Archaeogenomic analysis of Chesapeake Atlantic sturgeon illustrates shaping of its populations in recovery from severe overexploitation.

Atlantic sturgeon (Acipenser oxyrinchus ssp. oxyrinchus) has been a food resource in North America for millennia. However, industrial-scale fishing activities following the establishment of European colonies led to multiple collapses of sturgeon stocks, driving populations such as those in the Chesapeake area close to extinction. While recent conservation efforts have been successful in restoring census numbers, little is known regarding genomic consequences of the population bottleneck. Here, we characterize its effect on present-day population structuring and genomic diversity in James River populations. To establish a pre-collapse baseline, we collected genomic data from archaeological remains from Middle Woodland Maycock's Point (c. 200-900 CE), as well as Jamestown and Williamsburg colonial sites. Demographic analysis of recovered mitogenomes reveals a historical collapse in effective population size, also reflected in diminished present-day mitogenomic diversity and structure. We infer that James River fall- and spring-spawning populations likely took shape in recent years of population recovery, where genetic drift enhanced the degree of population structure. The mismatch of mitogenomic lineages to geographical-seasonal groupings implies that despite their homing instinct and differential adaptation manifested as season-specific behaviour, colonization of new rivers has been a key ecological strategy for Atlantic sturgeon over evolutionary timescales.

Morphometrics and Phylogenomics of Coca (Erythroxylum spp.) Illuminate Its Reticulate Evolution, With Implications for Taxonomy.

South American coca (Erythroxylum coca and E. novogranatense) has been a keystone crop for many Andean and Amazonian communities for at least 8,000 years. However, over the last half-century, global demand for its alkaloid cocaine has driven intensive agriculture of this plant and placed it in the center of armed conflict and deforestation. To monitor the changing landscape of coca plantations, the United Nations Office on Drugs and Crime collects annual data on their areas of cultivation. However, attempts to delineate areas in which different varieties are grown have failed due to limitations around identification. In the absence of flowers, identification relies on leaf morphology, yet the extent to which this is reflected in taxonomy is uncertain. Here, we analyze the consistency of the current naming system of coca and its four closest wild relatives (the "coca clade"), using morphometrics, phylogenomics, molecular clocks, and population genomics. We include name-bearing type specimens of coca's closest wild relatives E. gracilipes and E. cataractarum. Morphometrics of 342 digitized herbarium specimens show that leaf shape and size fail to reliably discriminate between species and varieties. However, the statistical analyses illuminate that rounder and more obovate leaves of certain varieties could be associated with the subtle domestication syndrome of coca. Our phylogenomic data indicate extensive gene flow involving E. gracilipes which, combined with morphometrics, supports E. gracilipes being retained as a single species. Establishing a robust evolutionary-taxonomic framework for the coca clade will facilitate the development of cost-effective genotyping methods to support reliable identification.

Phylogenomics and the rise of the angiosperms.

Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods1,2. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So far, the angiosperm tree of life has been determined primarily by means of analyses of the plastid genome3,4. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins5-7. However, the limited and biased sampling of both taxa and genomes undermines confidence in the tree and its implications. Here, we build the tree of life for almost 8,000 (about 60%) angiosperm genera using a standardized set of 353 nuclear genes8. This 15-fold increase in genus-level sampling relative to comparable nuclear studies9 provides a critical test of earlier results and brings notable change to key groups, especially in rosids, while substantiating many previously predicted relationships. Scaling this tree to time using 200 fossils, we discovered that early angiosperm evolution was characterized by high gene tree conflict and explosive diversification, giving rise to more than 80% of extant angiosperm orders. Steady diversification ensued through the remaining Mesozoic Era until rates resurged in the Cenozoic Era, concurrent with decreasing global temperatures and tightly linked with gene tree conflict. Taken together, our extensive sampling combined with advanced phylogenomic methods shows the deep history and full complexity in the evolution of a megadiverse clade.

The origin and speciation of orchids.

Orchids constitute one of the most spectacular radiations of flowering plants. However, their origin, spread across the globe, and hotspots of speciation remain uncertain due to the lack of an up-to-date phylogeographic analysis. We present a new Orchidaceae phylogeny based on combined high-throughput and Sanger sequencing data, covering all five subfamilies, 17/22 tribes, 40/49 subtribes, 285/736 genera, and c. 7% (1921) of the 29 524 accepted species, and use it to infer geographic range evolution, diversity, and speciation patterns by adding curated geographical distributions from the World Checklist of Vascular Plants. The orchids' most recent common ancestor is inferred to have lived in Late Cretaceous Laurasia. The modern range of Apostasioideae, which comprises two genera with 16 species from India to northern Australia, is interpreted as relictual, similar to that of numerous other groups that went extinct at higher latitudes following the global climate cooling during the Oligocene. Despite their ancient origin, modern orchid species diversity mainly originated over the last 5 Ma, with the highest speciation rates in Panama and Costa Rica. These results alter our understanding of the geographic origin of orchids, previously proposed as Australian, and pinpoint Central America as a region of recent, explosive speciation.

Museum Genomics Provide Evidence for Persistent Genetic Differentiation in a Threatened Seabird Species in the Western Atlantic.

Connectivity among wildlife populations facilitates exchange of genetic material between groups. Changes to historical connectivity patterns resulting from anthropogenic activities can therefore have negative consequences for genetic diversity, particularly for small or isolated populations. DNA obtained from museum specimens can enable direct comparison of temporal changes in connectivity among populations, which can aid in conservation planning and contribute to the understanding of population declines. However, museum DNA can be degraded and only available in low quantities, rendering it challenging for use in population genomic analyses. Applications of genomic methodologies such as targeted sequencing address this issue by enabling capture of shared variable sites, increasing quantity and quality of recovered genomic information. We used targeted sequencing of ultra-conserved Elements (UCEs) to evaluate potential changes in connectivity and genetic diversity of roseate terns (Sterna dougallii) with a breeding distribution in the northwestern Atlantic and the Caribbean. Both populations experienced range contractions and population declines due to anthropogenic activity in the 20th century, which has the potential to alter historical connectivity regimes. Instead, we found that the two populations were differentiated historically as well as contemporaneously, with little evidence of migration between them for either time period. We also found no evidence for temporal changes in genetic diversity, although these interpretations may have been limited due to sequencing artifacts caused by the degraded nature of the museum samples. Population structuring in migratory seabirds is typically reflective of low rates of divergence and high connectivity among geographically segregated subpopulations. Our contrasting results suggest the potential presence of ecological mechanisms driving population differentiation, and highlight the value of targeted sequencing on DNA derived from museum specimens to uncover long-term patterns of genetic differentiation in wildlife populations.

Revised Species Delimitation in the Giant Water Lily Genus Victoria (Nymphaeaceae) Confirms a New Species and Has Implications for Its Conservation.

Reliably documenting plant diversity is necessary to protect and sustainably benefit from it. At the heart of this documentation lie species concepts and the practical methods used to delimit taxa. Here, we apply a total-evidence, iterative methodology to delimit and document species in the South American genus Victoria (Nymphaeaceae). The systematics of Victoria has thus far been poorly characterized due to difficulty in attributing species identities to biological collections. This research gap stems from an absence of type material and biological collections, also the confused diagnosis of V. cruziana. With the goal of improving systematic knowledge of the genus, we compiled information from historical records, horticulture and geography and assembled a morphological dataset using citizen science and specimens from herbaria and living collections. Finally, we generated genomic data from a subset of these specimens. Morphological and geographical observations suggest four putative species, three of which are supported by nuclear population genomic and plastid phylogenomic inferences. We propose these three confirmed entities as robust species, where two correspond to the currently recognized V. amazonica and V. cruziana, the third being new to science, which we describe, diagnose and name here as V. boliviana Magdalena and L. T. Sm. Importantly, we identify new morphological and molecular characters which serve to distinguish the species and underpin their delimitations. Our study demonstrates how combining different types of character data into a heuristic, total-evidence approach can enhance the reliability with which biological diversity of morphologically challenging groups can be identified, documented and further studied.

Genome Sequencing of up to 6,000-Year-Old Citrullus Seeds Reveals Use of a Bitter-Fleshed Species Prior to Watermelon Domestication.

Iconographic evidence from Egypt suggests that watermelon pulp was consumed there as a dessert by 4,360 BP. Earlier archaeobotanical evidence comes from seeds from Neolithic settlements in Libya, but whether these were watermelons with sweet pulp or other forms is unknown. We generated genome sequences from 6,000- and 3,300-year-old seeds from Libya and Sudan, and from worldwide herbarium collections made between 1824 and 2019, and analyzed these data together with resequenced genomes from important germplasm collections for a total of 131 accessions. Phylogenomic and population-genomic analyses reveal that (1) much of the nuclear genome of both ancient seeds is traceable to West African seed-use "egusi-type" watermelon (Citrullus mucosospermus) rather than domesticated pulp-use watermelon (Citrullus lanatus ssp. vulgaris); (2) the 6,000-year-old watermelon likely had bitter pulp and greenish-white flesh as today found in C. mucosospermus, given alleles in the bitterness regulators ClBT and in the red color marker LYCB; and (3) both ancient genomes showed admixture from C. mucosospermus, C. lanatus ssp. cordophanus, C. lanatus ssp. vulgaris, and even South African Citrullus amarus, and evident introgression between the Libyan seed (UMB-6) and populations of C. lanatus. An unexpected new insight is that Citrullus appears to have initially been collected or cultivated for its seeds, not its flesh, consistent with seed damage patterns induced by human teeth in the oldest Libyan material.

Phylogenomic analysis points to a South American origin of Manihot and illuminates the primary gene pool of cassava.

The genus Manihot, with around 120 known species, is native to a wide range of habitats and regions in the tropical and subtropical Americas. Its high species richness and recent diversification only c. 6 million years ago have significantly complicated previous phylogenetic analyses. Several basic elements of Manihot evolutionary history therefore remain unresolved. Here, we conduct a comprehensive phylogenomic analysis of Manihot, focusing on exhaustive sampling of South American taxa. We find that two recently described species from northeast Brazil's Atlantic Forest were the earliest to diverge, strongly suggesting a South American common ancestor of Manihot. Ancestral state reconstruction indicates early Manihot diversification in dry forests, with numerous independent episodes of new habitat colonization, including into savannas and rainforests within South America. We identify the closest wild relatives to Manihot esculenta, including the crop cassava, and we quantify extensive wild introgression into the cassava gene pool from at least five wild species, including Manihot glaziovii, a species used widely in breeding programs. Finally, we show that this wild-to-crop introgression substantially shapes the mutation load in cassava. Our findings provide a detailed case study for neotropical evolutionary history in a diverse and widespread group, and a robust phylogenomic framework for future Manihot and cassava research.

A highly contiguous, scaffold-level nuclear genome assembly for the fever tree (Cinchona pubescens Vahl) as a novel resource for Rubiaceae research.

The Andean fever tree (Cinchona L.; Rubiaceae) is a source of bioactive quinine alkaloids used to treat malaria. C. pubescens Vahl is a valuable cash crop within its native range in northwestern South America, however, genomic resources are lacking. Here we provide the first highly contiguous and annotated nuclear and plastid genome assemblies using Oxford Nanopore PromethION-derived long-read and Illumina short-read data. Our nuclear genome assembly comprises 603 scaffolds with a total length of 904 Mbp (∼82% of the full genome based on a genome size of 1.1 Gbp/1C). Using a combination of de novo and reference-based transcriptome assemblies we annotated 72,305 coding sequences comprising 83% of the BUSCO gene set and 4.6% fragmented sequences. Using additional plastid and nuclear datasets we place C. pubescens in the Gentianales order. This first genomic resource for C. pubescens opens new research avenues, including the analysis of alkaloid biosynthesis in the fever tree.

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.

Population genomic structure of Eurasian and African foxtail millet landrace accessions inferred from genotyping-by-sequencing.

Foxtail millet [Setaria italica (L.) P. Beauv.] is the second most important millet species globally and is adapted to cultivation in diverse environments. Like its wild progenitor, green foxtail [S. viridis (L.) P. Beauv.], it is a model species for C4 photosynthetic pathways and stress tolerance genes in related bioenergy crops. We addressed questions regarding the evolution and spread of foxtail millet through a population genomic study of landraces from across its cultivated range in Europe, Asia, and Africa. We sought to determine population genomic structure and the relationship of domesticated lineages relative to green foxtail. Further, we aimed to identify genes involved in environmental stress tolerance that have undergone differential selection between geographical and genetic groups. Foxtail millet landrace accessions (n = 328) and green foxtail accessions (n = 12) were sequenced by genotyping-by-sequencing (GBS). After filtering, 5,677 single nucleotide polymorphisms (SNPs) were retained for the combined foxtail millet-green foxtail dataset and 5,020 for the foxtail millet dataset. We extended geographic coverage of green foxtail by including previously published GBS sequence tags, yielding a 4,515-SNP dataset for phylogenetic reconstruction. All foxtail millet samples were monophyletic relative to green foxtail, suggesting a single origin of foxtail millet, although no group of foxtail millet was clearly the most ancestral. Four genetic clusters were found within foxtail millet, each with a distinctive geographical distribution. These results, together with archaeobotanical evidence, suggest plausible routes of spread of foxtail millet. Selection scans identified nine candidate genes potentially involved in environmental adaptations, particularly to novel climates encountered, as domesticated foxtail millet spread to new altitudes and latitudes.

Multiproxy evidence highlights a complex evolutionary legacy of maize in South America.

Domesticated maize evolved from wild teosinte under human influences in Mexico beginning around 9000 years before the present (yr B.P.), traversed Central America by ~7500 yr B.P., and spread into South America by ~6500 yr B.P. Landrace and archaeological maize genomes from South America suggest that the ancestral population to South American maize was brought out of the domestication center in Mexico and became isolated from the wild teosinte gene pool before traits of domesticated maize were fixed. Deeply structured lineages then evolved within South America out of this partially domesticated progenitor population. Genomic, linguistic, archaeological, and paleoecological data suggest that the southwestern Amazon was a secondary improvement center for partially domesticated maize. Multiple waves of human-mediated dispersal are responsible for the diversity and biogeography of modern South American maize.