Rapid turnover of pathogen-blocking Wolbachia and their incompatibility loci.

At least half of all insect species carry maternally inherited Wolbachia alphaproteobacteria, making Wolbachia the most common endosymbionts in nature. Wolbachia spread to high frequencies is often due to cytoplasmic incompatibility (CI), a Wolbachia-induced sperm modification that kills embryos without Wolbachia. Several CI-causing Wolbachia variants, including wMel from Drosophila melanogaster, also block viruses. Establishing pathogen-blocking wMel in natural Aedes aegypti mosquito populations has reduced dengue disease incidence, with one study reporting about 85% reduction when wMel frequency is high. However, wMel transinfection establishment is challenging in many environments, highlighting the importance of identifying CI-causing Wolbachia variants that stably persist in diverse hosts and habitats. We demonstrate that wMel-like variants have naturally established in widely distributed holometabolous dipteran and hymenopteran insects that diverged approximately 350 million years ago, with wMel variants spreading rapidly among these hosts over only the last 100,000 years. Wolbachia genomes contain prophages that encode CI-causing operons (cifs). These cifs move among Wolbachia genomes - with and without prophages - even more rapidly than Wolbachia move among insect hosts. Our results shed light on how rapid host switching and horizontal gene transfer contribute to Wolbachia and cif diversity in nature. The diverse wMel variants we report here from hosts present in different climates offer many new options for broadening Wolbachia-based biocontrol of diseases and pests.

Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes.

Ascomycota account for about two-thirds of named fungal species.1 Over 98% of known Ascomycota belong to the Pezizomycotina, including many economically important species as well as diverse pathogens, decomposers, and mutualistic symbionts.2 Our understanding of Pezizomycotina evolution has until now been based on sampling traditionally well-defined taxonomic classes.3,4,5 However, considerable diversity exists in undersampled and uncultured, putatively early-diverging lineages, and the effect of these on evolutionary models has seldom been tested. We obtained genomes from 30 putative early-diverging lineages not included in recent phylogenomic analyses and analyzed these together with 451 genomes covering all available ascomycete genera. We show that 22 of these lineages, collectively representing over 600 species, trace back to a single origin that diverged from the common ancestor of Eurotiomycetes and Lecanoromycetes over 300 million years BP. The new clade, which we recognize as a more broadly defined Lichinomycetes, includes lichen and insect symbionts, endophytes, and putative mycorrhizae and encompasses a range of morphologies so disparate that they have recently been placed in six different taxonomic classes. To test for shared hidden features within this group, we analyzed genome content and compared gene repertoires to related groups in Ascomycota. Regardless of their lifestyle, Lichinomycetes have smaller genomes than most filamentous Ascomycota, with reduced arsenals of carbohydrate-degrading enzymes and secondary metabolite gene clusters. Our expanded genome sample resolves the relationships of numerous "orphan" ascomycetes and establishes the independent evolutionary origins of multiple mutualistic lifestyles within a single, morphologically hyperdiverse clade of fungi.

Using all Gene Families Vastly Expands Data Available for Phylogenomic Inference.

Traditionally, single-copy orthologs have been the gold standard in phylogenomics. Most phylogenomic studies identify putative single-copy orthologs using clustering approaches and retain families with a single sequence per species. This limits the amount of data available by excluding larger families. Recent advances have suggested several ways to include data from larger families. For instance, tree-based decomposition methods facilitate the extraction of orthologs from large families. Additionally, several methods for species tree inference are robust to the inclusion of paralogs and could use all of the data from larger families. Here, we explore the effects of using all families for phylogenetic inference by examining relationships among 26 primate species in detail and by analyzing five additional data sets. We compare single-copy families, orthologs extracted using tree-based decomposition approaches, and all families with all data. We explore several species tree inference methods, finding that identical trees are returned across nearly all subsets of the data and methods for primates. The relationships among Platyrrhini remain contentious; however, the species tree inference method matters more than the subset of data used. Using data from larger gene families drastically increases the number of genes available and leads to consistent estimates of branch lengths, nodal certainty and concordance, and inferences of introgression in primates. For the other data sets, topological inferences are consistent whether single-copy families or orthologs extracted using decomposition approaches are analyzed. Using larger gene families is a promising approach to include more data in phylogenomics without sacrificing accuracy, at least when high-quality genomes are available.

Stage-specific disruption of X chromosome expression during spermatogenesis in sterile house mouse hybrids.

Hybrid sterility is a complex phenotype that can result from the breakdown of spermatogenesis at multiple developmental stages. Here, we disentangle two proposed hybrid male sterility mechanisms in the house mice, Mus musculus domesticus and M. m. musculus, by comparing patterns of gene expression in sterile F1 hybrids from a reciprocal cross. We found that hybrid males from both cross directions showed disrupted X chromosome expression during prophase of meiosis I consistent with a loss of meiotic sex chromosome inactivation (MSCI) and Prdm9-associated sterility, but that the degree of disruption was greater in mice with an M. m. musculus X chromosome consistent with previous studies. During postmeiotic development, gene expression on the X chromosome was only disrupted in one cross direction, suggesting that misexpression at this later stage was genotype-specific and not a simple downstream consequence of MSCI disruption which was observed in both reciprocal crosses. Instead, disrupted postmeiotic expression may depend on the magnitude of earlier disrupted MSCI, or the disruption of particular X-linked genes or gene networks. Alternatively, only hybrids with a potential deficit of Sly copies, a Y-linked ampliconic gene family, showed overexpression in postmeiotic cells, consistent with a previously proposed model of antagonistic coevolution between the X- and Y-linked ampliconic genes contributing to disrupted expression late in spermatogenesis. The relative contributions of these two regulatory mechanisms and their impact on sterility phenotypes await further study. Our results further support the hypothesis that X-linked hybrid sterility in house mice has a variable genetic basis, and that genotype-specific disruption of gene regulation contributes to overexpression of the X chromosome at different stages of development. Overall, these findings underscore the critical role of epigenetic regulation of the X chromosome during spermatogenesis and suggest that these processes are prone to disruption in hybrids.

The Plot Thickens: Haploid and Triploid-Like Thalli, Hybridization, and Biased Mating Type Ratios in Letharia.

The study of the reproductive biology of lichen fungal symbionts has been traditionally challenging due to their complex lifestyles. Against the common belief of haploidy, a recent genomic study found a triploid-like signal in Letharia. Here, we infer the genome organization and reproduction in Letharia by analyzing genomic data from a pure culture and from thalli, and performing a PCR survey of the MAT locus in natural populations. We found that the read count variation in the four Letharia specimens, including the pure culture derived from a single sexual spore of L. lupina, is consistent with haploidy. By contrast, the L. lupina read counts from a thallus' metagenome are triploid-like. Characterization of the mating-type locus revealed a conserved heterothallic configuration across the genus, along with auxiliary genes that we identified. We found that the mating-type distributions are balanced in North America for L. vulpina and L. lupina, suggesting widespread sexual reproduction, but highly skewed in Europe for L. vulpina, consistent with predominant asexuality. Taken together, we propose that Letharia fungi are heterothallic and typically haploid, and provide evidence that triploid-like individuals are hybrids between L. lupina and an unknown Letharia lineage, reconciling classic systematic and genetic studies with recent genomic observations.

CAFE 5 models variation in evolutionary rates among gene families.

MOTIVATION: Genome sequencing projects have revealed frequent gains and losses of genes between species. Previous versions of our software, Computational Analysis of gene Family Evolution (CAFE), have allowed researchers to estimate parameters of gene gain and loss across a phylogenetic tree. However, the underlying model assumed that all gene families had the same rate of evolution, despite evidence suggesting a large amount of variation in rates among families. RESULTS: Here, we present CAFE 5, a completely re-written software package with numerous performance and user-interface enhancements over previous versions. These include improved support for multithreading, the explicit modeling of rate variation among families using gamma-distributed rate categories, and command-line arguments that preclude the use of accessory scripts. AVAILABILITY AND IMPLEMENTATION: CAFE 5 source code, documentation, test data and a detailed manual with examples are freely available at https://github.com/hahnlab/CAFE5/releases. SUPPLEMENTARY INFORMATION: Supplementary data are available at Bioinformatics online.

Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression.

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

Genomic and transcriptomic insights into Raffaelea lauricola pathogenesis.

BACKGROUND: Laurel wilt caused by Raffaelea lauricola is a lethal vascular disease of North American members of the Lauraceae plant family. This fungus and its primary ambrosia beetle vector Xyleborus glabratus originated from Asia; however, there is no report of laurel wilt causing widespread mortality on native Lauraceae trees in Asia. To gain insight into why R. lauricola is a tree-killing plant pathogen in North America, we generated and compared high quality draft genome assemblies of R. lauricola and its closely related non-pathogenic species R. aguacate. RESULTS: Relative to R. aguacate, the R. lauricola genome uniquely encodes several small-secreted proteins that are associated with virulence in other pathogens and is enriched in secondary metabolite biosynthetic clusters, particularly polyketide synthase (PKS), non-ribosomal peptide synthetase (NRPS) and PKS-NRPS anchored gene clusters. The two species also exhibit significant differences in secreted proteins including CAZymes that are associated with polysaccharide binding including the chitin binding CBM50 (LysM) domain. Transcriptomic comparisons of inoculated redbay trees and in vitro-grown fungal cultures further revealed a number of secreted protein genes, secondary metabolite clusters and alternative sulfur uptake and assimilation pathways that are coordinately up-regulated during infection. CONCLUSIONS: Through these comparative analyses we have identified potential adaptations of R. lauricola that may enable it to colonize and cause disease on susceptible hosts. How these adaptations have interacted with co-evolved hosts in Asia, where little to no disease occurs, and non-co-evolved hosts in North America, where lethal wilt occurs, requires additional functional analysis of genes and pathways.

Bark Beetle Population Dynamics in the Anthropocene: Challenges and Solutions.

Tree-killing bark beetles are the most economically important insects in conifer forests worldwide. However, despite >200 years of research, the drivers of population eruptions and crashes are still not fully understood and the existing knowledge is thus insufficient to face the challenges posed by the Anthropocene. We critically analyze potential biotic and abiotic drivers of population dynamics of an exemplary species, the European spruce bark beetle (ESBB) (Ips typographus) and present a multivariate approach that integrates the many drivers governing this bark beetle system. We call for hypothesis-driven, large-scale collaborative research efforts to improve our understanding of the population dynamics of this and other bark beetle pests. Our approach can serve as a blueprint for tackling other eruptive forest insects.

Wolbachia Acquisition by Drosophila yakuba-Clade Hosts and Transfer of Incompatibility Loci Between Distantly Related Wolbachia.

Maternally transmitted Wolbachia infect about half of insect species, yet the predominant mode(s) of Wolbachia acquisition remains uncertain. Species-specific associations could be old, with Wolbachia and hosts codiversifying (i.e., cladogenic acquisition), or relatively young and acquired by horizontal transfer or introgression. The three Drosophila yakuba-clade hosts [(D. santomea, D. yakuba) D. teissieri] diverged ∼3 MYA and currently hybridize on the West African islands Bioko and São Tomé. Each species is polymorphic for nearly identical Wolbachia that cause weak cytoplasmic incompatibility (CI)-reduced egg hatch when uninfected females mate with infected males. D. yakuba-clade Wolbachia are closely related to wMel, globally polymorphic in D. melanogaster We use draft Wolbachia and mitochondrial genomes to demonstrate that D. yakuba-clade phylogenies for Wolbachia and mitochondria tend to follow host nuclear phylogenies. However, roughly half of D. santomea individuals, sampled both inside and outside of the São Tomé hybrid zone, have introgressed D. yakuba mitochondria. Both mitochondria and Wolbachia possess far more recent common ancestors than the bulk of the host nuclear genomes, precluding cladogenic Wolbachia acquisition. General concordance of Wolbachia and mitochondrial phylogenies suggests that horizontal transmission is rare, but varying relative rates of molecular divergence complicate chronogram-based statistical tests. Loci that cause CI in wMel are disrupted in D. yakuba-clade Wolbachia; but a second set of loci predicted to cause CI are located in the same WO prophage region. These alternative CI loci seem to have been acquired horizontally from distantly related Wolbachia, with transfer mediated by flanking Wolbachia-specific ISWpi1 transposons.

Temporal genomic contrasts reveal rapid evolutionary responses in an alpine mammal during recent climate change.

Many species have experienced dramatic changes in their abundance and distribution during recent climate change, but it is often unclear whether such ecological responses are accompanied by evolutionary change. We used targeted exon sequencing of 294 museum specimens (160 historic, 134 modern) to generate independent temporal genomic contrasts spanning a century of climate change (1911-2012) for two co-distributed chipmunk species: an endemic alpine specialist (Tamias alpinus) undergoing severe range contraction and a stable mid-elevation species (T. speciosus). Using a novel analytical approach, we reconstructed the demographic histories of these populations and tested for evidence of recent positive directional selection. Only the retracting species showed substantial population genetic fragmentation through time and this was coupled with positive selection and substantial shifts in allele frequencies at a gene, Alox15, involved in regulation of inflammation and response to hypoxia. However, these rapid population and gene-level responses were not detected in an analogous temporal contrast from another area where T. alpinus has also undergone severe range contraction. Collectively, these results highlight that evolutionary responses may be variable and context dependent across populations, even when they show seemingly synchronous ecological shifts. Our results demonstrate that temporal genomic contrasts can be used to detect very recent evolutionary responses within and among contemporary populations, even in the face of complex demographic changes. Given the wealth of specimens archived in natural history museums, comparative analyses of temporal population genomic data have the potential to improve our understanding of recent and ongoing evolutionary responses to rapidly changing environments.

Two Basidiomycete Fungi in the Cortex of Wolf Lichens.

Since the late 1800s, mycologists have been detecting fungi above and beyond the assumed single fungus in lichen thalli [1-6]. Over the last century, these fungi have been accorded roles ranging from commensalists to pathogens. Recently, Cyphobasidiales yeasts were shown to be ubiquitous in the cortex layer of many macrolichens [7], but for most species, little is known of their cellular distribution and constancy beyond visible fruiting structures. Here, we demonstrate the occurrence of an additional and distantly related basidiomycete, Tremella, in 95% of studied thalli in a global sample of one of the most intensively studied groups of lichens, the wolf lichens (genus Letharia). Tremella species are reported from a wide range of lichen genera [8], but until now, their biology was deduced from fruiting bodies (basidiomata) formed on lichen thalli. Based on this, they have been thought to be uncommon to rare, to occur exclusively in a hyphal form, and to be parasitic on the dominant fungal partner [9, 10]. We show that, in wolf lichens, Tremella occurs as yeast cells also in thalli that lack basidiomata and infer that this is its dominant stage in nature. We further show that the hyphal stage, when present in Letharia, is in close contact with algal cells, challenging the assumption that lichen-associated Tremella species are uniformly mycoparasites. Our results suggest that extent of occurrence and cellular interactions of known fungi within lichens have historically been underestimated and raise new questions about their function in specific lichen symbioses.

Recurrent symbiont recruitment from fungal parasites in cicadas.

Diverse insects are associated with ancient bacterial symbionts, whose genomes have often suffered drastic reduction and degeneration. In extreme cases, such symbiont genomes seem almost unable to sustain the basic cellular functioning, which comprises an open question in the evolution of symbiosis. Here, we report an insect group wherein an ancient symbiont lineage suffering massive genome erosion has experienced recurrent extinction and replacement by host-associated pathogenic microbes. Cicadas are associated with the ancient bacterial co-obligate symbionts Sulcia and Hodgkinia, whose streamlined genomes are specialized for synthesizing essential amino acids, thereby enabling the host to live on plant sap. However, our inspection of 24 Japanese cicada species revealed that while all species possessed Sulcia, only nine species retained Hodgkinia, and their genomes exhibited substantial structural instability. The remaining 15 species lacked Hodgkinia and instead harbored yeast-like fungal symbionts. Detailed phylogenetic analyses uncovered repeated Hodgkinia-fungus and fungus-fungus replacements in cicadas. The fungal symbionts were phylogenetically intermingled with cicada-parasitizing Ophiocordyceps fungi, identifying entomopathogenic origins of the fungal symbionts. Most fungal symbionts of cicadas were uncultivable, but the fungal symbiont of Meimuna opalifera was cultivable, possibly because it is at an early stage of fungal symbiont replacement. Genome sequencing of the fungal symbiont revealed its metabolic versatility, presumably capable of synthesizing almost all amino acids, vitamins, and other metabolites, which is more than sufficient to compensate for the Hodgkinia loss. These findings highlight a straightforward ecological and evolutionary connection between parasitism and symbiosis, which may provide an evolutionary trajectory to renovate deteriorated ancient symbiosis via pathogen domestication.

The Evolution of Polymorphic Hybrid Incompatibilities in House Mice.

Resolving the mechanistic and genetic bases of reproductive barriers between species is essential to understanding the evolutionary forces that shape speciation. Intrinsic hybrid incompatibilities are often treated as fixed between species, yet there can be considerable variation in the strength of reproductive isolation between populations. The extent and causes of this variation remain poorly understood in most systems. We investigated the genetic basis of variable hybrid male sterility (HMS) between two recently diverged subspecies of house mice, Mus musculus domesticus and Mus musculus musculus We found that polymorphic HMS has a surprisingly complex genetic basis, with contributions from at least five autosomal loci segregating between two closely related wild-derived strains of M. m. musculus One of the HMS-linked regions on chromosome 4 also showed extensive introgression among inbred laboratory strains and transmission ratio distortion (TRD) in hybrid crosses. Using additional crosses and whole genome sequencing of sperm pools, we showed that TRD was limited to hybrid crosses and was not due to differences in sperm motility between M. m. musculus strains. Based on these results, we argue that TRD likely reflects additional incompatibilities that reduce hybrid embryonic viability. In some common inbred strains of mice, selection against deleterious interactions appears to have unexpectedly driven introgression at loci involved in epistatic hybrid incompatibilities. The highly variable genetic basis to F1 hybrid incompatibilities between closely related mouse lineages argues that a thorough dissection of reproductive isolation will require much more extensive sampling of natural variation than has been commonly utilized in mice and other model systems.

The genome and microbiome of a dikaryotic fungus (Inocybe terrigena, Inocybaceae) revealed by metagenomics.

Recent advances in molecular methods have increased our understanding of various fungal symbioses. However, little is known about genomic and microbiome features of most uncultured symbiotic fungal clades. Here, we analysed the genome and microbiome of Inocybaceae (Agaricales, Basidiomycota), a largely uncultured ectomycorrhizal clade known to form symbiotic associations with a wide variety of plant species. We used metagenomic sequencing and assembly of dikaryotic fruiting-body tissues from Inocybe terrigena (Fr.) Kuyper, to classify fungal and bacterial genomic sequences, and obtained a nearly complete fungal genome containing 93% of core eukaryotic genes. Comparative genomics reveals that I. terrigena is more similar to ectomycorrhizal and brown rot fungi than to white rot fungi. The reduction in lignin degradation capacity has been independent from and significantly faster than in closely related ectomycorrhizal clades supporting that ectomycorrhizal symbiosis evolved independently in Inocybe. The microbiome of I. terrigena fruiting-bodies includes bacteria with known symbiotic functions in other fungal and non-fungal host environments, suggesting potential symbiotic functions of these bacteria in fungal tissues regardless of habitat conditions. Our study demonstrates the usefulness of direct metagenomics analysis of fruiting-body tissues for characterizing fungal genomes and microbiome.

Know your farmer: Ancient origins and multiple independent domestications of ambrosia beetle fungal cultivars.

Bark and ambrosia beetles are highly specialized weevils (Curculionidae) that have established diverse symbioses with fungi, most often from the order Ophiostomatales (Ascomycota, Sordariomycetes). The two types of beetles are distinguished by their feeding habits and intimacy of interactions with their symbiotic fungi. The tree tissue diet of bark beetles is facilitated by fungi, while ambrosia beetles feed solely on fungi that they farm. The farming life history strategy requires domestication of a fungus, which the beetles consume as their sole food source. Ambrosia beetles in the subfamily Platypodinae originated in the mid-Cretaceous (119-88 Ma) and are the oldest known group of farming insects. However, attempts to resolve phylogenetic relationships and the timing of domestication events for fungal cultivars have been largely inconclusive. We sequenced the genomes of 12 ambrosia beetle fungal cultivars and bark beetle associates, including the devastating laurel wilt pathogen, Raffaelea lauricola, to estimate a robust phylogeny of the Ophiostomatales. We find evidence for contemporaneous diversification of the beetles and their associated fungi, followed by three independent domestication events of the ambrosia fungi genus Raffaelea. We estimate the first domestication of an Ophiostomatales fungus occurred ~86 Ma, 25 million years earlier than prior estimates and in close agreement with the estimated age of farming in the Platypodinae (96 Ma). Comparisons of the timing of fungal domestication events with the timing of beetle radiations support the hypothesis that the first large beetle radiations may have spread domesticated "ambrosia" fungi to other fungi-associated beetle groups, perhaps facilitating the evolution of new farming lineages.

Range expansion underlies historical introgressive hybridization in the Iberian hare.

Introgressive hybridization is an important and widespread evolutionary process, but the relative roles of neutral demography and natural selection in promoting massive introgression are difficult to assess and an important matter of debate. Hares from the Iberian Peninsula provide an appropriate system to study this question. In its northern range, the Iberian hare, Lepus granatensis, shows a northwards gradient of increasing mitochondrial DNA (mtDNA) introgression from the arctic/boreal L. timidus, which it presumably replaced after the last glacial maximum. Here, we asked whether a south-north expansion wave of L. granatensis into L. timidus territory could underlie mtDNA introgression, and whether nuclear genes interacting with mitochondria ("mitonuc" genes) were affected. We extended previous RNA-sequencing and produced a comprehensive annotated transcriptome assembly for L. granatensis. We then genotyped 100 discovered nuclear SNPs in 317 specimens spanning the species range. The distribution of allele frequencies across populations suggests a northwards range expansion, particularly in the region of mtDNA introgression. We found no correlation between variants at 39 mitonuc genes and mtDNA introgression frequency. Whether the nuclear and mitochondrial genomes coevolved will need a thorough investigation of the hundreds of mitonuc genes, but range expansion and species replacement likely promoted massive mtDNA introgression.

The Composite Regulatory Basis of the Large X-Effect in Mouse Speciation.

The disruption of meiotic sex chromosome inactivation (MSCI) has been proposed to be a major developmental mechanism underlying the rapid evolution of hybrid male sterility. We tested this idea by analyzing cell-specific gene expression across spermatogenesis in two lineages of house mice and their sterile and fertile reciprocal hybrids. We found pervasive disruption of sex chromosome gene expression in sterile hybrids at every stage of spermatogenesis. Failure of MSCI was developmentally preceded by increased silencing of autosomal genes, supporting the hypothesis that divergence at the hybrid incompatibility gene, Prdm9, results in increased rates of autosomal asynapsis which in turn triggers widespread silencing of unsynapsed chromatin. We also detected opposite patterns of postmeiotic overexpression or hyper-repression of the sex chromosomes in reciprocal hybrids, supporting the hypothesis that genomic conflict has driven functional divergence that leads to deleterious X-Y dosage imbalances in hybrids. Our developmental timeline also exposed more subtle patterns of mitotic misregulation on the X chromosome, a previously undocumented stage of spermatogenic disruption in this cross. These results indicate that multiple hybrid incompatibilities have converged on a common regulatory phenotype, the disrupted expression of the sex chromosomes during spermatogenesis. Collectively, these data reveal a composite regulatory basis to hybrid male sterility in mice that helps resolve the mechanistic underpinnings of the well-documented large X-effect in mice speciation. We propose that the inherent sensitivity of spermatogenesis to X-linked regulatory disruption has the potential to be a major driver of reproductive isolation in species with chromosomal sex determination.

Basidiomycete yeasts in the cortex of ascomycete macrolichens.

For over 140 years, lichens have been regarded as a symbiosis between a single fungus, usually an ascomycete, and a photosynthesizing partner. Other fungi have long been known to occur as occasional parasites or endophytes, but the one lichen-one fungus paradigm has seldom been questioned. Here we show that many common lichens are composed of the known ascomycete, the photosynthesizing partner, and, unexpectedly, specific basidiomycete yeasts. These yeasts are embedded in the cortex, and their abundance correlates with previously unexplained variations in phenotype. Basidiomycete lineages maintain close associations with specific lichen species over large geographical distances and have been found on six continents. The structurally important lichen cortex, long treated as a zone of differentiated ascomycete cells, appears to consistently contain two unrelated fungi.