Downloaded by guest on September 25, 2021 www.pnas.org/cgi/doi/10.1073/pnas.1616063114 a hotspot Xing Yaowu biodiversity temperate a Mountains, Hengduan the in diversification Uplift-driven biogeography augment to template hotspots. a biodiversity as other used in studies be such could radi- and endemic examining individually of ations com- method thus and prevalent It more space. rate and the time the plements across comparing jointly assembly by biotic of hypothesis mode the and region, tests this generally, in more diversification uplift-driven quanti- for shows congruent evidence study tative temporally This orogeny. diversification, of dispropor- estimates situ independent assembled with in thus recent was by rel- flora tionately remained accumulation. Mountains diversification lineage Hengduan situ dominating The in colonization with of flat, rate during atively the Himalayas and period QTP same the in the older contrast, geologically By Himalayas. the Hengduan species. and the in QTP in in that increased exceeding diversification richer situ significantly and in Mountains, of million area rate 8 the in about ago that y smaller show is analyses phylogenetic and Time-calibrated (since Miocene) recently compari- more late uplifted in was the Himalayas We which and regions. region, QTP the across Mountains with son Hengduan and the diversifi- time infer situ on through to in focused assembly versus plants biotic (colonization of of mode cation) phylogenetic groups and (rate) multiple the tempo Plateau of using the Qinghai–Tibetan histories ranges, the geographic mountain of and adjoining tested context We and the lineages. (QTP) resident in of hypothesis speciation this situ conditions in creates rapid orogeny 2016) favoring 26, diversification—that September mountains review uplift-driven in for found (received biodiversity is rich 2017 the 27, for February hypothesis approved common and A MA, Cambridge, University, Harvard Edwards, V. Scott by Edited and China; 666303, Korea Yunnan South Sciences, Chungcheongnam-do, of Seocheon-gun, Academy Chinese Garden, Botanical Tropical oatruhteln fhsoia igorpy nparticular, In biogeography. historical of remarkable lens this km the of origins diver- through 500,000 the about understand flora about plant better of of to in flora seek area we vascular richest study an a the in with these, species Mountains, 12,000 Of Hengduan the 1). is (Fig. sity the (4) Moun- (Altai of Hengduan region the mountains east and tains Asian Himalayas, and the Central south, ranges), biodi- the Tianshan west, of and desert: the hotspots high to distinct central lie three QTP’s respectively form that mountains The versity from 7). 4, interest understood (3, poorly increasing Mediter- remains and assembly despite nor biotic their floras, tropical Moreover, biogeographers, neither temperate climate. are richest in they ranean world’s hotspots) the other of (unlike one enigmatic: and harbor Among surrounding unusual They are (1–6). ranges (QTP) mountain lineages Plateau Qinghai–Tibetan the resident the hotspots, of biodiversity speciation global that situ is in conditions hypothesis creates favoring common orogeny a diversification—that species, uplift-driven time of terrestrial in of vary fraction ate these why diver- and lineage process, how situ know (the in space. to mode and or wish and dispersal We accumulation) via sification). colonization interest of primary by rate Of whether (the accumulate? tempo species resident is did how and C ieSine eto,ItgaieRsac etr h il uem hcg,I 60605; IL Chicago, Museum, Field The Center, Research Integrative Section, Sciences Life o onan,wl-nw o abrn disproportion- a harboring for well-known mountains, For osdrtoso itcasml:Fragvnrgo,when region, given are a biodiversity For assembly: of biotic patterns of global considerations understanding to entral | a,b,1 aclrplants vascular n ihr .Ree H. 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(3, time contributed has and diversification uplift-driven regions that idea across the quently, them coloniza- and compare diversification and anal- of tion rates quantitative measure are explicitly studies However, that yses these 24–27). from refs. lacking (e.g., phylogenetic conspicuously divergences explain to phylogeographic invoked over and favored commonly clearly being been of has colonization, hypothesis bio- diversification the situ In in clades, accelerated. uplift-driven QTP-associated been diversi- of have situ studies must adjacent in geographic processes colonization, with both Either compared or mode? fication, Miocene, of what late but ele- the in regions, an since rich suggests conspicuously this tempo orogeny, but vated tracks area, assembly in floristic If small species. relatively and QTP the late (18–23). the Pliocene between late mainly and occurring believed recent, Miocene generally and is rapid 1), been eleva- (Fig. have current to margin Mountains southeastern their Hengduan the the reached at of had uplift region, contrast, north By late 15–17). and (12, QTP the west, tions the surrounding By south, mountains 14). the the of (11, to all Mya, Miocene 10 uplifted to early 8 was subsequent the Miocene, with plateau by Mya, 40 central extensions as the early outward as syn- that “proto-QTP” recent a is forming from One first, emerged 11–13). have (4, consensus How- theses of inferences. points differ- conflicting yielding some with often ever, controversial, evidence remain of details lines ent many and complex, is Hengduan the of uplift by accelerated Mountains? diversification situ in was uhrcnrbtos ..adRHR eindrsac,promdrsac,analyzed research, performed research, designed R.H.R. and Y.X. contributions: Author owo orsodnesol eadesd mi:rree@fieldmuseum.org. Email: addressed. be should correspondence whom To work. this to equally contributed R.H.R. and Y.X. yohssadhligt xli h rvlneo moun- of original prevalence hotspots. the the biodiversity global explain supporting as to tains uplift, evolved helping its that and during species hypothesis of region disproportionately the flora up within Mountains the made Hengduan to thus The and is mountains, immigration. older species adjacent time, of for that rate during rate increase the significant to a relative this show years, fact million in a 8 does region, last rate Mountains the over Hengduan uplifted China’s evolve hotspot and In biodiversity divide ones. species new resident form which to that at etc.) rate barriers, the dispersal increase but habitats, environ- popular creates (new A uplift conditions mountains? tectonic mental in that is occur hypothesis species little-tested many so do Why Significance h egunMutisaetu one hnters of rest the than younger thus are Mountains Hengduan The ranges surrounding its and QTP the of history geological The c ainlIsiueo clg,11 emagr,Maseo-myeon, Geumgang-ro, 1210 Ecology, of Institute National b e aoaoyo rpclFrs clg,Xishuangbanna Ecology, Forest Tropical of Laboratory Key . www.pnas.org/lookup/suppl/doi:10. NSEryEdition Early PNAS | f8 of 1

EVOLUTION PNAS PLUS number of events is 192 versus 411. The relative contribution of in situ speciation to floristic assembly is thus 508/(508 + 335) = 0.603 for the Hengduan Mountains, and 192/(192 + 411) = 0.318 for the Himalayas–QTP. In other words, in situ specia- tion has contributed almost twice as much to the assembly of the Hengduan Mountains flora as it has to the Himalayas–QTP flora, especially since the late Miocene.

Regional Rates of in Situ Speciation and Dispersal Through Time. The rate of in situ speciation for the Hengduan Mountains region, in events per resident lineage per million years, increased almost twofold over the past 10 Ma, whereas for the Himalayas–QTP, it remained more or less constant (Fig. 3). Dispersal rates between the Hengduan Mountains and Himalayas–QTP increase gradu- Fig. 1. Map of the Hengduan Mountains region in relation to the QTP and ally over the last 4 to 5 Ma, and sharply in the last 1 Ma. By con- Himalayas. trast, dispersal from each region to temperate/boreal East Asia increases only slightly in the same time period (Fig. 4).

disproportionately to floristic assembly in the Hengduan Moun- Shifts in Diversification Rate. Seven out of the 19 clades showed tains has yet to be rigorously tested. strong evidence (Bayes factor >15) for one or more shifts in In this study we used the evolutionary histories of multi- diversification regime (Table 1). However, inspection of branch- ple plant groups to study the floristic assembly of the Heng- specific evidence (the cumulative probability of occurring in the duan Mountains region, focusing on comparisons to adjacent credible set of shift configurations, and the marginal odds ratio regions, especially the Himalayas and other geologically older in favor of a shift) in light of ancestral-range reconstructions parts of the QTP (Fig. 1). We inferred regional rates of diver- does not reveal any clear geographic patterns in the phylogenetic sification and colonization through time from fossil-calibrated locations of regime shifts (SI Appendix, Fig. S2). That is, across molecular chronograms and reconstructions of ancestral range clades, macroevolutionary jumps in diversification rate are not and rates of lineage diversification, using data from 19 clades of vascular plants chosen for their potential to inform the biogeo- graphic history of the Hengduan Mountains. Our primary aim was to discover the differences in tempo and mode of biotic assembly that help account for the remarkable diversity of the Hengduan flora. Results Contrasting Histories of Floristic Assembly. Reconstructed biogeo- graphic histories of the selected clades reveal distinct patterns of floristic assembly across regions when plotted as the cumula- tive number of colonization and in situ speciation events through time (Fig. 2). We focus here on contrasting the Hengduan Moun- tains region with a combined Himalayas–QTP region to the west and temperate/boreal East Asia to the east (Delimitation of Biogeographic Regions). Given geological and paleontological evidence that the Hengduan Mountains are younger than the Himalayas–QTP, we expected to find that its flora was assembled more recently. Instead, we found surprisingly deep phylogenetic histories of Hengduan occupancy, with initial assembly of its flora predating that of the Himalayas–QTP. In more than 95% of the pseudoreplicated joint histories the earliest colonization event occurs by 64 Ma for the Hengduan Mountains and by 59 Ma for the Himalayas–QTP; in situ speciation begins later, starting by 34 Ma and 19 Ma, respectively. By contrast, in temperate/boreal East Asia, which was commonly reconstructed as the root ances- tral area for clades, in situ speciation initially occurs by 155 Ma and colonization initially occurs by 60 Ma. For all regions, species accumulation by each process is Fig. 2. Assembly of regional floras by colonization and in situ specia- approximately exponential (log-linear) following initiation until tion events in 19 plant clades, inferred from ancestral-range reconstructions about the last 8 Ma. During this earlier “constant” phase, assem- on time-calibrated molecular phylogenies. Shaded regions indicate the 5 bly in both the Hengduan Mountains and Himalayas–QTP is to 95% quantile intervals for the cumulative number of events through dominated by colonization, whereas in temperate/boreal East time from 500 pseudoreplicated joint biogeographic histories designed to Asia the dominant process is in situ speciation. Following this account for phylogenetic uncertainty (discussed in the text). Panels on the phase, the assembly dynamics of the Hengduan Mountains and right focus on the last 20 Ma, in which differences in regional assembly are Himalayas diverge considerably, with relatively little change in most apparent. In the Hengduan Mountains region, cumulative in situ spe- ciation overtakes colonization about 8 Ma, whereas for the Himalayas–QTP temperate/boreal East Asia. In the Hengduan Mountains, the colonization remains the dominant process. In situ speciation thus seems cumulative number of in situ speciation events overtakes that to have played a disproportionately large role in assembling the Hengduan of colonization around 8 Ma, and by the present the median Mountains flora since the late Miocene compared with the Himalayas–QTP, number is 508 versus 335. In the Himalayas–QTP in situ specia- consistent with the theory of uplift-driven diversification in the Hengduan tion never overtakes colonization, and by the present the median Mountains region.

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Ma, of Fig. 37 and uplift Appendix, species; Ma (SI the 28 Hengduan (about predate the shifts rate of respectively) these of most times the hold ancestrally however, are together that clades and in Hengduan inferred are Heng- increases S2 clade’s separate Fig. the two of , Appendix most Ma (SI containing 1.7 species branch about duan a inferred of is stem diversification the In net along and 5). in region (Fig. increase Hengduan species an independently the Hengduan surea, increased by in dominated originated diversification currently each of net are that window Ma clades a two 15 in in to that 9 suggest Macroevo- Lagrange of about Analysis and (Bayesian Mixtures) BAMM lutionary from results which in any of occupancy or colonization region. particular the with associated obviously Hengduan the to the relative with speciation Ma, situ in 8 in about increase Himalayas–QTP. the diverge striking in a to (discussed showing his- begin Mountains uncertainty joint rates phylogenetic pseudoreplicated Regional for 500 text). account from to intervals designed quantile areas tories 95% shaded to and biogeo- medians 5 indicate inferred Lines indicate clades. from plant 19 regions of histories Himalayas–QTP graphic and Mountains Hengduan 3. Fig. igadRee and Xing before so did QTP after central only and Himalayas height the the whereas current that time, their indicate this achieved paleontology and Mountains because geology Hengduan the point, of reference context, studies important this an previous the speciation as In emerges of situ Miocene activity. late prediction in mountain-building the that with con- particular increases hypothesis reflect in diversification Hengduan to orogeny, the uplift-driven of differences of one times regional that of trasting expected floras, assembly temperate We the richest Mountains. lin- to world’s situ the colonization in of of and contributions diversification relative eage the quantifies analysis Our Discussion informative. less shift geographic the the of rendering context phylogeny, as the of reconstructed most is Bayes across region by ancestral Mountains supported Hengduan not the in are and but shifts factors, respectively, regime Ma, with 5 models and cases con- 7 both the about in ancestry clade Hengduan each of for text diversification net in increase one show Cremanthodium–Parasenecio oal xeto oti eea atr is pattern general this to exception notable A oln siae fi iuseito ae hog iefrthe for time through rates speciation situ in of estimates Rolling ope,bac-pcfi measures branch-specific complex, .Smlry nDelphineae, in Similarly, O). Isodon n the and Rhododendron, Ligularia– Saus- n iaaa–T nrae ntels arltv odseslbetween dispersal to Asia. relative East temperate/boreal Ma Mountains and 2 region Hengduan last either the the in between 500 increases Dispersal Himalayas–QTP from text). and intervals the indicate quantile in uncer- (discussed Lines 95% phylogenetic for tainty to account clades. to 5 designed plant histories indicate joint 19 pseudoreplicated areas shaded of and regions histories medians Asia biogeographic East inferred temperate/boreal from and Himalayas–QTP, Mountains, duan 4. Fig. Hengduan accu- the of more orogeny be with could coincident diversification as of some interpreted least cases rately at that referenced suggest the results our of and advice, in that is of Himalayas–QTP spirit the the species- from more 7). region and p. Mountains younger 13, Hengduan the (ref. rich Karako- distinguishing E” on the and to focus Pamir Mountains our the Hengduan Here, and N, W, the the the in to to those ram range and TP Kunlun the in the of keep biota Himalayas, the also in differences should expected recom- discussions mind and “Biogeographical uplift, QTP that and to mended divergence (Miocene lineage young liter- of relatively estimates sciences later) attributed Earth incorrectly the and misinterpreted ature have studies logenetic lineages. affected turnover the and ancestral extinction in subsequent and and/or ages time, deeper clade in greater ranges the estimating by masked with be associated could pulse uncertainty alter- a gradually; such is of more It signal S4). uplifted the Fig. natively, were Appendix, Himalayas (SI the separately that or as 3) possible treated (Fig. are QTP Himalayas the the of whether part evident diversifi- is uplift-driven none of but pulse similar cation, a predict would 28) 21, (15, situ esti- in independent orogeny. recent with of mates by temporally coincides Mountains disproportionately that Hengduan assembled diversification the been remarkable that has indicates colo- a flora This overtakes yielding 2). speciation (Fig. cumulative 3), nization which (Fig. at increased Mountains diversification point situ inflection Hengduan in of the rate the in Ma show 8 events, about geological after of timing that make the which about inferences, assumptions phylogenetic prior our no Here, 21). 17, 15, 13, (4, narcn eiw enr(3 rudta ueosphy- numerous that argued (13) Renner review, recent a In Miocene middle to early the during orogeny Himalayan Rapid oln siae fclnzto ae hog iefrteHeng- the for time through rates colonization of estimates Rolling NSEryEdition Early PNAS | f8 of 3

EVOLUTION PNAS PLUS Table 1. Bayes factor support for shifts in diversification in sampled clades, relative to the null hypothesis of no shifts No. of regime shifts

Clade 1 2 3 4 5 6 7 8 9 10 11

Acer 31.76 71.62 26.07 5.59 1.05 0.12 Allium 14.24 182.48 1,048.16 3,836.48 6,668.16 7,038.72 5,401.60 3,015.68 1,382.40 409.60 163.84 Clematidinae + Anemoninae 6.74 6.82 4.10 1.72 0.44 0.16 0.05 Cyananthus 0.96 0.52 0.18 0.06 0.02 0.00 Delphineae 377.43 5,871.71 6,889.71 4,316.57 1,872.00 566.86 137.14 36.57 Isodon 8.18 8.60 5.23 2.23 0.94 0.19 0.06 Ligularia–Cremanthodium– Parasenecio complex 1.64 1.41 0.80 0.32 0.12 0.04 0.01 Lilium + Nomocharis 0.17 0.041 0.01 Meconopsis 0.77 0.32 0.10 0.02 0.01 Microsoroideae 3.83 4.37 2.79 1.19 0.38 0.11 0.07 Pinaceae 40.78 29.36 10.15 2.17 0.34 0.05 Polygoneae 550.12 1,841.18 7,241.41 8,086.59 5,225.41 2,304.00 783.06 165.65 Primulaceae 2.13 2.18 1.54 0.77 0.36 0.09 0.06 0.02 Rhodiola 1.94 1.92 1.33 0.71 0.26 0.08 0.02 Rhododendron 17.76 87.97 247.00 289.51 215.75 111.64 40.47 9.76 2.30 Rosa 1.31 0.90 0.42 0.18 0.03 0.01 Saussurea 7.30 20.21 21.68 13.56 6.26 2.01 0.35 Saxifragaceae + Grossulariaceae 1.91 1.52 0.72 0.26 0.04 0.00 Thalictrum 1.57 1.25 0.67 0.28 0.10 0.02 0.01

Strong support (value >15) is indicated in bold.

region, not the older QTP. Indeed, several of the studies cited rently and jointly set a stage of ecological/evolutionary oppor- in Renner (13) are the original sources of molecular data for tunity. During the early to middle Miocene, the southern QTP the clades analyzed here and include many Hengduan species. had already achieved its current elevation (15) and was covered It thus seems important to emphasize that, despite precedent by coniferous and deciduous-leaved forests (36, 37). As Heng- in the literature for considering the Hengduan Mountains to be duan uplift proceeded, falling temperatures would have driven simply part of a greater biogeographic region that includes the the treeline lower, increasing the extent of shrublands, mead- Himalayas and QTP (e.g., refs. 26, 27, 29, and 30), the Heng- ows, and scree slopes—habitats where most of the species in our duan region actually has a very distinct history of assembly that dataset occur and would have diversified. Similar changes would reflects its younger age. also have occurred in the Himalayas and QTP, but in compar- Why did in situ diversification in the Hengduan Mountains ison with those areas moisture in the Hengduan region would increase since the late Miocene, and, more specifically, to what have been abundant, because by then the summer monsoon was extent was it driven by orogeny? Further studies are needed. One established, and the central QTP and Central Asian interior might look for contrasts between the Hengduan Mountains and had aridified (13). This predicts that carrying capacities—and by adjacent regions in the evolution of ecological traits and envi- extension, diversification potential—of the Hengduan region’s ronmental tolerances (e.g., ref. 31) across multiple clades. These newly formed habitats were enhanced by greater summer may reveal, for example, the extent to which speciation within rainfall. a region is associated with adaptive divergence and niche-filling, Although not a driver of diversification per se, it is important as opposed to nonadaptive processes such as genetic isolation to consider the effects of glaciation and climatic oscillations dur- and drift arising from dispersal limitation and topographic effects ing the Pleistocene, and the possibility that our results can be (vicariance, emergence of sky islands, etc.). These analyses would explained, at least in part, by regional differences in extinction require denser and more fine-grained taxonomic and geographic caused by these factors. In the Hengduan region, the north–south sampling than was possible here, in addition to the requisite trait orientation of major valleys suggests that extinction was relatively data. However, we suspect that evidence for common processes low, because species would have been able to persist by migrat- will prove elusive, because the proximate causes of diversifica- ing relatively unhindered toward southern ice-free areas during tion are likely to be idiosyncratic and involve a variety of con- glacial cycles; as a result, the region’s history of in situ diversifi- tingencies and associated variables (e.g., refs. 32 and 33). For cation would be better preserved in time-calibrated phylogenies, many clades, factors unrelated to uplift per se, such as biotic simply because fewer branches would have been “pruned” by interactions, are almost certain to have played important roles extinction. By contrast, in the Himalayas–QTP, the east–west ori- (3, 13, 34). For example, in Pedicularis (Orobanchaceae) diversi- entation of valleys would have inhibited southern displacement, fication of the many Hengduan species may have been facilitated leading to greater extinction. In this case, the pruning effect of by recurrent divergence in floral traits associated with pollina- extinction would yield lower estimates of in situ diversification tor sharing and reproductive interference (e.g., ref. 35), in com- during the Pleistocene. bination with other mechanisms promoting population isolation, This pattern is probably not due solely to differences in glacial including uplift and associated aspects of landscape and resource extent. Numerous studies of species distributions (e.g., refs. 38 heterogeneity. and 39) and phylogeography (e.g., refs. 40–43) support the idea A coarser-grained view is that diversification in the Heng- that refugia occurred along the southeastern margin of the QTP duan region reflects a macroevolutionary response to the rapid as well as in areas further west and north, even at high ele- expansion of moist temperate montane and alpine habitats in vation (e.g., refs. 44–46). This aligns with geological evidence the late Miocene. At this level the effects of orogeny and cli- that ice-free areas were present across the QTP and adjacent mate change are not clearly separable, because they concur- mountains throughout the Quaternary (47). It may be that

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EVOLUTION PNAS PLUS colonized the relatively depauperate regions to the west and ered jointly. This helps explain why previous analyses of single north. clades have not yielded the pattern inferred here. Other than plants, the group that has received the most bio- The validity of our results hinges on the degree to which the geographic scrutiny in relation to the QTP and adjacent regions data are representative of the focal regions (Hengduan Moun- is birds, which present similar patterns (49), notably that in the tains and Himalayas–QTP). The clades we selected span a wide species-rich Hengduan Mountains region and adjacent forests taxonomic range, and the species exhibit a diversity of growth of SE Asia, in situ diversification during and subsequent to the forms, life histories, and habitat preferences. Taxon sampling, Miocene led to repeated colonization of the Himalayas and QTP although incomplete, is not generally biased with respect to the (e.g., refs. 31, 50, and 51). In the Himalayas, the lack of in situ focal regions (SI Appendix, Table S1) and therefore should not diversification of songbirds has been attributed to the filling of unduly affect inferences of the relative rates of assembly pro- niches by preadapted colonizing lineages (52). cesses across regions. We also expect the phylogenetic distribu- Among studies inferring biodiversity hotspot assembly from tion of unsampled species within each clade to be effectively ran- multiple clades, quantitative analyses of in situ diversification dom, which means that reconstructed phylogenies would tend and/or colonization are still rare, and ours estimates rates of to be missing more nodes—and thus inferred biogeographic both processes through time and across regions. This com- events—closer to the present. In other words, the extent to which parative framework has allowed us to characterize, at a very we have underestimated the frequencies of those events is likely basic level, changes in the tempo (rate) and mode (process) greater in the Pliocene and Quaternary than in the Miocene and of biotic assembly in relation to independently inferred time- earlier. lines of regional orogeny and climate change. By contrast, stud- Another potential source of error is in the demarcation of dis- ies of other hotspots have tended to focus on single regions or crete areas as required for biogeographic analysis. Although the biomes, and subsets of these dimensions (time, space, tempo, QTP, Himalayas, and Hengduan Mountains may have broadly and mode). For example, the high species diversity in the distinct orogenic histories, this does not translate into clearly California Floristic Province is associated with lower rates of defined borders, and to the extent such borders existed they extinction more than elevated speciation or immigration, using surely would have shifted through time, leading to ambiguity in models in which rates of lineage birth, death, and movement the present. Our definitions of these areas (Fig. 1) are thus nec- are dependent on geographic occupancy but not time (53). essarily somewhat subjective and represent our best attempts to Assembly of the Cerrado biome in Brazil has been charac- capture the essential elements of this complex system. That being terized by recent (late Miocene onward) in situ adaptation said, our results are robust to the treatment of the Himalayas and of lineages to fire resistance (54), with some clades, espe- QTP as a single biogeographic area; an analyis of recoded species cially in the campos rupestres highlands, showing evidence of range data treating them as separate areas yielded the same sig- endemic radiation [e.g., Mimosa (54, 55), Calliandra (56), and nature of uplift-driven Hengduan diversification (SI Appendix, Chamaecrista (57)]. In the P´aramo biome of the Andes, analy- Additional Analyses of Biotic Assembly and Figs. S3–S5). ses of net diversification (but not immigration) yielded the high- est average rate compared with eight other hotspots and appear Materials and Methods driven more by Pleistocene climate oscillations than orogeny Clade Selection and Phylogeny Reconstruction. Our criteria were that each (58). Clearly, for the Hengduan Mountains, much remains to clade (i) included a substantial number of species that occur in the Heng- be studied about how patterns of assembly through time break duan Mountains, as well as their closest known relatives in other biogeo- graphic regions, (ii) had sufficient molecular data available to infer a phy- down at a finer scale of particular biomes and habitats within logeny that was broadly representative of the clade’s taxonomic diversity the region. and geographic range, and (iii) had fossil data suitable for molecular clock The Andes, perhaps the world’s richest mountain hotspot (2), calibration or secondary calibrations inferred from fossil dated phylogenies. are a compelling subject for comparison with the present results. We found 19 clades—17 of angiosperms and one each of gymnosperms The tropical montane/alpine habitats of the Andes are geo- (Pinaceae) and ferns (Microsorioideae)—that met these criteria. The com- graphically isolated, whereas the temperate Hengduan region bined taxon sample included 4,668 ingroup species, of which 930 occur in is embedded in a network of high mountains surrounding the the Hengduan Mountains region, 703 in the Himalayas–QTP, and 1,045 in QTP and proximate to cool high-latitude habitats. It thus stands the remainder of temperate/boreal East Asia (Delimitation of Biogeographic to reason that dispersal figures prominently in Hengduan biotic Regions). About 370 species are shared between the Hengduan Mountains and Himalayas–QTP regions. Across clades, the proportion of species sam- assembly, compared with the Andes, in which endemic radiations pled ranged from 20 to 97% globally and 26 to 94% for the Hengduan are the more dominant pattern (e.g., refs. 5, 7, 34, 59, and 60). Mountains region (SI Appendix, Table S1). Prevalence of dispersal is likely the main reason that we find For each clade, we assembled molecular sequence alignments (Dataset little evidence of macroevolutionary jumps in diversification rate S1) and fossil calibration data and used relaxed molecular clock mod- associated with Hengduan colonization in individual clades. In els implemented in BEAST (Bayesian Evolutionary Analysis Sampling Trees) our phylogenies, clades tend not to be entirely endemic to the (62, 63) to generate a Bayesian posterior sample of time-calibrated phylo- Hengduan Mountains or Himalayas–QTP; dispersal is common genies and the associated maximum-clade-credibility tree (SI Appendix). and reflects the fact that these regions are not defined by differ- Inference of Range Evolution and Lineage Diversification. ences in biome but share broad physiographic similarities that Delimitation of biogeographic regions. We delimited 11 biogeographic presumably have facilitated biogeographic exchange. That is, regions (SI Appendix, Fig. S1) and scored the range of each sampled species dispersal between these regions should not necessarily require as its presence or absence in these regions based on floras, online databases, extensive ecophysiological adaptations that may be difficult to and published datasets (SI Appendix and Dataset S2). Delimitations reflected evolve (61), countering expectations of infrequent colonization our need to accommodate the global distributions of the selected clades events followed by endemic radiations (cf. ref. 60). For this rea- and the granularity of available species range data, and most importantly son our data are perhaps not well-suited for BAMM, which to focus on distinguishing the Hengduan Mountains region from adjacent, models diversification shifts as relatively rare events. Moreover, geologically older parts of the QTP, especially the Himalayas (Fig. 1). the link between dispersal events and shifts in diversification The Hengduan Mountains region, following Boufford (8), is bounded to the west by the Yarlung Tsangpo River in eastern Xizang (Tibet), to the regime is further obscured by the inherent uncertainty associated northwest by the high plateau in Qinghai, to the north by the Tao River with inferring their phylogenetic locations. The most appropriate in southern Gansu, to the east by the Sichuan Basin, and to the south by interpretation may simply be that the signal of higher diversifica- subtropical forests and the Yunnan–Guizhou Plateau (Fig. 1). We delimited tion in the Hengduan region is more or less diffuse across clades the complementary “Himalayas–QTP” region as including the plateau itself, and emerges only when their biogeographic histories are consid- the Himalayas to the south, the Kunlun Mountains to the north, and the

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For ages bio- logenetic distribution regions. the that a Himalayas–QTP about inferred so explic- or beliefs we We Mountains dispersal, (SI prior Hengduan 3. on of adjacency the to constraints independent of set spatial were temporal was on inferences size any based geographic range placing maximum allowed avoided the was itly and dispersal S1) Fig. which Appendix, in Lagrange 65) in model (64, dispersal-extinction-cladogenesis a using ingroups all for South and reconstruction. America, range Canal). Ancestral North Panama the Europe, the of Africa, of (south Australasia America (south Lanka), Papuasia), India Sri Asia Pacific), and including southeast southwestern Himalyas, the Malesia, Range), and China, Kunlun Zealand, New the of including Uyghur (Australia, of regions Asia, Xinjiang north tropical East the the (including of (including to regions Asia Region temperate central/western Autonomous and Taiwan), Russia and of Japan part boreal ern con- of purpose region. Hengduan the the serves with effectively trasting which delimitation, combined the on Appendix, (SI outcomes on do Assembly to effect attempted species no We bio- them. with on for between so, data differentiate unit to available difficult single it of a made granularity ranges as the the treatment however, of their analysis; histories against geographic geological argue distinct QTP The and northeast. Himalayas the to Mountains Qilian igadRee and Xing .L W iJ(93 rlmnr oitcsuyo h edpat rmtergo of region radia- the from plants seed plant the on study alpine floristic preliminary A Mountains. (1993) of J Hengduan Li China’s XW, ubiquity Li hotspot: 9. Biodiversity The (2014) D (2015) Boufford 8. GW Atchison CE, Ericaceae. the of Hughes radiations The mountains: 7. the as old As (2015) abiotic al. et The O, Schwery (2016) CC 6. Davis the A, for Mulch Plateau A, Qinghai-Tibetan the Antonelli of FL, uplift Condamine LP, the Lagomarsino of role 5. The (2015) al. et plants of A, diversifications Favre Evolutionary (2014) H 4. Sun Y, powerhouse. Zhong ZL, diversity Nie JQ, plant Zhang J, Andean Wen tropical mountain 3. from The Biodiversity (2016) (2013) CE A Hughes Antonelli A, 2. Mulch V, Mosbrugger C, Hoorn 1. h te ein edlmtdaetmeaebra atAi teeast- (the Asia East temperate/boreal are delimited we regions other The 0 oeua-lc aeshv ikdspoe eetulf oyugnd ages. node young to uplift recent supposed Biogeogr linked have papers molecular-clock 100 contradictions. and review. 297–311. Mountain. Hengduan Mountains. Hengduan the 72:24–35. to Andes the 282. From tions: Phytol (Campanulaceae). bellflowers Andean in diversification rapid Phytol New of drivers biotic and biotas. Tibetan of evolution Plateau. Qinghai-Tibetan the on 210:1152–1154. building. years. Tibet. central basin, Nature 207:355–367. Tectonophysics ,btw r otcndn ihaaye based analyses with confident most are we but S3–S5), Figs. and a Geosci Nat 43:1479–1487. 210:1430–1442. 421:622–624. alSiRev Sci Natl Nature 6:154–154. Yunnan-zhiwu-yanjiu 621:1–43. 439):677–681. ilRev Biol 2:417–437. rn Genet Front eetmtdacsrlgorpi ranges geographic ancestral estimated We 90:236–253. 15:217–231. 5:1–16. diinlAaye fBiotic of Analyses Additional efcsdoraayi on analysis our focused We e Phytol New p Bot Jpn J e Phytol New 207:275– Arnoldia New 63: J 7 a D arsA,Zo D eX 21)Eouinr vnsin events Evolutionary (2013) XJ He SD, Zhou AJ, Harris YD, Gao 27. out dispersal and radiation Rapid radia- (2014) GY Island-like Rao J, (2009) Wen GA, J Allen SY, Meng Liu JQ, Zhang R, 26. Milne E, Raab-Straube von A, Susanna Y, Wang diversification 25. and Radiation (2006) RJ Abbott infer O, Hideaki to AL, Wang climates YJ, Wang and JQ, Liu vegetation 24. Neogene Reconstructing (2011) al. Basin: Sichuan et western BN, Shan, Emei Sun the 23. of Uplift (2016) G Wang E, Wang buried a K, by Meng revealed Gorge Tsangpo 22. Yarlung of control during Tectonic Tibet (2014) eastern al. et in P, topography Wang high 21. of growth Two-phase (2012) al. Tibet. et southeastern E, of Wang uplift Cenozoic 20. Late (2005) al. et MK, Clark 19. 8 ib ,e l 20)Lt eooceouino h atr agno h Tibetan the of margin eastern the of evolution Cenozoic the Late from (2002) Evidence al. et Plateau: E, Tibetan Kirby the 18. of uplift Cenozoic (2012) al. anti- et Laojunmiao Y, Cenozoic Wang late 17. the of Magnetostratigraphy (2005) al. et X, Fang 16. odPsdcoa elwhpa h il uem ws dacdPost- Advanced Swiss by Museum, supported Field P300P3 was the Fellowship work at This doc.Mobility Fellowship drafts. Postdoctoral previous Boyd on a comments valuable for ers ACKNOWLEDGMENTS. configurations. shift distinct of sam- set individual credible for shifts shift) 95% regime a the of clade, of and favor each in branches, numbers evidence For distinct (relative burn-in. ratios the odds as marginal for run sam- pled, the factors effective of Bayes the 10% calculated first calculating we the and discarding trace visually after by size likelihood convergence ple the assessed ran of and generations We plots 1/1,000 million shifts. of inspecting 10 expected frequency for 10 sampling analysis of a Carlo prior with documenta- Monte a BAMM chain tested the Markov also BAMM in we each recommended expected clades as the larger 1, on for to prior tion; geometric shifts all the regime For set of function. we number species setBAMMpriors 500 the than using smaller clades empirically level Appendix set finest (SI were the incom- at possible extinction for fractions resolution sampling statistically taxonomic assigned account we of can so It sampling, tree. taxon plete phylogenetic time- possibly a distinct death, on and of birth locations dependent) lineage and of proce- parameters, (rates Carlo number, regimes Monte the macroevolutionary chain estimate the Markov jointly and uses to 2.5 BAMM dures version (66). BAMM package using R lengths, BAMMtools branch mean maximum-clade-credibility posterior clade’s with each tree, for rate diversification Bayesian of generated inferences we geography, of of rates independently in diversification heterogeneity lineage diversification. understand better to and of analysis regional-process in rates confidence data. and topologies sequence support, Geography-independent the tree clade by of particular provided levels any times, the divergence on his- reflect condition and joint lengths not pseudoreplicated branch do the or thus from results calculated Our were tories. quantiles) 95% to (5 iaineet farea of events nization rmo h hns cdm fSine YX) n S rn DEB-1119098 Grant NSF and (Y.X.), R.H.R.). Sciences (to of Academy Chinese the of gram between colonization of extinc- rates local capita minus per colonization as rolling regions and (the calculated period speciation also previous situ We the in tion). in region of the in sum lineages period cumulative inferred 1-My a of in number region the per a in is inferred of events speciation estimates situ in rolling of as of calculated rates estimates speciation We situ region-specific in time. capita allowed through This processes periods. the assembly 1-My affecting into events and them extinction Asia, binned East local temperate/boreal and and Himalayas–QTP, Mountains, colonization, Hengduan speciation, situ in iica)aetmoal orltdwt rgne fteQTplateau Q–T the of Mountains. orogenies Hengduan with the and correlated temporally are Liliaceae) Nomocharis, lineage plant alpine Evol an Phylogenet of Mol Plateau Qinghai-Tibetan the of Plateau. of tion Plateau. Qinghai-Tibetan the of uplift the within China. Yunnan, 304:328–336. western in uplift tectonic Miocene. Early in Sci Plateau Tibetan Earth the of propagation eastward for Implication Tibet. Southern in canyon Cenozoic. the 528. 1–20. lta:Ifrne rm4a/9rad(-h/ethermochronology. (U-Th)/He and 40ar/39ar from Inferences Plateau: Basin. Qaidam western 187. the of evolution tectonic–sedimentary Tibetan northern the for implications its and uplift. Mountains Plateau Qilian northern the in cline Saussurea ilJLn Soc Linn J Biol d 115:29–39. ij Ligularia–Cremanthodium–Parasenecio (t ) a Geosci Nat c hn e D Ser China Sci = c Atrca:Crua)tigrdb pit fteQinghai–Tibetan the of uplifts by triggered Cardueae) (Asteraceae: ij (t 77:147–158. )/n 97:893–903. etakD ofodadtreaoyosreview- anonymous three and Boufford D. thank We j 5:640–645. i rmarea from Science (t − 48:1040–1051. o hlgntEvol Phylogenet Mol ) where 1), λ(t 346:978–981. 558 h ine ude aet Pro- Talents Hundred Pioneer the 158528, ) o hlgntEvol Phylogenet Mol i = o l siae,cndneintervals confidence estimates, all For . s(t c aaoeg,Pleciao,Palaeoecol Palaeoclimatol, Palaeogeogr, )/n(t ij (t stenme fifre colo- inferred of number the is ) − ope Atrca)tigrdby triggered (Asteraceae) complex .Pir o pcainand speciation for Priors ). 68:443–460. ) where 1), NSEryEdition Early PNAS ocmlmn the complement To 38:31–49. Rhodiola s(t esiFront Geosci stenumber the is ) Lilium Geology t (Crassulaceae). and Tectonics (including | n(t 33:525– Asian J 3:175– f8 of 7 − 21: 1)

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