Chromosome-wide linkage disequilibrium as a consequence of meiotic drive

Abstract

Adaptation by natural selection proceeds most efficiently when alleles compete solely on the basis of their effects on the survival and reproduction of their carriers. A major condition for this is equal Mendelian segregation, but meiotic drive can short-circuit this process. The evolution of drive often involves multiple, interacting genetic components, together with enhancers and suppressors of drive. Chromosomal inversions that suppress crossing over are also frequently associated with drive systems. This study investigates the effects of these processes on patterns of molecular evolution in the fly Drosophila recens, which is polymorphic for a driving X chromosome (X(D)). Whereas standard wild-type chromosomes exhibit high levels of polymorphism at multiple loci, all of the X(D) chromosomes effectively carry a single multilocus haplotype that spans at least 130 cM. The X(D) is associated with a complex set of inversions that completely suppresses recombination between the standard wild-type chromosome and X(D) in heterozygous females, which maintain nonrandom associations among loci that presumably interact epistatically for the expression of drive. The long-term costs of foregoing recombination may be substantial; in combination with its low equilibrium frequency, this makes the X(D) chromosome susceptible to the accumulation of deleterious mutations. Consistent with this, X(D) chromosomes are apparently fixed for a recessive mutation that causes female sterility. Thus, the X(D) in D. recens appears to be in chromosome-wide linkage disequilibrium and in the early stages of mutational degradation.

Fig. 1.

Kosambi-corrected map distances among loci and haplotype structure of sampled chromosomes. Each column is a sampled chromosome. Gray lines indicate a site that is identical to the consensus X^ST sequence, and white lines indicate a difference from the X^ST consensus. Only parsimony informative sites were included; sites with segregating indels and singleton polymorphisms were excluded for clarity.

Fig. 2.

MLE of the ratio of the N_e of X^D relative to X^ST. The MLE of this ratio of 0.0276 is indicated by the dotted line, and the 2-unit support interval of 0.0118–0.054 is indicated by the gray line.

Fig. 3.

Phylogenetic tree made from the concatenated sequences of the 14 X^D and 23 X^ST chromosomes of D. recens, using D. subquinaria to root the tree. The tree was constructed by using the neighbor-joining algorithm with Kimura two-parameter adjusted branch lengths. Support values were generated from 10,000 bootstrap replicates. Sites with gaps were excluded from the analyses, resulting in a total of 3,757 bp.

Fig. 4.

Polytene X chromosomes of X^D/X^ST female. Inversion shifts, which indicate overlapping inversions, are noted by the black arrows, and the tip of the chromosome is indicated by the white arrow.