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Large-scale introgression shapes the evolution of the mating-type chromosomes of the filamentous ascomycete Neurospora tetrasperma - PubMed

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Large-scale introgression shapes the evolution of the mating-type chromosomes of the filamentous ascomycete Neurospora tetrasperma

Yu Sun et al. PLoS Genet. 2012.

Abstract

The significance of introgression as an evolutionary force shaping natural populations is well established, especially in animal and plant systems. However, the abundance and size of introgression tracts, and to what degree interspecific gene flow is the result of adaptive processes, are largely unknown. In this study, we present medium coverage genomic data from species of the filamentous ascomycete Neurospora, and we use comparative genomics to investigate the introgression landscape at the genomic level in this model genus. We revealed one large introgression tract in each of the three investigated phylogenetic lineages of Neurospora tetrasperma (sizes of 5.6 Mbp, 5.2 Mbp, and 4.1 Mbp, respectively). The tract is located on the chromosome containing the locus conferring sexual identity, the mating-type (mat) chromosome. The region of introgression is confined to the region of suppressed recombination and is found on one of the two mat chromosomes (mat a). We used Bayesian concordance analyses to exclude incomplete lineage sorting as the cause for the observed pattern, and multilocus genealogies from additional species of Neurospora show that the introgression likely originates from two closely related, freely recombining, heterothallic species (N. hispaniola and N. crassa/N. perkinsii). Finally, we investigated patterns of molecular evolution of the mat chromosome in Neurospora, and we show that introgression is correlated with reduced level of molecular degeneration, consistent with a shorter time of recombination suppression. The chromosome specific (mat) and allele specific (mat a) introgression reported herein comprise the largest introgression tracts reported to date from natural populations. Furthermore, our data contradicts theoretical predictions that introgression should be less likely on sex-determining chromosomes. Taken together, the data presented herein advance our general understanding of introgression as a force shaping eukaryotic genomes.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogenetic relationship of the investigated lineages of N. tetrasperma.

The tree was generated by maximum likelihood analysis of 1,978 concatenated autosomal genes. Bootstrap value from 100 replicates is shown by each branch.

Figure 2
Figure 2. Pair-wise divergences of the mating-type (mat) chromosomes and one selected autosome of Neurospora tetrasperma lineages and Neurospora crassa.

The pair-wise divergences were calculated as the fraction of differences (in bp) between the sequences, using a sliding window over the seven-way alignment. Lines represent 500 kb window size (step size 100 kb) sliding along the chromosome. The divergences are shown for the mat chromosome (LGI, left) and one of the autosomes (LGII, right). A: Intra-lineage comparisons (mat A vs mat a) of the three investigated lineages of N. tetrasperma: L1, L4 and L9. B: Comparisons of genomes from different lineages of N. tetrasperma (inter-lineage comparisons, dashed lines), and of N. tetrasperma and N. crassa (inter-species comparisons, solid lines). Note that the mat A – mat A inter-lineage comparisons (L1A–L4A, L1A–L9A and L4A–L9A) are plotted with blue lines. C: GC content in N. crassa (black line) and N. tetrasperma L1 (red line). Window size is 100 kb, step size 20 kb. Black bars indicate gene density in L1A.

Figure 3
Figure 3. Schematic illustration of the mating-type (mat) chromosomes of the three N. tetrasperma lineages included in the study.

Regions of elevated intra-lineage divergence and introgression are defined based on genome divergence estimates. Genes positioned below the chromosomes were used for the phylogenetic and Bayesian concordance analyses. In bold are genes for which representatives of all known heterothallic species and subgroups of Neurospora were included in the phylogenetic analyses. The figure is drawn to scale.

Figure 4
Figure 4. Phylogenies reconstructed for four microsatellite flanking loci (DMG, QMA, TMI, and TML) located on the autosomes of Neurospora.

Each tree includes representatives of three N. tetrasperma lineages (red), and ten heterothallic Neurospora species (blue). Neurospora discreta was used as outgroup in all analyses. Chromosomal location (linkage group, right or left flank) is given within parenthesis by each locus name. The topologies shown are from the Maximum likelihood phylogenetic analyses, with the bootstrap supports for the analysis shown below the branches and the posterior probabilities from the Bayesian phylogenetic analysis shown above the branches.

Figure 5
Figure 5. Gene genealogies for nit-2, eth-1, cys-9, and phr located on the mating-type (mat) chromosome of Neurospora.

The genes nit-2 and phr are located in the left and right pseudoautosomal (PA) flank, respectively. The genes eth-1 and cys-9 are located in the central region of the chromosome, for which the mat a chromosomes of all lineages of N. tetrasperma (L1a, L4a and L9a) show indications of introgression. Each genealogy includes representatives of the three investigated N. tetrasperma lineages (red), and ten heterothallic Neurospora species (blue). Neurospora discreta was used as outgroup in all analyses. The topologies shown are from the Maximum likelihood phylogenetic analysis with the bootstrap supports for the analysis shown below the branches and the posterior probabilities from the Bayesian phylogenetic analysis shown above the branches.

Figure 6
Figure 6. Bayesian concordance factors of selected clades, for the autosomes and the mating-type chromosomes (mat A and mat a) of Neurospora.

Bayesian concordance factors and 95% credibility intervals (error bars) estimated for 10 loci on the autosomes and 16 loci on the mat chromosomes. Concordance factors are given for the three hypotheses illustrated as clades in the plot, red: N. tetrasperma L9 sister species to N. crassa; blue: N. tetrasperma L4 sister species to N. hispaniola; green: N. tetrasperma monophyletic. The results displayed were calculated with the prior alpha set to 1.

Figure 7
Figure 7. Concordance factors on the mating-type (mat) chromosome support a post-introgression crossover between the Neurospora tetrasperma L4 mat chromosomes.

The concordance factors are plotted to the left and right of the crossover event described by Menkis et al. (2010) for both the mat A (A and B) and mat a (C and D) chromosomes. Concordance factors are given for the three hypotheses illustrated as clades in the plot, red: N. tetrasperma L9 sister species to N. crassa; blue: N. tetrasperma L4 sister species to N. hispaniola; green: N. tetrasperma monophyletic. The results displayed were calculated with the prior alpha set to 1.

Figure 8
Figure 8. A possible scenario explaining the evolution of the mating-type (mat) chromosomes in lineages of N. tetrasperma.

A putative scenario for the evolutionary processes leading to the results observed in this study. We speculate that a rearrangement on the mat A chromosome was associated with the evolution of pseudohomothallism in N. tetrasperma. During the subsequent divergence of the N. tetrasperma lineages, additional rearrangements, introgressions and a crossover took place.

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