Units of species and speciation.

<p>The Neo-Darwinian view of the Modern Synthesis is that "speciation genes" are the units driving speciation across the genome. Alternatively, if gene sets (including consortia of genes like plasmids or other mobile genetic elements) are sufficiently decoupled from their host genomes, this will lead to "gene ecology," in which gene sets, not species, determine reproductive isolation and/or adapt to ecological niches. Speciation could also be maintained (or potentially driven) by microbial symbionts or by host genes that select for particular symbionts, resulting in hologenome species. All of these speciation mechanisms can potentially be driven by selection or drift, and the list of units and mechanisms (arrows) is not exhaustive.</p

Models of speciation under different regimes of selection and recombination.

<p>In all models, a single population of chromosomes (circles) splits into two nascent species, distinguishable by sets of genetic differences. At each time point, the most frequent multilocus genotype is shown, but other chromosomes could be segregating in the population at lower frequencies. Different haplotypes (or clonal frames) are shown as black or white circles. The ancestral niche is shown in blue and a new niche in orange. Gene flow (recombination) between species is indicated by horizontal connections between branches. (<b>A</b>) In the simplest model of speciation with gene flow, a single mutation controlling sexual isolation (but not under selection) is the only divergent locus (yellow square), with other loci experiencing gene flow between incipient species. (<b>B</b>) Selection during speciation can produce a pattern of genetic diversity across the genome very similar to (A), but species are expected to be longer-lived. Mutations under selection at early and later stages of speciation are shown as orange stars. (<b>C</b>) Allopatric speciation with a population bottleneck and neutral divergence of species. As in (A), competitive exclusion should lead to the extinction of one species if they come back into contact. (<b>D</b>) Without gene flow, the mutation under selection between species (orange star) will purge diversity genome-wide as it sweeps through one population, resulting in genome-wide divergence from the other population.</p

Protein divergence in the RNApII (black) and the NPC (grey) in the <i>Saccharomyces sensu stricto</i> group.

<p>Evolutionary trees were drawn for all proteins of a complex and are on the same scale (proportion of different amino acids). Distribution of protein divergence between <i>Scer</i> and <i>Skud</i> was calculated from multiple-sequence alignments available for 5261 orthologous proteins <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003161#pgen.1003161-Scannell1" target="_blank">[23]</a>. Arrows indicate protein divergence covered by the two complexes.</p

Evidence for the Robustness of Protein Complexes to Inter-Species Hybridization

<div><p>Despite the tremendous efforts devoted to the identification of genetic incompatibilities underlying hybrid sterility and inviability, little is known about the effect of inter-species hybridization at the protein interactome level. Here, we develop a screening platform for the comparison of protein–protein interactions (PPIs) among closely related species and their hybrids. We examine <em>in vivo</em> the architecture of protein complexes in two yeast species (<em>Saccharomyces cerevisiae</em> and <em>Saccharomyces kudriavzevii</em>) that diverged 5–20 million years ago and in their F1 hybrids. We focus on 24 proteins of two large complexes: the RNA polymerase II and the nuclear pore complex (NPC), which show contrasting patterns of molecular evolution. We found that, with the exception of one PPI in the NPC sub-complex, PPIs were highly conserved between species, regardless of protein divergence. Unexpectedly, we found that the architecture of the complexes in F1 hybrids could not be distinguished from that of the parental species. Our results suggest that the conservation of PPIs in hybrids likely results from the slow evolution taking place on the very few protein residues involved in the interaction or that protein complexes are inherently robust and may accommodate protein divergence up to the level that is observed among closely related species.</p> </div

The absence of Nup120-Nup145C interaction in <i>Skud</i> is likely a PPI loss.

<p>(<i>A</i>) Spot assays on Methotrexate medium (six days of growth at 30°C) to dissect the interaction in <i>Scer</i> (red), <i>Skud</i> (blue), <i>Suva</i> (yellow) and their hybrids. The interaction between Nup145C from <i>Scer</i> and Nup120 from <i>Scer</i>, <i>Skud</i> or <i>Suva</i> is detected, whereas it is lost when Nup145C comes from <i>Skud</i>. The interaction was also absent when it involved Nup120 from <i>Skud</i> and Nup145 from <i>Suva</i>. (<i>B</i>) Schematic structure of the <i>Scer</i> Nup120-Nup85-Nup145 sub-complex adapted from Fernandez-Martinez <i>et al. </i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003161#pgen.1003161-FernandezMartinez1" target="_blank">[43]</a>. The three interacting domains are indicated in black. (<i>C</i>) Interactions between Nup85 and Nup145C or Nup120 in three species and their hybrids confirm that not all Nup145C interactions are lost. (<i>D</i>) Evolutionary tree of <i>Scer</i>, <i>Skud</i> and <i>Suva</i> and schematic representation of Nup145-Nup120-Nup85 interactions in species and hybrids according to spot assays (<i>A–C</i>), revealing several other loss of interaction in hybrids with <i>Suva</i>. Line width is proportional to the number of spot growth observed for each interaction. (<i>E</i>) Similar growth for BY4741 <i>Scer</i> wild type (WT) and modified strains (Δ<i>Skud-NUP145</i>) suggest that <i>Skud-Nup145</i> complements the absence of <i>Scer-Nup145</i> (YPD medium, two days of growth at 30°C), as <i>Nup145</i> is essential for growth in <i>Scer</i>.</p

The NPC and RNApII networks are largely conserved between <i>Scer</i> and <i>Skud</i>.

<p>(<i>A</i>) Comparison of SI values (strains growth signal index; log₁₀) between species. Grey dotted lines indicate SI threshold values (<i>t</i>). SI values were considered to correspond to interactions when greater than <i>t</i> in both species (purple) or specific to one species when greater than <i>t</i> only in <i>Scer</i> (red), or only in <i>Skud</i> (blue). Black dotted lines indicate 5%, 1% and 0.1% threshold above which SI residuals significantly deviate from the <i>Scer-Skud</i> regression (black line). (<i>B</i>) Overlapped networks of <i>Scer</i> and <i>Skud</i>. Only SI above <i>t</i> and comparable interactions are represented. Line width is proportional to SI values measured between proteins in <i>Scer</i> (red) and <i>Skud</i> (blue) in the NPC (left) and the RNApII (right). Interactions appear in purple when <i>Scer</i> and <i>Skud</i> SI values overlap. Different degrees of purple depend on whether the interaction could be tested in reciprocal ways or not. (<i>C</i>) Venn diagram indicating the overlap of PPIs detected by PCA of other methods (BioGRID) in <i>Scer</i>, and by PCA in <i>Skud</i>. Reciprocal combinations of PPIs were collapsed. (<i>D</i>) Representation of PPIs shared (purple lines) or unique to <i>Scer</i> (red lines) or <i>Skud</i> (blue lines) in the NPC. Only proteins involving divergences in PPIs are showed. Only the difference in the Nup120-Nup145 PPI was significant (**: <i>p</i><0.01).</p

The NPC and RNApII are robust to hybridization.

<p>SI values compared between <i>Scer</i> (red) or <i>Skud</i> (blue) and <i>Scer-Skud</i> hybrids (green). Examples of proteins Nup82 (<i>A–B</i>) and Nup145 (<i>E–F</i>) in the NPC and Rpb3 (<i>C–D</i>) in the RNApII. Segment width is proportional to SI (dotted line if SI<<i>t</i>). For each comparison, networks on left show interactions measured between the protein of interest tagged in <i>MATa</i> (center) and other proteins of the same complex tagged in <i>MATα</i>. Networks on right show the reciprocal interactions. The protein of interest comes from <i>Scer</i> (red ring) or <i>Skud</i> (blue ring) and is in the species background (outer ring) or in the hybrid background (inner ring). Asterisks indicate whether the SI value measured in hybrid is significantly different from that measured in species (*: <i>p</i><0.05; **: <i>p</i><0.01; ***: <i>p</i><0.001). Only the absence of <i>Scer</i>Nup120-<i>Skud</i>Nup145 is significant in reciprocal comparisons (<i>E</i>). Protein names were blurred when strains were unavailable.</p

<i>S</i>. <i>eubayanus</i> distribution and phylogeography.

<p>A) Geographic distribution of <i>S</i>. <i>eubayanus</i> isolates. B) Maximum-Likelihood (ML) phylogenetic tree reconstructed using the concatenated multi-locus Dataset A (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006155#pgen.1006155.s001" target="_blank">S1 Text</a>). Bar colors are defined in the legend in panel A. Asterisks highlight new isolates or strains not previously studied together [<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006155#pgen.1006155.ref020" target="_blank">20</a>]. EU: Europe; QI: Qinghai (China); LA: Lanin (Argentina); NC: North Carolina (USA); NH: Nahuel Huapi (Argentina); NZ: New Zealand; SH: Shaanxi (China); SI: Sichuan (China); T: Tibet (China); VP: Villa Pehuenia (Argentina); WA: Washington (USA). C) ML phylogenetic tree reconstructed using the complete genome sequence data. Phylogenetic trees were rooted using <i>S</i>. <i>uvarum</i> (CBS7001) as the outgroup. The scale bars show the number of substitutions per site. The strain FM1318 is a monosporic derivative of CRUB1568^T (= CBS12357^T = PYCC6148^T). Bootstrap values above 50 are reported at their corresponding nodes. D) Neighbor-Net phylogenetic network reconstructed with the SNP dataset. In phylogenetic networks, incongruent data are represented by nodes subtended by multiple edges. Blue and red arrows indicate the fractional genomic contributions from PB-1 and PA-2, respectively. The scale bar represents the number of substitutions. Note that the admixed strains from Wisconsin [<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006155#pgen.1006155.ref020" target="_blank">20</a>] and New Brunswick (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006155#pgen.1006155.g002" target="_blank">Fig 2</a>) are only shown in panel D to avoid implying a linear bifurcating ancestry.</p

Genome-wide analysis of admixed strains.

<p>A) Pairwise nucleotide sequence divergence of the admixed strain yHKS210 compared to strains from the Patagonia A and Patagonia B populations. Average pairwise divergence comparisons are represented with red and blue dots for Patagonia A and Patagonia B, respectively. Standard deviations of pairwise divergence among Patagonia A and Patagonia B are represented by shadows, with broader regions corresponding to higher genetic diversity within populations. B) To directly visualize which population is closest to each region of the genome, we calculated the log₂ ratio of the minimum PB-Admixed nucleotide sequence divergence (d_B-Ad) and the minimum PA-Admixed nucleotide sequence divergence (d_A-Ad) in 50-kbp windows. log₂ < 0 or >0 indicate that part of the genome is more closely related to Patagonia A or Patagonia B, respectively. Regions lacking values are due to filters imposed based on coverage, data quality, or their absence in some strains (see <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006155#pgen.1006155.s001" target="_blank">S1 Text</a>). C) Admixture ancestry assignment based on PCAdmix (i.e. an inference of which population is contributed that portion of the genome). Portions are defined by 20 SNPs. Blue indicates a chromosomal region inferred to share ancestry with PB-1, red indicates shared ancestry with PA-2, and white indicates that the method cannot make an inference. Roman numerals represent chromosomes. D) Unrooted ML phylogenetic tree reconstructed using SNPs. The scale bar shows the number of substitutions per site, corrected for invariant sites.</p

Genome-wide pairwise nucleotide sequence divergence to lager yeasts.

<p>A) and C) are pairwise nucleotide divergence comparisons to a Saaz and a Frohberg representative, respectively. Comparisons are made to the Patagonia A population, the Patagonia B strains, the two North Carolina strains, and the Tibetan representative. Dots represent average values, while standard deviations from the average are represented by the colored shadow area; red for Patagonia A, dark blue for Patagonia B, blue for Tibet (T), and light blue for North Carolina (NC). B) and D) are the log₂ ratios of the minimum NC-Lager divergence (d_NC-X) and the T-Lager nucleotide divergence (d_T-X) in 50-kbp windows, where X is B) Saaz (S) or D) Frohberg (F). log₂ < 0 or >0 indicate whether that part of the genome is more closely related to T or NC, respectively. Red lines in B) and D) are significance thresholds established by permutation tests (unbiased <i>P <</i> 0.019). Regions lacking values are due to filters imposed based on coverage, data quality, or their absence in some strains (see <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1006155#pgen.1006155.s001" target="_blank">S1 Text</a>). Roman numerals represent chromosomes.</p