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Disparity, Diversity, and Duplications in the Caryophyllales

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Disparity, Diversity, and Duplications in the Caryophyllales Research Disparity, diversity, and duplications in the Caryophyllales Stephen A. Smith1, Joseph W. Brown1, Ya Yang2, Riva Bruenn3, Chloe P. Drummond3, Samuel F. Brockington4, Joseph F. Walker1, Noah Last2, Norman A. Douglas3 and Michael J. Moore3 1Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48103, USA; 2Department of Plant Biology, University of Minnesota-Twin Cities, 1445 Gortner Avenue, St Paul, MN 55108, USA; 3Department of Biology, Oberlin College, 119 Woodland St, Oberlin, OH 44074-1097, USA; 4Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK Summary Author for correspondence: The role played by whole genome duplication (WGD) in plant evolution is actively debated. Stephen A. Smith WGDs have been associated with advantages such as superior colonization, various adapta- Tel: +1 734 615 5510 tions, and increased effective population size. However, the lack of a comprehensive mapping Email: [email protected] of WGDs within a major plant clade has led to uncertainty regarding the potential association Received: 30 May 2017 of WGDs and higher diversification rates. Accepted: 28 July 2017 Using seven chloroplast and nuclear ribosomal genes, we constructed a phylogeny of 5036 species of Caryophyllales, representing nearly half of the extant species. We phylogenetically New Phytologist (2017) mapped putative WGDs as identified from analyses on transcriptomic and genomic data and doi: 10.1111/nph.14772 analyzed these in conjunction with shifts in climatic occupancy and lineage diversification rate. Thirteen putative WGDs and 27 diversification shifts could be mapped onto the phylogeny. Key words: Caryophyllales, climatic occupancy, diversification rates, duplications, Of these, four WGDs were concurrent with diversification shifts, with other diversification phylogenomics. shifts occurring at more recent nodes than WGDs. Five WGDs were associated with shifts to colder climatic occupancy. While we find that many diversification shifts occur after WGDs, it is difficult to consider diversification and duplication to be tightly correlated. Our findings suggest that duplications may often occur along with shifts in either diversification rate, climatic occupancy, or rate of evolution. WGD broadly to include putative ancient WGD events (pale- Introduction opolyploidy) and ancient aneuploidy events. WGD events are Understanding the causes and correlates of diversification within thought to be a common occurrence and have been associated flowering plants has been a central goal of evolutionary biologists. with an estimated 15% of angiosperm speciation events (Wood Genomic and transcriptomic data have reinvigorated hypotheses et al., 2009). However, whether speciation by WGD is correlated associating whole genome duplication (WGD) with lineage with higher diversification rates remains highly debated (Mayrose diversification rate increases (e.g. Levin, 1983, 2002; Barker et al., 2011; Estep et al., 2014; Soltis et al., 2014; Tank et al., et al., 2009, 2016; Estep et al., 2014; Soltis et al., 2014; Edger 2015; Kellogg, 2016). Analyses based on recent WGD events et al., 2015; Puttick et al., 2015; Tank et al., 2015; Huang et al., have concluded that immediate extinction rates are higher for 2016; McKain et al., 2016; Laurent et al., 2017). It is not self- polyploid plants (Mayrose et al., 2011; Arrigo & Barker, 2012). evident why WGDs would be associated with increases in lineage This may result from small initial population sizes and an diversification. One hypothesis suggests that the additional increased dependence on selfing. Alternatively, despite the disad- genetic material provides a basis to generate new adaptations vantages of WGD, others have suggested that polyploids may be (Edger et al., 2015), although this itself assumes a co-occurrence superior colonizers (Soltis & Soltis, 2000). of adaptation and lineage proliferation (Levin, 1983). The appar- Indeed, extreme environments are associated with high ent lack of precise co-occurrence of adaptation and lineage prolif- amounts of WGD, with up to 87% of species restricted to areas eration has been explained by the potential of a lag model that were glaciated during the last ice age consisting of polyploids (Schranz et al., 2012; Tank et al., 2015) where diversification (Brochmann et al., 2004). However, in the example from Arctic may follow WGD events. In the absence of overwhelming correl- plants, the high amount of WGD has occurred post-glaciation, ative signal, we are often unable to discern true ancient WGD representing a microevolutionary period, whereas previous stud- events from aneuploidy without advanced genomic information ies often focus at much deeper macroevolutionary timescales such as synteny mapping (Dohm et al., 2012). Because it is often (Mayrose et al., 2011; Soltis et al., 2014; Tank et al., 2015). From difficult to distinguish the two, for simplicity we will define the perspective of a short timescale, polyploidy has the Ó 2017 The Authors New Phytologist (2017) 1 New Phytologist Ó 2017 New Phytologist Trust www.newphytologist.com New 2 Research Phytologist disadvantages of higher error rates in mitosis (Storchova et al., locations of WGD events. Moreover, the growth in the number 2006) and masking of deleterious mutations, allowing them to of plant taxa on GenBank that are represented by traditional tar- accumulate to higher frequencies in a population (Otto & Whit- geted sequences (e.g. rbcL, matK, ITS, etc.) and the growth of ton, 2000). A suite of advantages may also arise, however, includ- publicly available collections data (e.g. GBIF, iDigBio) provide ing gain of asexuality (Miller & Venable, 2000) and varying excellent opportunities to apply phylogenetic and climate diversi- effects of heterosis (Comai, 2005). The net role played by these fication approaches at fine scales in Caryophyllales. advantages and disadvantages on the macroevolutionary scale is By examining WGDs and diversification within the difficult to determine from either the purely short-term or purely Caryophyllales, we present an important example. Not only does long-term timescales previously used. the dataset examined have a high density of transcriptomic sam- The long-term consequence of WGD is a central question in pling, the diversification of the bulk of Caryophyllales occurred macroevolution and comparative genomics. However, with a during a time frame intermediate to that of most published stud- suite of advantages and disadvantages, much debate surrounds ies that have probed a link between WGD and macroevolution. the importance and patterns of correlation of WGD (Comai, This time frame, between 10 and 100 Ma, is important for 2005). While polyploidization events can cause instant specia- angiosperms, as much of the diversification that has led to the tion, there is no reason to assume that these singular speciation modern flora occurred during this period and most modern events in themselves would influence large-scale diversification angiosperm families appeared by this time. Discussion of specia- rate shifts when considering lineage survivorship. Instead, there tion rates, climate occupancy shifts, and WGDs would be flawed may be other factors, such as the increase in genetic material, per- without accurate mappings of WGD events within this timescale. haps increasing genetic diversity or enabling adaptation, that We compiled a dataset with extensive and precise mapping of cause long-term shifts in rates of diversification. Adaptations need WGD combined with a species-level phylogeny. The megaphy- not be associated with shifts in the tempo of diversification and logeny approach has been used extensively in the past to combine those adaptations and shifts in diversification may not co-occur data from many gene regions and across broad taxonomic groups on the same branch (i.e. there may be a lag time; Donoghue, to address evolutionary questions (Smith et al., 2009). Here, we 2005; Smith et al., 2011; Schranz et al., 2012; Donoghue & San- use this approach to help inform analyses from phylogenomic derson, 2015; Tank et al., 2015; Dodsworth et al., 2016). In the studies, and provide a broad context in which to examine these broader context of plant evolution, there are several possible out- genomic phenomena. With half of the species sampled, this rep- comes of WGD in relation to the evolution and diversification of resents one of the largest and most exhaustive studies of WGDs, clades: no relationship between WGD and speciation rate or diversification rate, and adaptive shifts. habitat shift/adaptation; WGD coincides with an increase of spe- ciation rate, with or without a lag time; WGD promotes dispersal Materials and Methods and habitat shifts, which has a mixed relationship with speciation rate; and a mixture (some association, some not), similar to the Sanger sequencing and assembly previous hypothesis but without explicitly promoting dispersal or habitat shift or speciation (e.g. adaptation could be more promi- A total of 248 new matK sequences were included in this study nent than dispersal and habitat shift). Here, we contribute to this (Table 1). To generate these sequences, leaf samples were col- discussion on diversification and WGDs with an in-depth exami- lected in silica in the field or from cultivated material, or were nation of the intersection of diversification and WGDs happen- collected from herbarium sheets. DNA was isolated using either ing at a range of scales within the hyperdiverse Caryophyllales. the Nucleon Phytopure
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