Risk-spreading and bet-hedging in insect population biology.

In evolutionary ecology, risk-spreading (i.e. bet-hedging) is the idea that unpredictably variable environments favor genotypes with lower variance in fitness at the cost of lower arithmetic mean fitness. Variance in fitness can be reduced by physiology or behavior that spreads risk of encountering an unfavorable environment over time or space. Such risk-spreading can be achieved by a single phenotype that avoids risks (conservative risk-spreading) or by phenotypic variation expressed by a single genotype (diversified risk-spreading). Across these categories, three types of risk-spreading can be usefully distinguished: temporal, metapopulation, and within-generation. Theory suggests that temporal and metapopulation risk-spreading may work under a broad range of population sizes, but within-generation risk-spreading appears to work only when populations are small. Although genetic polymorphisms have sometimes been treated as risk-spreading, the underlying mechanisms are different, and they often require different conditions for their evolution and thus are better treated separately. I review the types of evidence that could be used to test for risk-spreading and discuss evidence for risk-spreading in facultative diapause, migration polyphenism, spatial distribution of oviposition, egg size, and other miscellaneous traits. Although risk-spreading theory is voluminous and well developed in some ways, rarely has it been used to generate detailed, testable hypotheses about the evolution of risk-spreading. Furthermore, although there is evidence for risk-spreading, particularly in facultative diapause, I have been unable to find any definitive tests with unequivocal results showing that risk-spreading has been a major factor in the evolution of insect behaviors or life histories. To advance our understanding of risk-spreading in the wild, we need (a) explicit empirical models that predict levels of diversifying risk-spreading for several insect populations in several environments that vary in uncertainty, and (b) tests of these models using measurements of phenotypes and their fitnesses over several generations in each environment.

[1]  P. Kareiva,et al.  Is risk-spreading so unrealistic? , 1986 .

[2]  D. Roff,et al.  Quantitative genetics of the trade-off between fecundity and wing dimorphism in the cricket Allonemobius socius , 1996, Heredity.

[3]  P. J. Boer.  The survival value of dispersal in terrestrial arthropods , 1990 .

[4]  R. Bigelow.  INTERSPECIFIC HYBRIDS AND SPECIATION IN THE GENUS ACHETA (ORTHOPTERA, GRYLLIDAE) , 1960 .

[5]  R. Levins.  Evolution in Changing Environments: Some Theoretical Explorations. (MPB-2) , 1968 .

[6]  D. Janzen.  What Are Dandelions and Aphids? , 1977, The American Naturalist.

[7]  D. Moss,et al.  Spatial synchrony and asynchrony in butterfly population dynamics , 1996 .

[8]  D. Roff.  Habitat Persistence and the Evolution of Wing Dimorphism in Insects , 1994, The American Naturalist.

[9]  H. Dingle,et al.  VARIATION IN BODY SIZE AND FLIGHT PERFORMANCE IN MILKWEED BUGS (ONCOPELTUS) , 1980, Evolution; international journal of organic evolution.

[10]  J. Cronin,et al.  SUBSTANTIALLY SUBMAXIMAL OVIPOSITION RATES BY A MYMARID EGG PARASITOID IN THE LABORATORY AND FIELD , 1993 .

[11]  R. Levins.  Some Demographic and Genetic Consequences of Environmental Heterogeneity for Biological Control , 1969 .

[12]  D. Roff,et al.  Bet hedging and the diapause strategies of the cricket Allonemobius fasciatus , 1993 .

[13]  S. Tanaka.  The Significance of Embryonic Diapause in a Japanese Strain of the Migratory Locust, Locusta migratoria (Orthoptera, Acrididae) , 1992 .

[14]  D. Goodman.  Risk spreading as an adaptive strategy in iteroparous life histories. , 1984, Theoretical population biology.

[15]  J. Endler.  Natural selection in the wild , 1987 .

[16]  A. G. Gatehouse.  Behavior and ecological genetics of wind-borne migration by insects. , 1997, Annual review of entomology.

[17]  F. Taylor,et al.  Geographical Patterns in the Photoperiodic Induction of Hibernal Diapause , 1986 .

[18]  Andrew P. Martin,et al.  Temporal Variation in Insect Life Cycles , 1990 .

[19]  T. Mittler,et al.  Biotypes and Clonal Variation in Greenbug (Homoptera: Aphididae) Populations from a Locality in California , 1991 .

[20]  P. J. Boer,et al.  Spreading of risk and stabilization of animal numbers , 1968 .

[21]  Alan Hastings,et al.  Dispersal strategies in patchy environments , 1984 .

[22]  S. Stearns.  Life-History Tactics: A Review of the Ideas , 1976, The Quarterly Review of Biology.

[23]  R. R. Strathmann.  The Spread of Sibling Larvae of Sedentary Marine Invertebrates , 1974, The American Naturalist.

[24]  A. Hastings,et al.  Metapopulation Dynamics and Genetics , 1994 .

[25]  W. S. Cooper,et al.  The Evolution of Developmental Plasticity in Reproductive Characteristics: An Application of the "Adaptive Coin-Flipping" Principle , 1984, The American Naturalist.

[26]  J. Gillespie.  Natural selection for within-generation variance in offspring number II. Discrite haploid models. , 1975, Genetics.

[27]  S. Courtney.  Why insects move between host patches: some comments on risk-spreading , 1986 .

[28]  Peter Chesson,et al.  Coexistence of Competitors in Spatially and Temporally Varying Environments: A Look at the Combined Effects of Different Sorts of Variability , 1985 .

[29]  Peter Kareiva,et al.  THE SEARCH FOR RESOURCES BY CABBAGE BUTTERFLIES (PIERIS RAPAE): ECOLOGICAL CONSEQUENCES AND ADAPTIVE SIGNIFICANCE OF MARKOVIAN MOVEMENTS IN A PATCHY ENVIRONMENT' , 1984 .

[30]  T. Philippi,et al.  Hedging one's evolutionary bets, revisited. , 1989, Trends in ecology & evolution.

[31]  J. Gillespie.  The Role of Migration in the Genetic Structure of Populations in Temporally and Spatially Varying Environments. III. Migration Modification , 1981, The American Naturalist.

[32]  R. Dennis Cook,et al.  The Statistics of Natural Selection. , 1987 .

[33]  J H Gillespie,et al.  Nautural selection for within-generation variance in offspring number. , 1974, Genetics.

[34]  K. Vepsäläinen.  Wing Dimorphism and Diapause in Gerris : Determination and Adaptive Significance , 1978 .

[35]  D. Roff,et al.  ADAPTATION TO SEASONALITY IN A CRICKET: PATTERNS OF PHENOTYPIC AND GENOTYPIC VARIATION IN BODY SIZE AND DIAPAUSE EXPRESSION ALONG A CLINE IN SEASON LENGTH , 1989, Evolution; international journal of organic evolution.

[36]  F. Taylor.  The fitness functions associated with diapause induction in arthropods I. The effects of age structure , 1986 .

[37]  T. Southwood.  MIGRATION OF TERRESTRIAL ARTHROPODS IN RELATION TO HABITAT , 1962 .

[38]  Pierre-Henri Gouyon,et al.  Metapopulation Genetics and the Evolution of Dispersal , 1995, The American Naturalist.

[39]  S. Wratten.  Reproductive strategy of winged and wingless morphs of the aphids Sitobion avenae and Metopolophium dirhodum. , 1977, The Annals of applied biology.

[40]  M. Mangel,et al.  Patch‐leaving rules for parasitoids with imperfect host discrimination , 1994 .

[41]  J. R. Bradley,et al.  Geographic and Genetic Variation in Time Required for Emergence of Diapausing Heliothis zea1,2,3,4 , 1976 .

[42]  F. Taylor.  Diapause induction in changing photoperiods , 1989 .

[43]  Leslie A. Real,et al.  Fitness, Uncertainty, and the Role of Diversification in Evolution and Behavior , 1980, The American Naturalist.

[44]  H. G. Andrewartha,et al.  The distribution and abundance of animals. , 1954 .

[45]  R. Levins.  Theory of Fitness in a Heterogeneous Environment. I. The Fitness Set and Adaptive Function , 1962, The American Naturalist.

[46]  F. R. Groeters.  The adaptive role of facultative embryonic diapause in the grasshopper Caledia captiva (Orthoptera: Acrididae) in southeastern Australia , 1994 .

[47]  F. Taylor.  The fitness functions associated with diapause induction in arthropods ii. the effects of fecundity and survivorship on the optimum , 1986 .

[48]  J. Gillespie.  Natural Selection for Variances in Offspring Numbers: A New Evolutionary Principle , 1977, The American Naturalist.

[49]  J. Gillespie.  Natural selection with varying selection coefficients – a haploid model , 1973 .

[50]  M. Johnston,et al.  Developmental instability as a bet-hedging strategy , 1997 .

[51]  E. Charnov,et al.  Life-History Consequences of Natural Selection: Cole's Result Revisited , 1973, The American Naturalist.

[52]  J. Dempster.  7 – Fragmentation, Isolation and Mobility of Insect Populations , 1991 .

[53]  A. Dixon,et al.  Laboratory studies on aggregation, size and fecundity in the black bean aphid, Aphis fabae Scop. , 1971 .

[54]  R. J. Hoffman.  Environmental Uncertainty and Evolution of Physiological Adaptation in Colias Butterflies , 1978, The American Naturalist.

[55]  F. Taylor,et al.  Timing of diapause in relation to temporally variable catastrophes , 1989 .

[56]  R. Brandl,et al.  Metapopulation Dynamics of the Tephritid Fly Urophora cardui: An Evaluation of Incidence-Function Model Assumptions with Field Data , 1996 .

[57]  W. Bradshaw,et al.  Evolution of Phenology and Demography in the Pitcher-Plant Mosquito, Wyeomyia smithii , 1990 .

[58]  R. Denno,et al.  Density-Related Migration in Planthoppers (Homoptera: Delphacidae): The Role of Habitat Persistence , 1991, The American Naturalist.

[59]  M. Kimura,et al.  An introduction to population genetics theory , 1971 .

[60]  J. Cronin,et al.  Superparasitism and mutual interference in the egg parasitoid Anagrus delicatus (Hymenoptera: Mymaridae) , 1993 .

[61]  C. Pires,et al.  Mixed risk-spreading strategies and the population dynamics of a Brazilian pasture pest, Deois flavopicta (Homoptera: Cercopidae). , 1995 .

[62]  T. Caraco,et al.  RISK AND FORAGING IN STOCHASTIC ENVIRONMENTS , 1986 .

[63]  D. Cohen,et al.  Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. , 1967, Journal of theoretical biology.

[64]  O. Leimar,et al.  Metapopulation extinction and genetic variation in dispersal-related traits , 1997 .

[65]  L. Real,et al.  On the Tradeoff Between the Mean and the Variance in Foraging: Effect of Spatial Distribution and Color Preference , 1982 .

[66]  W. J. Bell,et al.  Seasonal adaptations of insects. , 1987 .

[67]  Daniel J. Cohen.  Optimization of Seasonal Migratory Behavior , 1967, The American Naturalist.

[68]  F. Taylor,et al.  Fitness Functions for Alternative Developmental Pathways in the Timing of Diapause Induction , 1988, The American Naturalist.

[69]  H. Dingle.  Migration: The Biology of Life on the Move , 1996 .

[70]  D. Tallamy,et al.  Alternative Life History Patterns in Risky Environments: An Example from Lacebugs , 1981 .

[71]  J. Ciborowski,et al.  Effects of emergence date and maternal size on egg development and sizes of eggs and first-instar nymphs of a semelparous aquatic insect , 1997, Oecologia.

[72]  H. Dingle.  Geographic Variation and Behavioral Flexibility in Milkweed Bug Life Histories , 1981 .

[73]  D. Roff,et al.  AN EMPIRICAL MODEL OF DIAPAUSE STRATEGIES OF THE CRICKET ALLONEMOBIUS SOCIUS , 1997 .

[74]  C. Simon,et al.  Evolutionary ecology of periodical insects. , 1994, Trends in ecology & evolution.

[75]  R. Green,et al.  Optimal Egg Distribution Among Host Patches for Parasitoids Subject to Attack by Hyperparasitoids , 1993, The American Naturalist.

[76]  V. Novotný.  Relation between temporal persistence of host plants and wing length in leafhoppers (Hemiptera: Auchenorrhyncha) , 1994 .

[77]  Population survival in a variable environment. , 1971, Journal of theoretical biology.

[78]  J. Capinera.  Qualitative Variation in Plants and Insects: Effect of Propagule Size on Ecological Plasticity , 1979, The American Naturalist.

[79]  L. V. Valen.  GROUP SELECTION AND THE EVOLUTION OF DISPERSAL. , 1971 .

[80]  Daniel J. Cohen.  A Theoretical Model for the Optimal Timing of Diapause , 1970, The American Naturalist.

[81]  M. Hoy.  Variability in Diapause Attributes of Insects and Mites: Some Evolutionary and Practical Implications , 1978 .

[82]  R. Denno,et al.  Physiology and ecology of dispersal polymorphism in insects. , 1997, Annual review of entomology.

[83]  P. Wellings,et al.  Seasonality and reproduction in aphids , 1982 .

[84]  J. Kingsolver.  Thermal and Hydric Aspects of Environmental Heterogeneity in the Pitcher Plant Mosquito , 1979 .

[85]  D. Roff,et al.  Wing Dimorphisms and the Evolution of Migratory Polymorphisms among the Insecta , 1991 .

[86]  D. Roff.  The evolution of flightlessness in insects , 1990 .

[87]  H. Dingle,et al.  VARIATION IN PHOTOPERIODIC RESPONSE WITHIN AND AMONG SPECIES OF MILKWEED BUGS (ONCOPELTUS) , 1980, Evolution; international journal of organic evolution.

[88]  C. Istock.  Natural Selection and Life History Variation: Theory plus Lessons from a Mosquito , 1981 .

[89]  Chris D. Thomas,et al.  Effects of habitat patch size and isolation on dispersal by Hesperia comma butterflies : implications for metapopulation structure , 1996 .

[90]  D. Cohen.  A General Model of Optimal Reproduction in a Randomly Varying Environment , 1968 .

[91]  R. Lewontin,et al.  On population growth in a randomly varying environment. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[92]  H. Dingle,et al.  The Nature of Genetic Variance Influencing Photoperiodic Diapause in a Migrant Insect, Oncopeltus fasciatus , 1977, The American Naturalist.

[93]  C. Istock.  Fitness Variation in a Natural Population , 1978 .

[94]  M. Rossiter,et al.  Maternal effects generate variation in life history : consequences of egg weight plasticity in the gypsy moth , 1991 .

[95]  D. Cohen.  Optimizing reproduction in a randomly varying environment. , 1966, Journal of theoretical biology.

[96]  P. Watson.  Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa (Linyphiidae) , 1991, Animal Behaviour.

[97]  W. S. Cooper,et al.  Adaptive "coin-flipping": a decision-theoretic examination of natural selection for random individual variation. , 1982, Journal of theoretical biology.