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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.
2011 Project Description
In 2011 we continued to explore how the genetic load of insects (i.e., the pool of deleterious recessive alleles in a population that are expressed by inbreeding) is influenced by ecological and environmental conditions, and the consequences of this genetic load for patterns of inbreeding depression.
Our focus was on three related topics, using seed beetles (Callosobruchus maculatus and Stator limbatus) as model species.
(1) The major theme of our research is how environmental variation, in particular ecological stress, affects the expression of the inbreeding load (measured as inbreeding depression). Ecological stressors cause selection in natural populations, including selection on offspring size (larger offspring generally tolerate ecological stress better than do smaller offspring). This year we examined how inbreeding mediates selection on offspring size and found that although inbreeding depresses offspring survival it does not change the shape of the relationship between fitness and offspring size (i.e., inbreeding changes mean fitness but does not change natural selection). We also performed an experiment to disentangle the relative effects during the larval versus adult stages of development on expression of inbreeding depression in adults. Our results have been surprising in finding especially large effects of the larval environment, and small effects of the adult environment, on inbreeding depression in adult survival (lifespan).
(2) Our second main project this year was an examination of the cost of phenotypic plasticity in egg size, the trait under natural selection in response to ecological stress in the experiments discussed above. Our main result is that the ability of females to be phenotypically plastic comes at a significant cost of a delay in reproduction; genotypes that are more phenotypically plastic require time to assess the quality of the environment in which they will lay eggs, and adjust the size of their eggs as necessary.
(3) Our third main project was an examination of how male inbreeding status affects the fitness of females with whom they mate. Females mated to inbred males were less likely to lay eggs, but lived longer than did females mated to outbred males. The observed effect on fecundity is likely mediated by male sperm production; ejaculates of inbred males contained fewer sperm, on average, than did ejaculates of outbred males.
Inbreeding depression is pervasive in nature and has substantial impacts in both agricultural and conservation contexts. Our work aims to understand the variables that influence inbreeding depression, and the consequences of this variation in inbreeding depression, in both agricultural and conservation contexts.
Our recent and continuing studies have helped disentangle the interactions between mating system (and resulting inbreeding) and various source of ecological stress (diet, heat shock, larval competition, maternal age, temperature) on insect fitness. In particular, we have identified a general relationship between the magnitude of stress experienced by populations and the relative effect of inbreeding depression. We have also identified a novel consequence of inbreeding; females mated to inbred males have lower fecundity than females mated to outbred males, mediated by male sperm production (inbred males produce fewer sperm than do inbred males, and this negatively affects female egg production).
Previous studies have demonstrated that inbred males are often less successful in mating, and that inbred males often produce sperm that are less motile, less viable or have a greater frequency of abnormalities, all of which can reduce the fertilization success and fitness of inbred males relative to outbred males. Our study is the first to begin linking these effects of inbreeding to female egg production and the potential consequences for population growth and the evolution of insect mating systems.
Fox CW & DH Reed. 2010. Inbreeding depression increases with maternal age in a seed-feeding beetle. Evolutionary Ecology Research 12: 961-972.
Abbot P., et al. (137 authors listed alphabetically). 2011. Inclusive fitness theory and eusociality. Nature 471: E1-E4.
Amarillo-Suarez AR, RC Stillwell & CW Fox. 2011. Natural selection on body size is mediated by multiple interacting factors: a comparison of beetle populations varying naturally and experimentally in body size. Ecology and Evolution 1: 1-14.
Messina FJ & CW Fox. 2011. Egg-dumping behavior is not correlated with wider host acceptance in the seed beetle Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Annals of the Entomological Society of America 104: 850-856.
Fox CW, JD Wagner, S Cline, FA Thomas & FJ Messina. 2011. Rapid evolution of lifespan in a novel environment: sex-specific responses and underlying genetic architecture. Evolutionary Biology 38: 182-196.
Fox CW & DH Reed. 2011. Inbreeding depression increases with environmental stress: An experimental study and meta-analysis. Evolution 65: 246-258.
Fox CW, RC Stillwell, WG Wallin, CL Curtis & DH Reed. 2011. Inbreeding-environment interactions for fitness: Complex relationships between inbreeding depression and temperature stress in a seed-feeding beetle. Evolutionary Ecology 25: 25-43.