Circadian clock- and temperature-associated genes contribute to overall genomic differentiation along elevation in lichenized fungi.

Circadian regulation is linked to local environmental adaptation, and many species with broad climatic niches display variation in circadian genes. Here, we hypothesize that lichenizing fungi occupying different climate zones tune their metabolism to local environmental conditions with the help of their circadian systems. We study two species of the genus Umbilicaria occupying similar climatic niches (Mediterranean and the cold temperate) in different continents. Using homology to Neurospora crassa genes, we identify gene sets associated with circadian rhythms (11 core, 39 peripheral genes) as well as temperature response (37 genes). Nucleotide diversity of these genes is significantly correlated with mean annual temperature, minimum temperature of the coldest month and mean temperature of the coldest quarter. Furthermore, we identify altitudinal clines in allele frequencies in several non-synonymous substitutions in core clock components, for example, white collar-like, frh-like and various ccg-like genes. A dN/dS approach revealed a few significant peripheral clock- and temperature-associated genes (e.g. ras-1-like, gna-1-like) that may play a role in fine-tuning the circadian clock and temperature-response machinery. An analysis of allele frequency changes demonstrated the strongest evidence for differentiation above the genomic background in the clock-associated genes in U. pustulata. These results highlight the likely relevance of the circadian clock in environmental adaptation, particularly frost tolerance, of lichens. Whether or not the fungal clock modulates the symbiotic interaction within the lichen consortium remains to be investigated. We corroborate the finding of genetic variation in clock components along altitude-not only latitude-as has been reported in other species.

Pericentromeric recombination suppression and the 'large X effect' in plants.

X chromosome was reported to be a major contributor to isolation between closely related species-the 'large X' effect (LXE). The causes of LXE are not clear, but the leading theory is that it is caused by recessive species incompatibilities exposed in the phenotype due to the hemizygosity of X-linked genes in the heterogametic sex. However, the LXE was also reported in species with relatively recently evolved sex chromosomes where Y chromosome is not completely degenerate and X-linked genes are not hemizygous, such as the plant Silene latifolia. Recent genome sequencing and detailed genetic mapping in this species revealed a massive (> 330 Mb) non- or rarely-recombining pericentromeric region on the X chromosome (Xpr) that comprises ~ 90% of the chromosome and over 13% of the entire genome. If any of the Xpr genes are involved in species incompatibilities, this would oppose interspecific gene flow for other genes tightly linked in the Xpr. Here we test the hypothesis that the previously reported LXE in S. latifolia is caused by the lack of recombination on most of the X chromosome. Based on genome-wide analysis of DNA polymorphism and gene expression in S. latifolia and its close cross-compatible relative S. dioica, we report that the rarely-recombining regions represent a significant barrier for interspecific gene flow. We found little evidence for any additional factors contributing to the LXE, suggesting that extensive pericentromeric recombination suppression on the X-chromosome is the major if not the only cause of the LXE in S. latifolia and S. dioica.

The role of recombination landscape in species hybridisation and speciation.

It is now well recognised that closely related species can hybridize and exchange genetic material, which may promote or oppose adaptation and speciation. In some cases, interspecific hybridisation is very common, making it surprising that species identity is preserved despite active gene exchange. The genomes of most eukaryotic species are highly heterogeneous with regard to gene density, abundance of repetitive DNA, chromatin compactisation etc, which can make certain genomic regions more prone or more resistant to introgression of genetic material from other species. Heterogeneity in local recombination rate underpins many of the observed patterns across the genome (e.g. actively recombining regions are typically gene rich and depleted for repetitive DNA) and it can strongly affect the permeability of genomic regions to interspecific introgression. The larger the region lacking recombination, the higher the chance for the presence of species incompatibility gene(s) in that region, making the entire non- or rarely recombining block impermeable to interspecific introgression. Large plant genomes tend to have highly heterogeneous recombination landscape, with recombination frequently occurring at the ends of the chromosomes and central regions lacking recombination. In this paper we review the relationship between recombination and introgression in plants and argue that large rarely recombining regions likely play a major role in preserving species identity in actively hybridising plant species.

Rapid evolution of hybrid breakdown following recent divergence with gene flow in Senecio species on Mount Etna, Sicily.

How do nascent species evolve reproductive isolation during speciation with on-going gene flow? How do hybrid lineages become stabilised hybrid species? While commonly used genomic approaches provide an indirect way to identify species incompatibility factors, synthetic hybrids generated from interspecific crosses allow direct pinpointing of phenotypic traits involved in incompatibilities and the traits that are potentially adaptive in hybrid species. Here we report the analysis of phenotypic variation and hybrid breakdown in crosses between closely-related Senecio aethnensis and S. chrysanthemifolius, and their homoploid hybrid species, S. squalidus. The two former species represent a likely case of recent (<200 ky) speciation with gene flow driven by adaptation to contrasting conditions of high- and low-elevations on Mount Etna, Sicily. As these species form viable and fertile hybrids, it remains unclear whether they have started to evolve reproductive incompatibility. Our analysis represents the first study of phenotypic variation and hybrid breakdown involving multiple Senecio hybrid families. It revealed wide range of variation in multiple traits, including the traits previously unrecorded in synthetic hybrids. Leaf shape, highly distinct between S. aethnensis and S. chrysanthemifolius, was extremely variable in F2 hybrids, but more consistent in S. squalidus. Our study demonstrates that interspecific incompatibilities can evolve rapidly despite on-going gene flow between the species. Further work is necessary to understand the genetic bases of these incompatibilities and their role in speciation with gene flow.

The Role of Interspecific Hybridisation in Adaptation and Speciation: Insights From Studies in Senecio.

Hybridisation is well documented in many species, especially plants. Although hybrid populations might be short-lived and do not evolve into new lineages, hybridisaiton could lead to evolutionary novelty, promoting adaptation and speciation. The genus Senecio (Asteraceae) has been actively used to unravel the role of hybridisation in adaptation and speciation. In this article, we first briefly describe the process of hybridisation and the state of hybridisation research over the years. We then discuss various roles of hybridisation in plant adaptation and speciation illustrated with examples from different Senecio species, but also mention other groups of organisms whenever necessary. In particular, we focus on the genomic and transcriptomic consequences of hybridisation, as well as the ecological and physiological aspects from the hybrids' point of view. Overall, this article aims to showcase the roles of hybridisation in speciation and adaptation, and the research potential of Senecio, which is part of the ecologically and economically important family, Asteraceae.

Multi-level patterns of genetic structure and isolation by distance in the widespread plant Mimulus guttatus.

An understanding of genetic structure is essential for answering many questions in population genetics. However, complex population dynamics and scale-dependent processes can make it difficult to detect if there are distinct genetic clusters present in natural populations. Inferring discrete population structure is particularly challenging in the presence of continuous genetic variation such as isolation by distance. Here, we use the plant species Mimulus guttatus as a case study for understanding genetic structure at three spatial scales. We use reduced-representation sequencing and marker-based genotyping to understand dispersal dynamics and to characterise genetic structure. Our results provide insight into the spatial scale of genetic structure in a widespread plant species, and demonstrate how dispersal affects spatial genetic variation at the local, regional, and range-wide scale. At a fine-spatial scale, we show dispersal is rampant with little evidence of spatial genetic structure within populations. At a regional-scale, we show continuous differentiation driven by isolation by distance over hundreds of kilometres, with broad geographic genetic clusters that span major barriers to dispersal. Across Western North America, we observe geographic genetic structure and the genetic signature of multiple postglacial recolonisation events, with historical gene flow linking isolated populations. Our genetic analyses show M. guttatus is highly dispersive and maintains large metapopulations with high intrapopulation variation. This high diversity and dispersal confounds the inference of genetic structure, with multi-level sampling and spatially-explicit analyses required to understand population history.

Life history evolution, species differences, and phenotypic plasticity in hemiparasitic eyebrights (Euphrasia).

PREMISE: Species delimitation in parasitic organisms is challenging because traits used to identify species are often plastic and vary depending on the host. Here, we use species from a recent radiation of generalist hemiparasitic Euphrasia to investigate trait variation and trait plasticity. We tested whether Euphrasia species show reliable trait differences, investigated whether these differences correspond to life history trade-offs between growth and reproduction, and quantified plasticity in response to host species. METHODS: Common garden experiments were used to evaluate trait differences between 11 Euphrasia taxa grown on a common host, document phenotypic plasticity when a single Euphrasia species is grown on eight different hosts, and relate observations to trait differences recorded in the wild. RESULTS: Euphrasia exhibited variation in life history strategies; some individuals transitioned rapidly to flowering at the expense of early season growth, while others invested in vegetative growth and delayed flowering. Life history differences were present between some species, though many related taxa lacked clear trait differences. Species differences were further blurred by phenotypic plasticity-many traits were plastic and changed with host type or between environments. CONCLUSIONS: Phenotypic plasticity in response to host and environment confounds species delimitation in Euphrasia. When grown in a common garden environment, some morphologically distinct taxa can be identified, though others represent morphologically similar shallow segregates. Trait differences present between some species and populations demonstrate the rapid evolution of distinct life history strategies in response to local ecological conditions.

Strong divergent selection at multiple loci in two closely related species of ragworts adapted to high and low elevations on Mount Etna.

Recently diverged species present particularly informative systems for studying speciation and maintenance of genetic divergence in the face of gene flow. We investigated speciation in two closely related Senecio species, S. aethnensis and S. chrysanthemifolius, which grow at high and low elevations, respectively, on Mount Etna, Sicily and form a hybrid zone at intermediate elevations. We used a newly generated genome-wide single nucleotide polymorphism (SNP) dataset from 192 individuals collected over 18 localities along an elevational gradient to reconstruct the likely history of speciation, identify highly differentiated SNPs, and estimate the strength of divergent selection. We found that speciation in this system involved heterogeneous and bidirectional gene flow along the genome, and species experienced marked population size changes in the past. Furthermore, we identified highly-differentiated SNPs between the species, some of which are located in genes potentially involved in ecological differences between species (such as photosynthesis and UV response). We analysed the shape of these SNPs' allele frequency clines along the elevational gradient. These clines show significantly variable coincidence and concordance, indicative of the presence of multifarious selective forces. Selection against hybrids is estimated to be very strong (0.16-0.78) and one of the highest reported in literature. The combination of strong cumulative selection across the genome and previously identified intrinsic incompatibilities probably work together to maintain the genetic and phenotypic differentiation between these species - pointing to the importance of considering both intrinsic and extrinsic factors when studying divergence and speciation.

Adaptive Evolution Is Common in Rapid Evolutionary Radiations.

One of the most long-standing and important mysteries in evolutionary biology is why biological diversity is so unevenly distributed across space and taxonomic lineages. Nowhere is this disparity more evident than in the multitude of rapid evolutionary radiations found on oceanic islands and mountain ranges across the globe [1-5]. The evolutionary processes driving these rapid diversification events remain unclear [6-8]. Recent genome-wide studies suggest that natural selection may be frequent during rapid evolutionary radiations, as inferred from work in cichlid fish [9], white-eye birds [10], new world lupins [11], and wild tomatoes [12]. However, whether frequent adaptive evolution is a general feature of rapid evolutionary radiations remains untested. Here we show that adaptive evolution is significantly more frequent in rapid evolutionary radiations compared to background levels in more slowly diversifying lineages. This result is consistent across a wide range of angiosperm lineages analyzed: 12 evolutionary radiations, which together comprise 1,377 described species, originating from some of the most biologically diverse systems on Earth. In addition, we find a significant negative correlation between population size and frequency of adaptive evolution in rapid evolutionary radiations. A possible explanation for this pattern is that more frequent adaptive evolution is at least partly driven by positive selection for advantageous mutations that compensate for the fixation of slightly deleterious mutations in smaller populations.

Repeated species radiations in the recent evolution of the key marine phytoplankton lineage Gephyrocapsa.

Phytoplankton account for nearly half of global primary productivity and strongly affect the global carbon cycle, yet little is known about the forces that drive the evolution of these keystone microscopic organisms. Here we combine morphometric data from the fossil record of the ubiquitous coccolithophore genus Gephyrocapsa with genomic analyses of extant species to assess the genetic processes underlying Pleistocene palaeontological patterns. We demonstrate that all modern diversity in Gephyrocapsa (including Emiliania huxleyi) originated in a rapid species radiation during the last 0.6 Ma, coincident with the latest of the three pulses of Gephyrocapsa diversification and extinction documented in the fossil record. Our evolutionary genetic analyses indicate that new species in this genus have formed in sympatry or parapatry, with occasional hybridisation between species. This sheds light on the mode of speciation during evolutionary radiation of marine phytoplankton and provides a model of how new plankton species form.