Synteny Identifies Reliable Orthologs for Phylogenomics and Comparative Genomics of the Brassicaceae

Large genomic data sets are becoming the new normal in phylogenetic research, but the identification of true orthologous genes and the exclusion of problematic paralogs is still challenging when applying commonly used sequencing methods such as target enrichment. Here, we compared conventional ortholog detection using OrthoFinder with ortholog detection through genomic synteny in a data set of 11 representative diploid Brassicaceae whole-genome sequences spanning the entire phylogenetic space. Then, we evaluated the resulting gene sets regarding gene number, functional annotation, and gene and species tree resolution. Finally, we used the syntenic gene sets for comparative genomics and ancestral genome analysis. The use of synteny resulted in considerably more orthologs and also allowed us to reliably identify paralogs. Surprisingly, we did not detect notable differences between species trees reconstructed from syntenic orthologs when compared with other gene sets, including the Angiosperms353 set and a Brassicaceae-specific target enrichment gene set. However, the synteny data set comprised a multitude of gene functions, strongly suggesting that this method of marker selection for phylogenomics is suitable for studies that value downstream gene function analysis, gene interaction, and network studies. Finally, we present the first ancestral genome reconstruction for the Core Brassicaceae which predating the Brassicaceae lineage diversification ∼25 million years ago

Lineage-specific adaptation to climate involves flowering time in North American Arabidopsis lyrata

Adaptation to local climatic conditions is commonly found within species, but whether it involves the same intraspecific genomic variants is unknown. We studied this question in North American Arabidopsis lyrata, whose current distribution is shaped by post‐glacial range expansion from two refugia, resulting in two distinct genetic clusters covering comparable climatic gradients. Using pooled whole‐genome sequence data of 41 outcrossing populations, we identified loci associated with three niche‐determining climatic variables in the two clusters and compared these outliers. Little evidence was found for parallelism in climate adaptation for single nucleotide polymorphisms (SNPs) and for genes with an accumulation of outlier SNPs. Significantly increased selection coefficients supported them as candidates of climate adaptation. However, the fraction of gene ontology (GO) terms shared between clusters was higher compared to outlier SNPs and outlier genes, suggesting that selection acts on similar pathways but not necessarily the same genes. Enriched GO terms involved responses to abiotic and biotic stress, circadian rhythm and development, with flower development and reproduction being among the most frequently detected. In line with GO enrichment, regulators of flowering time were detected as outlier genes. Our results suggest that while adaptation to environmental gradients on the genomic level are lineage‐specific in A. lyrata, similar biological processes seem to be involved. Differential loss of standing genetic variation, probably driven by genetic drift, can in part account for the lack of parallel evolution on the genomic level

What drives species’ distributions along elevational gradients? Macroecological and -evolutionary insights from Brassicaceae of the central Alps

Aim: Geographic distribution limits of organisms are often affected by climate, but little is known of how the impacts of climate evolve within sets of related taxa. Here we identified the climate variables most closely associated with low-elevation limits, optimal elevations, and high-elevation limits of plant species’ distributions and compared evolutionary lability of niche values predicting the three aspects of distribution best. Location: Central Alps. Time period: Current. Major taxa studied: The plant family Brassicaceae. Methods: We modelled the occurrence of 110 brassicaceous species in the central European Alps and used response curves of predicted occurrence on climatic variables to reveal those variables most strongly associated with elevational distribution. We produced a phylogeny of the species, applied phylogenetic comparative analysis and tested whether niche values predicting the low and high limits and the optimum of elevational distribution were similar among related taxa. Results: Upper limits were closely associated with the length of the vegetation season for the majority of species, while summer or spring temperatures were strongly allied with both the occurrence optimum and the lower limit. Furthermore, niche values predicting the upper limit and the optimum of elevational distribution were less conserved in contrast to niche values predicting the lower limit of distribution. Main conclusions: These results highlight constraints on adaptation at the warm end of the climate niche and may explain observed range retractions at warm range edges due to ongoing climate change.</p

Recent speciation associated with range expansion and a shift to self-fertilization in North American Arabidopsis

The main processes classically evoked for promoting reproductive isolation and speciation are geographic separation reducing gene flow among populations, divergent selection, and chance genomic change. In a case study, we present evidence that the additional factors of climate change, range expansion and a shift in mating towards inbreeding can initiate the processes leading to parapatric speciation. At the end of the last Pleistocene glaciation cycle, the North American plant Arabidopsis lyrata expanded its range and concomitantly lost its reproductive mode of outcrossing multiple times. We show that in one of the newly colonized areas, the self-fertilizing recolonization lineage of A. lyrata gave rise to selfing A. arenicola, which expanded its range to subarctic and arctic Canada and Greenland, while the parental species remained restricted to temperate North America. Despite the vast range expansion by the new species, mutational load did not increase, probably because of selfing and quasi-clonal selection. We conclude that such peripheral parapatric speciation combined with range expansion and inbreeding may be an important but so far overlooked mode of speciation

What drives species’ distributions along elevational gradients? Macroecological and ‐evolutionary insights from Brassicaceae of the central Alps

Aim Geographic distribution limits of organisms are often affected by climate, but little is known of how the impacts of climate evolve within sets of related taxa. Here we identified the climate variables most closely associated with low‐elevation limits, optimal elevations, and high‐elevation limits of plant species’ distributions and compared evolutionary lability of niche values predicting the three aspects of distribution best. Location Central Alps. Time period Current. Major taxa studied The plant family Brassicaceae. Methods We modelled the occurrence of 110 brassicaceous species in the central European Alps and used response curves of predicted occurrence on climatic variables to reveal those variables most strongly associated with elevational distribution. We produced a phylogeny of the species, applied phylogenetic comparative analysis and tested whether niche values predicting the low and high limits and the optimum of elevational distribution were similar among related taxa. Results Upper limits were closely associated with the length of the vegetation season for the majority of species, while summer or spring temperatures were strongly allied with both the occurrence optimum and the lower limit. Furthermore, niche values predicting the upper limit and the optimum of elevational distribution were less conserved in contrast to niche values predicting the lower limit of distribution. Main conclusions These results highlight constraints on adaptation at the warm end of the climate niche and may explain observed range retractions at warm range edges due to ongoing climate change

Genomic Blocks in Aethionema arabicum Support Arabideae as Next Diverging Clade in Brassicaceae

The tribe Aethionemeae is sister to all other crucifers, making it a crucial group for unraveling genome evolution and phylogenetic relationships within the crown group Brassicaceae. In this study, we extend the analysis of Brassicaceae genomic blocks (GBs) to Aethionema whereby we identified unique block boundaries shared only with the tribe Arabideae. This was achieved using bioinformatic methods to analyze synteny between the recently updated genome sequence of Aethionema arabicum and other high-quality Brassicaceae genome sequences. We show that compared to the largely conserved genomic structure of most non-polyploid Brassicaceae lineages, GBs are highly rearranged in Aethionema. Furthermore, we detected similarities between the genomes of Aethionema and Arabis alpina, in which also a high number of genomic rearrangements compared to those of other Brassicaceae was found. These similarities suggest that tribe Arabideae, a clade showing conflicting phylogenetic position between studies, may have diverged before diversification of the other major lineages, and highlight the potential of synteny information for phylogenetic inference.</p

The impact of chromosomal rearrangements in speciation: From micro- to macroevolution

Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics. While an important role for CRs in speciation has been suggested, evidence primarily stems from theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon pairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at a macroevolutionary level has been supported by associations between species diversity and rates of evolution of CRs across phylogenies, these findings are limited to a restricted range of CRs and taxa. Now that more broadly applicable and precise CR detection approaches have become available, we address the challenges in filling some of the conceptual and empirical gaps between micro- and macroevolutionary studies on the role of CRs in speciation. We synthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life

Parallel reduction in flowering time from de novo mutations enable evolutionary rescue in colonizing lineages

Understanding how populations adapt to abrupt environmental change is necessary to predict responses to future challenges, but identifying specific adaptive variants, quantifying their responses to selection and reconstructing their detailed histories is challenging in natural populations. Here, we use Arabidopsis from the Cape Verde Islands as a model to investigate the mechanisms of adaptation after a sudden shift to a more arid climate. We find genome-wide evidence of adaptation after a multivariate change in selection pressures. In particular, time to flowering is reduced in parallel across islands, substantially increasing fitness. This change is mediated by convergent de novo loss of function of two core flowering time genes: FRI on one island and FLC on the other. Evolutionary reconstructions reveal a case where expansion of the new populations coincided with the emergence and proliferation of these variants, consistent with models of rapid adaptation and evolutionary rescue

The Gynandropsis gynandra genome provides insights into whole-genome duplications and the evolution of C4 photosynthesis in Cleomaceae.

Gynandropsis gynandra (Cleomaceae) is a cosmopolitan leafy vegetable and medicinal plant, which has also been used as a model to study C4 photosynthesis due to its evolutionary proximity to C3 Arabidopsis (Arabidopsis thaliana). Here, we present the genome sequence of G. gynandra, anchored onto 17 main pseudomolecules with a total length of 740 Mb, an N50 of 42 Mb and 30,933 well-supported gene models. The G. gynandra genome and previously released genomes of C3 relatives in the Cleomaceae and Brassicaceae make an excellent model for studying the role of genome evolution in the transition from C3 to C4 photosynthesis. Our analyses revealed that G. gynandra and its C3 relative Tarenaya hassleriana shared a whole-genome duplication event (Gg-α), then an addition of a third genome (Th-α, +1×) took place in T. hassleriana but not in G. gynandra. Analysis of syntenic copy number of C4 photosynthesis-related gene families indicates that G. gynandra generally retained more duplicated copies of these genes than C3T. hassleriana, and also that the G. gynandra C4 genes might have been under positive selection pressure. Both whole-genome and single-gene duplication were found to contribute to the expansion of the aforementioned gene families in G. gynandra. Collectively, this study enhances our understanding of the polyploidy history, gene duplication and retention, as well as their impact on the evolution of C4 photosynthesis in Cleomaceae