Molecular Clocks and Archeogenomics of a Late Period Egyptian Date Palm Leaf Reveal Introgression from Wild Relatives and Add Timestamps on the Domestication.

The date palm, Phoenix dactylifera, has been a cornerstone of Middle Eastern and North African agriculture for millennia. It was first domesticated in the Persian Gulf, and its evolution appears to have been influenced by gene flow from two wild relatives, P. theophrasti, currently restricted to Crete and Turkey, and P. sylvestris, widespread from Bangladesh to the West Himalayas. Genomes of ancient date palm seeds show that gene flow from P. theophrasti to P. dactylifera may have occurred by ∼2,200 years ago, but traces of P. sylvestris could not be detected. We here integrate archeogenomics of a ∼2,100-year-old P. dactylifera leaf from Saqqara (Egypt), molecular-clock dating, and coalescence approaches with population genomic tests, to probe the hybridization between the date palm and its two closest relatives and provide minimum and maximum timestamps for its reticulated evolution. The Saqqara date palm shares a close genetic affinity with North African date palm populations, and we find clear genomic admixture from both P. theophrasti, and P. sylvestris, indicating that both had contributed to the date palm genome by 2,100 years ago. Molecular-clocks placed the divergence of P. theophrasti from P. dactylifera/P. sylvestris and that of P. dactylifera from P. sylvestris in the Upper Miocene, but strongly supported, conflicting topologies point to older gene flow between P. theophrasti and P. dactylifera, and P. sylvestris and P. dactylifera. Our work highlights the ancient hybrid origin of the date palms, and prompts the investigation of the functional significance of genetic material introgressed from both close relatives, which in turn could prove useful for modern date palm breeding.

The ecology of palm genomes: repeat-associated genome size expansion is constrained by aridity.

Genome size varies 2400-fold across plants, influencing their evolution through changes in cell size and cell division rates which impact plants' environmental stress tolerance. Repetitive element expansion explains much genome size diversity, and the processes structuring repeat 'communities' are analogous to those structuring ecological communities. However, which environmental stressors influence repeat community dynamics has not yet been examined from an ecological perspective. We measured genome size and leveraged climatic data for 91% of genera within the ecologically diverse palm family (Arecaceae). We then generated genomic repeat profiles for 141 palm species, and analysed repeats using phylogenetically informed linear models to explore relationships between repeat dynamics and environmental factors. We show that palm genome size and repeat 'community' composition are best explained by aridity. Specifically, Ty3-gypsy and TIR elements were more abundant in palm species from wetter environments, which generally had larger genomes, suggesting amplification. By contrast, Ty1-copia and LINE elements were more abundant in drier environments. Our results suggest that water stress inhibits repeat expansion through selection on upper genome size limits. However, elements that may associate with stress-response genes (e.g. Ty1-copia) have amplified in arid-adapted palm species. Overall, we provide novel evidence of climate influencing the assembly of repeat 'communities'.

A robust phylogenomic framework for the calamoid palms.

Well-supported phylogenies are a prerequisite for the study of the evolution and diversity of life on earth. The subfamily Calamoideae accounts for more than one fifth of the palm family (Arecaceae), occurs in tropical rainforests across the world, and supports a billion-dollar industry in rattan products. It contains ca. 550 species in 17 genera, 10 subtribes and three tribes, but their phylogenetic relationships remain insufficiently understood. Here, we sequenced almost one thousand nuclear genomic regions for 75 systematically selected Calamoideae, representing the taxonomic diversity within all calamoid genera. Our phylogenomic analyses resolved a maximally supported phylogenetic backbone for the Calamoideae, including several higher-level relationships not previously inferred. In-depth analysis revealed low gene tree conflict for the backbone but complex deep evolutionary histories within several subtribes. Overall, our phylogenomic framework sheds new light on the evolution of palms and provides a robust foundation for future comparative studies, such as taxonomy, systematics, biogeography, and macroevolutionary research.

Hundreds of nuclear and plastid loci yield novel insights into orchid relationships.

PREMISE: The inference of evolutionary relationships in the species-rich family Orchidaceae has hitherto relied heavily on plastid DNA sequences and limited taxon sampling. Previous studies have provided a robust plastid phylogenetic framework, which was used to classify orchids and investigate the drivers of orchid diversification. However, the extent to which phylogenetic inference based on the plastid genome is congruent with the nuclear genome has been only poorly assessed. METHODS: We inferred higher-level phylogenetic relationships of orchids based on likelihood and ASTRAL analyses of 294 low-copy nuclear genes sequenced using the Angiosperms353 universal probe set for 75 species (representing 69 genera, 16 tribes, 24 subtribes) and a concatenated analysis of 78 plastid genes for 264 species (117 genera, 18 tribes, 28 subtribes). We compared phylogenetic informativeness and support for the nuclear and plastid phylogenetic hypotheses. RESULTS: Phylogenetic inference using nuclear data sets provides well-supported orchid relationships that are highly congruent between analyses. Comparisons of nuclear gene trees and a plastid supermatrix tree showed that the trees are mostly congruent, but revealed instances of strongly supported phylogenetic incongruence in both shallow and deep time. The phylogenetic informativeness of individual Angiosperms353 genes is in general better than that of most plastid genes. CONCLUSIONS: Our study provides the first robust nuclear phylogenomic framework for Orchidaceae and an assessment of intragenomic nuclear discordance, plastid-nuclear tree incongruence, and phylogenetic informativeness across the family. Our results also demonstrate what has long been known but rarely thoroughly documented: nuclear and plastid phylogenetic trees can contain strongly supported discordances, and this incongruence must be reconciled prior to interpretation in evolutionary studies, such as taxonomy, biogeography, and character evolution.

Introgression across evolutionary scales suggests reticulation contributes to Amazonian tree diversity.

Hybridization has the potential to generate or homogenize biodiversity and is a particularly common phenomenon in plants, with an estimated 25% of plant species undergoing interspecific gene flow. However, hybridization in Amazonia's megadiverse tree flora was assumed to be extremely rare despite extensive sympatry between closely related species, and its role in diversification remains enigmatic because it has not yet been examined empirically. Using members of a dominant Amazonian tree family (Brownea, Fabaceae) as a model to address this knowledge gap, our study recovered extensive evidence of hybridization among multiple lineages across phylogenetic scales. More specifically, using targeted sequence capture our results uncovered several historical introgression events between Brownea lineages and indicated that gene tree incongruence in Brownea is best explained by reticulation, rather than solely by incomplete lineage sorting. Furthermore, investigation of recent hybridization using ~19,000 ddRAD loci recovered a high degree of shared variation between two Brownea species that co-occur in the Ecuadorian Amazon. Our analyses also showed that these sympatric lineages exhibit homogeneous rates of introgression among loci relative to the genome-wide average, implying a lack of selection against hybrid genotypes and persistent hybridization. Our results demonstrate that gene flow between multiple Amazonian tree species has occurred across temporal scales, and contrasts with the prevailing view of hybridization's rarity in Amazonia. Overall, our results provide novel evidence that reticulate evolution influenced diversification in part of the Amazonian tree flora, which is the most diverse on Earth.

Resolving relationships in an exceedingly young Neotropical orchid lineage using Genotyping-by-sequencing data.

Poor morphological and molecular differentiation in recently diversified lineages is a widespread phenomenon in plants. Phylogenetic relationships within such species complexes are often difficult to resolve because of the low variability in traditional molecular loci. Furthermore, biological phenomena responsible for topological incongruence such as Incomplete Lineage Sorting (ILS) and hybridisation complicate the resolution of phylogenetic relationships among closely related taxa. In this study, we employ a Genotyping-by-sequencing (GBS) approach to disentangle evolutionary relationships within a species complex belonging to the Neotropical orchid genus Cycnoches. This complex includes seven taxa distributed through Central America and the Colombian Chocó, and is nested within a clade estimated to have first diversified in the early Quaternary. Previous phylogenies inferred from few loci failed to provide support for internal relationships within the complex. Our Neighbour-net and coalescent-based analyses inferred from ca. 13,000 GBS loci obtained from 31 individuals belonging to six of the seven traditionally accepted Cycnoches taxa provided a robust phylogeny for this group. The genus Cycnoches includes three main clades that are further supported by morphological traits and geographic distributions. Similarly, a topology reconstructed through maximum likelihood (ML) inference of concatenated GBS loci produced results that are comparable with those reconstructed through coalescence and network-based methods. Our comparative phylogenetic informativeness analyses suggest that the low support evident in the ML phylogeny might be attributed to the abundance of uninformative GBS loci, which can account for up to 50% of the total number of loci recovered. The phylogenomic framework provided here, as well as morphological evidence and geographical patterns, suggest that the six entities previously thought to be different species or subspecies might actually represent only three distinct segregates. We further discuss the limited phylogenetic informativeness found in our GBS approach and its utility to disentangle relationships within recent and rapidly evolving species complexes. Our study is the first to demonstrate the utility of GBS data to reconstruct relationships within young (~2 Ma) Neotropical plant clades, opening new avenues for studies of species complexes that populate the species-rich orchid family.

Australasian orchid biogeography at continental scale: Molecular phylogenetic insights from the Sun Orchids (Thelymitra, Orchidaceae).

Australia harbours a rich and highly endemic orchid flora, with c. 90% of species endemic to the country. Despite that, the biogeographic history of Australasian orchid lineages is only poorly understood. Here we examined evolutionary relationships and the spatio-temporal evolution of the sun orchids (Thelymitra, 119 species), which display disjunct distribution patterns frequently found in Australasian orchid lineages. Phylogenetic analyses were conducted based on one nuclear (ITS) and three plastid markers (matK, psbJ-petA, ycf1) using Maximum Likelihood and Bayesian inference. Divergence time estimations were carried out with a relaxed molecular clock in a Bayesian framework. Ancestral ranges were estimated using the dispersal-extinction-cladogenesis model and an area coding based on major disjunctions. The phylogenetic analyses clarified intergeneric relationships within Thelymitrinae, with Epiblema being sister to Thelymitra plus Calochilus, both of which were well-supported. Within Thelymitra, eight major and several minor clades were retrieved in the nuclear and plastid phylogenetic reconstructions. Five major clades corresponded to species complexes previously recognized based on morphological characters, whereas other previously recognized species groups were found to be paraphyletic. Conflicting signals between the nuclear and plastid phylogenetic reconstructions provided support for hybridization and plastid capture events both in the deeper evolutionary history of the genus and more recently. Divergence time estimation placed the origin of Thelymitra in the late Miocene (c. 10.8 Ma) and the origin of the majority of the main clades within Thelymitra during the late Pliocene and early Pleistocene, with the majority of extant species arising during the Pleistocene. Ancestral range reconstruction revealed that the early diversification of the genus in the late Miocene and Pliocene took place predominantly in southwest Australia, where most species with highly restricted distributional ranges occur. Several long-distance dispersal events eastwards across the Nullarbor Plain were inferred, recurrently resulting in lineage divergence within the genus. The predominant eastwards direction of long-distance dispersal events in Thelymitra highlights the importance of the prevailing westerly winds in the Southern Hemisphere for the present-day distribution of the genus, giving rise to the Thelymitra floras of Tasmania, New Zealand and New Caledonia, which were inferred to be of comparatively recent origin.

Is Amazonia a 'museum' for Neotropical trees? The evolution of the Brownea clade (Detarioideae, Leguminosae).

The flora of the Neotropics is unmatched in its diversity, however the mechanisms by which diversity has accumulated are debated and largely unclear. The Brownea clade (Leguminosae) is a characteristic component of the Neotropical flora, and the species within it are diverse in their floral morphology, attracting a wide variety of pollinators. This investigation aimed to estimate species divergence times and infer relationships within the group, in order to test whether the Brownea clade followed the 'cradle' or 'museum' model of diversification, i.e. whether species evolved rapidly over a short time period, or gradually over many millions of years. We also aimed to trace the spatio-temporal evolution of the clade by estimating ancestral biogeographical patterns in the group. We used BEAST to build a dated phylogeny of 73 Brownea clade species using three molecular markers (ITS, trnK and psbA-trnH), resulting in well-resolved phylogenetic relationships within the clade, as well as robust divergence time estimates from which we inferred diversification rates and ancestral biogeography. Our analyses revealed an Eocene origin for the group, after which the majority of diversification happened in Amazonia during the Miocene, most likely concurrent with climatic and geological changes caused by the rise of the Andes. We found no shifts in diversification rate over time, suggesting a gradual accumulation of lineages with low extinction rates. These results may help to understand why Amazonia is host to the highest diversity of tree species on Earth.

Why Do Some Lineages Radiate While Others Do Not? Perspectives for Future Research on Adaptive Radiations.

Understanding the processes that drive phenotypic diversification and underpin speciation is key to elucidating how biodiversity has evolved. Although these processes have been studied across a wide array of clades, adaptive radiations (ARs), which are systems with multiple closely related species and broad phenotypic diversity, have been particularly fruitful for teasing apart the factors that drive and constrain diversification. As such, ARs have become popular candidate study systems for determining the extent to which ecological features, including aspects of organisms and the environment, and inter- and intraspecific interactions, led to evolutionary diversification. Despite substantial past empirical and theoretical work, understanding mechanistically how ARs evolve remains a major challenge. Here, we highlight a number of understudied components of the environment and of lineages themselves, which may help further our understanding of speciation and AR. We also outline some substantial remaining challenges to achieving a detailed understanding of adaptation, speciation, and the role of ecology in these processes. These major challenges include identifying factors that have a causative impact in promoting or constraining ARs, gaining a more holistic understanding of features of organisms and their environment that interact resulting in adaptation and speciation, and understanding whether the role of these organismal and environmental features varies throughout the radiation process. We conclude by providing perspectives on how future investigations into the AR process can overcome these challenges, allowing us to glean mechanistic insights into adaptation and speciation.

The genome sequence of the tree of heaven, Ailanthus altissima (Mill.) Swingle, 1916.

We present a genome assembly from an individual Ailanthus altissima (tree of heaven; Streptophyta; Magnoliopsida; Sapindales; Simaroubaceae). The genome sequence is 939 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules. The mitochondrial and plastid genome assemblies are 661.1 kilobases and 161.1 kilobases long, respectively.