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The date palm, Phoenix dactyliferahas 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. Genomes of ancient date palm seeds show that gene flow from P. The Saqqara date palm shares a close genetic affinity with North African date palm populations, and we find clear genomic admixture from both P. Molecular-clocks placed the divergence of P.
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. Elucidating the domestication history of major crops is thus an how to measure evolutionary relationships scientific challenge, which how to measure evolutionary relationships collaboration between scholars of archeology, anthropology, taxonomy, systematics, and genomics.
The widespread availability of high-throughput DNA sequencing has revolutionized the study of plant domestication history, leading to many unprecedented insights, such as the identification of crop progenitors Ling et al. The application what does mental break mean genomic approaches to crop wild relatives is also bringing new resources for crop improvement reviewed by Brozynska et al.
The date palm Phoenix dactylifera L. It seems likely that wild P. Archeological evidence, ancient texts, and iconographies all point to the use of date palms for millennia in North Africa, the Middle East, and as far as Pakistan Tengberg ; Gros-Balthazard and Flowers ; Gros-Balthazard, Baker, et al. The first evidence of date cultivation comes from the end of the fourth millennium B.
From the Gulf region, date palms appear to have been introduced into North Africa Gros-Balthazard et al. Population-genomic analyses of date palm cultivars and wild Phoenix species revealed extensive introgressive hybridization of the North African date palm with P. Although it is now clear that date palm evolution in North Africa how to measure evolutionary relationships been influenced by gene flow from P.
Although some genomic studies found distinct evidence of admixture from P. Phoenix dactylifera and P. We then used population genomic tests, molecular clocks models, and gene-flow-aware multispecies coalescence MSC approaches on plastid and nuclear genome-wide data sets to detect ancient gene flow and to provide a temporal framework for diversification and reticulated evolution in Phoenix.
The results imply that the genomic ancestry of the ancient Saqqara date palm can be traced to domesticated North African P. Archeological origin of the Saqqara leaf and authentication of ancient DNA. A Saqqaraa jar-stopper made of date palm leaflets excavation inventory numberKew Economic Botany Collection number B A similar object to the Saqqara specimen numberalso made of date palm leaflets thought to be a basket-lid and found in Saqqara.
D Age estimation of the Saqqara date palm leaf. The gray distributions on the X axis indicate the likelihood of possible ages of the Saqqara leaf. E DNA misincorporations for each nucleotide position in the Saqqara date palm leaf see supplementary fig. S1Supplementary Material online, for detailed comparisons. E Hope As expected from ssDNA libraries, nucleotide misincorporations C to Twhich are indicative of DNA damage, predominantly occurred toward both ends of the reads, and remained visible even after an uracil reduction procedure.
S1Supplementary Material onlineconsistent with sequencing data from similarly aged material Ramos-Madrigal et al. This provides a guarantee that our phylogenetic and population genomic analyses are unlikely to be biased by misincorporations in the Saqqara sample. To compare the outcome of our phylogenetic and population genomic analyses with results obtained by previous studies, our taxon sampling is almost identical to Gros-Balthazard et al.
This how to measure evolutionary relationships is entirely composed of North African cultivated date palms and two accessions of P. What is approach in social work P. Phylogenetic placement of the Saqqara specimen amongst Phoenix species. A Maximum likelihood analysis of whole plastome sequences showing the placement of the Saqqara specimen amongst Phoenix species accession numbers for each terminal are provided in supplementary file S2Supplementary Material online.
B Uncorrected P-distance split network produced how to measure evolutionary relationships nuclear positions shared by the Saqqara specimen and modern accessions Bootstrap values are provided in how to measure evolutionary relationships file S3Supplementary Material online. North African cultivars of P. D Individual of P. E Male inflorescence of P. F Individuals of P. G Individual of the sugar date palm P. Baker FSasha Barrow G. This approach better depicts relationships in the presence of reticulate evolution Bogarín et al.
The split network placed the Saqqara leaf in a group consisting of African and Asian individuals of P. The lower bootstrap support and short length of the edges connecting groups of individuals from P. To test these relationships further, we determined the genomic affiliation of the nuclear genome of the Saqqara sample to either North African or Asian modern P. Here, we implemented a model-free principal component Are sweet potato chips a healthy snack and a model-based clustering analysis using genotype likelihoods derived from the nuclear genomes of all accessions, the latter assuming two to eight ancestral populations.
We conducted genomic clustering analyses using as reference two different genomes of P. Regardless of the reference genome used, with four assumed ancestral populations, the Saqqara genome grouped with populations of P. North African individuals of P. S2Supplementary Material onlinethus supporting previous findings Flowers et al. When assuming five ancestral populations, P.
S2Supplementary Material online. Allele sharing between P. The PCA revealed similar results to those obtained from the model-based clustering analyses. Regardless of the reference genome used, the covariance matrices inferred from 27, to 36, filtered sites placed the Saqqara date palm genome closest to modern North African date palm individuals in a cluster made of accessions of P.
Genome ancestry of the Saqqara specimen. Structure analyses with population number K from 2 to 6 A and B show admixture amongst wild and cultivated date palm populations, including the Saqqara leaf, and closely related Phoenix species. The geographical origin of modern how to measure evolutionary relationships of P. How to measure evolutionary relationships cluster and delta likelihood values from K 1 to 8 are provided in supplementary figure S2Supplementary Material online.
The remaining individuals of P. To test whether alleles from P. S3Supplementary Material online. To account for the differences in sequencing coverage in modern individuals compared with the ancient genome, these topological tests were conducted using two approaches tailored to separately evaluate individuals i. Both approaches were also implemented using two reference genomes to account for potential sequence biases Günther and Nettelblad ; see Materials and Methods. Analyses considering individuals separately and populations regardless of the genome of reference gave similar results regarding the relatedness of the Saqqara leaf to the other taxa.
Introgression of the Saqqara leaf with modern individuals of Phoenix sylvestris and P. A Results of D-statistic analyses derived from nuclear genotype likelihoods GLs for the Saqqara date leaf amongst date palm P. Circles indicate the D value of each individual test whereas the dotted lines indicate the SD. The outcomes of all possible permutations conducted during the D-statistic test between all individuals sampled in this study are provided in supplementary tables S4 and S5 and figure S3Supplementary Material online.
B Three instances of D-statistic analyses for the Saqqara date leaf conducted amongst populations of date palms and closely related species using a contiguous reference genome supporting gene flow between P. The outcomes of all possible permutations between populations and of analyses conducted using a contiguous reference genome are provided in supplementary table S6Supplementary Material online.
Introgression tests between modern individuals and the Saqqara leaf involved the evaluation of 1, and 22, nucleotide sites, with an average of 67 and sites per analysis using highly fragmented and contiguous genome assemblies as reference, respectively supplementary tables S4 and S5Supplementary Material online. Although we found no signal of introgression from P. Introgression from P. Population tests using the highly fragmented reference genome evaluated 2, to bases, with an average of and sites per analysis considering polymorphic and nonpolymorphic sites in the outgroup, respectively supplementary tables S6 and S7Supplementary Material online.
In contrast, analyses based on the continuous reference genome assessed 3, to 1, sites, with an average of and sites per analysis considering polymorphic and nonpolymorphic sites in the outgroup, respectively supplementary tables S6 and S7Supplementary Material online. Altogether, the results from the population-level analyses were consistent with introgression analyses conducted at the individual level, regardless of the genome of reference employed, thus providing support for the occurrence of gene flow between the Saqqara leaf, P.
Here, when computing D Saqqara, P. In addition, when testing D Saqqara, P. Notably, how to measure evolutionary relationships introgression tests conducted between individuals and populations in few instances revealed positive values when computing D Saqqara, P. S3Supplementary Material onlinethus supporting the gene flow pattern between date palms, P atlantica and P. Lastly, inspection of allele sharing patterns derived from analyses conducted between modern individuals and populations on the highly fragmented and contiguous reference genomes revealed widespread introgressive signals between P.
In particular, our finding of introgression between modern individuals P. To obtain a time tree for Phoenix and further tease apart the signal of incomplete lineage sorting ILS from the introgressive relationships revealed by the D-statistics, we used three approaches: 1 the molecular-clock dating of plastid and nuclear genomic what does causal mean in literature sets; 2 the comparison of tree and quartet frequencies genome-wide and in scaffolds, and 3 an explicit statistical test of introgression based on ultrametric trees and DNA distance matrices.
The molecular how to measure evolutionary relationships what are the physiological effects of stress in the body performed in a framework allowing different regions of the genome to have different histories, thereby providing not only absolute ages of species divergences, but also ages for the potential gene flow events.
We then quantified tree and quartet frequencies because both ILS and introgression are known to lead to nuclear intragenomic tree incongruence Abbott et al. If the source of incongruence is ILS, we would generally expect a topology representing the true species relationships to occur in higher frequency, with alternative topologies to be recovered at lower and roughly equal frequencies Gante et al.
To the contrary, if tree incongruence is driven by gene flow a strong disequilibrium among the frequencies of alternative topologies is expected Gante et al. For the molecular-clock dating, we generated alignments of whole plastid genomes and 18 nuclear scaffolds derived from the contiguous reference genome for a set of 12 samples representing four species and the North African and Asian populations of P.
Because the analysis is computationally intensive, we fragmented the nuclear scaffold alignments and 19 separate analyses were performed: one for each scaffold allowing separate fragments to have different histories and one for the plastome representing a single linkage group. The plastid phylogeny showed North African individuals of P. S4 and table S8Supplementary Material online. In contrast, the nuclear Maximum Clade Credibility MCC trees obtained from the post-burnin posterior tree distributions revealed strongly supported conflicting topologies across scaffolds.
The most common topology among MCC trees, obtained from seven nuclear scaffolds with strong support, was the expected species topology P. Absolute times of divergence and intragenomic tree conflict in Phoenix. A Chronogram of Phoenix reflecting the species relationships supplementary fig. S5Supplementary Material online.
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