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Inbreeding and the Fitness Consequences of Colonizing Novel Environments in Herbivorous Insects
Department of Entomology
Colonization of new environments by pest insects causes population bottlenecks (short-term periods of very small population size). One consequence of a population bottleneck is an increase in the frequency of inbreeding. Inbreeding increases expression of recessive alleles (alleles that are otherwise masked by dominant alleles), increasing expression of new advantageous alleles (facilitating adaptation to novel environments) and deleterious alleles (causing inbreeding depression). However, we have a very poor understanding of how inbreeding affects genetic variation, and thus facilitates adaptation, in any organism.
I will examine (a) the role of inbreeding in facilitating adaptation of stored products insects (bean beetles) to new storage environments, and (b) the ecology and genetics underlying inbreeding depression in seed-feeding insects. Understanding the role of inbreeding in facilitating adaptation will provide new insights into the mechanisms facilitating diet expansion and the evolution of novel insect physiological mechanisms for overcoming plant defenses. These insights will guide the development of novel strategies for (a) minimizing insect colonization of stored products (beans and grains) and (b) slowing insect adaptation to resistant crop cultivars.
2009 Project Description
In 2009 we continued to explore how the genetic load of insects (i.e., the pool of deleterious recessive alleles in a population) (a) evolves in response to colonization of new environments, and (b) varies in expression in response to ecological conditions.
Regarding the evolution of the genetic load following colonization of new populations, previous studies on a non-pest bean beetle species by my laboratory have shown that the serial inbreeding that necessarily occurs during colonization of new resource patches leads to elimination of deleterious recessive alleles ("purging" of the genetic load) and thus the rapid evolution of increased beetle performance. In 2009, we completed a large highly-replicated experiment (that was begun in 2008) testing whether the genetic load of Callosobruchus maculatus, a pest insect (beetle) on dry beans in storage, is also purged following colonization of seed stores by individual adult females. We found that, in contrast to the rapid purging observed in the non-pest beetle species, serial inbreeding following colonization of new resource patches does not lead to purging or to the evolution of increased fitness in C. maculatus. This is a very intriguing result because it demonstrates that the genetics underlying inbreeding depression are different in this beetle species than in most other insect species. We continue to explore the causes and consequences of this variation among species, with a primary interest in understanding why Callosobruchus maculatus retains its genetic load after experiencing a bottleneck (such as occurs when it colonizes a new grain facility) whereas the genetic load is rapidly purged following a population bottleneck in a similar non-pest species.
Regarding the ecological dependence of the expression of the genetic load, in 2009 we examined how expression of the genetic load varies with maternal age. Specifically, as mothers age they allocate fewer resources to offspring. We found that these poorly resourced offspring produced by older mothers are much more sensitive to inbreeding depression. We are currently replicating the experiment by manipulating various sources of stress encountered during development to determine whether increased stress increases expression of the age-specific genetic load.
Our studies demonstrate that the genetic load in plant-feeding insects can evolve rapidly following population bottlenecks that occur during colonization of new environments. This study, in combination with our previous studies regarding the ecology of expression of the genetic load in insect populations, are part of our continuing exploration the consequences of the genetic load in facilitating or impeding adaptation of plant-feeding insects to novel host species, and the implications for pest management strategies.
Fox CW & ME Czesak. 2009. Adaptive maternal effects: A case study of egg size plasticity in a seed-feeding beetle. Pp 781-815 in DW Whitman & TN Ananthakrishnan (editors) Phenotypic plasticity of insects: Mechanisms and consequences. Science Pub Inc.
Carroll SP & CW Fox. 2009. The evolution of life histories. Pp 567-570 in M Ruse & J Travis (editors) Evolution: The First Four Billion Years. Belknap Press, Cambridge, MA.
Fox CW & J Moya-Larano. 2009. Diet affects female mating behavior in a seed-feeding beetle. Physiological Entomology 34: 370-378.
Saeki Y, PH Crowley, CW Fox & DA Potter. 2009. A sex-specific size-number trade-off in clonal broods. Oikos 118: 1552-1560.
Fox CW & RC Stillwell. 2009. Environmental effects on sex differences in the genetic load for adult lifespan in a seed-feeding beetle. Heredity 103: 62-72.
Stillwell RC & CW Fox. 2009. Geographic variation in body size, sexual size dimorphism and fitness components of a seed beetle: Local adaptation vs. phenotypic plasticity. Oikos 118: 703-712.
Fox CW, JD Wagner, S Cline, FA Thomas & FJ Messina. 2009. Genetic architecture underlying convergent evolution of egg-laying behavior in a seed-feeding beetle. Genetica 136: 179-187.