Repeated upslope biome shifts in Saxifraga during late-Cenozoic climate cooling.

Mountains are among the most biodiverse places on Earth, and plant lineages that inhabit them have some of the highest speciation rates ever recorded. Plant diversity within the alpine zone - the elevation above which trees cannot grow-contributes significantly to overall diversity within mountain systems, but the origins of alpine plant diversity are poorly understood. Here, we quantify the processes that generate alpine plant diversity and their changing dynamics through time in Saxifraga (Saxifragaceae), an angiosperm genus that occurs predominantly in mountain systems. We present a time-calibrated molecular phylogenetic tree for the genus that is inferred from 329 low-copy nuclear loci and incorporates 73% (407) of known species. We show that upslope biome shifts into the alpine zone are considerably more prevalent than dispersal of alpine specialists between regions, and that the rate of upslope biome shifts increased markedly in the last 5 Myr, a timeframe concordant with a cooling and fluctuating climate that is likely to have increased the extent of the alpine zone. Furthermore, alpine zone specialists have lower speciation rates than generalists that occur inside and outside the alpine zone, and major speciation rate increases within Saxifraga significantly pre-date increased rates of upslope biome shifts. Specialisation to the alpine zone is not therefore associated with speciation rate increases. Taken together, this study presents a quantified and broad scale perspective of processes underpinning alpine plant diversity.

Neophytes may promote hybridization and adaptations to a changing planet.

Human activities erode geographic barriers, facilitating hybridization among previously isolated taxa. However, limited empirical research exists on the consequences of introduced species (neophytes) for hybridization and subsequent evolutionary outcomes. To address this knowledge gap, we employed a macroecological approach. First, we examined the spatial and phylogenetic overlap between neophytes and hybrids by integrating the Plants of the World Online database with the Global Naturalized Alien Flora database. Second, leveraging the largest dated plant phylogeny available, we compared diversification rates between genera containing hybrids and neophytes versus those without. Third, focusing on the extensively studied hybrid flora of Britain, we studied the spatial distributions of hybrids in relation to neophyte and native parents, assessing potential adaptations to anthropogenic disturbances and impacts on native species. Overall, our findings highlight positive ties between contemporary biodiversity redistribution and hybridization. Spatially (across countries) and phylogenetically (across genera), neophyte incidence was positively associated with hybrid incidence. Genera comprising both hybrids and neophytes displayed significantly higher diversification rates. Neophyte hybrids primarily occupied areas with a higher human footprint, with limited evidence of hybrids threatening native species throughout their range in more natural habitats. These results challenge the notion that species naturalizations and hybridizations exclusively yield negative outcomes for biodiversity. While it is conceivable that anthropogenic hybridization may facilitate recombination of genetic variation and contribute to conserving genetic diversity in disturbed environments, further research is needed to fully understand these processes.

Evolution of an Apomixis-Specific Allele Class in Supernumerary Chromatin of Apomictic Boechera.

Asexual reproduction through seeds in plants (i.e., apomixis) is a heritable trait, and apomixis- linked loci have been identified in multiple species. However, direct identification of genomic elements is typically hindered as apomixis-linked loci and are commonly found in recombination-suppressed and repetitive regions. Heterochromatinized elements, such as B chromosomes and other supernumerary chromosomal DNA fragments have long been known to be associated with asexuality in both plants and animals and are prime candidate regions for the evolution of multiple apomixis factors controlling the individual elements of apomixis. Here, we examined molecular evolution, gene regulation, and chromosomal location of a male apomeiosis factor (UPG2), a long noncoding RNA gene, in sexual and apomictic Boechera with and without male apomeiosis (i.e., balanced and unbalanced apomicts). We revealed the origin of the gene in the apomixis genome on an apomixis-specific, supernumerary heterochromatic Boechera chromosome (Boe1). The UPG2 is active in the tapetum at male meiosis. We found allele classes specific to apomictic and sexual Boechera accessions and a third class that shares the features of both and points to a convergent transition state. Sex alleles are found only in some of the sexual accessions and have higher nucleotide divergence and lower transcriptional activity compared to apo alleles. These data demonstrate selective pressure to maintain the function of UPG2 for unreduced pollen formation in apomicts as the occasional transmission of the allele from unbalanced apomicts into sexual organisms that lead to pseudogenization and functional decay of copies in sexual organisms.

Exploiting High-Throughput Indoor Phenotyping to Characterize the Founders of a Structured B. napus Breeding Population.

Phenotyping is considered a significant bottleneck impeding fast and efficient crop improvement. Similar to many crops, Brassica napus, an internationally important oilseed crop, suffers from low genetic diversity, and will require exploitation of diverse genetic resources to develop locally adapted, high yielding and stress resistant cultivars. A pilot study was completed to assess the feasibility of using indoor high-throughput phenotyping (HTP), semi-automated image processing, and machine learning to capture the phenotypic diversity of agronomically important traits in a diverse B. napus breeding population, SKBnNAM, introduced here for the first time. The experiment comprised 50 spring-type B. napus lines, grown and phenotyped in six replicates under two treatment conditions (control and drought) over 38 days in a LemnaTec Scanalyzer 3D facility. Growth traits including plant height, width, projected leaf area, and estimated biovolume were extracted and derived through processing of RGB and NIR images. Anthesis was automatically and accurately scored (97% accuracy) and the number of flowers per plant and day was approximated alongside relevant canopy traits (width, angle). Further, supervised machine learning was used to predict the total number of raceme branches from flower attributes with 91% accuracy (linear regression and Huber regression algorithms) and to identify mild drought stress, a complex trait which typically has to be empirically scored (0.85 area under the receiver operating characteristic curve, random forest classifier algorithm). The study demonstrates the potential of HTP, image processing and computer vision for effective characterization of agronomic trait diversity in B. napus, although limitations of the platform did create significant variation that limited the utility of the data. However, the results underscore the value of machine learning for phenotyping studies, particularly for complex traits such as drought stress resistance.

Latent Space Phenotyping: Automatic Image-Based Phenotyping for Treatment Studies.

Association mapping studies have enabled researchers to identify candidate loci for many important environmental tolerance factors, including agronomically relevant tolerance traits in plants. However, traditional genome-by-environment studies such as these require a phenotyping pipeline which is capable of accurately measuring stress responses, typically in an automated high-throughput context using image processing. In this work, we present Latent Space Phenotyping (LSP), a novel phenotyping method which is able to automatically detect and quantify response-to-treatment directly from images. We demonstrate example applications using data from an interspecific cross of the model C4 grass Setaria, a diversity panel of sorghum (S. bicolor), and the founder panel for a nested association mapping population of canola (Brassica napus L.). Using two synthetically generated image datasets, we then show that LSP is able to successfully recover the simulated QTL in both simple and complex synthetic imagery. We propose LSP as an alternative to traditional image analysis methods for phenotyping, enabling the phenotyping of arbitrary and potentially complex response traits without the need for engineering-complicated image-processing pipelines.

Complex patterns of differentiation and gene flow underly the divergence of aposematic phenotypes in Oophaga poison frogs.

Hybridization and introgression can have complex consequences for both species evolution and conservation. Here, we investigated the origin and characteristics of a putative hybrid zone between two South American poison dart frog species, Oophaga anchicayensis and the critically endangered Oophaga lehmanni, which are heavily sought after on the illegal pet market. Using a combination of phenotypic (49 traits) and genomic (ddRADseq) data, we found that the putative hybrids are morphologically distinct from their parental species and confirmed genomic signatures of admixture in these populations. Several lines of evidence (hybrid indices, interspecific hybrid heterozygosity, genomic clines, comparisons with simulated hybrids and demographic modelling) support the conclusion that these populations are not comprised of early-generation hybrids and thus, they probably did not arise as a result of illegal translocations associated with wildlife trafficking. Instead, they probably represent an independent lineage which has persisted through isolation and has only relatively recently re-established gene flow with both parental species. Furthermore, we detected signals of differential introgression from parental species into these hybrid populations which suggest relaxed stabilizing selection on these aposematic colour morphs, potentially via context-dependent female choice. These populations thus provide a fascinating window into the role of hybridization, isolation and female choice in the diversification of South American poison dart frogs. In addition, our results underline the importance of landscape conservation measures to protect, not only known localities of nominal species, but also the phenotypic and genomic variation harbored by admixed lineages which represent crucial repositories for the impressive diversity in this system.