Monarchs in the Classroom

Liz Goehring & Karen Oberhauser
University Scientist
University of Minnesota
St. Paul MN

Insect Diapause

Organisms living in temperate regions face seasonal challenges, such as absence of food, harsh winter conditions, and the need to synchronize reproduction with suitable conditions for breeding. Insect adaptations to these challenges include migration, dormancy, and seasonal phenotypic variation; various combinations of these traits constitute a diapause syndrome (Andrewartha 1952; Tauber et al. 1986; Danks 1987; Leather et al. 1993). Diapause is a state of arrested development, characterized by low metabolic activity, reduced motor activity and increased resistance to environmental extremes, and is usually hormonally controlled in insects (Nijhout 1994). Diapause can occur during any insect life stage; reproductive diapause refers to delayed reproductive development in the adult stage.

The course of diapause includes changes in the insect's physiology and sensitivity to environmental stimuli against a backdrop of seasonal changes. Diapause induction occurs along a spectrum ranging from complete control by external factors to complete control by genetic factors (Tauber et al., 1986). External stimuli that induce diapause almost always precede adverse conditions, and include both abiotic and biotic factors (reviews by Tauber et al., 1986; Leather et al., 1993). After the onset of diapause, there is typically a period of intensification followed by maintenance and eventual termination. These steps are referred to as diapause development (Tauber et al. 1986). Diapause development may end via multiple pathways, following a predetermined course not influenced by external cues or terminating in response to external stimuli. Hodek (1983) refers to these pathways as "horotelic" (Greek: hora = right time, telos = fulfilment) and "tachytelic" (Greek: tachys = quick) respectively. These pathways may operate singly or together. The rate of diapause development is often driven by temperature, but other stimuli include photoperiod, food, moisture, parasitoid / host interactions and mating (reviewed in Tauber et al. 1986; Danks 1987).

Once reproductive diapause development is complete, insects are capable of reproduction and characteristics of diapause such as reduced metabolism and cold-hardiness disappear. If the prevailing environmental conditions are not suitable for reproduction, the insect may remain dormant, in a postdiapause “quiescence” (Tauber et al. 1986).

Monarch diapause

The monarch butterfly is a tropical species that has expanded its range into temperate regions, taking advantage of the distribution of its host plant genus, Asclepias (Brower, 1985; Masters et al., 1988). Not adapted to survive temperature extremes of their expanded North American range, monarchs undergo long-distance migration each autumn (Urquhart & Urquhart, 1978) and delay reproduction until the following spring, entering a state of reproductive diapause with minimal reproductive tract development (Herman, 1973; Brower et al., 1977; Herman et al., 1989). Eastern and western North American monarchs migrate to overwintering sites in central Mexico and California respectively, where they remain until adults migrate north. The eastern population exhibits a refractory period during which butterflies do not undergo gonadal development in response to 10 days of summer-like conditions (25 °C and 16 h photophase), while this refractory period is either shorter or non-existent in the western population (Herman et al., 1989). Monarchs in Australia also diapause to a lesser degree (James, 1993). Monarch ovarian dormancy in Australia (and possibly California) is classified more accurately as oligopause, an intermediate condition that lacks the refractory period associated with diapause (James, 1982). This dormancy can be induced by exposure to cool temperatures after adult eclosion, and is associated with longer flight distances than seen in adults exposed to warm post-eclosion temperatures (James, 1983).

The neurohormonal control of eastern North American monarch diapause has been elucidated (Barker & Herman, 1973; Herman, 1975, 1981, 1985), and photoperiod and temperature have been shown to influence reproductive development in post-eclosion monarchs (Barker & Herman, 1976). Barker and Herman identified only optimal and inhibitory conditions, however, and their results did not allow distinction between diapause per se and the slow development of reproductive organs under cool conditions.

References

Andrewartha, H.C. (1952) Diapause in relation to the ecology of insects. Biological Review, 27, 50-107.

Barker, J.F. & Herman, W.S. (1973) On the neuroendocrine control of ovarian development in the monarch butterfly. Journal of Experimental Zoology, 183, 1-10.

Barker, J.F. & Herman, W.S. (1976) Effect of photoperiod and temperature on reproduction of the monarch butterfly, Danaus plexippus. Journal of Insect Physiology, 22, 1565-1568.

Brower, L.P. (1985) New perspectives on the migration biology of the Monarch butterfly, Danaus plexippus L. Migration: Mechanisms and Adaptive Significance (ed. by M. A. Rankin), pp. 748-785. University of Texas Marine Institute Contributions to Marine Science, 27 (Supplement),Austin, U.S.A.

Brower, L.P., Calvert, W.H., Hendrick, L.E. & Christian, J. (1977) Biological observations of an overwintering colony of monarch butterflies (Danaus plexippus, Danaidae) in Mexico.Journal of the Lepidopterists' Society, 31, 232-242.

Danks, H.V. (1987) Insect Dormancy: an Ecological Perspective. Entomological Society of

Canada, Ottawa.

Herman, W.S. (1973) The endocrine basis of reproductive inactivity in monarch butterflies overwintering in central California. Journal of Insect Physiology, 19, 1883-1887.

Herman, W.S. (1975) Endocrine regulation of posteclosion enlargement of the male and female reproductive glands in monarch butterflies. General and Comparative Endocrinology, 26, 534-540.

Herman, W.S. (1981) Studies on the adult reproductive diapause of the monarch butterfly, Danaus plexippus. Biological Bulletin, 160, 89-106.

Herman, W.S. (1985) Hormonally mediated events in adult monarch butterflies. Migration: Mechanisms and Adaptive Significance (ed. by M. A. Rankin), pp. 799-815. University of Texas Marine Institute Contributions to Marine Science, 27 (Supplement), Austin, U.S.A.

Herman, W.S., Brower, L.P. & Calvert, W.H. (1989). Reproductive tract development in monarch butterflies overwintering in California and Mexico. Journal of the Lepidopterists' Society, 43, 50-58.

Hodek, I. 1983. Role of environmental factors and endogenous mechanisms in the seasonality of reproduction in insects diapausing as adults. In K. V. Brown and I. Hodek, eds.), Diapause and life cycle strategies in insects. pp. 9-33. Dr W. Junk Publishers, The Hague

James, D.G. (1982) Ovarian dormancy in Danaus plexippus (L.) (Lepidoptera Nymphalidae) - oligopause not diapause. Journal of the Australian Entomological Society, 21, 31-35.

James, D.G. (1983) Induction of reproductive dormancy in Australian monarch butterflies, Danaus plexippus (L.). Australian Journal of Zoology, 31, 491-498.

James, D.G. (1993) Migration biology of the Monarch butterfly in Australia. Biology and Conservation of the Monarch Butterfly (ed. by S .B. Malcolm and M .P. Zalucki), pp.189-200.

Natural History Museum of Los Angeles County, Los Angeles, California.

Leather, S.R., Walters, K.F.A. & Bale, J.S. (1993) The Ecology of Insect Overwintering. University Press, Cambridge.

Masters, A.R., Malcolm, S.B. & Brower, L.P. (1988) Monarch butterfly (Danaus plexippus) thermoregulatory behavior and adaptations for overwintering in Mexico. Ecology, 69, 458-467.

Nijhout, H.F. (1994) Insect Hormones.

Princeton University Press, Princeton, New Jersey.

Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. Oxford University Press,New York.

Urquhart, F.A. & Urquhart, N.R. (1978) Autumnal migration routes of the eastern population of the monarch butterfly (Danaus p. plexippus L.; Danaidae; Lepidoptera) in North America to the overwintering site in the Neovolcanic Plateau of Mexico. Canadian Journal of Zoology, 56, 1759-1764.