Academic journal article Genetics

Additivity and Trans-Acting Effects on Gene Expression in Male Drosophila Simulans

Academic journal article Genetics

Additivity and Trans-Acting Effects on Gene Expression in Male Drosophila Simulans

Article excerpt

ABSTRACT

Understanding how genetic variation is maintained begins with a comprehensive description of what types of genetic variation exist, the extent and magnitude of the variation, and patterns discernable in that variation. However, such studies have focused primarily on DNA sequence data and have ignored genetic variation at other hierarchical levels of genetic information. Microarray technology permits an examination of genetic variation at the level of mRNA abundance. Utilizing a round-robin design, we present a quantitative description of variation in mRNA abundance in terms of GCA (general combining ability or additive variance). We test whether genes significant for GCA are randomly distributed across chromosomes and use a nonparametric approach to demonstrate that the magnitude of the variation is not random for GCA. We find that there is a paucity of genes significant for GCA on the X relative to the autosomes. The overall magnitude of the effects for GCA on the X tends to be lower than that on the autosomes and is contributed by rare alleles of larger effect. Due to male hemizygosity, GCA for X-linked phenotypes must be due to trans-acting factors, while GCA for autosomal phenotypes may be due to cis- or trans-acting factors. The contrast in the amount of variation between the X and the autosomes suggests that both cis and trans factors contribute to variation for expression in D. simulans with the preponderance of effects being trans. This nonrandom patterning of genetic variation in gene expression data with respect to chromosomal context may be due to hemizygosity in the male.

STUDIES describing and quantifying genetic variation, and putting it in an evolutionary context, have a rich history, beginning with pioneering investigations of protein variation almost 40 years ago (HARRIS 1966; HUBBY and LEWONTIN 1966; LEWONTIN and Hubby 1966). This work suggested that widespread overdominance was not the major force maintaining genetic variation and was criticized as incomplete, because only a fraction of the variation present in aDNAsequence can be detected on a protein gel. Subsequently, an intensive examination of genetic variation at the sequence level ensued, including development of statistical tests of neutrality (HUDSON et al. 1987). While these studies have demonstrated large amounts of variation and the pervasiveness of selection, they have raised additional questions, namely how selective events shape DNA sequence variation (ANDOLFATTO 2001). Moreover, a complete picture of genetic variation includes far more than sequence variation, but should span hierarchical levels of genetic information systems. Recently, descriptions of variation in abundance and distribution of mRNA have been pioneered (JIN et al. 2001; ARBEITMAN et al. 2002; RANZ et al. 2003; RIFKIN et al. 2003), but due to the expense of such studies, they have necessarily been limited in scope. Here we present a systematic study of variation in levels of mRNA in males of Drosophila simulans using a round-robin breeding design, which allows us to make inferences about additivity and epistatic variation in mRNA abundance.

Gene expression studies have identified genes whose expression varies among individuals (WOLFINGER et al. 2001; OLEKSIAK et al. 2002). However, the genetic architecture of the phenotype of gene expression remains to be described, particularly whether or not expression exhibits quantifiable additive genetic variation. To understand the genetic architecture of gene expression, a controlled crossing scheme is used, where the specific mating design allows for estimation and testing of inferences about the underlying genetic architecture of the phenotype of interest. With this in mind, we modified a classical quantitative genetic breeding design: the diallel (GRIFFING 1956a,b). Diallel designs can generate empirical estimates of general combining ability (GCA) and specific combining ability (SCA). SCA is not considered further here, as it cannot be independently estimated for our modified diallel crossing design. …

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