RESUMEN
In all species, new chromosomal inversions are constantly being formed by spontaneous rearrangement and then stochastically eliminated from natural populations. In Drosophila, when new chromosomal inversions overlap with a preexisting inversion in the population, their rate of elimination becomes a function of the relative size, position, and linkage phase of the gene rearrangements. These altered dynamics result from complex meiotic behavior wherein overlapping inversions generate asymmetric dyads that cause both meiotic drive/drag and segmental aneuploidy. In this context, patterns in rare inversion polymorphisms of a natural population can be modeled from the fundamental genetic processes of forming asymmetric dyads via crossing-over in meiosis I and preferential segregation from asymmetric dyads in meiosis II. Here, a mathematical model of crossover-dependent female meiotic drive is developed and parameterized with published experimental data from Drosophila melanogaster laboratory constructs. This mechanism is demonstrated to favor smaller, distal inversions and accelerate the elimination of larger, proximal inversions. Simulated sampling experiments indicate that the paracentric inversions directly observed in natural population surveys of D. melanogaster are a biased subset that both maximizes meiotic drive and minimizes the frequency of lethal zygotes caused by this cytogenetic mechanism. Incorporating this form of selection into a population genetic model accurately predicts the shift in relative size, position, and linkage phase for rare inversions found in this species. The model and analysis presented here suggest that this weak form of female meiotic drive is an important process influencing the genomic distribution of rare inversion polymorphisms.
RESUMEN
Recombination suppression in chromosomal inversion heterozygotes is a well-known but poorly understood phenomenon. Surprisingly, recombination suppression extends far outside of inverted regions where there are no intrinsic barriers to normal chromosome pairing, synapsis, double-strand break formation, or recovery of crossover products. The interference hypothesis of recombination suppression proposes heterozygous inversion breakpoints possess chiasma-like properties such that recombination suppression extends from these breakpoints in a process analogous to crossover interference. This hypothesis is qualitatively consistent with chromosome-wide patterns of recombination suppression extending to both inverted and uninverted regions of the chromosome. The present study generated quantitative predictions for this hypothesis using a probabilistic model of crossover interference with gamma-distributed inter-event distances. These predictions were then tested with experimental genetic data (>40,000 meioses) on crossing-over in intervals that are external and adjacent to four common inversions of Drosophila melanogaster. The crossover interference model accurately predicted the partially suppressed recombination rates in euchromatic intervals outside inverted regions. Furthermore, assuming interference does not extend across centromeres dramatically improved model fit and partially accounted for excess recombination observed in pericentromeric intervals. Finally, inversions with breakpoints closest to the centromere had the greatest excess of recombination in pericentromeric intervals, an observation that is consistent with negative crossover interference previously documented near Drosophila melanogaster centromeres. In conclusion, the experimental data support the interference hypothesis of recombination suppression, validate a mathematical framework for integrating distance-dependent effects of structural heterozygosity on crossover distribution, and highlight the need for improved modeling of crossover interference in pericentromeric regions.
Asunto(s)
Inversión Cromosómica , Drosophila melanogaster , Animales , Drosophila melanogaster/genética , Recombinación Genética , Cromosomas , Heterocigoto , Intercambio GenéticoRESUMEN
Sex-Ratio (SR) chromosomes are selfish X-chromosomes that distort Mendelian segregation and are commonly associated with inversions. These chromosomal rearrangements suppress recombination with Standard (ST) X-chromosomes and are hypothesized to maintain multiple alleles important for distortion in a single large haplotype. Here, we conduct a multifaceted study of the multiply inverted Drosophila pseudoobscura SR chromosome to understand the evolutionary history, genetic architecture, and present-day dynamics that shape this enigmatic selfish chromosome. The D. pseudoobscura SR chromosome has three nonoverlapping inversions of the right arm of the metacentric X-chromosome: basal, medial, and terminal. We find that 23 of 29 Mb of the D. pseudoobscuraX-chromosome right arm is highly differentiated between the Standard and SR arrangements, including a 6.6 Mb collinear region between the medial and terminal inversions. Although crossing-over is heavily suppressed on this chromosome arm, we discover it is not completely eliminated, with measured rates indicating recombination suppression alone cannot explain patterns of differentiation or the near-perfect association of the three SR chromosome inversions in nature. We then demonstrate the ancient basal and medial inversions of the SR chromosome contain genes sufficient to cause weak distortion. In contrast, the younger terminal inversion cannot distort by itself, but contains at least one modifier gene necessary for full manifestation of strong sex chromosome distortion. By parameterizing population genetic models for chromosome-wide linkage disequilibrium with our experimental results, we infer that strong selection acts to maintain the near-perfect association of SR chromosome inversions in present-day populations. Based on comparative genomic analyses, direct recombination experiments, segregation distortion assays, and population genetic modeling, we conclude the combined action of suppressed recombination and strong, ongoing, epistatic selection shape the D. pseudoobscura SR arrangement into a highly differentiated chromosome.
Asunto(s)
Inversión Cromosómica , Epistasis Genética , Selección Genética , Cromosoma X/genética , Animales , Drosophila , Evolución Molecular , Genes Modificadores , Desequilibrio de Ligamiento , Recombinación Genética , Supresión GenéticaRESUMEN
The gene arrangements of Drosophila have played a prominent role in the history of evolutionary biology from the original quantification of genetic diversity to current studies of the mechanisms for the origin and establishment of new inversion mutations within populations and their subsequent fixation between species supporting reproductive barriers. This review examines the genetic causes and consequences of inversions as recombination suppressors and the role that recombination suppression plays in establishing inversions in populations as they are involved in adaptation within heterogeneous environments. This often results in the formation of clines of gene arrangement frequencies among populations. Recombination suppression leads to the differentiation of the gene arrangements which may accelerate the accumulation of fixed genetic differences among populations. If these fixed mutations cause incompatibilities, then inversions pose important reproductive barriers between species. This review uses the evolution of inversions in Drosophila pseudoobscura and D. persimilis as a case study for how inversions originate, establish and contribute to the evolution of reproductive isolation.
Asunto(s)
Adaptación Fisiológica/genética , Inversión Cromosómica/genética , Drosophila/genética , Especiación Genética , Aclimatación/genética , Animales , Evolución Molecular , Orden Génico , Genoma de los Insectos/genética , Aislamiento ReproductivoRESUMEN
Larvae of the marine gastropod Crepidula fornicata must complete a transition from the plankton, where they are highly dispersed, to an aggregated group of benthic adults. Previous research has shown that selective settlement of larvae on conspecific adults is mediated by a water-borne chemical cue. However, variable experimental conditions have been used to study this cue, and standardization is needed in order to investigate factors that may have weak effects on settlement. In this study, we developed a time-course bioassay based on a full-factorial design with temporal blocking and statistical analysis of larval settlement rates in the lab. We tested this bioassay by examining settlement in the presence of an abiotic cue (KCl), and biotic cues (water conditioned with adult conspecifics and conspecific pedal mucus). Results confirmed settlement in the presence of both KCl and adult-conditioned water, and discovered the induction of settlement by pedal mucus. This optimized, standardized bioassay will be used in future experiments to characterize the complex process of larval settlement in C. fornicata, particularly to measure components of potentially small effect.