IPBRG Investigators: Spence Behmer, Xiangfeng Jing

Collaborators: Patrick Abbot (Vanderbilt University), Angela Douglas (Cornell University),
                         Bob Grebenok (Canisius College)

Sterols serve three critical functions in insects: (1) they are important components of cellular membranes, (2) they are precursors for many hormones (e.g. 20-OH ecdysone) and (3) they play a role in regulating genes involved in developmental processes. Insects, however, differ from most other animals in that they have a dietary requirement for sterols because they lack the ability to biosynthesise sterols. Cholesterol (right) is the dominant sterol found in most insects, but since plants rarely contain it, insect herbivores must either metabolise plant sterols or use them as they are. Cholesterol is characterized by a double bond at position 5, and no alkyl group on the side chain.

At least 100 different sterols have been identified in plants (e.g. sitosterol, stigmasterol and spinasterol - see below), but metabolic constraints in insects can limit the range of phytosterols that can be converted to cholesterol. I am interested in how small structural differences can influence insect behaviour and physiology, including utilisation and metabolism, and the manner in which these subtle differences can influence evolutionary processes.

Variation in Plant Sterol Structure. Sitosterol is the most abundant and common plant sterol. It has a double bond at position 5 (similar to cholesterol), but like most plant sterols it has an alkyl group (green structure) on the side chain. Stigmasterol is another relatively common plant sterol. In contrast to sitosterol, it has a double bond at position 22 on the side chain. Spinasterol, a plant sterol found in spinach, also has a double bond at position 22, but differs from sitosterol and stigmasterol by having a double bond at position 7 in the sterol nucleus. From a grasshoppers point of view, sitosterol is a "good" sterol since it can be metabolised to cholesterol. On the other hand, stigmasterol and spinasterol are considered "bad" sterols since they cannot be metabolised to cholesterol (for more details, see Behmer et al. 1999b).

So far most of the research into insect sterol biology has been conducted on grasshoppers, and in these insects we find that extreme sterol metabolic constraints are a shared trait (Behmer and Elias 2000). Particularly fascinating, though, is that grasshoppers suffer high levels of mortality when they accumulate unmetabolized "bad" sterols above a certain threshold, even if the proper amount of a "good" sterol is obtained (Behmer and Elias 1999a, 2000). It remains unknown, however, whether this is due to interruption of cell structural features or an inability to make the important cholesterol-derived steroid hormones.

Grasshoppers cannot directly taste sterols, but they can still regulate the intake of bad sterols by associating, post-ingestively, the presence of unsuitable sterols with the taste of the food that contains them (Behmer and Elias 1999b, Behmer et al. 1999a). This learned association develops quickly, usually after a meal or two, and we have proposed that constraints on sterol use, combined with aversion learning responses, may partially explain patterns of food use in insect herbivores, especially highly mobile generalists (Behmer and Elias 2000).

Sterol metabolic constraints can also have consequences on population dynamics. In a multiple generation study using a small specialist caterpillar (Plutella xylostella), strong negative cumulative effects on development, fecundity and population growth were observed when this caterpillar was reared on diets containing unfamiliar sterols (Behmer and Grebenok 1998). This result suggests that modifying plant sterol profiles might provide a novel and effective way to control economically important pest species. However, this same study also found that variation in sterol metabolic capacity can exist within populations, which begs the question of whether, and to what extent, lability in sterol metabolic capacity can evolve.

We are currently looking at sterol use in a range of pest caterpillars, both on artificial diets with different sterol combinations, and on transgenically modified tobacco plants. This work is part of Xiangfeng Jing's Ph.D. research, and it is being funded by a grant from the USDA.

Key Publications:

Behmer, S.T. and Nes, W. D. (2003) Insect sterol nutrition and physiology: a global
     overview. Advances in Insect Physiology 31, 1-72. [pdf]

Behmer, S.T. and Elias, D.O. (2000) Sterol metabolic constraints as a factor contributing
     to the maintenance of diet mixing in grasshoppers (Orthoptera: Acrididae). Physiological
     and Biochemical Zoology 73, 219-230. [pdf]

Behmer, S.T., Elias, D.O. and Bernays, E.A. (1999a) Post-ingestive feedbacks and
     associative learning regulate the intake of unsuitable sterols in a generalist
     grasshopper. Journal of Experimental Biology 202, 739-748. [pdf]

Behmer, S.T., Elias, D.O. and Grebenok, R.J. (1999b) Phytosterol metabolism and
     absorption in the generalist grasshopper Schistocerca americana (Orthoptera: Acrididae).
     Archives of Insect Biochemistry and Physiology 42, 13-25. [pdf]

Behmer, S.T. and Elias, D.O. (1999a) The nutritional significance of sterol metabolic
     constraints in the generalist grasshopper Schistocerca americana. Journal of Insect
     Physiology 45, 339-348. [pdf]

Behmer, S.T. and Elias, D.O. (1999b) Phytosterol structure as a basis of food aversion
     learning in the grasshopper Schistocerca americana (Orthoptera: Acrididae).
     Physiological Entomology 24, 18-27. [pdf]

Behmer, S.T. and Grebenok, R.J. (1998) Impact of dietary sterols on life-history traits of
     a caterpillar. Physiological Entomology 23, 165-175. [pdf]