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I&ff>ACTOF THE EOCENE ON Constance I. _lfilEar2 THE EVOLUTION OF PI;\-L-S L."

Pinus evolved in middle latitudes of the Northern Hemisphere in the middle Mesozoic. By the late Cretaceous pines had spread east and west throughout Laurasia, attaining high diversity in eastern Asia, the eastern United States, and western Europe, but having little representation at high northern latitudes. Changing climates in the early Tertiary established warm and humid tropical/subtropical conditions in a broad zone to 70QN throughout middle latitudes. Pines and their relatives disappeared from many middle-latitude areas during this time and were replaced by diverse angiosperm taxa of the boreotropical flora, which were adapted to the equable, tropical climate. The effect of this climate change and spread of boreotropical flora was to displace pines from their former habitats. A hypothesis is defended that pines shifted, during the three warm periods of the Eocene, into three major refugial areas in the Northern Hemisphere: high latitudes, low latitudes, and upland regions of middle latitudes, especially in western North America. Some of these refugial areas (e.g., Mexico/Central America) underwent active volcanism and mountain- building in the Eocene and became secondary centers of pine diversity. Many phylogenetic patterns within Pinus can be traced to this fragmentation, isolation, and evolution in Eocene refugia. Subsections Oocarpae and Sabinianae appear to have originated from refugia in Mexico and Central America. Older subsections such as Sylvestres, Ponderosae, Contortae, and Strobi were distributed over several refugia; subsections Leiophyllae, Australes, and Cernbroides evolved in southern refugia in Rorth America; and Canarienses evolved in southern refugia along the Tethys seaway in Eurasia. Following the cooling and drying of the climate at the end of the Eocene, many angiosperm taxa of the boreotropical flora became extinct and pines recolonized middle latitudes, a zone they have occupied to the present. Migration out of refugia provided additional opportunities for hybridization and introgression, as formerly isolated lineages expanded and met.

The past two decades have seen an explosion of understanding of the origin of the genus (Miller, information on the paleohistory of the Earth. Ev- 1976, 1977, 1982, 1988; Robison, 1977; Black- idence on plate tectonics has clarified the position well, 1984; Stockey & Ueda, 1986; Stockey & of continents in different ages, continental geo- Nishida, 1986). Similarly, studies on the Quater- morphology, and the dynamics of inland seaways nary history of pines have led to new interpretations and changing coastlines. Physical and biological about the impact of recent paleohistoric events on evidence has been used to infer paleoclimates with the genetic structure and evolutionary relationships finer resolution in time and space. New fossil dis- of extant species (Critchfield, 1984, 1985). coveries have added to the record of past vege- The broad-scale events that influenced the evo- tation, and new diagnostics for identifying taxa lution of the genus between its origins in Mesozoic have led to systematic revisions of many fossil (Table 1) and its present diversity remain obscure. floras. The widespread use of radioisotope dating How did important secondary centers of pine di- has added precision to determining the ages of fossil versity in Mexico, western North America, and floras. eastern Asia originate? How do these areas relate This information, together with phylogenetic to the primary centers of origin for the genus? analyses of extant taxa, has contributed new in- What events triggered the diversifications of taxa sights and a revised understanding of evolution for within the genus, and how have historical events many plant groups. In pines (family Pinaceae, ge- influenced current and fossil distribution? Although nus Pinus L.), major syntheses have focused on there have been important contributions to under- two time periods in the history of the genus. Studies standing regional biogeography and evolution of on the Mesozoic history of the pine family. and pines in the Tertiary (Eguiluz Piedra, 1985, 1988; especially Pinus, have significantly changed our Axelrod. 1986; Lauria, 199l), the impact of Pa-

I especially thank B. B. Kinloch for valuable discussion and review of the manuscript. I also thank D. Axelrod, L. Loveless. C. Miller, S. Strauss, E. Zavarin, and an anonymous reviewer for critical comments on the manuscript. I dedicate this paper to the late W-. B. Critchfield (1923-19891, whose studies on the impacts of the Pleistocene on conifers demonstrated that genetic structure of extant species cannot be understood without looking to the past. ' Institute of Forest Genetics, Pacific Southwest Research Station, U.S.D.A. Forest Service, Berkeley, California 94701, U.S.A. Annals of the Missouri Botanical Garden

TABLE1. Approximate ages and durations of geological eras from the Mesozoic to present.

Duration (millions Millions of Era Period Epoch of years) years ago Cenozoic Quaternary Holocene Approximately the last 10,000

Pleistocene 2.4 2.5 Tertiary Neogene Pliocene 4.5

-7 1 Miocene 19 2 6 Paleogene Oligocene 12 34' Eocene 16 54 Paleocene 11 6 5 Mesozoic Cretaceous

Jurassic

Triassic

' The Oligocene-Eocene boundary is accepted to be 34 Ma, coinciding with the terminal Eocene event. Authors publishing before the middle 19170s and some current ones accept the boundary as 38 Ma. leogene (Paleocene through Oligocene) events, es- 1989). At tropical latitudes, pines occur only in pecially the Eocene, on the evolution of the genus uplands or semi-arid regions. as a whole has not been analyzed. In this paper, I Pinus contains more species than any other attempt to synthesize recent information on plate genus of conifers, although Podocarpus may rival tectonics, climate, fossils, and biogeography of pines it. Pines have been recognized since Classical times, and other dominant plant groups as they affected and more than 40 classification systems have been pine evolution. From this synthesis, I argue that proposed (Critchfield & Little, 1966; Mirov, 1967; the Eocene was one of the most important phases Little & Critchfield, 1969; Price, 1989; Millar & in pine evolution. Kinloch, 1991). The most widely accepted is the system of Little & Critchfield (1969), which built upon and modified the classification of Shaw (19 14, SYSTEMATICSAND CURRENT 1924). Little & Critchfield (1969) divided Pinus BIOGEOGRAPHYOF PIW s into 3 subgenera, 5 sections, 15 subsections, and The genus Pinus is one of the most widely dis- 94 species (Fig. 3). They updated the classification tributed genera of trees in the Northern Hemi- by incorporating new types of information based sphere. Pines occur predominantly at middle lati- on genetic data, especially from contemporary tudes (30'-55ON), but important centers of pine studies on hybridization and biochemical variation. species also exist at high (> 5S0N)and low latitudes Thus, their classification implicitly suggests phy- (< 30°K) (Figs. 1, 2; Critchfield & Little, 1966). logenetic relationships and common origins of spe- Pines are abundantly represented in North Amer- cies and groups of species. Since the time of Little ica, Central America, Europe, and Asia, with some and Critchfield's classification, several new species taxa extending into northern Africa. Within their have been described, especially from species-rich range, pines occur in diverse habitats, extend from and as yet still incompletely known regions such sea level to 3,700 m, and dominate natural veg- as Mexico. In this paper, I accept Little and Critch- etation in many regions. They are absent from hot, field's authority for species, and cite authors of wet, tropical environments, where they are poor taxonomic names only for those taxa outside of competitors with other taxa (Mirov, 1967; Bond, their system. I also accept most aspects of their Volume 80, Number 2 Millar 1993 Evolution of Pinus Annals of the Missouri Botanical Garden a, 0 231 c 3 a- The Genus PINUS Little and Critchfield re, ru

Subgenus: I --C------4 Section: Ducampopinus I Subsection: KreTp'ani Cembrae Strobi Cembroides6 Gerardianae Balfourianae Cananenses Leiophyllae Plneae Sylvestresm Ponderosae Australes Contortae &Carpa@ Sabinianae

Species: albi&ulis strobus cananensis biophylta pinea resinosa cembra monticola edulis bungeana longasva roxbumhii lumhokii tropicalis washoensis taeda wnforta attenuata couheri echinata virginiana muricata tormyana sibirica lambertiana quadrifolia aristata nigra jeffreyi koraiensis flexilis monophylla engelmannii Qlabra dausa Patufa pumila strobifarmis cuIminimla durangensis n9aa 9regQti mugo serotina oocafpa ayacahuite maximartinen' i pinaster pinceana montezumae Pungens pringbi w- hawegii elliottii amandii nelsonii brutia gnffithii sykestris michoacana caribaea dalatensis dens#lora pseudostrobus occidentafis pawiflora thunbergiana douglasiana cubensis morrisonicola massoniana teoCOfe fenzeliana taiwanensis lawSonii wangii luchuensis hwangs- hanensis tabulaefomis yunnanensis insularis merkusii

FICLJRE3. Taxonorny of the genus Pirtus according to Little & Critchfield (1969), showing the species classified into subgenera, sections, and subsections. Annals of the Missouri Botanical Garden

classification as the best presently available hy- The earliest known pine. P. belgica, from the early pothesis of ph)-logenetic relationships among the Cretaceous (about 130 Ma) was found in Belgium. groups of extant taxa. Pollen of an early Cretaceous pine was also found in amber deposits from Alaska (Larigenheim et ai.. 1960). All other pine fossils are known from middle to late Cretaceous deposits. ORIGIN OF PIKES The taxonomic diversity of fossil pines in the The prevailing hypothesis until the mid- 1970s Cretaceous record is broad: two major subgenera on the origin of the genus relied on the contem- and five subsections are represented. The origin of porary interpretation of I\#esozoic fossil flora and the genus is thought to be early-middle Mesozoic. the prevailing theories of the origin of cool tem- although probably not the Paleozoic as suggested perate vegetation (Chaney, 1940; Mirov, 1967; by Mirov (Miller, 1976; Eguiluz Piedra, 1985; Mirov & Hasbrouck, 1976). Fossil pines had been Axelrod, 1986; Millar & Kinloch, 1991). A major described from Triassic, Jurassic, and abundant change from Mirov's thinking concerns the location Cretaceous locales. with pines especially abundant of the center of origin of the genus and the paths and diverse at high northern paleolatitudes. Mirov's of subsequent radiation. At the beginning of the widely cited interpretation dated the genus to the Mesozoic, there was one land mass, Pangaea (Smith late Paleozoic or earliest Mesozoic, with its origin et al., 1981). By the early Jurassic, a northern centered in a far-northern circumpolar continent supercontinent, Laurasia, separated and began to known as Beringia. According to Mirov, the sub- drift from a southern continent, Gondwanaland. sequent evolution of pines unfolded in a steady and Although there may have been more land above progressive migration southward during the Me- sea in northern latitudes than at present (Wolfe, sozoic and Tertiary, culminating in a final south- 1985) little evidence exists for a circumpolar con- ward thrust toward the equator during the Pleis- tinent, Beringia, that would have supported the tocene. origin of pines (Hickey et al., 1983; Eguiluz Piedra, This interpretation was cast into doubt by sys- 1985; Wolfe, 1985). tematic revisions of Mesozoic coniferous fossils. Most importantly, no fossil evidence exists for Alvin, Creber, Miller, Stockey, and others com- a high-latitude Mesozoic center of origin for pines. pared internal anatomy of fossil and extant pina- Mesozoic pine fossils occur between 3 ION and 50°N ceous cones and found four diagnostic traits that latitude, with only two records from higher latitudes characterize Pinu s (summarized in Miller, 1976). (Table 2). Similarly, fossils of six species of Pseu- When previously described fossils were reanalyzed, doaraucaria and over 20 species of Pityostrobus, many that were originally ascribed to Pint~~were genera considered most closely related to Pinus reclassified in the extinct pinaceous genera Pityo- and most likely to have been the ancestral gene strobus and Pseudoaraucaria. This applied to all pool to Pinus, also occurred exclusively at middle the known pinaceous remains from the Triassic latitudes, concentrated in eastern North America and Jurassic, and many from the Cretaceous. In and western Europe (Miller, 1976, 1988). Hence, particular, all of the high-latitude macrofossils, pri- a circumpolar origin for Pinus is unsupported, and marily in the collections of Heer, 1868-1883, pine origins in middle latitudes are more likely. The originally treated as Pinus were reclassified, in regions of the northeastern United States and west- some cases, even as angiosperms. ern Europe, which would have been contiguous in The revisions. combined with new fossil discov- the early and middle Mesozoic (Smith et al.. 198l), eries in the last two decades, result in a Cretaceous are the current candidates for the center of origin fossil record of about 25 species of pines from eight of the genus (Miller. 1976; Eguiluz Piedra, 1985; Northern Hemisphere regions (Table 2; Fig. 4). Axelrod, 1986; Millar & Kinloch, 1991). Alter- About half are known from petrified cones whose natively, the diversity of Cretaceous pines and Pit- internal anatomy has been confirmed as Pinus. yostrobus in Japan suggests that pines might have Others are needle, wood, or pollen fossils, generally evolved in eastern Asia. accepted to be Pinus. Of special note is the dis- tribution of these fossil pines. Although a geograph- DISTRIBUTION OF PINES AND ic bias may be expected due to proximity of fossil CLIMATE OF THE LATE CRETACEOUS locations to active paleobotanists, fossil pines occur at middle and a few high latitudes, widely spread To understand the impact of the early Tertiary east and west, with apparent centers in the north- on pines, it is important to stress the Late Creta- eastern United States, Japan, and western Europe. ceous distribution of pines and the prevailing cli- Volume 80, Number 2 Millar 1993 Evolution of Pinus TABLE2. Distribution and affinities of fossil pines from Cretaceous deposits listed in approximate order of age (old to yourig). Paleocoordiriates from Smith et al. P (1981).

Latitude/longitude Age Identification Affinity Location Current Paleo (Ma) Reference Y. belgiccz .Sylz~rstrrs Belgium, Wealden 130 Alviri ( 1960) Pi r~uapollen gerius Alaska, Kuk River Early Larigenheim et al. (1960) P1nu.s pollen gerius Mary land Late Early Brenner (1063) Ptntls pollen genus Delaware Late Early Croot et al. (1061) IJ. ~oolzlgcrnltr hi subg. f'trtn r France Late Early Alvin (1 960) I-'. pottdero.socclcs f'onderosae/ Mississiltpi, Prentiss Co. Early Late Blackwell (1984) AILJ~TCL~C) Plr2u.s pollen Sylne\trcc Minnesota Early Late Pierce (1 957) Y. c'lernprttstl Sj lt)p,stre\ Minnesota Late Charley (1954) 1'111us sp. S? lt~cstres Delaware Late Penny (1947) I'. trrphylla Sylvestre~/ Massachusetts Laate Robison (1977) IActophyllae New York, Staten Island Late I-iollick & Jeffrey (1009) Japari, Hokkaido Late Stockey & Nishida (1986) 1'. tctmphylln Japan, Hokkaido Late Stockey & Nishida (1 986) Y. b!foli~~tu Japan, Hokkaido Late Stockey & Nishida (1986) Y. pseudotetrajjhy lln Japan, Hokkaido Late Stockey & Nishida (1986) P. jlnbelll_/>lia Japan, Hokkaido Late Ogura (1932), Stockey & Nishida (1986) Kansas Late Lesquereux (1883) Massachusetts Late Penny (1947), Robisorl (1977) New York, Staten Island Late Hollick & Jeffrey (14)09) Japan, Hokkaido Late Stockey & Nishida (1986) Japan, Hokkaido Late IJeda & Nishida (1982) Japan, Hokkaido Late Ogura (1932), Stockey & Nishida ( 1986) Y. p~cz~do~abell!fi,lrrr~~ Japan, Hokkaido Late Ueda & Nishicia (1982) I-'.lznrborcnsis Japan, Hokkaido Late Stockey & Nishida (1986) P. hokka~doc~n.srs Japan, Hokkaido Late Stockey & TJeda (1986)

New Jersey, Magothy Late Miller & Malirlky (1986) Volume SO, Number 2 Millar 1993 Evolution of Pinus

mate at the end of the hfesozoic. By the Late Cretaceous, pines had reached eastern and western edges of Laurasia and occurred at middle latitudes in many locations between these extremes (Table 2; Fig. 4). The widespread distribution of pines in Laurasia by this time indicates that wherever within middle latitudes they originated, their main route of migration was east and west, and not predom- inately southward, as Mirov suggested. Migration from eastern North America to western Europe was not impeded until late in the Mesozic, by which time Laurasia had begun to split into North Amer- ica and Europe. Laurasia severed first in the south and last in the north. High-latitude connections in the North Atlantic became increasingly reduced toward the end of the Mesozoic, and low seas may have covered the land (Ziegler et al., 1983; Tiff- ney, 1985a; Parrish, 1987). This region would have provided only minor corridors for pine mi- gration. Evidence also exists for land connections at high latitudes in the Bering Sea region between Siberia and Alaska being used as corridors for temperate-adapted flora. Within the new continents, continuing east-west migration in the late Cretaceous must have been hindered by seaways that extended the full north- south length of the continents (Kurten, 1966; Tiff- ney, 1985a). These seaways divided the continents into separate phytogeographic provinces, creating greater floristic affinities between eastern North America and western Europe, and western North America and eastern Asia, than between the east- west parts of each continent (Wolfe, 1975; Tiffney, 1985a). The Late Cretaceous was a time of climatic quiescence and equability (Parrish, 1987; Up- church & Wolfe, 1987; McCowran, 1990). Sea levels were high, and tectonic activity low, creating stable global climates. Although the breakup of Pangaea had commenced, paleocontinents were still relatively undispersed, resulting in average tem- peratures in the middle and high latitudes about 10'-20°C warmer than the present (Savin, 1977; Shackleton &- Boersma, 1981; Parrish, 1987; Up- church & Wolfe, 1987). Evidence on rainfall in the Cretaceous inferred from foliar physiognomy of angiosperms indicates that rainfall patterns were zonal. The Northern Hemisphere had a humid re- gion around the paleoequator, a dry zone at low- middle latitudes. and a zone of higher rainfall above 45ON (Parrish, 1987). In general, however, lati- tudinal gradients were shallower, and changes in temperature with latitude were about M-?4 of pres- ent gradients (Parrish, 1987; Upchurch & Wolfe, 1987). Temperature and rainfall appear to have Annals of the Missouri Botanical Garden

been stable annually, with little seasonality at Iat- %arm and wet, and high latitudes were cool and itudes below 45's (Upchurch & Wolfe, 1987). At dry (Parrish, 1987; Wolfe, 1978). Truly arid zones higher latitudes, day lengths and precipitation ap- apparently did not exist; there is no evidence for parently varied seasonallj-. The major cordillera of Paleogene arid deserts or tundra (Axefrod. 1979). the Northern Hemisphere were not developed, or Although these general trends in temperature existed only at low elevations. Volcanic activity and humidity existed throughout a broad latitudinal was minor, so there were few orographic effects zone worldwide, there was geographic heteroge- on climate and little regional diversity in climate. neity in the intensity of conditions. The warm hu- mid zone was widest in North America and western Europe, and narrower in central and eastern Asia (Chaney, 1940; Parrish, 1987; Hsu, 1983). In CHANGING CLIMATES general, continental elevations were low throughout Major changes in climate and vegetation char- the Paleogene, and upland areas apparently existed acterized the early Tertiary (Wolfe, 1990). Al- primarily in one middle-latitude region of western though these events have long been discussed by North America and in Antarctica (Axelrod, 1966; paleobotanists interested in angiosperm evolution Wolfe, 1985, 1987; Wolfe & Wehr, 1987; Wing, (Wolfe, 1975; Tiffney, 1985a, b; Friis et al., 1987), 1987). In the upland area of western North Amer- their impact on conifer evolution has not been ica, the climate was anomalously temperate com- analyzed. In general, average temperatures rose pared to other middle-latitude areas. Volcanism and and rainfall increased in the early Tertiary. The mountain-building in this area during the Eocene trends toward increasing temperature and humidity also created heterogeneity in local climates and started in the early Paleocene and continued into habitats. the Eocene, reaching maxima in the early Eocene, about 52 Ma. By this time, average ternperatures THE ANGIOSPERM BOREOTROPICAI, FLORA had increased 5"-7"C above the Late Cretaceous (Savin, 1977), and tropical/subtropical conditions The changes in climate during the early Tertiary apparently extended at many middle and high lat- drastically affected global floristics (Friis et al., itudes to 70"-80°N (Wolfe, 1985; McGowran, 1987; Wolfe, 1975, 1978, 1985). Diverse tropical 1990). High temperatures and humidity, however, and subtropical angiosperm floras appeared with did not persist stably throughout the Eocene. A1- increasing geographic representation during the though the late Paleocene/early Eocene (54-52 Paleocene and the warm intervals of the Eocene Ma) was the warmest and wettest period, there throughout broad zones at middle latitudes in both were at least two other warm periods, from about Northern and Southern Hemispheres. Originally 46 to 42 Ma, and about 36 to 34 Ma, separated identified from the London Clay formations of En- by cooler intervals that were approximately equal gland (Reid & Chandler, 1933), similar angiosperm in duration to the warm periods (Fig. 6; Wolfe, floras have been described from many deposits 1978, 1985; McGowran, 1990). Average annual elsewhere, including western and eastern North temperatures may have fluctuated as much as 7O- America (from the Pacific Coast to Nebraska and 10°C between warm and cool periods of the Eocene Texas; Vermont, Alabama), western and eastern (Wolfe, 1978). Several causes for these climatic Europe (including England, France, Belgium, Ger- developments have been suggested, including ma- many, Bulgaria, Ukraine, and Russia), northern jor tectonic events, changes in sea level, and sub- Egypt, China, and Japan (Mai, 1970; Graham, marine volcanism resulting in accumulation of at- 1972; Wolfe, 1975, 1985; Tiffney, 1985a, b). mospheric carbon dioxide and greenhouse heating Subtropical assemblages occurred north as far as (Wolfe, 1978; Parrish, 1987; McGowran, 1990; 70° in Alaska, and at other high-latitude locations Kerr, 1991). Alternatively, large amounts of car- in Canada, Greenland, and Siberia (Wolfe, 1977, bon dioxide may have been produced as a result 1985). In North America, the average zone ex- of ocean-atmosphere interactions following a major tended from 30°N to 50°N (W-olfe, 1985). The extraterrestrial impact at the Cretaceous/Tertiary origin and major radiation of many angiosperm boundary (O'Keefe & Ahrens, 1989), which led taxa is documented in these diverse Aoras. to greenhouse warming (Wolfe, 1990). Plant communities in these Paleogene floras were Although latitudinal gradation was not great, the adapted to warm, humid, and equable conditions. pattern in the Eocene differed from both the Cre- These taxa were similar to those found in modern taceous and the later Tertiary and Quaternary: in rainforest vegetation of Malaysia and other extant general, many low-latitude locations were relatively tropical rainforest regions and show comparable warm and seasonally dry, middle latitudes were adaptations. Common genera include Engelhard- Volume 80, Number 2 Millar 1993 Evolution of Phus

tia, Ficus, Pterocarya. bypa, Plat3-caryu. Feth- Wehr. 19871, Idaho (Axelrod. 19861, and Colo- erelr'ia, Atangiun, and 1Cyssa. -4 few gymno- rado (TiSCPodehouse,1933; JfacGinite, 1953) (Table sperms such as Glp-ptostrobus. Taxodium, and 3: Fig. 5). Western Yorth America in general occasionally Seqttoia occurred in these floras, but contains some of the richest plant-bearing deposits they, too, were apparently adapted to warm, humid from the Eocene in the world, and dozens of fossil conditions. floras have been described. Only a few of these Recognizing their northern locations and their contain pines and other temperate taxa. and these adaptations to warm, humid conditions, Wolfe are all concentrated in northern Idaho, central (1975, 1977) referred to these widespread angio- Wyoming. north to central Idaho, and British Co- sperm assemblages as the "boreotropical flora." lumbia. This is the region that has been identified While this assemblage in no way suggests an or- as an upland area with average elevations of 1,200- ganic, indivisible unit, it does imply that similarly 1,500 m (Axelrod, 1965; Axelrod & Raven, 1985; adapted individual taxa migrated east and west Wolfe, 1987). Pine deposits in some of these areas rapidly and unimpeded, at middle latitudes are associated with active volcanos and high ele- throughout North America and Eurasia in the early vations (e.g., Bull Run, Thunder Mountain, Axel- Tertiary. The boreotropical flora reached its great- rod, 1965, 1986; Creede. 2,500 m, Wolfe & est development in the warm periods of the Eocene. Schorn, 1989). During cool intervals, its latitudinal extent shrank. The warm humid period of the middle Eocene is represented by few pine fossils (Table 3). Pine was present at high latitudes in the Mackenzie Delta EOCENE PIKES of Alaska (80°N, Norris, 1982), at low-middle lat- The early Tertiary radiation of many angio- itudes in Borneo (ZON,Muller, 1966) and southern sperm lineages and the migration of angiosperm Alabama (36ON7 Gray, 1960), and also at a few boreotropical taxa east and west at middle latitudes middle latitudes in Nevada (50°N, Axelrod, 1966, has many parallels with the late Mesozoic radiation 1968), within the upland plateau of western North and migration patterns of pines. Boreotropical flo- America. ras occur in the same locations worldwide during Pine fossils from the subsequent cool period of the early Tertiary as pines did in the late Mesozoic. the later Eocene occurred at middle latitudes in With very few exceptions, pines are not found in Washington (Miller, 1974), Nevada (Axelrod, boreotropical fossil floras. This prompts the ques- 1966. 1968), Colorado (Leopold & MacGinite, tion, where did the pines go? 1972; Axelrod, 1986), New Mexico (Leopold & The Tertiary record of pines begins in the Eo- MacGinite, 1972), and Japan (Huzioka & Taka- cene; no pines are known from the Paleocene. Pines hashi, 1970; Tanai, 1970, interpreted by Wolfe, of the earliest Eocene occur primarily in high (65'- 1985 to be early-late Eocene), Fushun, China (Hsu, 80°N) and low (ZON) latitude deposits in North 19831, as well as a continuing presence in Borneo America and Eurasia (Table 3; Fig. 5). High-lati- (Muller, 1966) and at high latitudes (Norris, 1982) tude locations include central Alaska (Wahrhaftig (Table 3). et al., 1969; Dickinson et al., 1987; Fredericksen The latest Eocene marks the final widespread et al., 1988), Ellsmere Island, Greenland, Iceland, period of tropical conditions at middle latitudes in and Spitsbergen (Manum, 1962; Schweitzer, 1974). the Paleogene (Fig. 6). Pine fossils from the late Low-latitude pines occurred in Borneo (Muller, Eocene occur primarily at high latitudes in western 1966) and from one low-middle latitude location Siberia (Dorofeev, 1963), Alaska (Norris, 19821, of the late early Eocene. near San Diego, California British Columbia (Hopkins et al., 1972), at low (Axelrod, 1986). Pines in these deposits were as- latitudes in Borneo (Muller, 1966), and along the sociated with other pinaceous conifers and with Tethys seaway in southeastern Europe (Chiguriae- cool temperate angiosperms such as Retula, ACnus, va. 1952). Pines from the southeast coast of China, and II7rnu.s. Ages of these fossils correspond to the in the provinces of Jiang-su. Zhejian, and Fujian first warm humid period of the Eocene (Fig. 6). (Hsu, 1983). may also be from this period (Table Fossil pines from the middle Eocene continue 3 1. to be represented at high and low latitudes, but appeared for the first time in the Tertiary in middle- THE TERMINAL EOCENE EVENT AND high latitude locations in North America and Eur- PINE EXPANSIONS asia. Most of the known fossils from the cool period of the earlier middle Eocene are in western North The end of the Eocene was marked by the most America, from British Columbia (Miller, 1973; profound climatic event of the Tertiary (Burchardt, Stockey, 1983, 1984), Washington (Wolfe & 1978; Wolfe, 1978; Parrish, 1987: McGowran, 'I'ABI,E3. f)istribution arid affinities of fossil pines frorri Eocene deposits listed in approxiniate order of age (old to young). Paleocoordinates from Srriith et al. (ISSl).

Latitude /longitude Age Identificatiori Affinity L,ocation Current Paleo (Ma) Reference

1'1 ntr 5 pollen gc'Ilkli Alasha, Nerlarla 54 Wahrhaftig et al. (1969) 1" rin 5 pollen grnui Alaska, C:olville Early Frederiksen et al. (1988) /'l~/ll~? pollen gtt1us Alaska, Death Valley Early Dickinson et al. (1987) (1)isaccdtr grcllrli) 1'1 1111\ polleri g('1llli (:anada, Ellsrnere Island Early Manurri ( 1962) 1'1 nil r pollen gerltii (;rec~nlartd Early Manu~n(1 962) 13rnrr\ polleri gellui It*eland Early Marirlni (1962) I3riu 5 pollert gtwtii Spitsbergeri Early Manurri ( 1 9621, Scllweitzer (1974') 1'1r/lt5 polle11 genus North Dakota, Durin Early Leopold & MacGinite ( 1972) l'irtli \ polleri gt'rllli Northwestern Borneo Late Early Mttller (1966) 1'. rlclrrzclrcrtsi \ iuhg. Strol)us Southerr1 California 47-48 Axelrod ( 1986) 1'1nlLS ['ollerl C,'crrrt)roltiec. Sotttlierrl California 47-48 Axelrod & Raver~(1 985)

1'1 rru 5 pollen l'or/drrro\(~f, Southern (:aliftrrnia 47-48 Axelrod & Rave11 (1985) I'rnrc~ pollen gcr1ui Northeastern (kina, Mid and Late Surtg & Liu (1'376), Flsu Fuihun (1983) C'c'rnhrortJ~s (:olorado. Green River 4 7 Wodehousc: (1933), Brown (1934) S)11 cl\trfxc/ British Coltirnbia. Srliithers 46-47 Stockey (1983)

I+or/tl~ro\trc~/ -itr\trnlc,s S y Lr,cslrcs British Columbia, 46-47 Miller (1973), Stockey Princeton (1984) ~bg.Stro1)u \ Britih (:olurribia, 46- 47 Miller ( 1973) Priricetctn Sq Izlcslr(>s British Columbia, 46-47 Stockey (1984) Princeton I "orttleroaczc British Coltlmbia, 46 -47 Stockey (1984) Prirlceton 1'1rtri s pollen genus Wasllington, Republic 46-47 Wolfe & Wehr (1987) 1'. t)a!fi~rrrortics Hnl/o~cr~ctncrc Idaho, Thurider Mountain 46-47 Brown (1937), Axelrod ( 1986) Latitude /longitude Age Identification Affinity Location Current Paleo (Ma) Reference f-'rr?rr.\ pollen genus Canada, MacKenzie Delta Mid-Late Norris ( 1982) I'irzu 5 pollen genus Alabama, Claiborne Bluffs Middle Gray (1960) P. .r*lh~~lerr Strohr Nevada, Elko 4 2 Axelrod ( 1968) I-'. cro~srr Itnlfourlnncrc~ Nevada, Copper Basin 40-44 Axelrod (1966) I'. wolf PI Sj*lz,cstrca/ Washington, Little Falls Early Late Miller (1974) (,'ontortae (,'ontort UP Nevada, Bull Ruri 3 8 Axelrod ( 1968) genus New Mexico, Bernalillo 3 8 Leopold & MacGinite (1972) Southwestern Japan, Ube Early Late Huzioka & 'Takahashi (1970) I'inrrs sp. genus Japan, Kushiro Early Late Tanai (1972) I'inrrs pollen gerius Colorado. Chaffee 36-37 Leopold & MacGinite (1 972) 15clzu.spollen gerius British Columbia, Parsnip 35 Hopkirls et al. (1972) River Ylillls sp. genus Siberia, Tavda River Late Dorofeev ( 1963) 1'1~~F SF). genni Siberia, Ob River Late Dorofeev ( 1963) Prrlzls ip. gerilli Siberia, Tyrn River Late Dorofeev (1 963) l'. Sj"l1o.s" Sylt cl~trcs/ Siberia, Irtysch River Late Dorofeev ( 1963) I'or~dt~rosac. I'inus pollen gentis [Jkraine, River Dori Late Chiguriaeva (1952) I'. str~rgisri Strohr Colorado, Florrissant 34-35 MacGinite (19S3), Axelroci (1986) Strohi Colorado, Florrissant 34-35 MacGinite (1953), Axelrod ( 1986) Colorado, Florrissant 34-35 MacGinite (195 3), Axelrod ( 1986) I'inus pollen gerius Southeasterri China Late Hsu ( 1983) Annals of the Missouri Botanical Garden Volume 80, Number 2 Millar 1993 Evolution of Pinus

l6 yrs

7 Paleocene Eocene Oligocene

~aleogene I Neogene : FIGIJRE6. Estimated temperatures from four latitudes in North America during the Tertiary (based on percentage of entire leaves), indicating the warm and cool episodes in the Eocene and the drop in temperature at the end of the Eocene (terminal Eocene event). From Wolfe (1978). Reprinted by permission of American Scientist, journal of Sigma Xi, The Scientific Research Society.

1990). The fluctuations from warm to cool periods major cooling (Barron, 1985; McGowran, 1990). during the Eocene were minor compared to the Another possibility is that the formation of giant drop in regional temperatures at the end of the uplifted plateaus in southern Asia and the American Eocene. Average annual temperatures dropped ap- West led to accelerated chemical weathering, a proximately 10'-13OC, in some areas over only decline in atmospheric carbon dioxide, and a one million years (Fig. 6). The decline in average "greenhouse cooling" effect (Ruddiman & Kutz- temperatures was accompanied by a large decrease back, 1989, 1991). in rainfall and increase in seasonality. Whereas in This terminal Eocene event (Wolfe, 1978) was the Eocene the mean annual range of temperatures marked by widespread extirpation of boreotropical (seasonality) is estimated as only 3'-5'C, in the angiosperm taxa from many middle latitudes world- early Oligocene it is estimated as 25'C-about wide, leaving only remnants in a few areas where twice the range of the present (Wolfe, 1971). In the climate presumably remained mild. The ex- rnany parts of the world, complex continental cli- tinctions of boreotropical floras were mirrored by mate patterns developed, possibly for the first time, great expansion of pines and other cool-adapted and continental ice sheets first occurred in the taxa into rnany middle-latitude locations. Many of Oligocene (PtifcGowran, 1990j. Extensive volca- the same fossil-bearing sites that contained boreo- nism and mou11tai11-building in the Rocky itfoun- tropical taxa in their Iate Eocene horizons were tains, Himalayas, and Mexican ranges created local dominated by cool-temperate conifer taxa in early climatic diversity. Major tectonic events have been Oligocene horizons. In some localities, this change associated with the climatic cooling at the end of occurred in only one million years (,4xeIrod, 1965). the Eocene with two schools of thought on their The existing record suggests that pines made effect. One line of evidence suggests that changing their first Tertiary appearance at many middle- positions of the Earth's continents and oceans had latitude locations during the Oligocene (Table 4; direct effects on the Earth's climate, leading to Fig. 7), recolonizing areas where they had occurred Annals of the Missouri Botanical Garden TABLE4. Distribution anti affinities of fossil pines from Oligocene deposits listed in approximate order of age (old to young). Paleocoortfnates from Smith et al. (1981).

Latitude/longitude Age Iderltificatiori Affiriit y Location Current Paleo (Ma) Refererice I'tnrrs pollen gerlrls Oregon, Bridge Creek 3 1 Wolfe (1981), Mason (1927) I'ir~rfi pollen ge1mUS Oregon, Lyoris 3 1 Wolfe (1981) Pirrrrs pollen gerius North Dakota, Dunn County Early L'eopold & MacCinite ( 1972) f'tnus pollen geri~ts Montana, Ruby Basin 32-36 Becker (196 1), Wolfe (1 977) 1'. crossit Ra dfbl~~11zrza~ New Mexico, Hillsboro 32 Axelrod & Bailey (1976) IJ1 rz~spollen gerius British Columbia, Early Pie1 (197 11, Rouse & Matthews Australian Creek (1979) COII~~~I(LPBritish Columbia, Early-Late Banks et a!. (1981) Escalante Island Prnus polleri gerius Northwestern Borneo Early-Late Muller ( 1966) f'trrus pollen genus Gulf of Alaska Late Wolfe (1972, 1977) P. hrtchnnrcr~rr I'o ntlcr 0,cnc Washington, Olympic Late IJrlderwood & Miller ( 1 980) I). (L~~OfZ(~t2\l.5 l'ontlr~~osac Montana, Avon Late? Miller ( 1969) 1'. czrrtlrrc~rzz~ua Strobr Idaho, Coal Creek 29 Axelrot1 ( 1986) 1'. balfourortlos l~nljourtancz~ Idaho, Coal Creek 29 Axelrod ( 1986) f'rrru c pollerl genus Montana, Beaverhead Basin Laate Becker (1961), Leopold & MacGinite (1972) I'r nrc pollen gerius Colorado, Chaffee Late Leopold & MacGinite (1972) 1'. crosrrr Rolforrnnnc~~ Colorado, Creede 27 Schorn & Wolfe (1989) I'. rtogr(1trdc I'ond~rosar Colorado, Creede 27 Schorn & Wolfe (1 989) 1'. ~~(L1lJ111Lr1P1131s (:etn hrotd~c Colorado, Creede 27 Axelrod (1986), Schorri & Wolfe (1989) I'rnits ip. (,'ant ort ae Colorado. Creede 27 Axelrod (1980), Schorn & Wolfe (cf. (L~?)OT(~CII\I 5) (1989) I'r //ti 5 pollen genus Mexico, Chiapas Late Langenheirn et al. (1967) (I grain) lJrrtus pollen genrli Northwestern China, Late? Hsu (1983) Quidam f'itzris pollen gc'rnls Nortl.>westernChina, Late Sung (1958) Northwestern Garisu .!Sj 11 f>stres Western Transcaucasia Late? Czeczott (1954) .S] /l cstrcs / Eastern Transcaucasia Late? Palibin (1 935) (,'or~tort(LC Annals of the Missouri Botanical Garden

in the Mesozoic. Pines are known frorn Oligocene lations (1j occurred throughout middle latitudes in deposits that range in North America from the Gulf the Mesozoic, (2) were fragmented and displaced of Alaska (Wolfe, 1912), British Columbia (Banks to high and low latitudes and to middle-latitude et al., 1981 ), Washington (Under~$ood& Illiller, uplands in the Eocene, and then (3) reappeared 1980), Montana (Miller, 1969; Leopold & widely throughout middle latitudes in the Oligocene MacGinite, 1972), Idaho (Axelrod, 1986), Oregon and Miocene, where they remained for the rest of (Wolfe, 1981 ), Colorado (Leopold & MacGinite, the Tertiary. 1972; Schorn & W-olfe, 1989), to a single spec- The Mesozoic origin and spread of pines east imen from Chiapas, Mexico (Langenheim et al., and west throughout Laurasia apparently occurred 1967) (Table 4). In Asia, Oligocene deposits are under a warm temperate climate that was equable in eastern and western Transcaucasia (Palibin, and had little latitudinal gradation. Early migration 1935; Czeczott, 1954), and in northwest China, and radiation of pines was favored in the Mesozoic in the Quidam Basin, and in the Jinguan Basin of not only by climatic conditions, but by the absence western Gansu (Sung, 1958; Hsu, 1983). In Japan, at high-middle latitudes of competing angiosperrn pine was present as a minor component of a few taxa. Although angiosperms apparently originated floras (Tanai, 1972). Pine was abundant in the about the same time as the pines in the Early Oligocene strata of Borneo (Muller, 1966). A1- Cretaceous (Taylor & Hickey, 1990), their rise to though some of the pine-bearing deposits were as- dominance in middle latitudes did not occur until sociated with areas of volcanism and mountain- the late Cretaceous (Wolfe & Upchurch, 1986). building, others were in lowland and coastal areas The shift in global climates toward warm humid where boreotropical flora had flourished in previous conditions of middle latitudes in the early Tertiary epochs. appears to have favored the migration and radiation The climatic deterioration of the early Oligocene of angiosperms at the expense of pines. Although was followed by an ameliorating and warming trend pines have broad tolerance of climatic and edaphic during the late Oligocene and into the Miocene. conditions, they do not survive or grow well in hot Rainfall, however, stayed moderately low and cli- and humid climates (Mirov, 1967). More impor- matic conditions remained temperate at middle lat- tantly, in these conditions they are poor competi- itudes. The record indicates that pines rose in abun- tors with angiosperms in seedling establishment, dance throughout middle latitudes in North America height growth, and reproduction. Conifers domi- (Axelrod, 1986), Europe (van der Burgh, 1973; nate in areas where angiosperrn competition is re- Klaus, 1989), and Asia (Hsu, 1983) in the Mio- duced, for example, by fire, cold, or nutrient short- cene; the direct ancestors of rnany modern pine ages (Bond, 1989). species can be traced to Miocene pines. The warm Such a situation apparently initiated widespread conditions of the Miocene supported expanded pine extirpations of pines over the lowlands at middle forests at high latitudes, such as Banks Island (78'- latitudes. The remaining areas of suitable pine hab- 80°N, Hills et al., 1974), MacKenzie Delta (72'- itat acted as refugia for pines during the warm, 85ON, Ritchie, 1984), and Wrangell Mountains, humid periods of the Paleogene. Alaska (68ON, Wolfe, 1969) (Table 5). Pine fossils In general, the fossil evidence indicates three in low-latitude deposits, such as Veracruz, Mexico important refugial zones. The circumpolar high- (17"N, Graham, 1976) indicate the continued pres- latitude zone originally thought by Mirov to be the ence of pines in mountainous low latitudes, despite cradle of Pinus emerges not as a primary Mesozoic the fact that lowlands in these latitudes were dom- center of origin but as an important Eocene re- inated by boreotropical flora. fugium. Although rnany Mesozoic fossils from the polar region that had been identified as pine were later discredited, credible new records, mostly pol- IMPACTOF EARLYTERTIARY len, confirm abundant pine at many high-latitude CLIMATEov PINEEVOLUTION locations in North America and Eurasia during the warm periods of the Eocene (Table 3). Pines may EOCENE PINE REFUCIA have been even more widespread during the early The preceding overview of biogeography pro- Tertiary in polar regions than indicated by the vides evidence for the hypothesis that pine distri- geography of present land masses. Much of the butions shifted latitudinally and that pines expand- Arctic Sea is shallow, and tectonic evidence sug- ed and contracted in elevational extent several gests that there may have been more land above times frorn the late Mesozoic to the middle Tertiary. sea level in polar regions in the early Tertiary than In general, the hypothesis states that pine popu- at present (Smith et al., 1981; Wolfe, 1985). Land Volume 80, Number 2 Millar 1993 Evolution of Pinus

connections between North America and Eurasia in the North Atlantic (Tiffney, 1985a, b) would have provided high-latitude corridors for east-west migration of pines during the Eocene (TiEney. 1985a, b). The major limiting condition for plant growth poleward now is light. The suggestion that the Earth may have had a lower angle of inclination in the early Tertiary (Wolfe, 19781, which would allow more light at high latitudes, has been discredited (Donn, 1982; McKenna, 1983; Barron, 1984). Alternatively, geophysical and climatic conditions of the early Tertiary may have increased avail- ability of carbon dioxide and permitted plants to photosynthesize under light regimes that were pro- hibitive under conditions of lower carbon dioxide concentrations that apparently followed the end of the Eocene (Berner et al., 1983; Creber & Chalo- ner, 1984; Ruddiman & Kutzbach, 1989, 1991; Kerr, 1991). Low latitudes in North America and Eurasia also appear to have been refugia for pines during the warm humid periods of the Eocene. There is ample evidence that conditions in general were warmer and drier at low latitudes than at middle latitudes in the Eocene. These conditions have been docu- mented for the southeastern United States, Central America, Taiwan (Wolfe, 1975), southern China and southeastern Asia (Guo, 1980; Hsu, 1983), and Borneo (Muller, 1966). During the Paleogene, the southern boundary of Eurasia was the Tethys seaway. Since the Indian subcontinent had not collided with Asia, the area of the present Hima- layas marked the Tethys coastline in Asia. Unlike circumpolar regions, the low-latitude dry areas were disjunct and disconnected, even between the south- eastern United States and Central America, and refugial populations were unlikely to have been connected by broad migration routes (Wolfe, 1975). There is less abundant fossil evidence for pines at low latitudes than at high latitudes during the Eocene. There are few early Tertiary plant-bearing deposits in the areas of special interest, such as Mexico, Central America, and the Mediterranean, primarily due to the lack of depositional sediments (Martin & Harrell, 1957; Eguiluz Piedra, 1985). Nevertheless, Eocene pine fossils have been found at low latitudes in southeastern Asia, the south- eastern and southwestern United States, and in areas of southeastern Europe that were at low latitudes during the Eocene (Table 3). In Mexico, the single specimen of pine at Chiapas (14ON) from the Oligocene (one of the earliest Tertiary plant records in Mexico), and the abundance of pines in Annals of the Missouri Botanical Garden

veracruz (17°N) from the Miocene suggest that SECOhD4RY CEljTERS OF pines may have been present in %Iexicoand Central PIVE DIX ERSITY America earlier (Table 4j. Similarly, pines were The widespread extirpation of pine populations present in the Oligocene and abundant in -2liocene from rniddle latitudes at the end of the hlesozoic deposits from southern Europe in the region of the is hypothesized to have led to extinction of many Tethys (Palibin. 1935; Czeczott, 1954; Klipper, pine species and to have greatly depleted genetic 1968; van der Burgh. 1973; Klaus, 1989). diversity in others. Many Cretaceous fossil pines Pines were not absent from middle latitudes dur- had combinations of traits not known in extant ing the Eocene. Their presence in select fossil de- species and represent lineages that went extinct. posits from interior western North America testifies Of two closely related pinaceous genera of the to the presence of mid-latitude refugia. Pines in Mesozoic, Pseudonraucarin fossils have not been these regions more commonly date to the cool found in rocks younger than the Late Cretaceous, periods of the Eocene. During these times pine and the youngest Pityostrobus fossils date to the populations apparently expanded, whereas during early Eocene (Miller, 1976). The disappearance in the warm humid periods they contracted into nar- these two genera of many diverse lineages closely row refugial areas where conditions were favorable. related to Pinus, represents major extinctions in During warm humid periods, pines in interior west- the pine farrtily during the early Tertiary. ern North America may have been fragmented into Despite this depletion of diversity in pines and small local refugia and, therefore, poorly repre- taxa related to pines, the tectonic events and con- sented in fossil deposits. sequent migrations of the early Tertiary appear to The interior of western North America was have culminated in the creation of several new anomalous for the Eocene world in having upland areas and centers of volcanism. Several of the pine- centers of pine diversity and the evolution of new bearing deposits occurred at high elevations in Eo- pine lineages. This change appears to have been cene calderas (Thunder Mountain, Idaho; Creede, due in large part to increased tectonic activity. Colorado), where climates were more temperate Although the period from the Mesozoic through than elsewhere at middle latitudes. This region has the Paleocene had been relatively quiescent and been documented for angiosperm flora as being one land elevations were generally low across the con- tinents, by the late Eocene several regions were of the first areas at middle latitudes in North Amer- active tectonically. In subsequent epochs, volca- ica where clirnatic conditions became temperate nism and mountain-building became increasingly during the Paleogene. Widespread volcanism along important locally and globally. the cordillera added many cubic meters to the The uplift of new mountain ranges and volcanic landscape in this region, building a highland that activity created environmental heterogeneity. Ar- stretched from Arizona to Canada (Leopold &- eas where active mountain-building coincided with MacGinite, 1972; Wing, 1987; Wolfe, 1987; Paleogene pine refugia are hypothesized to have Ruddiman & Kutzbach, 1991 ). become centers of pine radiation. Local climatic Other middle-latitude areas such as eastern Asia diversity was created by elevational differences, may have supported pines during the warm humid and rainshadow and other orographic effects de- periods of the Eocene, although only western North veloped. Diversity of soils evolved, with many areas America is known to have had important upland having newly disturbed sites following volcanic ac- regions. Although the early Tertiary fossil record tivity. Mountain-building created new barriers to of eastern Asia is not as complete as in western migration and gene flow, causing lineages to be North America, pines have been found at a few fragmented and isolated. A11 these conditions must middle-latitude locations in the Eocene. In Japan. have favored divergence and speciation in pines. the first Tertiary pines date to the last cool period Conversely, refugial areas that did not undergo of the Eocene and are not documented for the major early Tertiary mountain-building, such as warm period at the end of the Eocene (Huzioka &- the high-latitude zones, were centers from which Takahashi, 1970; Wolfe, 1985). These Eocene pines migrated in the Neogene, but did not become records may represent marginal populations of spe- important centers of pine speciation. cies that were centered farther north and expanded Although pines expanded and contracted from southward during the cool periods. Boreotropical refugial areas during the fluctuating warm and cool angiosperms occurred throughout Asia in the warm periods of the Eocene, it was the terminal Eocene humid periods of the Eocene, although they do not event that seemed to initiate major migrations out appear to have extended as far north as in North of refugia and to coincide with a time when pines America (Chaney, 1940; Hsu, 1983). appeared more widespread at middle latitudes. These Volume 80, Number 2 Miliar 1993 Evolution of Pinus

migrations provided further opportunities for di- the lineages leading to P. contorta and P. banksi- vergence. As new environments were encountered, ana clearly had northern origins and boreal ad- genetic isolation may have occurred, and possibil- aptations, whereas those leading to P. clausa and ities for genetic drift by founder effects arose, as P. uirgirziana had southeastern sanities. Eocene well as for hybridization with formerly isolated lin- fossils with affinities to Contortae have been found eages. in northern Washington, and Oligocene fossils in British Columbia, corroborating a northern refug- ium (Tables 3, 4). EVOLUTION WITHIN Ht f S IN Subsection Ponderosae also may have had both RELATION TO EOCENE REFUGIA northern and southern refugia. There are 10- 17 By the end of the Paleogene, all subsections of species endemic or nearly endemic to Mexico and Pinus, with the possible exception of Cembrae, had Central America, whereas wide-ranging Pinus pon- evolved (Axelrod, 1986; Millar & Kinloch, 1991). derosa has a northern distribution and northern The events of the early Tertiary probably gave rise ecological affinities in its habitat preference and to at least two subsections, speciation of lineages vegetation associates. Early Tertiary pines most within several subsections, and the current bioge- closely allied to Ponderosae have been found in ography of many subsections and groups within British Columbia (Eocene, Table 3), northern several subsections. Washington, and Montana (Oligocene, Table 4). Lineages of Ponderosae may have been concen- The hypothesis that pines were concentrated trated also in Rocky Mountain refugia, as suggested into refugial regions during the Eocene explains by Oligocene fossils from Colorado with affinities the current bimodal distribution and pattern of to this subsection (Table 3). A recent re-evaluation diversity of pines at low and high latitudes (see of evolutionary patterns in Ponderosae also indi- Axelrod, 1986, for maps of pine subsections). In cates northern and southern division in the sub- North America three subsections, Cernbroides, section (Lauria, 1991). Pinus ponderosa is con- Leiophyllae, and Australes, appear to have been sidered to originate in northern latitudes, while concentrated in southern refugia during the Eocene other distinct phylads had southern origins in Mex- and radiated from them subsequently (Axelrod, ico and Central America. 1986). Subsections Cembroides and Leiophyllae Subsection Strobi has northern and southern seem to have been limited to western North Amer- lineages in North America. Ancestral lineages of ica and Central American refugia whereas Aus- Pinus rnonticola and P. strobus would have mi- trales may have had refugial areas with a broader grated from northern refugia, and those of P. stro- southern distribution, including the Gulf Coast (Ta- bforrnis, P. ayacahuite, and P. chiupensis (Mar- bles 3, 4). The current distribution of Australes in tinez) Andresen (distinct from P. strobus, of which both the southeastern United States and in Central it was once classed as a variety; Andresen, 1964, America/Caribbea suggests that L4ustrales may 1966)would have migrated from southern refugia. have had refugia in both regions. Although not Northern refugia are corroborated by Eocene fossil identifiable to subsection, the abundant pine fossils pines allied to subsection Strobi from British Co- of the Eocene from southern Alabama (Table 3) lumbia (Table 3). Lineages of subsection Strobi are from a site that is within the range of several may also have been fragmented into middle-latitude extant species of Australes. Small genetic distances refugia in the Rocky Mountain region, represented between taxa of Australes versus Leiophyllae currently by P. jiexilis and possibly P. strobi$or- (Strauss & Doerksen, 1991) suggest that these mis, and by Oligocene fossils from Idaho and Col- subsections were in contact or did not diverge from orado (Table 4). each other until after the Mesozoic. The small subsection BaEfourianae is an ancient Four subsections in North America appear to lineage (Kossack, 1989; Strauss & Doerksen, 199 1 ; have been fragmented by Eocene events into sev- Millar & Kinloch, 1991) that appears to have been eral refugial regions. A division into northern and entirely concentrated in middle-latitude Rocky southern refugia in subsection .!!ylcestresis indi- Mountain refugia during the early Tertiary. Pres- cated by the extant lineages of P. resinosa (4O0- ent distribution of the three closely related species 5Z0N) and P. cubensis (restricted to Cuba, 2Z0N). is in the Rocky Mountain/Great Basidsierra- Eocene fossils with affinities to Sylvestres that sup- Cascades Ranges of the western United States be- port a northern refugium have been found in British tween 35ON and 41°N latitude. Early Tertiary fos- Columbia and northern Washington (Table 3). sils with probable affinities to this subsection were Subsection Contortae similarly seems to have found in Idaho (Eocene) and Colorado (Oligocene) been divided into northern and southern refugia: (Tables 3, 4). Annals of the Missouri Botanical Garden

In Eurasia, sequences of conifer-bearing depos- as represented by extant P. bungeanu, and by its from the early Tertiary are not as widely dis- early Tertiary deposits containing pine pollen in tributed as in riorth ,+merica. but evidence for pine China (Tables 3, 4). evolution in relation to refugia exists. Three ancient Refugia for subsection Strofii in Eurasia were subsections, Canarienses, Pineae, and Krempj- mostly along the Tethys. Of the eight extant Eur- ani, have extant species restricted to regions that asian species in the subsection, only P. parvijfloru mere along the Tethys sealbay. Fossil evidence ex- seems clearly allied to lineages derived from more ists for a Tethys refugial area of pines in southeast northerly refugia. The remaining seven modern Asia, in the region where P. kremptfii now occurs. species are all distributed along the former Tethys Pine was recorded in abundance throughout early region. No early Tertiary fossils from Eurasia have Tertiary strata and in coastal southeast China and been specifically allied with subsection Strobi, al- in northwest Borneo (Tables 3, 3). Other fossil though Miocene fossils of the subsection testify to floras for southeast Asia include temperate taxa, their presence in that region (Kiipper, 1968). suggesting that pines would have found favorable The consequence of certain Eocene refugia be- habitats. coming secondary centers of pine diversity is best In western Europe, the boreotropical angio- described for Mexico and Central America. Al- sperm flora was recorded abundantly from 45'8 though parts of the Mexican and Central American to 56ON (Chaney, 1940). Although there are no isthmuses were transiently under water during the fossil records from currently low latitudes in Eu- Mesozoic (Kellum, 1944; Eguiluz Piedra, 1985), rope, pine fossils are known from areas of southeast they were elevated during the Eocene and later Europe that were along the Tethys seaway (Chi- Tertiary. Tectonic activity was especially great in guriaeva, 1952; Mirov, 1967). Furthermore, there Mexico during the late Eocene and Oligocenei is indication of dry zones in the middle Eocene Miocene. Tertiary volcanic activity significantly along the European and north African Tethys, in- reshaped the Sierra Madre Occidental and created directly supporting the occurrence of pines there the Sierra Madre Oriental and the Transversal (Parrish et al., 1982; Parrish, 1987). Fossil pines Neovolcanic Axis. Uplift in the early Eocene rebuilt allied to Canariensis and Pineae were widespread almost the entire ranges of the Sierra Madre del along the Tethys seaway in western Europe during Sur and Sierra Madre de Chiapas (Eguiluz Piedra, the Miocene (reviewed in Klaus, 1989), suggesting 1985). more widespread distributions for both subsections Mexico and Central America are home to as in this region in the early Tertiary. many as 83 extant taxa of pines, including 48 As in North America, in Eurasia several sub- species, 2 1 varieties, and 14 forms (Eguiluz Piedra, sections appear to have been divided by Eocene 1985). Within many subsections, extensive radi- events into northern and southern refugia. In Syl- ation and speciation are ongoing, which has been vestres, lineages represented by extant P. sylves- attributed to active mountain-building that began tris most likely migrated from northern refugia. in the Eocene (Equiluz Piedra, 1985; Axelrod, Eocene pine fossils from high latitudes in western 1986; Karamangala & Nickrent, 1989; Lauria, Siberia allied to Sylvestres corroborate a northern 1991). Active radiation is evidenced by closely refugium in Eurasia. The remaining 14 extant spe- related species clusters, with subsections Ponde- cies in Sylvestres. excluding P. densijora, and P. rosae and Cembroides the best examples. There thunbergiana, and possibly P. yunnanensis, rep- are 10- 17 species of Ponderosae (Eguiluz Piedra, resent lineages from southern refugia. Although 1985) endemic to Mexico and Central America few Eocene deposits from southern Europe are and 10- 16 species in Cembroides (Zavarin, 1988). plant-bearing, abundant fossils allied to Sylcestres The difficulty of separating the taxa of Cembroides, are known from Oligocene and Miocene deposits implying close genetic relationship. has led some in the Tethys region (Table 5; Palibin, 1935; Czec- botanists to the conclusion that Cembroides is a zott, 1954; Klipper, 1968; van der Burgh, 1973; young subsection. Phylogenies based on DNA-se- Klaus, 1989). The exceptional three species may quence divergence indicate, however, that section represent lineages from middle-latitude refugia, as Parrya, including subsection Cembroides, is an- documented by fossil pollen of unknown affinity cient (Kossack, 1989; Strauss & Doerksen, 1991). from the Eocene and Oligocene of Japan and north- Ancestral Cembroides lineages would have been ern China (Tables 3, 4). Subsection Gerardianae concentrated in MexicaniCentral American refu- may have been divided between a southern Tethys gia during the early Tertiary, and the major pulse refugium, as represented by extant P. gerardiana, of radiations now occurring in the subsection may and a middle-latitude refugium in northern China, have begun in the early Tertiary. Volume 80, Number 2 Millar 1993 Evolution of Pinus

Two subsections may have originated in Mexi- ways the Pleistocene was analogous to the Eocene. canlcentral American refugia (Axelrod, 1980, The Pleistocene was also an epoch with fluctuating 1986). Unlike other subsections, Oocarpne and climates, but the deviation from temperate climates Sabinianae have no 3fesozoic fossil record and are in the Pleistocene was toward glacial conditions, not clearly documented until the Miocene. On the whereas in the Eocene it was toward tropical ep- basis of specialized and apparently derived rnor- isodes. The amplitude in average temperature be- phological adaptations (Shaw, 1913, 1924; Little tween glacial and interglacial periods of the Pleis- & Critchfield, 1969; Klaus. 1980; van der Burgh, tocene (So-10°C. Bowen, 1979) was about the 1984). these subsections have long been considered same as estimated for the cool and warn1 periods to have originated recently. Phylogenetic analysis of the Eocene. The Pleistocene differed in lasting of DNA divergence also confirms their relative only 2 million years (cf. 20 million years for the youth, especially of Oocarpae (Strauss & Doerk- Eocene), in having many more cycles (16- 18, sen, 1991). Using fossil and floristic evidence. Ax- Bowen, 1979), and in having alternating periods elrod (1980) traced the origins of the northern of unequal duration with glacials longer than in- (California/Baja California) elements of Oocarpae terglacial~. to mainland Mexico/Central America prior to the The events of the Pleistocene had enormous Miocene. The northern lineages appear to have effects on vegetation, including pines. In northern diverged by the time they reached California (Millar latitudes, pine distributions were displaced by con- et al., 1988), indicating that the radiation events tinental ice sheets (e.g., Pinus corztortn/ P. banks- occurred farther south in the early Tertiary. Al- iana, Critchfield, 1985); in mountainous regions though the systematic coherence of the extant Lat- elsewhere, species migrated up or down in elevation in American taxa of Oocarpae remains uncertain, (Miki, 1957; Van Devender 8: Spaulding, 1979). genetic relationships of some Latin American spe- Along coasts and in other lowlands, pine popula- cies link Oocarpae with Australes and Ponderosae tions shifted north and south in response to the (Critchfield, 1967), both of which have Mesozoic climate cycles (e.g., Oocarpae, Axelrod, 1980; fossil records, appear to have had Mexican/Central Millar, 1983). Concomitant to the shifts in distri- American Paleogene refugia, and may have been bution of pines were major changes in the genetic ancestral to Oocnrpae. structure of species. The flux of population expan- Subsection Sabinianae has a limited fossil rec- sion and contraction, coupled with drastically ord consisting of a single taxon allied to P. sabi- changing selection regimes, affected the structure niana and confined to southern California (Axelrod, of genetic variation within species and allowed some 1986). Fossils are known only frorn the late Mio- species to hybridize (Critchfield, 1984, 1985; Kin- cene through Quaternary, and Axelrod (1981) loch et al., 1986; Millar, 1989). traced the origin of the extant species to Mexican In general, however, the Pleistocene does not species of Ponderosae. Genetic relationships of ex- appear to have completely reshuffled the genus in tant taxa link Sabinianae with Ponderosae on the the way the Eocene did, and many of the Tertiary basis of terpene affinities (Zavarin et al., 1967) patterns and the evolutionary events that date to and crossing evidence (Critchfield, 1966; Conkle that period have been maintained. Notwithstanding & Critchfield, 1988). Together this evidence points the existence of local refugia, Pleistocene events to a Mexican/Central American origin of Sabi- primarily affected Pinus in a gradient frorn north nianae from early Tertiary Ponderosae lines. to south, with the effect that species and popula- tions shifted south then north (or down then up in elevation) following the cycle of the glacial and interglacial periods. In this paper I document that tectonic, climatic, The impact of the Eocene, by contrast, was and biogeographic events of the Eocene had a greatest in the latitudinal center of the genus and major impact on pine distributions and evolution. had the effect of dissecting the genus and concen- The question may arise whether the effects of the trating pines into widely disjunct regions. Further- Eocene were so confounded by subsequent events more, during the early Tertiary, and unlike the of the Tertiary and especially the Quaternary as Pleistocene, almost no upland regions (except in to be indecipherable. I will address only the Pleis- interior western North America) could offer local tocene, since its potential was probably the great- refuge from unfavorable climates. Whereas many est. pine species appear to have gone extinct in the The Pleistocene was a time of profound change early Tertiary. no pine extinctions in North Amer- unprecedented in the history of the Earth. In some ica are attributed to the Pleistocene (Critchfield, Annals of the Missouri Botanical Garden

1984). although western Europe suffered a signif- A%DREsE---.,J. W. 1964. The taxonomic status of Pznus icant impoverishment of pine flora (Klipper, 1968). chlapensis. Phytologia 10: 117-42 1. . 1966. -4 multivariate analysis of Pznus chza- Some speciation, for example, in Bct~ourianue, penscs-monttcola-strobuf phylad. Rhodora 68: 1- Cembroides, and Oacarpae, seems to have been 21. triggered by the Pleistocene, but no major new AXELROD,D. I. 1965. A method for determin~ngthe trends have emerged. altitudes of Tertiary floras. Palaeobotanist 14: 114- Insufficient time has elapsed since the close of 171. . 1966. The Eocene Copper Basin Flora of the Pleistocene for its full impact to be felt on northeastern Nevada. Univ. Calif. Publ. Geol. Sci. evolution in Pinus. Patterns initiated by the Pleis- 59. tocene appear minor compared to the effects of . 1968. Tertiary floras and topographic history the Eocene and are insufficient to erase the evo- of the Snake River basin, Idaho. Bull. Geol. Soc, Amer. 79: 713-734. lutionary impacts of the early Tertiary. Thus, many . 1979. Desert vegetation, its age and origin. of the major evolutionary patterns of the early Pp. 1-72 tn J. R. Goodin & D. K. Northington Tertiary can still be traced in the biogeography (editors), Arid Land Plant Resources. International and relationships of extant pines. Center for Arid and Semi-Arid Land Studies, Lub- bock, Texas. VALIDATIOKOF THE HYPOTHESIS . 1980. History of the maritime closed-cone The arguments developed in this paper result in pines, Alta and Baja California. Univ. Calif. Publ. Geol. Sci. 120: 1-143. a working hypothesis about the effect of the Eocene . 1981. Holocene climatic changes in relation on pine evolution. The hypothesis is a reconstruc- to vegetation disjunction and speciation. Amer. Nat- tion of pine history based on available information uralist 117: 847-870. from the fossil record, climatic and tectonic evi- . 1986. Cenozoic history of some western Amer- dence, and biogeographic record of angiosperms ican pines. Ann. Missouri Bot. Gard. 73: 565-641. & H. P. B~ILEY.1976. Tertiary vegetation, and conifers. Many gaps in information exist that, climate and altitude of the Rio Grande depression, if filled, would corroborate or negate this hypoth- New Mexico-Colorado. Paleobiology 2: 235-254. esis. These gaps fall into several categories. Ex- & P. H. R-\[~ly. 1985. Origins of the Cordil- panded fossil records are urgently needed, es- leran flora. J. Biogeogr. 12: 21 -47. B~NKS,If. P., A. ORTIZ-SOTOMAYOR& C. M. H~RTMAN. pecially in regions hypothesized as Eocene pine 1981. Psnus escalantensss, sp. nov. a new permi- refugia that currently have meager fossil docu- neralized cone from the Oligocene of British Colum- mentation. These include Paleogene records for bia. Bot. Gaz. (Crawfordsville) 142: 286-293. Central America and Mexico, low latitudes along B~RRON,E. J. 1984. Climatic implications of the vari- the European Tethys, and high latitudes in eastern able obliquity explanation of Cretaceous-Paleogene high latitude floras. Geology 12: 595-597. Asia. Technologies that allow more accurate iden- . 1985. Estimations of the Tertiary global cool- tification of fossil affinities for macro- and especially ing trend. Palaeogeogr. Palaeoclimatol. Palaeoecol. micro-fossils at intrageneric levels would help in 50: 45-61. tracking the biogeography and evolution of these BECKER,E. W. 1961. Oligocene plants from the upper Ruby River Basin, southwest Montana. Mem. Geo. groups. These technologies need to be applied to Soc. Amer. 82. published fossil floras, with revised taxonomic lists. BERPUER,R. A,, A. LASAGA& R. M. CARRELS.1983. Certain pine lineages have especially meager fossil The carbonate-silicate geochemical cycle and its ef- records, including Cretaceous records of sections fect on atmospheric carbon-dioxide over the past 100 Parrya, especially Gerardianae and Halfouria- million years. Amer. J. Sci. 283: 641-683. BLJCKWELL, W. H. 1984. Fossil Ponderosa-like pine nae, and Cretaceousiearly Tertiary records of sec- wood from the Upper Cretaceous of northeast Mis- tion Pinea. Accurate dating of fossils and corre- sissippi. Ann. Bot. (London) 53: 1 33- 136. lation with paleoclimatic and paleogeological events Bo~D,W. J. 1989. The tortoise and the hare: ecology will also help to track the fine scale paths of these of angiosperm dominance and gymnosperm persis- tence. J. Linn. Soc. Biol. 36: 227-249. pines. Finally, existing and emerging genetic and BOPIEV,D. Q. 1979. Geographical perspective on the molecular technologies should be applied to esti- Quaternary. Prog. Phys. Geogr. 3: 167- 186. mate genetic distances and divergence times among BRENNER,G. J. 1963. The spores and pollen of the subgeneric groups. Such genetic techniques will Potomac Group of Maryland. Dept. Geol. Mines Wa- allow tests of the hypothesized times of geographic ter Res. Bull. 27. BROWN,R. W. 1934. The recognizable species of the isolation. Green River flora. U.S. Geol. Surv. Prof. Paper 185- C: 45-77. . 1937. Additions to some fossil floras of the ALVIY,K. L. 1960. Further conifers of the Pinaceae western United States. U.S. Geol. Surv. Prof. Paper from the Wealden Formation of Belgium. Mem. Inst. 186-J: 163-206. Roy. Sci. Nat. Belgique. 146: 1-39. BURCHARDT,B. 1978. Oxygen isotope palaeotempera- Volume 80, Number 2 Millar 1993 Evolution of Pinus

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Genetic tographica 108B (3-6): 121 - 140. variation and hybridization of ponderosa pine. Pp. Gi (I, S. 1980. Late Cretaceous and Eocene floral prov- 27 -43 Ln Ponderosa Pine: The Species and its Man- inces. Inst. Geol. Palaeontol., Academia Sinica, Nan- agement. Washington State Univ. Coop. Ext. Pull- jing. man, Washington. HEER,0. 1868-1883. Flora Fossilis Arctica, 6 vol- CREBER,G. T. & W. G. CHALOYER.1984. Climatic umes. J. Wurster, Zurich. indications from tree rings in fossil woods. Pp. 49- HICKEY,L. J., R. M. WEST, M. R. DAWSON& D. K. 74 in P. T. Brenchley (editor), Fossils and Climate. CHOI. 1983. Arctic terrestrial biota: Paleomagnetic Wiley & Sons, New York. evidence of age disparity with mid-northern latitudes CRITCHFIELD,W-. B. 1966. Crossability and relationships during the late Cretaceous and early Tertiary. Sci- of the California big-cone pines. U.S.D.A. Forest ence 221: 1153-1156. Serv. Res. Pap. NC-6: 36-44. HILLS,L. V., J. E. KLOCAN& A. R. SWEET. 1974. . 1967. 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