Molecular Population Genetics and Evolution of Drosophila Meiosis Genes

By Anderson, Jennifer A.; Gilliland, William D. et al. | Genetics, January 2009 | Go to article overview

Molecular Population Genetics and Evolution of Drosophila Meiosis Genes


Anderson, Jennifer A., Gilliland, William D., Langley, Charles H., Genetics


ABSTRACT

While many functional elements of the meiotic process are well characterized in model organisms, the genetic basis of most of the natural phenotypic variation observed in meiotic pathways has not been determined. To begin to address this issue, we characterized patterns of polymorphism and divergence in the protein-coding regions of 33 genes across 31 lines of Drosophila melanogaster and 6 lines of Drosophila simulans. We sequenced genes known to be involved in chromosome segregation, recombination, DNA repair, and related heterochromatin binding. As expected, we found several of the genes to be highly conserved, consistent with purifying selection. However, a subset of genes showed patterns of polymorphism and divergence typical of other types of natural selection. Moreover, several intriguing differences between the two Drosophila lineages were evident: along the D. simulans lineage we consistently found evidence of adaptive protein evolution, whereas along the D. melanogaster lineage several loci exhibited patterns consistent with the maintenance of protein variation.

MEIOSIS is an essential part of sexual reproduction. While many meiotic pathways and genes are highly conserved across distantly related eukaryotes, others appear to diverge quite rapidly, even among individuals of the same species (for a review, see Gerton and Hawley 2005). For example, chiasmata are required for the proper segregation of meiotic homologs in most sexual organisms, and the main proteins mediating this process, such as the homologs of spo11 and Rad51, are ubiquitous (Zickler and Kleckner 1999). However, alternative systems that successfully segregate chromosomes in the absence of crossing over have evolved in several species (e.g.,White 1973;Hawleyet al. 1992), and it is possible that the evolution of lineage-specific genes has accompanied the appearance of these achiasmate pathways.

Recent studies have provided evidence that sequence variation in genes regulating meiosis can explain a portion of the variation in the fidelity of chromosome segregation found in natural populations. For example, Zwick et al. (1999) detected genetic variation in rates of nondisjunction among naturally occurring variants of nod, a chromokinesin required for achiasmate chromosome segregation in Drosophila melanogaster (Baker and Carpenter 1972; Carpenter 1973; Zhang and Hawley 1990; Zhang et al. 1990; Afshar et al. 1995a, b; Coop et al. 2008; Kong et al. 2008). In particular, they found two intermediate-frequency variants that were significantly associated with increased levels of female achiasmate nondisjunction in a sensitized background. To resolve this paradox (apparently deleterious alleles segregating at intermediate frequencies), they invoked the presence of true meiotic drive elements and their modifiers.

True meiotic drive can occur when meiosis is asymmetric, in the sense that all of the meiotic products are not included in the pronucleus of a gamete, as is the case in female multicellular eukaryotes (Sandler and Novitski 1957). Any variant that can increase a chromosome's probabilityofbecomingpartof the pronucleus therefore confers an immediate selective advantage. Zwick et al. (1999) argued that if a drive element (or its modifier) confers a deleterious pleiotropic effect, such as a high rate of chromosome nondisjunction, its selective advantage may be outweighed by its deleterious effect when it reaches intermediate or high frequencies in a population. Indeed, it is expected that many components of the meiotic pathway may experience strong selective pressure for faithful and accurate transmission of meiotic products every generation. Such factors are predicted to affect the relative fitness of a drive element by suppressing its segregation advantage (Sandler and Novitski 1957; Hiraizumi et al. 1960; Charlesworth and Hartl 1978; Zwick et al. 1999). Under these circumstances, a drive element would rarely fix, and a high level of nondisjunction, along with polymorphism at the driving and modifier loci, such as that observed for nod, would be maintained.

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