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Phylogeny and Biogeography of <I>Caryodaphnopsis</I

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Phylogeny and Biogeography of <I>Caryodaphnopsis</I TAXON 65 (3) • June 2016: 433–443 Li & al. • Phylogeny and biogeography of Caryodaphnopsis SYSTEMATICS AND PHYLOGENY Phylogeny and biogeography of Caryodaphnopsis (Lauraceae) inferred from low-copy nuclear gene and ITS sequences Lang Li,1 Santiago Madriñán2 & Jie Li1 1 Plant Phylogenetics and Conservation Group, Centre for Integrative Conservation, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, Yunnan 650223, P.R. China 2 Departamento de Ciencias Biológicas, Universidad de los Andes, CL 18-2 68, Bogotá, D.C. 111711, Colombia Author for correspondence: Jie Li, [email protected] ORCID JL, http://orcid.org/0000­0001­8067­749X DOI http://dx.doi.org/10.12705/653.1 Abstract Caryodaphnopsis is a small genus of the Lauraceae. It contains 16 known species with a disjunct tropical amphi­Pacific distribution; 8 species in tropical Asia and 8 species in tropical America. In the present study, RPB2, LEAFY and ITS sequences of 9 Caryodaphnopsis species and 22 other Lauraceae species were analyzed with maximum parsimony and Bayesian inference. Divergence time estimation employed the Bayesian Markov chain Monte Carlo method under a relaxed clock. Ancestral area reconstructions were conducted by using both the statistical dispersal­vicariance analysis and likelihood approach under the dispersal­extinction­cladogenesis model. Based on the results of the phylogenetic analyses, the monophyly of Caryodaphnopsis is strongly supported. Asian and American Caryodaphnopsis species form two well­supported monophyletic clades, respectively. Independent lineages for Caryodaphnopsis, Neocinnamomum and Cassytha are also suggested. According to the divergence time estimations and ancestral area reconstructions, we suggest that Caryodaphnopsis originated in Late Cretaceous Laurasia and its amphi­Pacific disjunction results from the disruption of ancestral boreotropical lineages between Eurasia and North America during the first cooling period of the Eocene. Keywords amphi­Pacific disjunction; biogeography; Caryodaphnopsis; Lauraceae; molecular phylogeny Supplementary Material Electronic Supplement (Fig. S1A–E) and DNA sequence alignment are available in the Supplementary Data section of the online version of this article at http://ingentaconnect.com/content/iapt/tax INTRODUCTION less thickened peduncle lacking a cupule (Rohwer, 1993; Li & al., 2008). Caryodaphnopsis Airy Shaw is a small genus of the Laur­ Recent molecular studies suggest that Caryodaphnopsis aceae. It contains 16 known species with a disjunct tropi­ is monophyletic and its phylogenetic position within Laur­ cal amphi­Pacific distribution (Fig. 1); 8 species in tropical aceae is between the Mezilaurus group + core Lauraceae and Asia and 8 species in tropical America (Airy Shaw, 1940; the Cryptocarya group (Chanderbali & al., 2001; Rohwer & Kostermans, 1974; Li & al., 1982 , 2008; Van der Werff & Rudolph, 2005; Wang & al., 2010). Using DNA sequences, Richter, 1985; Li & Li, 1991; Aymard & Romero­González, a sister relationship between Caryodaphnopsis and Neocin- 2009; Van der Werff, 2012; Liu & al., 2013). Caryodaphnopsis namomum H.Liou was suggested in Bayesian analyses, but was first described by Airy Shaw (1940), and Kostermans with only low to moderate support (Rohwer & Rudolph, 2005; (1957) placed the genus in synonymy with Persea Mill., but Wang & al., 2010), whereas an affinity between Neocinnamo- later reinstated and monographed the genus (Kostermans, mum and Cassytha L. was suggested by parsimony analyses 1974). Caryodaphnopsis was only known from tropical Asia (Chanderbali & al., 2001; Rohwer & Rudolph, 2005; Wang & until Van der Werff & Richter (1985) reported two neotropi­ al., 2010) and interpreted as an artifact caused by long­branch cal species, C. theobromifolia(A.H.Gentry) Van der Werff attraction. Based on the fossil record and molecular clock es­ & H.G.Richt. and C. inaequalis (A.C.Sm.) Van der Werff & timation, a Cretaceous Laurasian origin for Caryodaphnopsis H.G.Richt., based on floral and wood anatomical characters. has been suggested (Chanderbali & al., 2001), with an estimated The genus displays a unique combination of morphological Early Cretaceous (Berriasian) divergence time of ~140 Ma. characters within Lauraceae, having opposite (sub­opposite), This estimation, however, appears to be much too old, as the either trinerved, triplinerved or pinninerved leaves; unequal, earliest unquestionable lauraceous fossil (Mauldinia Drinnan deciduous tepals, with the outer three small and the inner & al.) is from the Cenomanian and only ~100 Ma (Drinnan & three very large; and a large fruit sitting on top of a more or al., 1990; Frumin & al., 2004). In contrast, Nie & al. (2007) Received: 2 Aug 2015 | returned for (first) revision: 12 Nov 2015 | (last) revision received: 2 Feb 2016 | accepted: 3 Feb 2016 || publication date(s): online fast track, 1 Jun 2016; in print and online issues, 24 Jun 2016 || © International Association for Plant Taxonomy (IAPT) 2016 Version of Record 433 Li & al. • Phylogeny and biogeography of Caryodaphnopsis TAXON 65 (3) • June 2016: 433–443 proposed a Late Cretaceous (Turonian) divergence time of informative to produce well­resolved molecular phylogenies. Caryodaphnopsis at ~90 Ma, which is more consistent with For example, the RPB2 gene encodes the second­largest subunit the relatively basal position of the genus within the family. of RNA polymerase II in eukaryotic cells, which is respon­ The tropical amphi­Pacific disjunct distribution of plants sible for DNA binding and RNA chain elongation (Woychik & is a well­known and classical biogeographic pattern seen in Young, 1990). Partial RPB2 gene sequences from introns 20–23 plants occurring in tropical regions on both sides of the Pacific were sufficiently variable and informative to produce a well­ Basin (Thorne, 1972; Raven, 1988). Studies of plant groups resolved molecular phylogeny with high statistical support at with tropical amphi­Pacific disjunctions such as Araliaceae different taxonomic levels in Litsea Lam. and related Lauraceae (Li & Wen, 2013), Fagaceae (Van der Hammen & Cleef, 1983), (Fijridiyanto & Murakami, 2009). Similarly, Li & al. (2011) Lauraceae (Chanderbali & al., 2001; Li & al., 2011), Magno­ investigated the phylogeny of the Persea group (Lauraceae) liaceae (Azuma & al., 2001), Styracaceae (Fritsch, 2001) and and its amphi­Pacific disjunction using the LEAFY gene, which Symplocaceae (Wang & al., 2004; Fritsch & al., 2015) sug­ regulates floral meristem induction during the early stages of gested that these disjunctions mostly seem to have resulted reproductive ontogeny (Schultz & Haughn, 1991; Blazquez, from the disruption of an ancestral boreotropical distribution 1997; Blazquez & al., 1997). Their study indicated that the by Mid­ to Late Eocene climatic cooling, followed by relatively second intron of LEAFY is an excellent molecular marker for re­ late immigration into Central and South America. Chanderbali solving phylogenetic relationships at lower taxonomic levels in & al. (2001) similarly estimated the separation between Asian Lauraceae due to its relatively high level of variation. Accord­ and American Caryodaphnopsis species at ~44 Ma as a result ingly, we chose RPB2 and LEAFY along with the universal of cooling following the Paleocene­Eocene Thermal Maximum ITS as molecular markers for phylogenetic reconstruction in (PETM) event, and Zeng & al. (2014) suggested that the un­ the present study. usual double layered lower leaf epidermis of Caryodaphnopsis The objectives of our study were to (1) explore the phylo­ might be related to climatic cooling and aridification. However, genetic utility of RPB2 and LEAFY in Caryodaphnopsis and although these studies provided important information about related Lauraceae; (2) place Caryodaphnopsis phylogenetically the phylogeny and biogeography of Caryodaphnopsis, their within the family; and (3) investigate the biogeographic his­ results are conflicting, possibly due to a combination of limited tory of Caryodaphnopsis focusing on its tropical amphi­Pacific taxon sampling and relatively low phylogenetic information distribution. seen in ITS and/or cpDNA sequences of some Lauraceae. Low­copy nuclear genes of plants show potential to im­ prove the robustness of phylogenetic reconstructions at all MATERIALS AND METHODS taxonomic levels, especially where widely used cpDNA and nrITS sequences fail to generate strong phylogenetic signal Taxon sampling and DNA extraction. — In the present (Sang, 2002). In particular, recent molecular studies in Laur­ study, 20 individuals were sampled as representatives of nine aceae suggest that low­copy nuclear genes are sufficiently Caryodaphnopsis species, three from tropical Asia and six from Fig. 1. The tropical amphi­Pacific disjunct distribution of Caryo- daphnopsis Airy Shaw (Laur ­ aceae). Stars represent fossils pos­ sibly related to Caryodaphnopsis, Caryodaphnopsoxylon richteri from Germany (Gottwald, 1992) and “Taxon B” from the U.S.A. (Eklund, 2000). 434 Version of Record TAXON 65 (3) • June 2016: 433–443 Li & al. • Phylogeny and biogeography of Caryodaphnopsis the Neotropics. Based on recent molecular studies (Chanderbali inference (BI) using the program MrBayes v.3.2.2 (Ronquist & al., 2001; Rohwer & Rudolph, 2005; Wang & al., 2010), 22 & Huelsenbeck, 2003). In the MP analysis, a heuristic search species of Neocinnamomum, Cassytha, the Cryptocarya group was performed with 1000 random addition sequence repli­ and core Lauraceae were selected as the outgroups
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