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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.
2010 Project Description
In 2010 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. Our focus was on two related topics.
(1) Interactions between inbreeding and maternal effects have received little attention in the literature. In 2010 we completed a series of experiments (started in 2009) in which we manipulated inbreeding level of offspring and age of mothers in Callosobruchus maculatus, our model organism for the study of inbreeding-environment interactions. The key result is that the decline in offspring fitness with increasing maternal age (which is commonly observed in insects) is greater for inbred offspring than for outbred offspring. This means that the expression of deleterious recessive alleles (the genetic load) in offspring is greater for offspring produced by older rather than younger mothers.
This novel result highlights the potential importance of an interaction between inbreeding and maternal effects. We are continuing this work by (a) examining how ecological variables (such as temperature and diet) interact with maternal age and other maternal effects to affect the expression of the genetic load in our model insect, and (b) using diet manipulation experiments to test mechanisms underlying this inbreeding-maternal effect interaction.
(2) We conducted a meta-analysis of the available data from published studies looking at stress and inbreeding depression. The meta-analysis confirmed that the effect of the environment on inbreeding depression scales linearly with the magnitude of stress; a population suffers one additional lethal equivalent, on average, for each 30% reduction in fitness induced by the stressful environment.
Studies using less-stressful environments may lack statistical power to detect the small changes in inbreeding depression. That the magnitude of inbreeding depression scales with the magnitude of the stress applied has numerous repercussions for evolutionary and conservation genetics and may invigorate research aimed at finding the causal mechanism involved in such a relationship.
The effects of inbreeding are heritable by subsequent generations, i.e., the inbreeding coefficient of parents affects the phenotype/fitness of their outbred offspring. However, studies of how maternal effects mediate inbreeding depression in offspring (i.e., the expression of an organism's genetic load) are largely lacking. In particular, maternal age represents a neglected source of variation in inbreeding depression.
Maternal age affects a wide diversity of traits in probably all taxonomic groups, and thus has the potential to be an ecologically important influence on patterns of inbreeding depression in nature. For example, the interaction between maternal age and inbreeding level is important for the demographics and evolution of populations. Inbreeding is known to have multigenerational effects, with the offspring or even grandoffspring of inbred parents having lowered fitness, despite the fact that the descendants are not themselves inbred. Similarly, maternal effects are also known to last for multiple generations.
Thus, an interaction between inbreeding and maternal age has the potential to produce complex and long-lasting effects on population dynamics and evolutionary trajectories. Future studies, both empirical and theoretical, should consider how the interaction between inbreeding and maternal age affects important problems regarding such disparate topics population viability, the evolution of mating systems, and the evolution of lifespan and aging.
Fox CW & DF Westneat. 2010. Adaptation. Pp 16-31 in DF Westneat & CW Fox (editors) Evolutionary Behavioral Ecology. Oxford University Press, NY
Fox CW, ML Bush & FJ Messina. 2010. Biotypes of the seed beetle Callosobruchus maculatus have differing effects on the germination and growth of their legume hosts. Agricultural and Forest Entomology 12: 353-362.
Stillwell RC, WU Blanckenhorn, T Teder, G Davidowitz & CW Fox. 2010. Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annual Review of Entomology 55: 227-245.
Fox CW. 2010. All that I am, I owe to my mother. Trends in Ecology and Evolution 25: 323-324.