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Home , Hengduan Mountains, Kunlun Mountains, Tibetan Plateau

Uplift-driven diversification in the , a temperate hotspot

Yaowu Xinga,b,1 and Richard H. Reea,c,1,2

aLife Sciences Section, Integrative Research Center, The Field Museum, Chicago, IL 60605; bKey Laboratory of Tropical , Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 666303, ; and cNational Institute of Ecology, 1210 Geumgang-ro, Maseo-myeon, Seocheon-gun, Chungcheongnam-do, South Korea

Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved February 27, 2017 (received for review September 26, 2016) A common hypothesis for the rich biodiversity found in mountains was in situ diversification accelerated by uplift of the Hengduan is uplift-driven diversification—that creates conditions Mountains? favoring rapid in situ speciation of resident lineages. We tested The geological history of the QTP and its surrounding ranges this hypothesis in the context of the –Tibetan is complex, and many details remain controversial, with differ- (QTP) and adjoining mountain ranges, using the phylogenetic ent lines of evidence often yielding conflicting inferences. How- and geographic histories of multiple groups of plants to infer ever, some points of consensus have emerged from recent syn- the tempo (rate) and mode (colonization versus in situ diversifi- theses (4, 11–13). One is that the central plateau was uplifted cation) of biotic assembly through time and across . We first, forming a “proto-QTP” as early as 40 Mya, with subsequent focused on the Hengduan Mountains , which in compari- outward extensions by the early Miocene (11, 14). By the late son with the QTP and was uplifted more recently (since Miocene, 8 to 10 Mya, all of the mountains surrounding the QTP the late Miocene) and is smaller in area and richer in species. to the south, west, and north had reached their current eleva- Time-calibrated phylogenetic analyses show that about 8 million tions (12, 15–17). By contrast, uplift of the Hengduan Mountains y ago the rate of in situ diversification increased in the Hengduan region, at the southeastern margin (Fig. 1), is generally believed Mountains, significantly exceeding that in the geologically older to have been rapid and recent, occurring mainly between the late QTP and Himalayas. By contrast, in the QTP and Himalayas during Miocene and late Pliocene (18–23). the same period the rate of in situ diversification remained rel- The Hengduan Mountains are thus younger than the rest of atively flat, with colonization dominating lineage accumulation. the QTP and relatively small in area, but conspicuously rich The Hengduan Mountains flora was thus assembled dispropor- in species. If floristic assembly tracks orogeny, this suggests an tionately by recent in situ diversification, temporally congruent elevated tempo since the late Miocene, compared with adja- with independent estimates of orogeny. This study shows quanti- cent regions, but what of mode? Either colonization, in situ tative evidence for uplift-driven diversification in this region, and diversification, or both processes must have been accelerated. more generally, tests the hypothesis by comparing the rate and In biogeographic studies of QTP-associated clades, the hypothe- mode of biotic assembly jointly across time and space. It thus com- sis of uplift-driven in situ diversification has been clearly favored plements the more prevalent method of examining endemic radi- over colonization, being commonly invoked to explain phyloge- ations individually and could be used as a template to augment netic and phylogeographic divergences (e.g., refs. 24–27). How- such studies in other biodiversity hotspots. ever, conspicuously lacking from these studies are quantitative analyses that explicitly measure rates of diversification and col- | vascular plants | molecular clocks | dispersal | speciation onization and compare them across regions and time (3, 4).

Significance entral to understanding global patterns of biodiversity are Cconsiderations of biotic assembly: For a given region, when and how did resident species accumulate? Of primary interest Why do so many species occur in mountains? A popular but is tempo (the rate of accumulation) and mode (the process, little-tested hypothesis is that creates environ- whether by colonization via dispersal or in situ lineage diver- mental conditions (new habitats, dispersal barriers, etc.) that sification). We wish to know how and why these vary in time increase the rate at which resident species divide and evolve and space. to form new ones. In China’s Hengduan Mountains region, a For mountains, well-known for harboring a disproportion- biodiversity hotspot uplifted over the last 8 million years, this ate fraction of terrestrial species, a common hypothesis is that rate does in fact show a significant increase during that time, of uplift-driven diversification—that orogeny creates conditions relative to the rate for adjacent older mountains, and to the favoring in situ speciation of resident lineages (1–6). Among rate of species immigration. The Hengduan Mountains flora global biodiversity hotspots, the mountain ranges surrounding is thus made up disproportionately of species that evolved the Qinghai– (QTP) are unusual and enigmatic: within the region during its uplift, supporting the original They harbor one of the world’s richest temperate floras, and hypothesis and helping to explain the prevalence of moun- (unlike other hotspots) they are neither tropical nor Mediter- tains as global biodiversity hotspots. ranean in climate. Moreover, despite increasing interest from Author contributions: Y.X. and R.H.R. designed research, performed research, analyzed biogeographers, their biotic assembly remains poorly understood data, and wrote the paper. (3, 4, 7). The mountains form three distinct hotspots of biodi- The authors declare no conflict of interest. versity that respectively lie to the west, south, and east of the QTP’s central high : the Central Asian mountains (Altai This article is a PNAS Direct Submission. and Tianshan ranges), the Himalayas, and the Hengduan Moun- Freely available online through the PNAS open access option. tains region (4) (Fig. 1). Of these, the richest in plant diver- See Commentary on page 4275. sity is the Hengduan Mountains, with a vascular flora of about 1Y.X. and R.H.R. contributed equally to this work. 2 12,000 species in an area of about 500,000 km (8–10). In this 2To whom correspondence should be addressed. Email: rree@fieldmuseum.org. study we seek to better understand the origins of this remarkable This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. flora through the lens of historical biogeography. In particular, 1073/pnas.1616063114/-/DCSupplemental.

E3444–E3451 | PNAS | Published online April 3, 2017 www.pnas.org/cgi/doi/10.1073/pnas.1616063114 Downloaded by guest on September 23, 2021 Downloaded by guest on September 23, 2021 fclnzto rud8M,adb h rsn h median specia- the situ present in Himalayas–QTP the the by In 335. that and versus overtakes Ma, 508 is events 8 number speciation around the situ colonization Mountains, in of Hengduan of the number in In cumulative change . little East relatively and this Mountains temperate/boreal with Following Hengduan considerably, the speciation. diverge of situ Himalayas dynamics in assembly East is the is temperate/boreal process phase, Himalayas–QTP dominant in and the whereas Asia Mountains colonization, Hengduan by the assem- dominated phase, both “constant” earlier in this During bly Ma. 8 until last the initiation about following (log-linear) exponential Ma approximately 155 by Ma. occurs 60 initially by occurs speciation initially situ colonization in and ances- clades, root for the as area temperate/boreal reconstructed tral commonly in was contrast, by which By Asia, starting respectively. East Ma, later, for 19 Ma begins and 59 speciation Ma by 34 situ and Mountains in Hengduan Himalayas–QTP; the event the for colonization Ma 64 the earliest by of the occurs 95% histories than more joint In pseudoreplicated Himalayas–QTP. the flora of its that of assembly predating initial phylogenetic with occupancy, deep Hengduan surprisingly of histories the found we assembled than was Instead, flora younger recently. its more that are find to Mountains expected we Hengduan Himalayas–QTP, (Delimitation the the paleontological east that and to the geological evidence Given to region Regions). Asia Biogeographic Himalayas–QTP East of combined temperate/boreal a and west with Moun- Hengduan region the contrasting on tains here through focus events We cumula- speciation 2). situ (Fig. the time in as and patterns plotted colonization of distinct when number regions reveal tive across clades assembly selected floristic the of of histories graphic Assembly. Floristic of Histories Contrasting biotic the Results of of diversity mode remarkable and the tempo for flora. in Hengduan account aim help differences primary that the Our assembly discover Mountains. biogeo- to Hengduan the inform the was to of of potential history clades their 19 graphic for from chosen data plants using diversification, range vascular lineage ancestral of diver- of fossil-calibrated rates of reconstructions and from rates and regional time chronograms inferred through molecular We colonization 1). older and (Fig. geologically Heng- sification QTP other adjacent the the and to of of Himalayas comparisons parts assembly the on floristic especially focusing the regions, region, study Mountains to duan groups plant ple tested. rigorously be to yet Hengduan has the Mountains in assembly con- floristic to has disproportionately diversification tributed uplift-driven that idea the Consequently, Himalayas. 1. Fig. igadRee and Xing o l ein,seisacmlto yec rcs is process each by accumulation species regions, all For multi- of histories evolutionary the used we study this In a fteHnda onan eini eaint h T and QTP the to relation in region Mountains Hengduan the of Map eosrce biogeo- Reconstructed .Ta s across is, That S2). Fig. reconstructions Appendix, ancestral-range (SI shifts phylogenetic of the regime in light of patterns locations geographic in clear any shift) ratio reveal odds not a marginal does of the and favor configurations, the in shift in of occurring of set probability credible cumulative branch- (the of evidence inspection specific However, 1). (Table regime factor diversification (Bayes evidence strong Rate. Diversification in 4). Shifts (Fig. con- period By time Asia Ma. same East 1 the last temperate/boreal in the slightly to in only region sharply increases each and Ma, from 5 dispersal to trast, 4 gradu- last the increase over Himalayas–QTP ally between and rates Mountains Dispersal 3). Hengduan it (Fig. the Himalayas–QTP, constant the less almost for or increased whereas more Ma, remained years, 10 past million the per in over region, twofold lineage Mountains resident Hengduan the per for events speciation situ in Time. Through of Dispersal rate and Speciation Situ in of Rates Regional Miocene. late flora, the Himalayas–QTP the the since of to especially assembly has the it as to flora much Mountains as Hengduan twice almost contributed has tion 0.318 nst pcaint oitcasml sthus of is contribution assembly relative floristic 0.603 The to 411. speciation versus situ 192 in median is the events present of the by number and colonization, overtakes never tion ossetwt h hoyo pitdie iesfiaini h Hengduan the in diversification uplift-driven region. Himalayas–QTP, of Mountains the theory with the compared with Hengduan Miocene seems the consistent late assembling the thus in since speciation role flora large situ Mountains disproportionately In a played process. have Himalayas–QTP dominant to the the for spe- whereas remains situ Ma, are colonization in 8 assembly about cumulative regional colonization region, in overtakes Mountains differences ciation Hengduan which the the in In on Ma, apparent. Panels 20 most last text). the the through on in to events focus (discussed designed right of uncertainty histories phylogenetic number biogeographic for cumulative joint account pseudoreplicated the 5 500 for the from indicate intervals time regions quantile Shaded 95% phylogenies. to reconstructions molecular ancestral-range from time-calibrated inferred on clades, plant 19 in events tion 2. Fig. o h iaaa–T.I te od,i iuspecia- situ in words, other In Himalayas–QTP. the for o h egunMutis and Mountains, Hengduan the for sebyo einlflrsb ooiainadi iuspecia- situ in and colonization by floras regional of Assembly PNAS ee u fte1 ldsshowed clades 19 the of out Seven | 5 o n rmr hfsin shifts more or one for >15) ulse nieArl3 2017 3, April online Published 12+41 = 411) + 192/(192 58+35 = 335) + 508/(508 | E3445 The

EVOLUTION SEE COMMENTARY PNAS PLUS (4, 13, 15, 17, 21). Here, our phylogenetic inferences, which make no prior assumptions about the timing of geological events, show that after about 8 Ma the rate of in situ diversification increased in the Hengduan Mountains (Fig. 3), yielding a remarkable inflection point at which cumulative speciation overtakes colo- nization (Fig. 2). This indicates that the Hengduan Mountains flora has been assembled disproportionately by recent in situ diversification that coincides temporally with independent esti- mates of orogeny. Rapid Himalayan orogeny during the early to middle Miocene (15, 21, 28) would predict a similar pulse of uplift-driven diversifi- cation, but none is evident whether the Himalayas are treated as part of the QTP (Fig. 3) or separately (SI Appendix, Fig. S4). It is possible that the Himalayas were uplifted more gradually; alter- natively, the signal of such a pulse could be masked by the greater uncertainty associated with estimating clade ages and ancestral ranges in deeper time, and/or subsequent extinction and turnover in the affected lineages. In a recent review, Renner (13) argued that numerous phy- logenetic studies have misinterpreted the Earth sciences liter- ature and incorrectly attributed relatively young (Miocene and later) estimates of lineage divergence to QTP uplift, and recom- Fig. 3. Rolling estimates of in situ speciation rates through time for the mended that “Biogeographical discussions should also keep in Hengduan Mountains and Himalayas–QTP regions from inferred biogeo- mind expected differences in the biota of the TP and those in the graphic histories of 19 plant clades. Lines indicate medians and shaded areas Himalayas, the range to the N, the Pamir and Karako- indicate 5 to 95% quantile intervals from 500 pseudoreplicated joint histo- ram to the W, and Hengduan Mountains to the E” (ref. 13, p. 7). ries designed to account for phylogenetic uncertainty (discussed in the text). Here, our focus on distinguishing the younger and more species- Regional rates begin to diverge about 8 Ma, with the Hengduan Mountains showing a striking increase in in situ speciation relative to the Himalayas–QTP. rich Hengduan Mountains region from the Himalayas–QTP is in the spirit of that advice, and our results suggest that at least some of the referenced cases of diversification could be more accu- rately interpreted as coincident with orogeny of the Hengduan clades, macroevolutionary jumps in diversification rate are not obviously associated with the colonization or occupancy of any particular region. A notable exception to this general pattern is Rhododendron, in which results from BAMM (Bayesian Analysis of Macroevo- lutionary Mixtures) and Lagrange suggest that in a window of about 9 to 15 Ma net diversification increased independently in two clades that each originated in the Hengduan region and are currently dominated by Hengduan species (Fig. 5). In Saus- surea, an increase in net diversification is inferred about 1.7 Ma along the stem of a branch containing most of the clade’s Heng- duan species (SI Appendix, Fig. S2O). Similarly, in Delphineae, two separate increases are inferred in clades that are ancestrally Hengduan and together hold most of the Hengduan species; however, the times of these rate shifts (about 28 Ma and 37 Ma, respectively) predate the uplift of the Hengduan Mountains (SI Appendix, Fig. S2D). Finally, in Isodon and the Ligularia– Cremanthodium–Parasenecio complex, branch-specific measures show one increase in net diversification for each clade in the con- text of Hengduan ancestry about 7 and 5 Ma, respectively, but in both cases models with regime shifts are not supported by Bayes factors, and the Hengduan Mountains region is reconstructed as ancestral across most of the phylogeny, rendering the geographic context of the shift less informative.

Discussion Our analysis quantifies the relative contributions of in situ lin- eage diversification and colonization to the assembly of one of the world’s richest temperate floras, that of the Hengduan Mountains. We expected regional differences to reflect con- trasting times of orogeny, in particular the prediction of the Fig. 4. Rolling estimates of colonization rates through time for the Heng- uplift-driven diversification hypothesis that in situ speciation duan Mountains, Himalayas–QTP, and temperate/boreal regions from inferred biogeographic histories of 19 plant clades. Lines indicate increases with mountain-building activity. In this context, the medians and shaded areas indicate 5 to 95% quantile intervals from 500 late Miocene emerges as an important reference point, because pseudoreplicated joint histories designed to account for phylogenetic uncer- previous studies of and paleontology indicate that the tainty (discussed in the text). Dispersal between the Hengduan Mountains Hengduan Mountains achieved their current height only after and Himalayas–QTP increases in the last 2 Ma relative to dispersal between this time, whereas the Himalayas and central QTP did so before either region and temperate/boreal East Asia.

E3446 | www.pnas.org/cgi/doi/10.1073/pnas.1616063114 Xing and Ree Downloaded by guest on September 23, 2021 Downloaded by guest on September 23, 2021 aecag r o lal eaal,bcuete concur- they cli- Ree and and because Xing orogeny separable, of clearly effects not the in are level habitats this change alpine At mate and Miocene. montane late rapid temperate the the to moist response of macroevolutionary expansion a reflects region duan resource and landscape heterogeneity. of aspects associated and com- isolation, uplift population in including promoting 35), pollina- mechanisms ref. other with (e.g., with interference associated bination reproductive traits and floral sharing in tor facilitated divergence been have recurrent may species by biotic Hengduan many roles as the important of in such fication played example, se, For have 34). to per For 13, (3, certain uplift 33). almost con- to and are of 32 unrelated interactions, variety refs. factors a (e.g., clades, involve variables many and associated diversifica- idiosyncratic and be of tingencies to causes likely proximate are the processes tion because common elusive, for prove evidence trait that will requisite suspect the we to However, addition in data. here, possible geographic was and than taxonomic sampling fine-grained more and would analyses denser These require etc.). isolation islands, sky genetic effects of topographic emergence as and (vicariance, limitation such dispersal from processes arising drift nonadaptive within and niche-filling, to and speciation divergence opposed which adaptive to as with associated extent is the region envi- example, a These and for clades. traits reveal, multiple across ecological may 31) of ref. (e.g., evolution tolerances and the ronmental Mountains in Hengduan regions the between adjacent One contrasts needed. what for are studies to look Further specifically, might orogeny? by more driven and, it was Miocene, extent late the since increase Heng- that assembly the of 30), history and age. distinct younger 29, very its a 27, reflects has the 26, actually includes refs. region that (e.g., duan region QTP biogeographic be and greater to precedent Himalayas a Mountains despite of Hengduan part the that, considering simply emphasize for for species. literature to Hengduan data the important in many molecular seems include of thus and sources cited It here studies original analyzed the the clades of are the several (13) Indeed, Renner QTP. in older the not region, 0.05 0.16 0.44 1.72 Pinaceae 4.10 Microsoroideae Meconopsis Lilium 6.82 Parasenecio Ligularia–Cremanthodium– 6.74 Isodon Delphineae Cyananthus Anemoninae + Clematidinae Allium shifts no Acer of hypothesis null the to relative clades, Clade sampled in diversification in shifts for support factor Bayes 1. Table airgca rsuaica .115 .202 .40.00 0.04 0.26 0.72 1.52 1.91 Thalictrum Grossulariaceae + Saxifragaceae Saussurea Rosa Rhododendron Rhodiola Primulaceae Polygoneae ore-rie iwi htdvricto nteHeng- the in diversification that is view coarser-grained A Mountains Hengduan the in diversification situ in did Why (value support Strong + Nomocharis complex 5 sidctdi bold. in indicated is >15) Pedicularis 7.35817 ,8.14365 ,7.0568 3.436.57 137.14 566.86 1,872.00 4,316.57 6,889.71 5,871.71 377.43 5.21811 ,4.18065 ,2.12340 8.6165.65 783.06 2,304.00 5,225.41 8,086.59 7,241.41 1,841.18 550.12 17 16 26.07 71.62 14.24 31.76 77 79 4.0295 1.5116 40.47 111.64 215.75 289.51 247.00 87.97 17.76 07 29.36 40.78 .886 .322 .401 0.06 0.01 0.19 0.02 0.00 0.94 0.10 0.01 0.02 2.23 0.32 0.041 0.06 5.23 0.77 0.18 0.17 8.60 0.52 8.18 0.96 .712 .702 .000 0.01 0.02 0.10 0.02 0.01 0.28 0.08 0.03 0.67 0.26 0.18 1.25 0.71 0.42 1.33 1.57 0.90 7.30 1.92 1.31 1.94 .414 .003 .200 0.01 0.04 0.12 0.32 0.80 1.41 1.64 .343 .911 .801 0.07 0.11 0.38 1.19 2.79 4.37 3.83 .321 .407 .600 .60.02 0.06 0.09 0.36 0.77 1.54 2.18 2.13 011 10 9 8 7 6 5 4 3 2 1 Ooacaee diversi- (Orobanchaceae) 8.81081 ,3.86681 ,3.25416 ,1.81324 409.60 1,382.40 3,015.68 5,401.60 7,038.72 6,668.16 3,836.48 1,048.16 182.48 02 21.68 20.21 01 .703 0.05 0.34 2.17 10.15 35 .620 0.35 2.01 6.26 13.56 .910 0.12 1.05 5.59 onan hogotteQaenr 4) tmyb that be may It adjacent (47). and ele- QTP Quaternary high the at evidence the across even geological throughout present with north, were mountains aligns and areas This west ice-free 44–46). further that refs. areas (e.g., in QTP vation the as of idea well margin southeastern the as the support along 40–43) 38 occurred refs. refugia refs. (e.g., that (e.g., phylogeography distributions and species 39) and of studies Numerous extent. diversification situ of in effect of Pleistocene. pruning estimates the the during lower case, yield this would In extinction extinction. displacement, greater southern inhibited to by have leading would “pruned” valleys ori- been of east–west the entation have Himalayas–QTP, the in would contrast, By branches extinction. diversifi- fewer situ phylogenies, in because time-calibrated of in simply preserved history better region’s be the would result, cation during a migrat- areas as by ice-free cycles; persist southern glacial to toward able unhindered been relatively have ing would species relatively because was extinction low, that extinction suggests north–south valleys in be the major region, differences of can Hengduan orientation regional the results In by factors. our these part, by that caused in possibility least the at and explained, dur- oscillations Pleistocene, climatic the and summer glaciation ing of greater effects the consider by to enhanced were habitats rainfall. region’s formed Hengduan interior the Asian newly by potential—of Central capacities—and diversification carrying and that extension, predicts QTP This (13). central aridified was would had the region summer the and Hengduan then compar- the established, by in because in but abundant, moisture been QTP, areas have and those Himalayas with the ison in would occurred changes Similar have our diversified. in also mead- have species would shrublands, the and of occur of most dataset where extent slopes—habitats the scree driven and increasing ows, have lower, Heng- would treeline As temperatures the 37). falling (36, proceeded, covered uplift was duan deciduous-leaved and QTP and (15) southern coniferous elevation the current by Miocene, its oppor- middle achieved ecological/evolutionary already to of had early stage the a During set tunity. jointly and rently hspteni rbbyntdesll odfeecsi glacial in differences to solely due not probably is pattern This important is it se, per diversification of driver a not Although o frgm shifts regime of No. PNAS | ulse nieArl3 2017 3, April online Published .62.30 9.76 | 163.84 E3447

EVOLUTION SEE COMMENTARY PNAS PLUS Fig. 5. Reconstructions of ancestral geographic range (Left) and net diversification rate (Right) on the maximum clade credibility tree, with branch lengths set to posterior means, for Rhododendron. Ancestral ranges are maximum-likelihood estimates at the start and end of each branch. Net diversification values are branch-segment means of the posterior distribution estimated by BAMM. Filled circles on the right indicate branches that appear in the 95% credible set of distinct shift configurations, with the size and label of a circle indicating the cumulative probability of the branch over all configurations in the credible set. On the left, the marginal odds ratio for a shift in diversification regime along a branch is drawn for branches where the ratio exceeds 20. Geographic regions are coded as follows: AUS, Australasia; CWA, central/; EAS, temperate-boreal East Asia; EUR, ; HEN, Hengduan Mountains; HIM, Himalayas–QTP; NAM, ; and SEA, . Hengduan species cluster primarily in two clades, both of which show evidence of ancestral shifts to higher diversification rate in the mid-to-late Miocene.

greater Pleistocene extinction in the Himalayas–QTP compared duan Mountains. However, we do not find any marked asym- with the Hengduan region was driven as much (or more) by arid- metry in dispersal between these regions through the end of ification as glaciation, because the former experienced reduced the Miocene; instead, rates in both directions are relatively low summer monsoon strength during interglacials (48). and increase only gradually until about 2 to 3 Ma, when both These effects may be reflected in temporal patterns of dis- increase more sharply, but more so from the Hengduan Moun- persal between the Hengduan Mountains and Himalayas–QTP. tains to the Himalayas–QTP (Fig. 4). That is, in the Quater- The older age of the latter predicts that its flora should have nary, the Hengduan Mountains seem to have acted as a bio- been an early source of lineage dispersal to the younger Heng- geographic source, from which lineages buffered from extinction

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(e.g., pattern dominant radiations more endemic the biotic which are in Hengduan , in the with prominently the compared stands figures assembly, thus surrounding dispersal It that mountains habitats. reason high-latitude high to cool of to geo- proximate network region and are a QTP Hengduan Andes in temperate embedded the the is of whereas isolated, habitats graphically results. montane/alpine present the tropical with comparison The for subject within compelling habitats a are and particular of break time scale region. through finer to the assembly a remains of at much patterns down orogeny how Mountains, about than Hengduan studied the oscillations be for climate Clearly, Pleistocene appear (58). and by hotspots other more eight high- driven with the compared yielded rate immigration) average not est (but diversification net of ses flnae ofierssac 5) ihsm lds espe- clades, of some evidence showing with adaptation Chamaecrista highlands, [e.g., (54), situ rupestres radiation charac- campos resistance in endemic been the fire onward) in has to Miocene cially (53). Brazil lineages (late time in recent of not biome by movement but Cerrado and terized occupancy the death, geographic of birth, Assembly on lineage the of dependent in of rates using are immigration, rates which diversity or lower in speciation species with models elevated high than associated more is the tempo, extinction Province space, example, Floristic or (time, regions For California dimensions single mode). these on focus of and to subsets tended and stud- have contrast, time- biomes, hotspots (process) By inferred other change. mode independently climate of and ies and to orogeny very (rate) relation regional a of in tempo com- lines at assembly the This characterize, biotic in to regions. of changes us of across level, allowed rates and basic has estimates time framework ours and through parative diversification rare, processes situ still both in are of colonization analyses and/or quantitative clades, multiple situ of in filling of the (52). lack lineages to the colonizing attributed preadapted Himalayas, been by the niches has In songbirds 51). of and diversification the 50, QTP to 31, and Himalayas subsequent refs. the and (e.g., of colonization during repeated diversification to forests led situ Miocene in the adjacent Asia, in and that SE region notably of Mountains (49), patterns Hengduan regions similar adjacent species-rich present and which QTP birds, the to is relation in and scrutiny geographic west the to regions depauperate north. relatively the colonized igadRee and Xing rvlneo ipra slkl h anrao htw find we that reason main the likely is dispersal of Prevalence (2), hotspot mountain richest world’s the perhaps Andes, The mn tde nern idvriyhtptasml from assembly hotspot biodiversity inferring studies Among bio- most the received has that group the plants, than Other 5).I h P the In (57)]. Mimosa ´ rm im fteAds analy- Andes, the of biome aramo 5,55), (54, Calliandra 5) and (56), ldrne rm2 o9%goal n 6t 4 o h Hengduan the for 94% to S1 26 and globally S1 ). Table 97% sam- Appendix, (SI to species region of 20 Mountains proportion from the ranged Mountains clades, pled Hengduan Across the regions. between Himalayas–QTP shared and are in species 1,045 370 Biogeographic and About of in Himalayas–QTP, Regions). (Delimitation Asia occur the East 930 temperate/boreal in of which 703 remainder the of region, species, gymnosperms Mountains com- ingroup Hengduan of The 4,668 the criteria. each included these sample one taxon met and bined (Microsorioideae)—that angiosperms ferns of and clades—17 (Pinaceae) 19 phylogenies. dated found fossil from We inferred diversity calibrations taxonomic secondary or clade’s (iii calibration the and of range, biogeo- geographic representative and other broadly in was relatives that known logeny closest (ii their regions, as graphic well as Mountains, duan (i Reconstruction. clade Phylogeny and Selection Clade Methods and Materials , Appendix Assembly (SI Biotic diversification of sig- Analyses same Hengduan Additional the uplift-driven yielded areas of separate nature as species them recoded treating of data analyis an and range area; Himalayas biogeographic the single of a treatment as the QTP to robust being are That results system. our complex to said, this attempts nec- of elements best thus essential our are the represent capture 1) they and (Fig. subjective areas in existed somewhat these ambiguity essarily of borders to definitions leading such Our time, present. clearly through extent the shifted into the have translate would to surely not and does borders, broadly this have defined histories, may orogenic Mountains Hengduan distinct the Although and analysis. Himalayas, biogeographic QTP, for required as areas crete and Miocene the in than likely Quaternary earlier. is and events Pliocene the those biogeographic in of greater frequencies which inferred the to extent underestimated thus the have words, we other nodes—and In tend present. more the would to events—closer missing phylogenies reconstructed be that ran- to effectively means be to which pro- distribu- clade each dom, phylogenetic assembly within the species of unsampled expect of rates also tion We relative not regions. the should across therefore of cesses and inferences S1) the affect Table to unduly respect Appendix, with (SI sampling, biased regions Taxon growth generally focal not preferences. of is habitat diversity incomplete, and a although exhibit histories, species life wide a the forms, span and selected Moun- range, we (Hengduan clades taxonomic regions The focal Himalayas–QTP). and the tains of representative are data single here. of inferred analyses pattern previous the yielded why not explain have clades helps This jointly. ered h iaaa otesuh h ulnMutist h ot,adthe and north, the to Mountains Kunlun the south, by the south itself, the to plateau to Himalayas the delimited River including and the We Tao as Basin, 1). region the (Fig. “Himalayas–QTP” complementary by Plateau the the the Yunnan–Guizhou north by to the the east and (), forests to the Xizang subtropical Qinghai, to eastern , in in southern plateau River in high Tsangpo the Yarlung by the northwest by west 1). the (Fig. Himalayas the adjacent, especially QTP, from the importantly region of most Mountains parts Hengduan and clades older geologically the data, selected distinguishing range the on species of focus available to distributions of global granularity the the and accommodate to need databases, our online floras, Appendix species on (SI based sampled datasets regions each published these and of in range absence the or presence scored its and as S1) Fig. Appendix, regions. (SI regions biogeographic of Diversification. Lineage Delimitation and Evolution Range of Inference phylo- Appendix time-calibrated (SI of tree sample maximum-clade-credibility posterior associated the Bayesian and Trees) a genies Sampling generate Analysis to Evolutionary 63) (Bayesian (62, BEAST in implemented els n oslclbaindt n sdrlxdmlclrcokmod- clock molecular relaxed used and data calibration fossil and ) o ahcae easmldmlclrsqec lgmns(Dataset alignments sequence molecular assembled we clade, each For dis- of demarcation the in is error of source potential Another the which to degree the on hinges results our of validity The h egunMutisrgo,floigBufr 8,i one to bounded is (8), Boufford following region, Mountains Hengduan The nlddasbtnilnme fseista cu nteHeng- the in occur that species of number substantial a included ) a ufiin oeua aaaalbet ne phy- a infer to available data molecular sufficient had ) PNAS a osldt utbefrmlclrclock molecular for suitable data fossil had ) | and ulse nieArl3 2017 3, April online Published .Dlmttosreflected Delimitations S2). 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EVOLUTION SEE COMMENTARY PNAS PLUS to the northeast. The distinct geological histories of the in situ speciation, colonization, and local extinction events affecting the Himalayas and QTP argue against their treatment as a single unit for bio- Hengduan Mountains, Himalayas–QTP, and temperate/boreal East Asia, and geographic analysis; however, the granularity of available data on species binned them into 1-My periods. This allowed region-specific estimates of ranges made it difficult to differentiate between them. We attempted to do assembly processes through time. We calculated rolling estimates of per so, with no effect on outcomes (SI Appendix, Additional Analyses of Biotic capita in situ speciation rates as λ(t) = s(t)/n(t − 1), where s(t) is the number Assembly and Figs. S3–S5), but we are most confident with analyses based of in situ speciation events inferred in a region in a 1-My period t and n(t−1) on the combined delimitation, which effectively serves the purpose of con- is the number of inferred lineages in the region in the previous period (the trasting with the Hengduan region. cumulative sum of in situ speciation and colonization minus local extinc- The other regions we delimited are temperate/boreal East Asia (the east- tion). We also calculated rolling per capita rates of colonization between ern boreal part of Russia and temperate regions of East Asia, including regions as dij(t) = cij(t)/ni(t − 1), where cij(t) is the number of inferred colo- Japan and Taiwan), central/western Asia (including the Uyghur nization events of area j from area i. For all estimates, confidence intervals Autonomous Region to the north of the Kunlun Range), southeast Asia (5 to 95% quantiles) were calculated from the pseudoreplicated joint his- (including tropical regions of China, Malesia, and Papuasia), Australasia tories. Our results thus do not condition on any particular tree topologies (, New Zealand, and the southwestern Pacific), India (south of the or branch lengths and reflect the levels of clade support, and confidence in Himalyas, including Sri Lanka), , Europe, North America, and South divergence times, provided by the sequence data. America (south of the Panama Canal). -independent rates of diversification. To complement the Ancestral range reconstruction. We estimated ancestral geographic ranges regional-process analysis and to better understand heterogeneity in rates of for all ingroups using a dispersal-extinction-cladogenesis model in Lagrange lineage diversification independently of geography, we generated Bayesian (64, 65) in which dispersal was allowed based on spatial adjacency (SI inferences of diversification rate for each clade’s maximum-clade-credibility Appendix, Fig. S1) and the maximum range size was set to 3. We explic- tree, with posterior mean branch lengths, using BAMM version 2.5 and the itly avoided placing any temporal constraints on dispersal, so that bio- BAMMtools R package (66). BAMM uses Markov chain Monte Carlo proce- geographic inferences were independent of prior beliefs about the ages dures to jointly estimate the number, parameters, and locations of distinct of the Hengduan Mountains or Himalayas–QTP regions. For each ingroup macroevolutionary regimes (rates of lineage birth and death, possibly time- we inferred a distribution of biogeographic histories to account for phy- dependent) on a phylogenetic tree. It can account statistically for incom- logenetic uncertainty. A single history was generated in three steps. First, plete taxon sampling, so we assigned sampling fractions at the finest level a chronogram was randomly sampled from the clade’s Bayesian poste- of taxonomic resolution possible (SI Appendix). Priors for speciation and rior distribution. Second, the maximum-likelihood set of ancestral ranges extinction were set empirically using the setBAMMpriors function. For all (geographic speciation scenarios) at internal nodes was estimated using clades smaller than 500 species we set the geometric prior on the expected Lagrange. Third, parsimonious sequences of dispersal and local extinction number of regime shifts to 1, as recommended in the BAMM documenta- events were randomly interpolated along branches having different ances- tion; for larger clades we also tested a prior of 10 expected shifts. We ran tral and descendant ranges. This procedure yielded a complete chronology each BAMM Markov chain Monte Carlo analysis for 10 million generations of biogeographic events (i.e., where and when ancestral lineages moved with a sampling frequency of 1/1,000 and assessed convergence by visually and underwent speciation and local extinction). To account for phyloge- inspecting plots of the likelihood trace and calculating the effective sam- netic uncertainty, one history was generated for each of 500 chronograms ple size after discarding the first 10% of the run as burn-in. For each clade, sampled from the posterior for each clade. we calculated Bayes factors for the distinct numbers of regime shifts sam- Regional assembly processes through time. We focused our analysis on pled, marginal odds ratios (relative evidence in favor of a shift) for individual the dynamics of the Hengduan Mountains region in comparison with the branches, and the 95% credible set of distinct shift configurations. Himalayas–QTP and temperate East Asia. Our objective was to estimate, for each region, rates of in situ diversification and colonization and their ACKNOWLEDGMENTS. We thank D. Boufford and three anonymous review- cumulative contributions to biotic assembly through time, while accounting ers for valuable comments on previous drafts. This work was supported by for phylogenetic uncertainy. Taking the biogeographic histories of clades a Boyd Postdoctoral Fellowship at the Field Museum, Swiss Advanced Post- from the ancestral-range analysis, we generated 500 pseudoreplicated joint doc.Mobility Fellowship P300P3 158528, the Pioneer Hundred Talents Pro- histories—sets of one history drawn randomly from each clade’s pool with- gram of the Chinese Academy of Sciences (Y.X.), and NSF Grant DEB-1119098 out replacement. From each joint history we extracted the chronology of (to R.H.R.).

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