Mitchell B. Baker

Colorado potato beetle resistance to insecticides

The Colorado potato beetle, Leptinotarsa decemlineata (Say), is widely regarded as the most important insect defoliator of potatoes. Its current range covers about 16 million km2 in North America, Europe, and Asia and continues to expand. This insect has a complicated and diverse life history, which is well-suited to agricultural environments, and makes it a complex and challenging pest to control. Dispersal, closely connected with diapause, feeding, and reproduction, allow the Colorado potato beetle to employ “bet-hedging” reproductive strategies, distributing its offspring in both space (within and between fields) and time (within and between years). The Colorado potato beetle played a large role in creating the modern pesticide industry, with hundreds of chemicals tested against it. High selection pressure, together with natural propensity to adapt to toxic substances, eventually resulted in a large number of insecticide-resistant Colorado potato beetle populations. Since the middle of the last century, the beetle has developed resistance to 52 different compounds belonging to all major insecticide classes. Resistance levels vary greatly among different populations and between beetle life stages, but in some cases can be very high (up to 2,000-fold). Known mechanisms of Colorado potato beetle resistance to insecticides include enhanced metabolism involving esterases, carboxylesterases and monooxygenases, and target site insensitivity, as well as reduced insecticide penetration and increased excretion. There is also some evidence of behavioral resistance. Resistance mechanisms are sometimes highly diverse even within a relatively narrow geographical area. Resistance is usually inherited as an incompletely dominant or incompletely recessive trait, with one or several genes involved in its determination. Because of pleiotropic effects of resistant alleles, insecticide-resistant beetles often have reduced relative fitness in the absence of insecticides. Rotating different classes of insecticides and reducing insecticidal pressure on pest populations by provision of temporal and spatial refuges from exposure to toxins have been proposed to delay evolution of resistance. However, insecticide resistance in this insect will likely remain a major challenge to the pest control practitioners. Still limited understanding of beetle biology, its flexible life history, and grower reluctance to adopt some of the resistance management techniques create impediments to successful resistance management. Overcoming these obstacles is not an easy task, but it will be crucial for sustainable potato production.ResumenEl escarabajo de Colorado de la papa [(Leptinotarsa decemlineata (Say)] es considerado el insecto defoliador más importante de la papa. Su acción cubre una área de 16 millones de km2 en Norteamérica, Europa y Asia y continúa expandiéndose. Este insecto tiene un ciclo de vida complicado y diverso, el cual esta bien adecuado a entornos agrícolas y lo hace una plaga difícil de controlar. Su dispersión, íntimamente conectada con su quiescencia, hábitos de alimentación y reproducción permite al escarabajo de Colorado de la papa emplear estrategias de reproducción de “riesgo calculado”distribuyendo su descendencia en espacio (dentro del campo y entre campos) y tiempo (dentro y entre años). El escarabajo de Colorado de la papa jugó un rol muy amplio en la creación de la industria moderna de pesticidas, con cientos de químicos evaluados para su control. La alta presión de selección, junto a la propensión natural para adaptarse a las sustancias tóxicas, resultó en un gran número de poblaciones resistentes a los insecticidas. Desde mediados del siglo pasado, el escarabajo ha desarrollado resistencia a 52 diferentes compuestos pertenecientes a todas las clases importantes de insecticidas. Los niveles de resistencia varían mucho entre las diferentes poblaciones y estadíos en el ciclo de vida, pero en algunos casos pueden variar mucho más (hasta 2,000 veces). Los mecanismos conocidos de resistencia de este escarabajo a los insecticidas incluyen un elevado metabolismo de las esterasas, carboxilesterasas y monooxigenasas e insensibilidad al sitio objetivo, lo mismo que una penetración del insecticida reducida y excreción incrementada. También hay evidencia de resistencia por comportamiento. Los mecanismos de resistencia son a veces altamente variados, aun dentro de una reducida área geográfica. La resistencia es a menudo heredada como un carácter incompletamente dominante o incompletamente recesivo, con uno o varios genes involucrados en su determinación. Debido a los efectos pleiotrópicos de alelos resistentes, los escarabajos resistentes tienen una aptitud relativa reducida en ausencia de insecticidas. La rotación de diferentes clases de insecticidas y la reducción de la presión insecticida sobre las poblaciones de insectos por provisión de refugios temporales y espaciales contra la exposición de toxinas han sido propuestas para demorar la evolución de la resistencia. Sin embargo, la resistencia a insecticidas de este insecto permanecerá siendo un desafío para los practicantes de control de plagas. Todavía hay un limitado conocimiento sobre la biología del escarabajo, su ciclo de vida flexible y la renuencia del productor para adoptar algunas de las técnicas de manejo de la resistencia impiden el manejo exitoso de la resistencia. El vencer estos obstáculos no es tarea fácil, pero será importante para una producción sostenible de papa.

Correcting biased estimates of dispersal and survival due to limited study area: theory and an application using wrentits

Accurate estimates of dispersal distributions and survival to breeding are essential for estimating gene flow and population demographics, and for testing the predictions of mechanistic models. We derive a method that corrects for the underestimate of dispersal and survival inherent in studies conducted within a finite area. Each dispersal event is weighted by the inverse of the probability of observing that event, calculated by dividing the observable dispersal events of a given distance by all possible dispersal events of that distance. The method takes into account the shape of the study area and suitability of habitat. The method is applied to a twelve-year field study of natal dispersal in Wrentits (Chamaea fasciata) resulting in an increase in the estimate of mean and median dispersal from observed values of 267 and 248 m to corrected values of 375 and 387 m. The correction method also estimates the number of second year birds recruiting to potential breeding territories on and off the study area. Seventy-five of the 799 locally born fledglings recruited onto the study plot (9.3%). We estimate that an additional 101 birds recruited off the study plot, increasing the estimate of yearling survival to recruitment from 9.3% to 21.9% of young fledged. We used a simulation approach to generate testable predictions that validate the assumptions and results of the method. The method is easy to apply, and is easily extended to incorporate greater realism and detail.

Persistence and Inheritance of Costs of Resistance to Imidacloprid in Colorado Potato Beetle

Abstract Reduced fitness among resistant versus susceptible individuals slows resistance evolution and makes it easier to manage. A loss of resistance costs could indicate novel adaptations or mutations contributing to resistance. We measured costs of resistance to imidacloprid in a Massachusetts resistant population compared with a Massachusetts susceptible population in 1999 in terms of fecundity, hatching success, egg development time, and sprint speed. Resistance was additive and seemed to be polygenic with high heritability. The fecundity cost appeared overdominant in 1999, and the hatch rate cost was partly recessive in 1999, but neither was significantly different from dominant or recessive. In 2004, we repeated our measures of resistance costs in Massachusetts in terms of fecundity and hatching success, and we added a new resistant population from Maine. In 2005, we compared development time of Maine resistant and the laboratory susceptible colony eggs. Significant fecundity costs of resistance were found in both population in both 1999 and 2004, and significant egg developmental time costs were found in 1999 and 2005. However, the hatching success costs of resistance were significant in 1999 and not apparent in 2004, suggesting some modification or replacement of the resistance genes in the intervening time.

Environmental Component of Latitudinal Clutch-size Variation in House Sparrows (Passer domesticus)

Many species of birds (Cody 1966) and mammals (Lord 1960, McNab 1980) show positive correlations of clutch or litter size with latitude. In birds, clutchsize gradients are also correlated with longitude (Lack 1968) and, in some species, altitude (Cody 1971). It is assumed that geographical clutch-size gradients are maintained by natural selection on additive genetic variance for clutch size. One mechanism may be increased predation acting to restrict clutch size at lower latitudes, but any factor that affects the fitness of different clutch sizes could be involved. It would represent a major advance if researchers could determine the proximate causes of clutch-size variation. There have been at least six studies of clutch size heritability, all evaluating within-population variation (Perrins and Jones 1974, Flux and Flux 1981, van Noordwijk et al. 1981, Gustaffson 1986, Findlay and Cooke 1987, Gibbs 1988). Five of the six have shown a significant heritable component to clutch size, with h2 ranging from 0.23 in Snow Geese (Chen caerulescens) to 0.5 in Great Tits (Parus major). Only one study, by Gibbs (1988) on Geospiza fortis (a Darwins finch), found a heritability not significantly different from 0. In an artificial-selection study on a wild population of European Starlings (Sturnis Vulgaris), selection for clutches of five eggs or greater raised the F1 clutch size by 0.12 eggs on average, which implied an h2 of 0.33 (Flux and Flux 1981). Variation among populations, if it is due to genetic causes, most likely is the result of natural selection on intrapopulation heritable variation for the trait. However, as Boag and van Noordwijk (1987) pointed out, high heritability of traits within populations does not imply that among-population differences are due to genetic causes. James (1983) conducted a reciprocal-transplant experiment between two pairs of populations of Red-winged Blackbirds (Agelaius phoeniceus) and showed that a significant portion of the variance between populations in some morphological traits was explained by nongenetic factors. Geographical trends for House Sparrows (Passer domesticus) in morphological and life-history traits have been extensively studied (Johnston and Selander 1971, 1973, Murphy 1978). Clutch size in House Sparrows varies with latitude in the New World, from over five eggs per clutch in Alberta, Canada (Murphy 1978), to

Sperm Precedence in Overwintered Colorado Potato Beetle (Coleoptera: Chrysomelidae) and Its Implications for Insecticide Resistance Management

Abstract Colorado potato beetle, Leptinotarsa decemlineata (Say), is the most important insect defoliator of potatoes and is infamous for its ability to develop insecticide resistance. Sperm precedence is an important consideration in developing resistance management plans. We determined the precedence of sperm from a postdiapause spring mating by using irradiated sterile males. We also investigated whether spring mating (with or without fertilization) affects reproduction of overwintered females. Precedence of sperm from spring matings versus overwintered sperm from fall matings was almost complete. Some fertilization from fall matings did take place in this experiment, but it exceeded 10% in only one of the 22 pairings. Females mated only the previous fall laid fewer eggs than spring-mated females, but spring mating did not seem to improve the hatch rate of deposited eggs. On average, mated females started laying 1.6 d sooner than fall-mated females, but this difference was not significant. Hatch rate did not change with time. Precedence of spring matings over stored sperm can help compensate for assortative summer mating among resistant individuals due to differences in developmental time between refuges and treated areas.

Invasions on Large and Small Scales: Management of a Well-established Crop Pest, the Colorado Potato Beetle

Understanding the movement of invading organisms is critical to predicting invasion dynamics. The Colorado potato beetle, Leptinotarsa decemlineata (Say), is an invasive species on multiple spatial and temporal scales, and can serve as a model for studies of invasion dynamics. It is the major insect defoliator of potato in North America, and successful management requires an understanding of CPB invasions of individual fields. Its origin, spread, and biology, especially the cycle of annual invasions of agricultural potato fields, are described. Approaches to reducing the size of colonizing populations include rotation, delay of planting, and treatments of field margins. Rotation and sub-lethal insecticide treatments can slow the establishment of invasions within fields. These approaches interact with a late season diapause switch away from reproduction to reduce the impact of CPB. The refuge approach to delaying the fixation of resistance alleles is designed to encourage alleles for susceptibility to invade treated areas. We present data from an experimental refuge crop planted adjacent to a field treated with imidacloprid, an insecticide for which there is high variation in resistance. The treated field was four times as resistant as the untreated side, and a cline in resistance was formed from the untreated to the treated portion of the field. The cline width of about 100 m provides an empirical basis for designing refuges to enhance the spread of alleles for susceptibility into treated areas and prevent fixation of resistance in the summer generation.

Variation in Fitness among Geographically Isolated Colorado Potato Beetle (Coleoptera: Chrysomelidae) Populations

ABSTRACT Colorado potato beetle, Leptinotarsa decemlineata (Say), is a major pest of potatoes in North America, Europe, and parts of Asia. It adapts quickly to adverse environments, thereby limiting the longevity of control strategies. Better understanding of variability among geographically isolated populations of this insect might create an opportunity to customize control techniques for local conditions. We investigated insecticide resistance, heat tolerance, and growth potential in six beetle populations collected from different locations in the United States. Significant differences were detected in insecticide resistance, egg mass size, and egg hatchability among the tested populations. Large egg mass size appeared to be offset by lower egg hatchability. We also observed a female-biased sex ratio at least in one of the strains. Population growth rates were different among the strains, but this parameter was not correlated to insecticide resistance. This suggests that using allopatric populations in comparative studies of insecticide resistance might result in confusing effects of geographic isolation with the effects of selection toward resistance.

Use of sperm precedence to infer the overwintering cost of insecticide resistance in the Colorado potato beetle

1 Resistance to insecticides is a model system for studying adaptation. Although selection for resistance is always strong in areas and seasons where populations are exposed to insecticides, costs of resistance, which may only be expressed in the absence of insecticide use, will shape how quickly resistance will evolve.

Mating Competition in Colorado Potato Beetles (Coleoptera: Chrysomelidae) Does Not Show a Cost of Insecticide Resistance

Abstract Resistance to insecticides is often linked with fitness costs. Although costs affecting lifetime reproduction in females will have the greatest effect on resistance evolution, fertilization costs in males, through less vigorous mating behavior or less effective sperm in resistant individuals, will slow the spread of resistance. We used a sterile male technique to measure the relative mating competitiveness of Colorado potato beetles, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae), resistant or susceptible to imidacloprid. We showed that 5,000 Krad from a cesium-137 source was sufficient to sterilize male beetles. We tested mating competitiveness by placing a single resistant and a single susceptible male beetle with a virgin susceptible female in circular acetate enclosures surrounding potted potato plants, and we observed frequency of mating or mounting with each male and subsequent fertilization success. Resistant males mate just as often as susceptible males during 24-h competitive interactions. Hatch rate was correlated with the proportion of matings or mounts observed with the nonirradiated male, but no effect of the first or last male, nor of resistance on fertilization success was observed, and resistance does not seem to incur a behavioral or sperm-competitive fertilization cost.

Geographic Variation in Cannibalism in Colorado Potato Beetle (Coleoptera: Chrysomelidae) Populations

ABSTRACT Cannibalism can have a large effect on population growth and survival in stressful environments, possibly including those created by insecticide use. In this study, we collected Colorado potato beetles from three isolated areas in the northeastern United States known for high levels of resistance to neonicotinoids. We measured resistance to imidacloprid in each of those populations, a laboratory susceptible population, and in hybrids between the three field populations and the laboratory susceptible population. We fed neonates eggs from resistant dams fed either imidaclopridtreated or untreated foliage to determine whether cannibals are exposed to toxins sequestered in eggs. We measured egg cannibalism by hatchlings within the clutch in each population and hybrids, and examined how fecundity and several variables associated with egg development varied among populations and with cannibalism, to see which traits might enhance or reduce cannibalism. Cannibalism varied significantly among populations, accounting for most of the variation in hatching success. Variability in egg development time and hatch rate in the absence of cannibalism in some populations affected rates of cannibalism. Resistance varied significantly among the field populations but was not related to cannibalism. Neonates fed eggs from dams on treated foliage showed signs of intoxication or death. Cannibalism appears to be part of a varying life history strategy in this species, with some populations laying larger and more cannibalistic clutches and the New York population laying smaller clutches with higher hatching success owing to reduced cannibalism.