Newsletter of the Biological Survey of Canada (Terrestrial Arthropods)

Canadian Perspectives: The Study of Insect Dormancies and Life Cycles

H.V. Danks
Biological Survey of Canada (Terrestrial Arthropods), Canadian Museum of Nature, P.O. Box 3443, Station D, Ottawa, ON K1P 6P4

Adaptations of insects in terms of life-cycle patterns and how these are controlled are especially striking and significant in northern countries such as Canada.

Dormancies are one of the key adaptations of insects to seasonal events and have attracted a great deal of study. But dormancies are only one component in the timing of insect life cycles, and recent syntheses suggest that a wider view of how life cycles evolve and are controlled is desirable. This perspective, explained in more detail by Danks (1987, 1991, 1992, 1993, 1994a, b, 1999b, 2001, 2002) is summarized here. A very similar summary in French is available in Danks (1999a).

Dormancies
There are two main kinds of dormancy, quiescence and diapause. During quiescence, development stops due to currently adverse conditions such as low temperatures. During diapause, morphological development is suppressed through a form of central control and not simply by the direct action of environmental factors. Many of the complexities of insect life cycles stem from forms of diapause. However, attempts to classify diapause into discrete categories are unsatisfactory, because the developmental programmes of different species represent a continuum of adaptations to a variety of circumstances, and so are extraordinarily diverse.

Control of development
Some factors act directly as simple regulators. For example, temperature plays this role in normal circumstances, because metabolism and hence development is typically faster at higher temperatures within the usual range. Development may also be controlled by cues or environmental tokens that act indirectly rather than as regulators. For example, the diapause of many species is influenced by photoperiod. In addition, some life-cycle stages respond to short-term stimuli, such as the specific conditions that prompt hatching of the eggs of mosquitoes and other species.

The life cycles of a few species are controlled entirely by direct effects, especially in sheltered habitats where conditions change regularly and predictably. However, patterns of development of most species include control by cues. Even when cues exert a dominant influence on how the life cycle is controlled, dormancy is only one element of the control, because growth rates and other elements are involved. For example, photoperiod and crowding can modify growth as well as development by their indirect action. Table 1 shows the wide range of environmental factors that have so far been reported to influence diapause and growth rate.

Table 1. Synopsis of environmental factors influencing seasonal development in insects (from Danks 1994a). + acts indirectly, as a cue or seasonal token; x acts directly, as a regulator; * can act either indirectly or directly.

Life-cycle pathways
Viewing the life cycle as a series of alternative pathways (for several examples see Danks 1987, 1991, 1994a) helps to visualize the effects of all of these possible influences. The alternatives are chosen during the development of each individual by a variety of internal (genetically programmed) mechanisms linked with various external or environmental controls.

The complexity of such pathways suggests that insect life cycles should be analysed not by static assessment of particular dormancies, but rather by means of flow charts that identify the options available to a given species and show how the individual elements are governed. Even complex life-cycle patterns can nonetheless be understood through concepts of ordinary development. Diapause and its completion are simply special forms of development, although sometimes they have long-term requirements for particular levels of environmental conditions or for changes in those conditions. Concepts such as regulation (continuous control of rates), switches (choices among set alternatives), gates (limits), potentiation (on-off switches) and successive requirements (a given stage must be reached before a subsequent development is feasible) apply to both dormant and non-dormant developmental pathways.

By examining life-cycle pathways in this way, entomologists can identify key decision points that govern the flow of the life cycle of a given species. Phenological variations among individuals and years, and other factors, can then be understood. Without such an approach, many entomologists will instead continue to monitor the incidence of diapause at a few temperatures and a few photoperiods, or to classify diapause into arbitrary types. Such procedures contribute little to our understanding of life cycles in nature because for most species they seriously underestimate environmental and genetic complexity

Levels of complexity
Different species have life cycles of different complexity, of course. More complex control systems typically generate more precise developmental responses or allow for adaptive flexibility and variability. Complex systems tend to include a large rather than a small number of dormant stages, multiple possible routes of development within a single dormant period rather than a single fixed pathway, a wider variety of environmental controls used to time the stages, and the control of growth as well as development by environmental cues. Many experiments on diapause have not been designed to take account of such possibilities.

Integration of responses
From a broad perspective, therefore, dormancy and other responses to the environment are integrated throughout the life cycle. The wide range of adaptations includes arrested, retarded or accelerated development, sensitivity and response to a wide range of environmental cues in almost any stage, and variation in the extent and duration of sensitivity. However, even a relatively small number of successive developmental choices can generate many different routes of development.

Trade-offs
Because resources of time, space and energy are finite, any species survives by maximizing fitness though multiple trade-offs between competing demands for the resources. For example, a given species is unlikely to be able to reach a very large size very quickly, because of constraints of food or physiology. It could complete the life cycle quickly but not at a huge size, or it could grow very large (and hence be able to deposit many eggs) but relatively slowly. Traits that depend on common elements tend to be correlated, and the developmental pathway may make certain trade-offs unfeasible.

Again, trade-offs must be integrated into the life cycle in a general sense, for example to achieve a balance between seasonal synchrony to take advantage of favourable times of year, flexibility to counter unexpected variations, and variability to buffer risk. Nevertheless, time, space and energy are not necessarily limiting in any particular situation. For example, there may be plenty of time for development to be completed before the end of the growing season. Consequently, identifying trade-offs (by modelling and other means) is complex, as for the life-cycle controls themselves. However, it provides another way to understand the structure of the life cycle.

Generalizations
Seasonal conditions vary very widely, so that different demands are placed on different species and on the same species in different places. A review of the many responses studied so far suggests generalizations such as the following.

Similar environmental challenges can be solved in many different ways. For example, species can avoid unsuitable conditions by moving between habitats or microhabitats, reducing the number of annual generations, modifying development, or switching foods.

Similar responses can evolve independently in different species. Parallel adaptations are very common. For example, winter diapause of many temperate species is induced by short photoperiods and low temperatures, and ended by exposure to cold.

Responses evolve in combination. Organisms survive all conditions and selective pressures simultaneously, so that responses are assembled in sets and not separately.

A single response may contribute to many functions in one species. For example, slower growth may help to increase survival when food is limited, permit ambiguous environmental signals to be monitored for a longer period, delay entry into the diapause stage and so reduce summer mortality of dormant individuals, allow additional food to be stored, and so on.

The same response may serve different functions in different species. For example, large egg size can reduce the duration of subsequent larval development, or resist adverse conditions better, or enhance larval survival, depending on the species.

Trade-offs between potentially interdependent traits are not inevitable. For example, resources may not be limiting in some circumstances, and priority needs such as individual survival are met first.

These generalizations confirm the diversity and complexity of the responses as well as their close integration.

Future work
The evolution of dormancies and other life-cycle components is governed largely by the range and predictability of seasonal conditions. Therefore, in order to understand life cycles, we need to assess habitat conditions and their variability in detail at the same time as the biological responses. Insights into life-cycle evolution are possible too by analysing potential selective forces related to the supply of time, space and energy, because life cycles integrate the use of available resources.

In other words, life cycles respond to broad forces and integrate many factors. Consequently, information from additional elementary experiments on diapause, or yet other examples of already well known responses to particular individual factors, will not be very helpful. Rather, multifaceted studies of insect life cycles as a whole are called for. A wide range of investigations should evaluate the ecological setting and combined responses of well characterized species from well characterized environments. Studying numerous life-cycle elements simultaneously in this way is most likely to reveal the principles underlying the evolution and control of life cycles and of their dormancy components.

References
Danks, H.V. 1987. Insect dormancy: an ecological perspective. Biological Survey of Canada (Terrestrial Arthropods), Ottawa. 439 pp.

Danks, H.V. 1991. Life-cycle pathways and the analysis of complex life cycles in insects. Can. Ent. 123: 23-40.

Danks, H.V. 1992. Long life cycles in insects. Can. Ent. 124: 167-187.

Danks, H.V. 1993. [Seasonal adaptations in insects from the high arctic.] pp. 54-66 in M. Takeda and S. Tanaka (Eds.), [Seasonal adaptation and diapause in insects]. Bun-ichi-Sogo Publ., Ltd., Tokyo. (In Japanese).

Danks, H.V. 1994a. Diversity and integration of life-cycle controls in insects. pp. 5-40 in H.V. Danks (Ed.), Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Kluwer Academic Publishers, Dordrecht.

Danks, H.V. 1994b. Insect life-cycle polymorphism: current ideas and future prospects. pp. 349-365 in H.V. Danks (Ed.), Insect life-cycle polymorphism: theory, evolution and ecological consequences for seasonality and diapause control. Kluwer Academic Publishers, Dordrecht.

Danks, H.V. 1999a. La dormance et les cycles biologiques. Antennae 6 (2): 5-8.

Danks, H.V. 1999b. The diversity and evolution of insect life cycles. Ent. Sci. 2: 651-660.

Danks, H.V. 2001. The nature of dormancy responses in insects. Acta Societatis Zoologicae Bohemicae 65 (3): 169-179.

Danks, H.V. 2002. The range of insect dormancy responses. Eur. J. Ent. 99: in press.