Abstract
Nucleotide variation was studied in a 1.1 kb section of the coding region of an Esterase gene (Est-A) that maps in the center of the segments rearranged by polymorphic inversions in the cactophilic Drosophila buzzatii. We examine 30 homozygous second-chromosome lines differing in gene arrangement and three D. koepferae isofemale lines as outgroups. Our data show that Est-A is a highly polymorphic gene at both synonymous and replacement sites. Significant departures from homogeneity in the distribution of the ratio of silent polymorphism to divergence predicted by the neutral theory reveals a local excess of silent polymorphism. This is consistent with the presence of two apparent narrow peaks of elevated silent polymorphism surrounding nonconservative amino acid substitutions. These polymorphisms as well as others at synonymous and nonsynonymous sites are shared with D. koepferae. We suggest that the presence of shared nucleotide polymorphisms is probably due to interspecific gene flow and/or balancing selection acting on replacement variants and/or to a decreased probability of loss of ancestral polymorphisms caused by linkage to an adaptive inversion polymorphism. Recurrent mutation and persistence of neutral ancestral polymorphisms cannot, however, be ruled out. The analysis of the distribution of nucleotide variation among the three chromosomal arrangements sampled reveals that derived arrangements (J and JZ(3)) are less polymorphic than the ancestral ST, and that the widely distributed ST and J arrangements are genetically differentiated. However, a significant number of polymorphisms are shared between arrangements, suggesting frequent exchange either from gene conversion or from double crossovers in heterokaryotypes. Finally, our present results in combination with data of sequence variation at the breakpoints of inversion J suggest that this old gene arrangement has risen in frequency in relatively recent times.
Highlights
The observation of parallel and reciprocating clines along geographic and/or climatic gradients in different continents, long-term trends, temporal cycles, and more sophisticated experimental approaches in natural populations supplied the types of data that give support to the hypothesis of the adaptive role of chromosomal inversion polymorphisms in Drosophila
We address the following questions: (1) Are nucleotide sequence data consistent with the cytogenetic phylogeny accepted for the species? (2) Are closely linked regions like those inside the inversion J complex monophyletic? (3) Is nucleotide variation at Esterase gene (Est-A) compatible with neutral expectations? (4) Have derived arrangements reached mutation-drift-flux equilibrium? (5) Are the patterns of distribution of nucleotide variation within and between arrangements compatible with the hypothesis that the inversion polymorphism is an old balanced polymorphism? (6) Does the analysis of nucleotide variation allow us to infer the evolutionary forces that shaped the history of the inversion polymorphism?
Variants found in D. koepferae sequence at the polymorphic sites in D. buzzatii are indicated in the last rows
Summary
The observation of parallel and reciprocating clines along geographic and/or climatic gradients in different continents, long-term trends, temporal cycles, and more sophisticated experimental approaches in natural populations supplied the types of data that give support to the hypothesis of the adaptive role of chromosomal inversion polymorphisms in Drosophila (reviewed in Krimbas and Powell 1992; Powell 1997). The utilization of sequencing techniques in population surveys has caused renewed interest in the study of inversion polymorphisms (Andolfatto, DePaulis, and Navarro 2001). Several issues of their evolutionary history, such as mutational origin, extent to which different recombination environments—near the breakpoints or in the center more recombining parts of the rearranged segment—affect nucleotide variation and the mechanisms involved in the maintenance of inversion polymorphisms, may be revisited within the framework of coalescent theory (Hudson 1990)
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