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Abstract Hybrids between species exhibit plastic genomic architectures that could foster or slow down their adaptation. When challenged to evolve in an environment containing a UV mimetic drug, yeast hybrids have reduced adaptation rates compared to parents. We find that hybrids and their parents converge onto similar molecular mechanisms of adaptation by mutations in pleiotropic transcription factors, but at a different pace. After 100 generations, mutations in these genes tend to be homozygous in the parents but heterozygous in the hybrids. We hypothesize that a lower rate of loss of heterozygosity (LOH) in hybrids could limit fitness gain. Using genome editing, we first demonstrate that mutations display incomplete dominance, requiring homozygosity to show full impact and to entirely circumvent Haldane’s sieve, which favors the fixation of dominant mutations. Second, tracking mutations in earlier generations confirmed a different rate of LOH in hybrids. Together, these findings show that Haldane’s sieve slows down adaptation in hybrids, revealing an intrinsic constraint of hybrid genomic architecture that can limit the role of hybridization in adaptive evolution.

Pathogenic fungi are a cause of growing concern. Developing an efficient and safe antifungal is challenging because of the similar biological properties of fungal and host cells. Consequently, there is an urgent need to better understand the mechanisms underlying antifungal resistance to prolong the efficacy of current molecules. A major step in this direction would be to be able to predict or even prevent the acquisition of resistance. We leverage the power of experimental evolution to quantify the diversity of paths to resistance to the antifungal 5-fluorocytosine (5-FC), commercially known as flucytosine. We generated hundreds of independent 5-FC resistant mutants derived from two genetic backgrounds from wild isolates of Saccharomyces cerevisiae. Through automated pin-spotting, whole-genome and amplicon sequencing, we identified the most likely causes of resistance for most strains. Approximately a third of all resistant mutants evolved resistance through a pleiotropic drug response, a potentially novel mechanism in response to 5-FC, marked by cross-resistance to fluconazole. These cross-resistant mutants are characterized by a loss of respiration and a strong tradeoff in drug-free media. For the majority of the remaining two thirds, resistance was acquired through loss-of-function mutations in FUR1, which encodes an important enzyme in the metabolism of 5-FC. We describe conditions in which mutations affecting this particular step of the metabolic pathway are favored over known resistance mutations affecting a step upstream, such as the well-known target cytosine deaminase encoded by FCY1. This observation suggests that ecological interactions may dictate the identity of resistance hotspots.

The genome sequences of archeological Saccharomyces cerevisiae isolates can reveal insights about the history of human baking, brewing and winemaking activities. A yeast strain called Jean-Talon was recently isolated from the vaults of the Intendant’s Palace of Nouvelle France on a historical site in Québec City. This site was occupied by breweries from the end of the 17th century until the middle of the 20th century when poisoning caused by cobalt added to the beer led to a shutdown of brewing activities. We sequenced the genome of the Jean-Talon strain and reanalyzed the genomes of hundreds of strains to determine how it relates to other domesticated and wild strains. The Jean-Talon strain is most closely related to industrial beer strains from the beer and bakery genetic groups from the United Kingdom and Belgium. It has numerous aneuploidies and Copy Number Variants (CNVs), including the main gene conferring cobalt resistance in yeast. The Jean-Talon strain has indeed higher tolerance to cobalt compared to other yeast strains, consistent with adaptation to the most recent brewing activities on the site. We conclude from this that the Jean-Talon strain most likely derives from recent brewing activities and not from the original breweries of Nouvelle France on the site.

Abstract Much of the research in biology aims to understand the origin of diversity. Naturally, ecological diversity was the first object of study, but we now have the necessary tools to probe diversity at molecular scales. The inherent differences in how we study diversity at different scales caused the disciplines of biology to be organized around these levels, from molecular biology to ecology. Here, we illustrate that there are key properties of each scale that emerge from the interactions of simpler components and that these properties are often shared across different levels of organization. This means that ideas from one level of organization can be an inspiration for novel hypotheses to study phenomena at another level. We illustrate this concept with examples of events at the molecular level that have analogs at the organismal or ecological level and vice versa. Through these examples, we illustrate that biological processes at different organization levels are governed by general rules. The study of the same phenomena at different scales could enrich our work through a multidisciplinary approach, which should be a staple in the training of future scientists.

Vascular wilts are important diseases caused by plant pathogenic fungi that result in the rapid death of their plant hosts. This is due to a systemic defense mechanism whereby the plant induces the compartmentalization of the infected vascular system in order to reduce the propagation of the fungus. The ascomycete class Sordariomycetes contains several species that cause vascular wilts in diverse plant hosts, and they can be classified into four taxonomic orders. The genetic mechanisms of pathogenesis have already been investigated in Fusarium and Verticillium species, but they have not yet been compared with other well-known wilt-causing species, especially fungi causing oak wilt or Dutch elm disease (DED). Here we analyzed 20 whole genome assemblies of wilt-causing fungi together with 56 other species using phylogenetic approaches to trace expansions and contractions of orthologous gene families and gene classes related to pathogenicity. We found that the wilt-causing pathogens evolved seven times, experiencing the largest fold changes in different classes of genes almost every time. However, some similarities exist across groups of wilt pathogens, particularly in Microascales and Ophiostomatales, and these include the common gains and losses of genes that make up secondary metabolite clusters (SMC). DED pathogens do not experience large-scale gene expansions, with most of the gene classes, except for some SMC families, reducing in number. We also found that gene family expansions in the most recent common ancestors of wilt pathogen groups are enriched for carbohydrate metabolic processes. Our study shows that wilt-causing species evolve primarily through distinct changes in their repertoires of pathogenicity-related genes and that there is the potential importance of carbohydrate metabolism genes for regulating osmosis in those pathogens that penetrate the plant vascular system.

Hybridization can contribute to diversity from the genomic to the species level. Here, Eberlein, Hénault et al. investigate genomic, transcriptomic and phenotypic variation among wild lineages of the yeast Saccharomyces paradoxus and suggest that an incipient species has formed by recurrent hybridization.

Linkage maps are widely used to investigate structure, function, and evolution of genomes. In speciation research, maps facilitate the study of the genetic architecture of reproductive isolation by allowing identification of genomic regions underlying reduced fitness of hybrids. Here we present a linkage map for European newts of the Lissotriton vulgaris species complex, constructed using two families of F2 L. montandoni × L. vulgaris hybrids. The map consists of 1146 protein-coding genes on 12 linkage groups, equal to the haploid chromosome number, with a total length of 1484 cM (1.29 cM per marker). It is notably shorter than two other maps available for salamanders, but the differences in map length are consistent with cytogenetic estimates of the number of chiasmata per chromosomal arm. Thus, large salamander genomes do not necessarily translate into long linkage maps, as previously suggested. Consequently, salamanders are an excellent model to study evolutionary consequences of recombination rate variation in taxa with large genomes and a similar number of chromosomes. A complex pattern of transmission ratio distortion (TRD) was detected: TRD occurred mostly in one family, in one breeding season, and was clustered in two genomic segments. This is consistent with environment-dependent mortality of individuals carrying L. montandoni alleles in these two segments and suggests a role of TRD blocks in reproductive isolation. The reported linkage map will empower studies on the genomic architecture of divergence and interactions between the genomes of hybridizing newts.

The original version of the Supplementary Information associated with this Article contained errors in Supplementary Figures 2, 12, 20 and 22. The HTML has been updated to include a corrected version of the Supplementary Information; the original incorrect versions of these Figures can be found as Supplementary Information associated with this Correction.