Chemical defense in a marine alga: heritability and the potential for selection by herbivores

Herbivores have major impacts on many marine algae and are assumed to have been important forces driving the evolution of algal chemical defenses. However, an evolutionary change in chemical defenses in response to herbivory requires that there is both heritable variation for that trait and a response by herbivores to such variation. The subtidal red alga Delisea pulchra produces four main secondary metabolites (furanones) that vary in concentration at a variety of spatial and temporal scales. Here we determined the heritability of furanone concentrations and then, with a series of feeding experiments, determined how feeding by herbivores associated with D. pulchra varied as a function of nonpolar extract and furanone concentration. Total furanone concentration showed significant broad-sense heritability (hC 2 = 0.234), but broad-sense heritability of the four individual furanones varied in magnitude, ranging from 0.058 to 0.321. Compound 3, which is often the most abundant furanone, was the only one of the four furanones to show significant genetic variation. However, all four furanones were strongly genetically correlated, indicating that selection acting on any one of them will cause a corresponding change in the others. With the exception of the mesograzer gastropod Phasianotrochus eximius, herbivores generally consumed D. pulchra at lower rates compared to other common macroalgae. Macrograzers (sea urchins and large gastropods) were mostly deterred by nonpolar extract that contained levels of furanones that spanned the range of furanone variation in the field. The amphipod Ampithoe ngana was not deterred at the lowest extract concentration, and P. eximius was not deterred by any naturally occurring extract concentration. Compound 3 was deterrent to macrograzers at 3 and 5 mg/g dry mass, but was not deterrent at 1 mg/ g dry mass. Compound 3 was also not deterrent to A. ngana at any of those concentrations. For the most part D. pulchra in the field contains concentrations of furanones that are strongly deterrent to most herbivores. However, at some places and times, furanones do occur at lower concentrations that are not deterrent to herbivores. Given the heritable variation for furanones, when this overlap occurs there is the potential for selection by herbivores for higher concentrations of furanones in D. pulchra.