Molecular Phylogenetics and Evolution 140 (2019) 106601 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Plastid phylogenomics and biogeographic analysis support a trans-Tethyan T origin and rapid early radiation of Cornales in the Mid-Cretaceous ⁎ Chao-Nan Fua,b,c, Zhi-Qiong Moa,c, Jun-Bo Yangb, Xue-Jun Ged, De-Zhu Lia,b,c, , ⁎ ⁎ Qiu-Yun (Jenny) Xiange, , Lian-Ming Gaoa, a CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China b Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China c Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, Yunnan 650201, China d Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangdong 510650, China e Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USA ARTICLE INFO ABSTRACT Keywords: The Cornales is a relatively small but morphologically diverse order in the basal position of the Asterids clade. Previous Biogeography study hypothesized that the order might have undergone ancient rapid radiation during the Cretaceous when major Character coding angiosperm lineages were established. We conducted the phylogenomic analysis of Cornales using 81 plastid genome Cornales sequences with 67 newly generated in this study to test the hypothesis. This sampling represents all the families and 31 Plastid genome out of 48 genera in the order. Phylogenetic analyses were conducted using different datasets to examine the effects of Phylogenomics different coding positions and character coding methods. We further conducted divergence time, diversification rate, and biogeographic analyses to understand the early evolutionary history of Cornales in space and time. Our phylo- genetic analyses of four datasets (the amino acid characters, the 1st and 2nd codon positions of protein coding genes, nucleotide characters with degenerated coding method, and noncoding regions) resulted in a robust phylogeny con- gruent with results of previous studies, showing (((Cornaceae-Alangiaceae)-(Curtisiaceae-Grubbiaceae))-(((Nyssaceae- Davidiaceae)-Mastixiaceae)-((Hydrostachyaceae-(Hydrangeaceae-Loasaceae)))). Phylogenetic relationships within fa- milies were also well resolved. Conflicts in the placement of Hydrostachyaceae were found from analyses oftwo datasets, the nucleotide characters of all codon position and the 3rd codon positions, where the family was united with Loasaceae, but not strongly supported. Results from divergence time analyses suggested a mid-Cretaceous origin of Cornales followed by rapid early diversification into major clades/families within 10 million years. The earlydi- versification of Cornales may have been facilitated by divergence in habitat and morphology following geographic dispersals. The ancestral distribution of the order was inferred as a widespread range covering Asia, Europe, North America, and Africa when including fossils in the analyses, suggesting an origin of the order likely along the Tethys Seaway where the areas were connected in the mid-Cretaceous. Inferred geographic origins of each family differed to some extent between analyses including fossils vs excluding fossils. In the analysis with extant and fossil species, the origins of the African Hydrostachyaceae and Grubbiaceae-Curtisiaceae clade were inferred to have involved two in- dependent events, an intercontinental dispersal from the northern hemisphere to Africa and an intercontinental vi- cariance between the northern hemisphere and Africa, respectively. Other families were inferred to have evolved in the northern hemisphere with subsequent intercontinental dispersal(s) to other areas including to Central and South America, during their subsequent diversification. Net diversification rate analysis based on treePL dated phylogeny using MEDUSA detected a nearly 5-fold decrease in the African endemic Curtisiaceae-Grubbiaceae (CuG) clade and an increase of rate in the Hydrangeaceae-Loasaceae (HL) clade. Within HL, a decrease in the Fendlera-Jamesia clade and an increase in the Philadelphus clade were also detected. The findings are also consistent with the level of present species diversity in these lineages. Our study demonstrated the value of plastid genome in phylogenomic study, but posed an old challenge of biogeographic study with fossil data and raised caution for the synonymous substitution sites of plastid genome in phylogenomics studies. ⁎ Corresponding authors at: CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming, Yunnan 650201, China (D.-Z. Li and L.-M. Gao). Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC 27695, USA (Q.- Y.(J) Xiang). E-mail addresses: [email protected] (D.-Z. Li), [email protected] (Q.-Y.J. Xiang), [email protected] (L.-M. Gao). https://doi.org/10.1016/j.ympev.2019.106601 Received 15 January 2019; Received in revised form 17 August 2019; Accepted 20 August 2019 Available online 21 August 2019 1055-7903/ © 2019 Elsevier Inc. All rights reserved. C.-N. Fu, et al. Molecular Phylogenetics and Evolution 140 (2019) 106601 1. Introduction (2011), for the families sampled (Fu et al., 2017). In this study, we increased data of Xiang et al. (2011) and taxa sampling of Fu et al. Cornales is a relatively small order comprising six to ten families, 48 (2017) to include the entire plastid genome sequences of 74 species genera, and approximately 605 species mostly occurring in Asia and from all families of Cornales to test previous hypothesis on the timing America. The order, alone or with Ericales, represent the first diverging and place of origin and the pattern of early evolution of Cornales. living lineage within the Asterids clade (APG IV, 2016; Zeng et al., It is well-recognized that results of phylogenetic inference using 2017; Gitzendanner et al., 2018b; Li et al., 2019). Modern families of genome-wide data sets is often affected by analytical methods, the scale the order are heterogeneous in morphology and habits, and most are of taxon sampling, character partitions, and character coding strategies small in size and biogeographically isolated (see Xiang, 2013). For ex- (Jeffroy et al., 2006; Som, 2015; Simmons, 2017). In practice, data from ample, all families have one to two genera except Hydrangeaceae and exons have been commonly coded for either nucleotide or amino acid Loasaceae and are restricted to eastern Asia, eastern or western North characters for phylogenetic inferences (Feuda et al., 2017; America, Central or South America, or Africa. The cornelean families Gitzendanner et al., 2018a; Yang et al., 2018). The nucleotide char- are mostly terrestrial plants except Hydrostachyaceae which are fresh acters are more variable than the amino acid characters, thus providing water aquatic herbs. The larger families of Cornales are the Hy- more phylogenetic signals. However, the amino acid data are more drangeaceae and Loasaceae. Hydrangeaceae has 17 genera and ap- conserved and less likely subjected to substitutional saturation proximately 270 species that are mainly north temperate shrubs, vines, (Simmons et al., 2004; Fong and Fujita, 2011). Nucleotide characters or herbs. Many genera in the family are also small with one to a few are likely subject to saturation, especially for deep-level phylogenetic species restricted to a small geographic area except Phildelphus and analysis. Convergent and reversed mutations would erase true phylo- Deutzia. Loasaceae has 21 genera and approximately 350 species, lar- genetic signals. It has been difficult for molecular models to dis- gely confined to seasonal dry or arid habitats in temperate and tropical criminate reliable source of the signal (homologies) from saturation America (mainly South America) with one genus (Kissenia) extending to (homoplasy) (Rota-Stabelli et al., 2013). The effect of compositional Africa. Hydrangeaceae and Loasaceae differ from the other families of bias and codon-usage bias also increases rapidly at synonymous sites Cornales in having branched styles in flower, capsular dry fruits, and (Jeffroy et al., 2006; Liu et al., 2014). Biased accumulation of specific unique iridoid compounds, whereas most of the other families make nucleotides in unrelated lineages could mislead the phylogenetic in- fleshy drupaceous fruits with unbranched style and a germination valve ference (Foster et al., 1997; Saccone et al., 1999). Compared to nu- in the fruit stone. cleotides, amino acids are expected to be less prone to the influence of Although many taxa of Cornales have geographically restricted saturation and compositional bias as they are less sensitive to the sy- modern distributions, most of them have fossils occurring in areas nonymous or silent substitutions. Therefore, amino acids data appear to outside their present ranges. For example, Curtisia and Grubbia are be more robust than nucleotides data for deeply phylogenetic inference, endemic to South Africa, but both have fossil fruits reported from the especially for resolving ancient relationships (Rota-Stabelli et al., northern hemisphere (Curtisia from the Eocene of London Clay; 2013). However, in addition to being less informative, amino acid data Manchester