J., and A.E. Manzi,  1999.  Waterborne and surface-associated carbohydrates as settlement cues for larvae of the specialist marine herbivore Alderia modesta.  Biological Bulletin 197: 94-103. PDF

 

Sperm navigation: sex and the single cell

 

From coral reefs to human beings, chemical communication between eggs and sperm plays a critical role in reproduction. Sperm cells can orient and accelerate towards an egg by tracking diffusing signal molecules, thereby enhancing fertilization success. This is especially important for broadcast-spawning organisms that shed their gametes into the sea, where they are rapidly diluted in the surrounding seawater. Species-specific sperm attractants may also function as pre-zygotic agents driving reproductive isolation and speciation, by allowing sperm to faithfully distinguish eggs of their own from related species. 

 

We identified the amino acid L-tryptophan as the sperm attractant from eggs of red abalone, a commercially valuable but endangered resource. Although such chemical signals might maintain species boundaries in these free-spawning animals, evidence indicates that soluble signals are less evolutionarily important that are rapidly evolving gamete recognition proteins. Ecologically, this work has implications for conservation, as low population densities of abalone may prevent appreciable fertilization from occurring due to gamete dilution. Improved understanding of chemical and biological mechanisms affecting reproductive success may thus aid management and restoration efforts for threatened species.

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Krug, P.J., Riffell, J., and R.K. Zimmer. 2009. Endogenous signaling pathways and chemical communication between sperm and egg. Journal of Experimental Biology, 212: 1092-1100. PDF

 

Riffell, J., Krug, P.J., and R.K. Zimmer. 2004. The ecological and evolutionary consequences of sperm chemoattraction.  Proceedings of the National Academy of Sciences USA 101: 4501-4506. PDF

 

Riffell, J., Krug, P.J., and R.K. Zimmer. 2002. Fertilization in the sea: The chemical identity of an abalone sperm attractant. Journal of Experimental Biology 205: 1439-1450. [Cover article] PDF

 

Predator-prey interactions

 

For predators and their prey, chemistry is a double-edged sword. Chemical plumes allow predators to track their prey, and help scavengers locate fresh foodfalls. On the other hand, vulnerable prey organisms can exploit chemistry to avoid being eaten. Many aquatic animals produce defensive structures upon sensing predators in the area. Seemingly vulnerable taxa like sea slugs and sponges can produce or acquire powerful toxins to deter would-be predators. 

 

Other projects have measured the natural flux of metabolites from live and dead prey organisms, to identify cues that trigger foraging behavior and aid navigation in predators and scavengers. To understand the attraction of isopods, common marine scavengers, we quantified the flux of amino acids and peptides from naturally aged prey flesh. Field studies are currently measuring the attraction of isopods to synthetic odor plumes that mimic the release of foraging cues. Another collaborative project with researchers at UCLA examines how newt larvae avoid being cannibalized by hungry adults, by recognizing adult defensive toxins and seeking refuge. These studies will provide new insights into the evolution of predator-prey interactions, and will further our understanding of sensory systems in important model organisms.

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Zimmer, R.K., Schar, D., Ferrer, R., Krug, P.J., Katz, L., and W. Michel. 2006. The scent of danger: Tetrodotoxin (TTX) as an olfactory cue of predation risk. Ecological Monographs 76: 585-600. PDF

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Krug, P.J., Boyd, K.G., and Faulkner, D.J. 1995. Isolation and synthesis of Tanyolides A and B, metabolites of the nudibranch Sclerodoris tanya. Tetrahedron 51: 11063-11074. PDF