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In reply to the Cannabis experts: plastome phylogenies support the parallel hypothesis for species concepts in the Cannabaceae (sensu stricto).

Many botanists have studied the extensive literature on Cannabis (Cannabaceae) to correctly classify species (Boutain, in review; Boutain & Boutain, in press; Clarke & Merlin, 2013; Laursen, 2015; Small, in press, 2015a). For example, Small (2015b) supports the monotypic treatment of Cannabis sativa Linnaeus (1753) based on the absence of evidence for reproductive barriers. In contrast, Clarke and Merlin (2015) advocate for three binomials with several subgroups based on putative ancestors and the extant gene pools recognized by Hillig (2005a, b) (i.e., C. sativa; C. indica Lamarck (1785); C. ruderalis Janischewsky (1924)). Likewise, I show three groups based on a parallel hypothesis with the sister taxa in Humulus (Boutain, 2014). More importantly, what remains to be understood is the evolutionary history and proper phylogenetic placement of the plant family, the Cannabaceae Martinov (1820). Here, an impression of fossils and a phylogeny of whole chloroplast genomes (plastomes) further supports a need for taxonomic revisions in the Cannabaceae. Moreover, this portion of a larger work in progress is to understand the unique evolutionary history of the Cannabaceae (sensu stricto) in relation to the Cannabaceae (sensu lato), which currently includes the Celtidaceae (Boutain, 2014; Yang et al, 2013). Therefore, in this reply with new and reinvented knowledge (McClatchey, 2005), I hope to clarify, not cause, conundrums regarding the early evolutionary history of Cannabis.

Figure 1 shows a combined maximum parsimony and maximum likelihood phylogeny that reconstructs the evolutionary history of Cannabis based on the currently assembled plastomes on GenBank (Benson et al., 2005), or elsewhere on the World Wide Web (Table 1). To promote accessibility, reproducibility, and transparency, the file used to generate this phylogeny is free on the web-based tools, Galaxy (Blankenberg et al., 2010; Giardine et al., 2005; Goecks et al., 2010) and Osiris (Oakley et al., 2014) (specifically see the URLs: <https://usegalaxy. org/u/boutain/h/collection-of-cannabaceae-ss-plastomes> and <http://galaxy-dev.cnsi.>). Importantly and because Fig. 1 contains only two samples of Cannabis that express a lot of tetrahydrocannabinol (THC), the clear distinction here for these two medical cultivars into either sativa or indica types is limited, mostly due to the small number of taxa used in this analysis (n = 7). Although with bootstrap values greater than 93 % and Hamulus as the outgroup, the medical cultivars are in one clade that is sister to the industrial hemp cultivars in a second clade (Fig. 1). Likewise, two groups are supported by van Bakel et ah (2011) and Sawler et ah (2015), while Boutain (2014), Clarke and Merlin (2013), Gilmore et ah (2007), and Henry (2015) advocate for three main groups. In contrast, Small (2015a) and Lynch et ah (2015) recognize only C. sativa because of the limited reproduction barriers and low genetic distance between the other putative groups. To dissolve this debate, an approach inclusive with the known Cannabaceae (sensu stricto) is necessary, especially when plants are an exception to the popular definition of a biological species (Burger, 1975; Curtu et al., 2007; Donoghue, 1985, 2008; Donoghue & Moore, 2003; dos Reis et al., 2016; Escudero et al., 2014; Gailing & Curtu, 2014; Hipp 2015; Hipp et al., 2013; Huang et al., 2015; Johnson, 2002; Mallet, 2001; Nichols & Johnson, 2008; Niirk et al., 2015; Ree & Hipp, 2015; Reeves & Richards, 2011; Schaal et al., 1998; Schwallier et al., 2016; Sharma & Wheeler, 2014; Slater et al., 2012; Soltis & Soltis, 2009; Valen 1976; Wood et al., 2013; Zobel, 2016).

For example, advancements in genomics and DNA sequencing, particularly with nanotechnology (Figs. 2 and 3; Boutain, 2015, in review; Boutain & Boutain, 2015, in press), support splitting Cannabis into at least three groups. The groups are: 1) plants with narrow, palmately compound leaves expressing a sativa type genome that produces a lot of THC; 2) plants with broad, palmately compound leaves expressing an indica type genome that produces a lot of THC; and 3) plants with an industrial hemp type expressing various ratios of THC to other cannabinoids. However, due to the lack of replicates for each known taxon, here 1 recommend a Cannabis classification following a parallel hypothesis that is based on Humulus phylogenomics (Boutain, 2014, in review; Boutain & Boutain, 2015, in press). With the intent to clearly present this hypothesis to scientists and non-scientists alike, the specific epithets previously described in the literature are maintained here (The Plant List, 2013; Tropicos, 2016). The parallel hypothesis states: one group includes C. sativa and H. lupulus Linnaeus (1753) that are originally distributed across the northern temperate zone; a second group includes C. indica and H. yunnanensis Hu (1936) that are originally localized near the Himalayan mountain range; and a third group includes C. ruderalis and H. scandens (Loureiro) Merrill (1935) that arise in-situ (Fig. 4; also see Boutain, 2014). Without a doubt, human intervention along trade routes, like the land and water passages of the popular Silk Road, have obscured the early evolutionary origins of the Cannabaceae (sensu stricto).

After using long and short DNA barcodes to surf Cannabaceae genomes, both Cannabis and Humulus are nearly identical, model systems in a unique plant family (Boutain, 2014, 2015, in review; Boutain & Boutain, 2015, in press). At present, the highly conserved plastome with a best-fit model of evolution suggests three separate groups in each genus. With fossils of the most recent common ancestor of the Angiospermae first appearing during the Early Cretaceous (i.e., approximately 125 million years ago for the Archaefructaceae Sun et al. (2002)), at least a Cretaceous, if not Laurasian, origin hypothesis is possible for the Cannabaceae (sensu stricto) (Boutain, 2014; He et al., 2013). Furthermore, the early ancestors of Cannabis and Humidas may have been interfertile for a very long time, probably since before the oldest known macrofossils were found near the K-T boundary in North America (see Johnson, 2002; Plate 6:1 for aff. Humulus sp. (HC 243), DMNH-19217, locality 9727 (2086); Plate 8:5 for Cannabaceae HC81, YPM-6205, 86100 (567).

An important conclusion after investigating the K-T boundary is no major plant groups disappeared except for taxa at the species level, which significantly contrasts the major extinctions from the animal kingdom, like the dinosaurs (Chaloner, 2009; Nichols & Johnson, 2008; Pigg, 2009). As new fossils are found and genomes are sequenced, the North American hypothesis for the origin of the Cannabaceae (sensu stricto) will be revisited (Boutain, 2014). Although, if genome wide studies conflict to support a monotypic treatment of Cannabis (Henry, 2015; Lynch et al., 2015), then perhaps a more ancestral species description is required. An ideal approach takes into account fossils, three-dimensional modeling of those fossils, phytogenies that combine morphological and molecular characters, as well as the more recent evolutionary history since anthropogenic extinctions (dos Reis et al, 2016; Gandolfo et al., 2008; Garwood & Dunlop, 2014; Huang et al, 2015; Sharma & Wheeler, 2014; Slater et al, 2012; Wood et al., 2013). A direct result from fossil reconstructions of the most recent common ancestors in the Cannabaceae (sensu stricto) will support both the stem and crown relationships on the Plantae family tree (e.g., Friedrich (1883), Saporta (1869), and specifically see Boutain (2014) for H. lupulus var. americanus J. Boutain, var. nov.; II. lupulus var. laurasiana J. Boutain, var. nov.; II. phytolaurasiana J. Boutain, sp. nov.). After all, revisiting the age and diversification of Angiospermae suggests an origin of approximately 167-199 million years ago (Bell et al, 2010).

Notably, when applying fossil dates with plastomes from different assembly methods and software, the phylogenetic outcomes may actually be a result of different lab practices and sequencing chemistries (e.g., human or homopolymer errors) (Boutain, 2014). Moreover, approaches with whole genome sequences, assembled plastomes, or single nucleotide polymorphisms find the phylogenetic analyses conducted with sequences from different data sets yield dissimilar topologies (Boutain, 2014; He et al., 2013; Henry, 2015; Wu et al., 2015; Yang et al., 2013). Accordingly, portable DNA devices, biologist-friend software, and educators are a potential resolution to biological conundrums (Boutain, in review; Boutain & Boutain, 2015, in press). Based on the highly conserved plastome (Boutain, 2014), a taxonomic revision is warranted for the Cannabaceae (sensu stricto) and sister families (Donoghue, 2008; Donoghue & Moore, 2003; Judd et al., 1994; Yang et al., 2013).

Overall, classification of natural and artificial systems is fraught with problems by design. When new samples, methods, and results support an alternative hypothesis to an accepted taxonomy, the species, genus, or family level recommendations require a complete review of: the current fossil record, historical collections, as well as the extant genomes in the system under revision. Today, many botanists agree that simply raising an extant variety to a new species based on morphology or phytochemistry alone does not necessarily advance science. Ultimately, new hypotheses that describe the observed natural phenomena of 'wild' taxa in relation to their recent domesticates must incorporate millions of years in a best-fit model of evolution before extant phenotypes are supported (Boutain, 2014). With the costs of genome projects significantly dropping and equating to a monthly paycheck, individuals can contribute major advancements to science. In some instances, the costs to publish genome data are more than the costs to conduct the projects. With genomes and fossils strongly supporting a likely minimum evolution and rapid radiation of Angiospermae much earlier in geological time (Bell et ah, 2010; Wang et al., 2009), the next obvious progression is generating in real-time, short and long DNA barcodes with portable sequencers in a field setting, as hypothesized to determine the origin of the enigmatic Cannabaceae (sensu stricto) (Boutain, 2014, in review; Boutain & Boutain, 2015, in press).

DOI 10.1007/s12229-016-9171-0

Acknowledgments Thank you: New York Botanical Garden and the editors of Botanical Review, Dennis Stevenson and Barbara Ambrose, for interest in this manuscript as a publication. Also, thank you. Patricia Polansky at the University of Hawai'i at Manoa Hamilton Library for assistance with translations concerning Cannabis ruderalis, as well as those individuals that helped search for literature on C. mderalis, including Esther Jackson at the New York Botanical Garden, Craig Brough at the Royal Botanical Gardens Kew, Keiko Nishimoto at the Harvard Botany Libraries, Barney Lipscomb at the Botanical Research Institute of Texas, and colleagues at the Yale Library- Additionally, thank you: Jianchu Xu and colleagues at the Kunming Institute of Botany, Chinese Academy of Sciences and the World Agroforestry Centre (ICRAF) for access to Humulus yumanensis herbarium specimens for the author's dissertation. Finally, thank you: Matthew Boutain (New Growth Botanical LLC), Timothy Gallaher (Iowa State University), Samantha Luhn, and three friendly reviewers for comments on an early version of this manuscript.

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Jeffrey R. Boutain (1,2,3,4)

(1) New Growth Botanical LLC, PO Box 32949, 1401 W Fort Street, Detroit, MI 4S232, USA

(2) Botanical Research Institute of Texas, 1700 University Drive, Fort Worth, TX 76107, USA

(3) PO Box 342107, Kailua, HI 96734, USA

(4) Author for Correspondence; e-mail:

Published online: 21 December 2016

Table 1 Accessions of plastomes used to generate an evolutionary
history of Cannabis rooted with Humulus (Cannabaccae). The common
hop, as well as the industrial hemp samples representing C. sativa,
are from northern Eurasia with one exception from Africa. The newly
domesticated but common medical cultivare, Purple Kush (breeding
parentage by clone only: Hindu Kush x Purple Afghani) and LA
Confidential (breeding parentage by DNA Genetics: O.G. LA Affie x
Afghani), possibly represent an almost pure genetic relative to C.
indica. Taxa and cultivar names are taken as is from the cited

Taxa                Cultivar name        Common name      # of base
                       (Region)                             pairs

Cannabis sativa   Cheungsam (Korea)    industrial hemp    153,848
  subsp. sativa

Cannabis sativa     Yomba Nigeria      industrial hemp    153,854

Cannabis sativa   Carmagnola (Italy)   industrial hemp    153,867

Cannabis sativa   Dagestani (Russia)   industrial hemp    153,871

Cannabis sativa      Purple Kush           pure indica    152,942
                    (Western USA)      medical cultivar

Cannabis sativa    LA Confidential         pure indica    153,805
  subsp. indica      (Amsterdam)       medical cultivar

Humulus lupulus         Saazer              common hop    153,751
                   (Czech Republic)        brewers hop

Taxa                  GenBank                References

Cannabis sativa   gi|873820236             Oh et al, 2015
  subsp. sativa   gb|KR184827.1

Cannabis sativa   gi|836692016             Oh et al., 2015

Cannabis sativa   gi|814071848           Vergara et al., 2015

Cannabis sativa   gi|915477544           Vergara et al., 2015

Cannabis sativa   PRJNA73819        The Cannabis Genome Browser,
                  SAMN02981385                  2016;

                                         Purple Kush, 2016;

                                        van Bakel et al., 2011

Cannabis sativa   PRJNA297710        LA Confidential, 2016a, b;
  subsp. indica   SAMN04145444              McKeman, 2015

Humulus lupulus   gi|927682664           Vergara et al., 2015


Please note: Some tables or figures were omitted from this article.
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Author:Boutain, Jeffrey R.
Publication:The Botanical Review
Article Type:Report
Date:Dec 1, 2016
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