Impact of the Eocene on the Evolution of Pinus L. Author(s): Constance I. Millar Reviewed work(s): Source: Annals of the Missouri Botanical Garden, Vol. 80, No. 2 (1993), pp. 471-498 Published by: Missouri Botanical Garden Press Stable URL: http://www.jstor.org/stable/2399795 . Accessed: 02/11/2011 13:05

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http://www.jstor.org IMPACT OF THE EOCENE ON Constance I. Millar2 THE EVOLUTION OF PINUS L.1

ABSTRACT

Pinus evolved in middlelatitudes of the NorthernHemisphere in the middleMesozoic. By the late Cretaceous pines had spread east and west throughoutLaurasia, attaininghigh diversityin eastern Asia, the eastern United States,4nd westernEurope, but having little representation at highnorthern latitudes. Changing climates in the early Tertiaryestablished warm and humidtropical/subtropical conditions in a broad zone to 70'N throughoutmiddle latitudes.Pines and theirrelatives disappeared from many middle-latitude areas duringthis time and were replaced by diverseangiosperm taxa of the boreotropicalflora, which were adapted to the equable, tropicalclimate. The effect of thisclimate change and spreadof boreotropicalflora was to displacepines from their former habitats. A hypothesis is defendedthat pines shifted,during the threewarm periods of the Eocene, intothree major refugialareas in the NorthernHemisphere: high latitudes, low latitudes,and uplandregions of middlelatitudes, especially in westernNorth America.Some of these refugialareas (e.g., Mexico/CentralAmerica) underwent active volcanismand mountain- buildingin the Eocene and became secondarycenters of pine diversity.Many phylogeneticpatterns within Pinus can be traced to thisfragmentation, isolation, and evolutionin Eocene refugia.Subsections Oocarpae and Sabinianae appear to have originatedfrom refugia in Mexico and Central America. Older subsectionssuch as Sylvestres, Ponderosae, Contortae,and Strobi were distributedover several refugia;subsections Leiophyllae, Australes,and Cembroidesevolved in southernrefugia in NorthAmerica; and Canarienses evolvedin southernrefugia along the Tethysseaway in Eurasia. Followingthe coolingand dryingof the climateat the end of the Eocene, manyangiosperm taxa of the boreotropicalflora became extinctand pines recolonizedmiddle latitudes, a zone theyhave occupied to the present.Migration out of refugiaprovided additional opportunities for hybridization and introgression,as formerly isolatedlineages expanded and met.

The past two decades have seen an explosion of understanding of the origin of the genus (Miller, informationon 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 differentages, continental geo- Nishida, 1986). Similarly, studies on the Quater- morphology, and the dynamics of inland seaways nary historyof 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 structureand evolutionaryrelationships 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 identifyingtaxa lution of the genus between its origins in Mesozoic have led to systematic revisions of many fossil (Table 1) and its present diversityremain obscure. floras. The widespread use of radioisotope dating How did important secondary centers of pine di- has added precision to determiningthe 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 diversificationsof 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- influencedcurrent and fossildistribution? Although nus Pinus L.), major syntheses have focused on there have been important contributionsto under- two time periods in the historyof 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 significantlychanged our Axelrod, 1986; Lauria, 1991), the impact of Pa-

l I especiallythank B. B. Kinlochfor valuable discussion and reviewof the manuscript.I also thankD. Axelrod, L. Loveless,C. Miller,S. Strauss,E. Zavarin,and an anonymousreviewer for critical comments on the manuscript. I dedicatethis paper to the late W. B. Critchfield(1923-1989), whosestudies on the impactsof the Pleistoceneon conifersdemonstrated that genetic structure of extantspecies cannotbe understoodwithout looking to the past. 2 Instituteof Forest Genetics,Pacific Southwest Research Station,U.S.D.A. ForestService, Berkeley,California 94701, U.S.A.

ANN. MISSOURI BOT. GARD. 80: 471-498. 1993. 472 Annals of the Missouri Botanical Garden

TABLE 1. Approximateages and durationsof geologicaleras fromthe Mesozoicto present.

Duration (millions Millionsof Era Period Epoch of years) years ago Cenozoic Quaternary Holocene Approximatelythe last 10,000 years

Pleistocene 2.4 2.5 Tertiary Neogene Pliocene 4.5 7 Miocene 19 26 Paleogene Oligocene 12 341 Eocene 16 54 Paleocene 11 65 Mesozoic Cretaceous 71 136 Jurassic 54 190 Triassic 35 225 The Oligocene-Eoceneboundary is accepted to be 34 Ma, coincidingwith the terminalEocene event. Authors publishingbefore the middle1970s and some currentones accept the boundaryas 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 informationon plate genus of conifers, although Podocarpus may rival tectonics, climate, fossils,and biogeographyof pines it. Pines have been recognized since Classical times, and other dominant plant groups as they affected and more than 40 classificationsystems 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 modifiedthe classificationof Shaw (1914, SYSTEMATICS AND CURRENT 1924). Little & Critchfield(1969) divided Pinus BIOGEOGRAPHY OF PINUS 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 informationbased sphere. Pines occur predominantly at middle lati- on genetic data, especially from contemporary tudes (30'-550N), but important centers of pine studies on hybridizationand biochemical variation. species also exist at high (> 550N) and low latitudes Thus, their classification implicitly suggests phy- (< 30'N) (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'sclassification, 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 fromhot, 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 (Do

00 ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ 0

160 120 80 40 0 40 80 120 160 (

-) a

+ ~~~~S/

Sy ~ ~ ~ ~ ~ 7~S 40~~~~~~~~~~~~~~~~~0 co

20~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ 'A~~~~~~~~~~~~~~~~~~~~~~~~~~~g-

0- + 2

FIGURE1. Distributionof Pinus subgenusPinus, showinggeneral locations of subsectionswithin the subgenus.A =Australes, Ca =Canarienses, Co =Contortae, L= Leiophyllae, 0 = Oocarpae, Pi =Pineae, Po =Ponderosae, Sa = Sabinianae, Sy= Sylvestres. 160 120 80 40 0 40 80 120 160

Cet D0 Ce ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~~~~~C

- 40 B1 Cs~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~C

= Ce = FIGURE 2. Distributionof Pinus subgenusStrobus and subgenusDucampopinus, showinggeneral locations of subsectionswithin the subgenus.B Balfourianae, Cembrae,Cs Cembroides,G = Gerardianae,S = Strobl, K = Krempfiani(Ducampopinus). C, o

CD

The Genus PINUS Littleand Critchfield

Subgenus: Ducampopinus Strobus Pinus

Pinus Section: Ducampopinus Strobus Parrya Pinea

Sabinianae Subsection:Krempfiani Cembrae Strobi Cembroides Gerardianae Balfourianae Cananenses Leiophyllae Pineae Sylvestres Ponderosae Australes Contortae Oocarpae

Species: kremptfi sabiniana albicaulis strobus cembroides gerardiana balfouriana canariensis keiophylla pinea resinosa ponderosa palustaiS banksiana radiata cembra monticola edulis bungeana longaeva roxburghii lumholtzsi tropicalis taeda atienuata couften washoensis cOgntoita torreyana sibirica lambertiana quadrifolia aristata nigra jeffreyi echinata virginiana muicata patula koraiensis flexilis monophylla heldreichDi engelmannl glabra causa culminicola mugo durangensis greggi m pumila strobifomnis rgida -m ayacahuite maximartinezii pinaster copeni serotina ooCarpa = peuce pinceana halepensis montezumae pungens pringlei amnandii nelsonii brutia hartwegii elliottiaC griffithii sylvestris michoacana carhiaean'-4 0 dalatensis densiflora pseudostrobus occidentalis parviflora thunbergiana douglasiana cubensis morrisonicola massoniana teocote fenzeliana taiwanensis lawsonii 0 wangii luchuensis hwangs- C hanensis tabulaeformis yunnanensis insulanis merkusii

FIGURE 3. Taxonomyof the genus Pinus accordingto Little& Critchfield(1969), showingthe speciesclassified into subgenera, sections, and subsections.

inus accor i I I I I I I , secti ions.~~~~~~~~~~~~~~~~~~~~~0 476 Annals of the Missouri Botanical Garden

classification as the best presently available hy- The earliest known pine, P. belgica, fromthe early pothesis of phylogenetic 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 (Langenheim et al., MESOZOIC BIOGEOGRAPHY 1960). All other pine fossilsare known frommiddle to late Cretaceous deposits. ORIGIN OF PINES 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 interpretationof Mesozoic 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 fromMirov's thinkingconcerns the location Cretaceous locales, with pines especially abundant of the center of origin of the genus and the paths and diverse at high northernpaleolatitudes. Mirov's of subsequent radiation. At the beginning of the widely cited interpretationdated 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-northerncircumpolar 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. originof pines (Hickey et al., 1983; Eguiluz Piedra, This interpretationwas 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-latitudeMesozoic center of origin for pines. pared internal anatomy of fossil and extant pina- Mesozoic pine fossilsoccur between 3 1N and 50'N ceous cones and found four diagnostic traits that latitude, withonly two records fromhigher latitudes characterize Pinus (summarized in Miller, 1976). (Table 2). Similarly, fossils of six species of Pseu- When previously described fossilswere reanalyzed, doaraucaria and over 20 species of Pityostrobus, many that were originally ascribed to Pinus 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-latitudemacrofossils, pri- a circumpolar origin for Pinus is unsupported, and marily in the collections of Heer, 1868-1883, pine originsin middle latitudes are more likely. The originally treated as Pinus were reclassified, in regions of the northeasternUnited 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., 1 981), eries in the last two decades, result in a Cretaceous are the current candidates for the center of origin fossilrecord of about 25 species of pines fromeight 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 petrifiedcones whose natively, the diversityof 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- tributionof these fossilpines. Although a geograph- DISTRIBUTION OF PINES AND ic bias may be expected due to proximityof 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 distributionof pines and the prevailing cli- 180 120 60 0 60 120 180

- 60| , , , -- SOX T~n 0 is X i 1+

ok ~~t + + + ~ \ >< + + m

60 - +l + [

FIGURE 4. Distributionofpine fossils from Cretaceous deposits, mapped by estimated paleocoordinates onmap of the late Cretaceous world. Base mapA) CambridgeUniversity Press 1981, taken fromSmith, Hurley & Briden,Phanerozoic paleocontinentalworld maps. TABLE 2. Distributionand affinitiesof fossilpines fromCretaceous deposits listed in approximateorder of age (old to young).Paleocoordinates from Smith et al. (1981).

Latitude/longitude Age Identification Affinity Location Current Paleo (Ma) Reference P. belgica Sylvestres Belgium,Wealden 50?N 40E 39?N 50E 130 Alvin(1960) Pinus pollen genus Alaska, Kuk River 70?N 160?W 80?N 100?W Early Langenheimet al. (1960) Pinus pollen genus Maryland 39?N 79?W 32?N 41?W Late Early Brenner(1963) Pinus pollen genus Delaware 39?N 75?W 31?N 39?W Late Early Grootet al. (1961) P. wohlgemuthi subg. Pinus France 48?N 40E 35?N 180E Late Early Alvin(1960) P. ponderosoides Ponderosae/ Mississippi,Prentiss Co. 34?N 88?W 31?N 52?W Early Late Blackwell(1984) Australes Pinus pollen Sylvestres Minnesota 44?N 95?W 40?N 55?W Early Late Pierce (1957) P. clementsii Sylvestres Minnesota 44?N 95?W 40?N 55?W Late Chaney (1954) Pinus sp. Sylvestres Delaware 39?N 75?W 32?N 40?W Late Penny (1947) P. triphylla Sylvestres/ Massachusetts 41?N 71?W 33?N 35?W Late Robison(1977) Leiophyllae New York, Staten Island 41?N 74?W 34?N 37?W Late Hollick & Jeffrey(1909) Japan,Hokkaido 42?N 1420E 48?N 1350E Late Stockey& Nishida(1986) P. tetraphylla Sylvestres Japan,Hokkaido 42?N 1420E 48?N 1350E Late Stockey& Nishida(1986) P. bifoliata Sylvestres Japan,Hokkaido 43?N 1420E 49?N 1350E Late Stockey& Nishida(1986) | P. pseudotetraphylla Sylvestres Japan,Hokkaido 43?N 1420E 49?N 1350E Late Stockey& Nishida(1986) P. flabellifolia Canarienses Japan,Hokkaido 43?N 1420E 49?N 1350E Late Ogura (1932), Stockey& Nishida(1986) - 0 P. quenstedti Ponderosae Kansas 38?N 99?W 34?N 61?W Late Lesquereux(1883) | P. quinquefolia Ponderosae Massachusetts 41?N 71oW 33?N 35?W Late Penny (1947), Robison CD (1977) New York, Staten Island 41?N 74?W 34?N 37?W Late Hollick & Jeffrey(1909) Japan,Hokkaido 42?N 1420E 48?N 1350E Late Stockey& Nishida(1986) P. pachydermata subg. Pinus Japan,Hokkaido 42?N 1420E 48?N 1350E Late Ueda & Nishida(1982) aCD P. pseudostrobifolia Ponderosae Japan,Hokkaido 43?N 1420E 49?N 1350E Late Ogura (1932), Stockey& Nishida(1986) P. pseudofiabellifolia subg. Pinus Japan,Hokkaido 44?N 1420E 50?N 1360E Late Ueda & Nishida(1982) P. harborensis Ponderosae Japan,Hokkaido 44?N 1420E 50?N 1360E Late Stockey& Nishida(1986) P. hokkaidoensis Ponderosae/ Japan,Hokkaido 44?N 1420E 50?N 1360E Late Stockey& Ueda (1986) Leiophyllae P. cliffwoodensis Australes/ New Jersey,Magothy 40?N 74?W 32?N 38?W Late Miller& Malinky(1986) Ponderosae Volume 80, Number2 Millar 479 1993 Evolutionof Pinus

mate at the end of the Mesozoic. By the Late Cretaceous, pines had reached eastern and western edges of Laurasia and occurred at middle latitudes

0.) in many locations between these extremes (Table 0.) 2; Fig. 4). The widespread distributionof pines in 0) CN N Laurasia by this time indicates that wherever within middle latitudes they originated, their main route (. 0) 0.) 0 0. 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 firstin the south and last in the north. High-latitude connections in cb cr c c 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- 0.)~~~~~ co co gration. Evidence also exists for land connections -o Z0 0 0 00 0 at high latitudes in the Bering Sea region between 4 0,L Siberia and Alaska being used as corridors for 0D 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- 0 ZZ south length of the continents(Kurten, 1966; Tiff- ney, 1985a). These seaways divided the continents into separate phytogeographic provinces, creating greater floristic affinitiesbetween eastern North America and western Europe, and western North U) a.) 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 c~~~~~ ~ ~ c quiescence and equability (Parrish, 1987; Up- -'0 0dC)4U) church & Wolfe, 1987; McGowran, 1990). Sea r0) levels were high, and tectonic activitylow, creating stable global climates. Although the breakup of Pangaea had commenced, paleocontinentswere still 0.) 0.) relatively undispersed, resulting in average tem- peratures in the middle and high latitudes about

0d 100-20'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 rainfallpatterns 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 rainfallabove 450N (Parrish, 1987). In general, however, lati- tudinal gradients were shallower, and changes in temperature withlatitude were about l/2-l/3of pres- ent gradients (Parrish, 1987; Upchurch & Wolfe, 1987). Temperature and rainfall appear to have 480 Annals of the MissouriBotanical Garden

been stable annually,with little seasonality at lat- warm and wet, and high latitudes were cool and itudesbelow 450N (Upchurch& Wolfe,1987). At dry (Parrish, 1987; Wolfe, 1978). Truly arid zones higherlatitudes, day lengthsand precipitationap- apparently did not exist; there is no evidence for parentlyvaried seasonally. The majorcordillera of Paleogene arid deserts or tundra (Axelrod, 1979). the NorthernHemisphere were not developed,or Although these general trends in temperature existed only at low elevations.Volcanic activity and humidityexisted throughouta broad latitudinal was minor,so there were few orographiceffects zone worldwide, there was geographic heteroge- on climateand littleregional diversity in climate. neity in the intensityof conditions. The warm hu- mid zone was widest in North America and western EARLY TERTIARY BIOGEOGRAPHY Europe, and narrower in central and eastern Asia (Chaney, 1940; Parrish, 1987; Hsu, 1983). In CHANGING CLIMATES general, continentalelevations were low throughout Major changesin climateand vegetationchar- the Paleogene, and upland areas apparently existed acterized the early Tertiary(Wolfe, 1990). Al- primarilyin one middle-latituderegion of western thoughthese eventshave long been discussedby North America and in Antarctica (Axelrod, 1966; paleobotanistsinterested in angiospermevolution Wolfe, 1985, 1987; Wolfe & Wehr, 1987; Wing, (Wolfe,1975; Tiffney,1985a, b; Friiset al., 1987), 1987). In the upland area of western North Amer- their impact on coniferevolution has not been ica, the climate was anomalously temperate com- analyzed. In general,average temperaturesrose pared to other middle-latitudeareas. Volcanism and and rainfallincreased in the early Tertiary.The mountain-buildingin this area during the Eocene trendstoward increasing temperature and humidity also created heterogeneity in local climates and startedin the early Paleocene and continuedinto habitats. the Eocene, reachingmaxima in the earlyEocene, about 52 Ma. By thistime, average temperatures THE ANGIOSPERM BOREOTROPICAL FLORA had increased50-70C above the Late Cretaceous (Savin, 1977), and tropical/subtropicalconditions The changes in climate during the early Tertiary apparentlyextended at manymiddle and highlat- drastically affected global floristics (Friis et al., itudes to 70'-80'N (Wolfe, 1985; McGowran, 1987; Wolfe, 1975, 1978, 1985). Diverse tropical 1990). Hightemperatures and humidity,however, and subtropical angiosperm floras appeared with did not persiststably throughout the Eocene. Al- increasing geographic representation during the thoughthe late Paleocene/earlyEocene (54-52 Paleocene and the warm intervals of the Eocene Ma) was the warmestand wettestperiod, there throughoutbroad zones at middle latitudes in both were at least two otherwarm periods, from about Northern and Southern Hemispheres. Originally 46 to 42 Ma, and about 36 to 34 Ma, separated identifiedfrom the London Clay formationsof En- by cooler intervalsthat were approximatelyequal gland (Reid & Chandler, 1933), similar angiosperm in durationto 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 temperaturesmay have fluctuatedas muchas 7?- America (from the Pacific Coast to Nebraska and 10?C betweenwarm and cool periodsof the Eocene Texas; Vermont, Alabama), western and eastern (Wolfe, 1978). Several causes for these climatic Europe (including England, France, Belgium, Ger- developmentshave been suggested,including ma- many, Bulgaria, Ukraine, and Russia), northern jor tectonicevents, changes in sea level, and sub- Egypt, China, and Japan (Mai, 1970; Graham, marinevolcanism resulting in accumulationof at- 1972; Wolfe, 1975, 1985; Tiffney, 1985a, b). mosphericcarbon dioxide and greenhouseheating Subtropical assemblages occurred north as far as (Wolfe, 1978; Parrish,1987; McGowran,1990; 70? in Alaska, and at other high-latitudelocations Kerr, 1991). Alternatively,large amountsof car- in Canada, Greenland, and Siberia (Wolfe, 1977, bon dioxidemay have been producedas a result 1985). In North America, the average zone ex- ofocean-atmosphere interactions following a major tended from 300N to 500N (Wolfe, 1985). The extraterrestrialimpact at the Cretaceous/Tertiary origin and major radiation of many angiosperm boundary(O'Keefe & Ahrens, 1989), whichled taxa is documented in these diverse floras. to greenhousewarming (Wolfe, 1990). Plant communitiesin these Paleogene floraswere Althoughlatitudinal gradation was notgreat, the adapted to warm, humid, and equable conditions. patternin the Eocene differedfrom both the Cre- These taxa were similar to those found in modern taceous and the laterTertiary and Quaternary:in rainforestvegetation of Malaysia and other extant general,many low-latitude locations were relatively tropical rainforest regions and show comparable warm and seasonally dry, middle latitudeswere adaptations. Common genera include Engelhard- Volume 80, Number2 Millar 481 1993 Evolutionof Pinus

tia, Ficus, Pterocarya,Nypa, Platycarya, Weth- Wehr, 1987), Idaho (Axelrod, 1986), and Colo- erellia, Alangium, and Nyssa. A few gymno- rado (Wodehouse, 1933; MacGinite, 1953) (Table sperms such as Glyptostrobus, Taxodium, and 3; Fig. 5). Western North America in general occasionally Sequoia 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 withaverage 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- throughoutNorth 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 PINES of Alaska (80'N, Norris, 1982), at low-middle lat- The early Tertiary radiation of many angio- itudes in Borneo (20N, Muller, 1966) and southern sperm lineages and the migration of angiosperm Alabama (360N, 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), withinthe 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 fromthe Paleocene. Pines hashi, 1970; Tanai, 1970, interpreted by Wolfe, of the earliest Eocene occur primarilyin high (65?- 1985 to be early-late Eocene), Fushun, China (Hsu, 80?N) and low (20N) latitude deposits in North 1983), 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 primarilyat high latitudes in western 1966) and from one low-middle latitude location Siberia (Dorofeev, 1963), Alaska (Norris, 1982), 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 Betula, Alnus, va, 1952). Pines fromthe southeast coast of China, and Ulmus. Ages of these fossils correspond to the in the provinces of Jiang-su, Zhejian, and Fujian firstwarm humid period of the Eocene (Fig. 6). (Hsu, 1983), may also be from this period (Table Fossil pines from the middle Eocene continue 3). to be represented at high and low latitudes, but appeared forthe firsttime 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 fromthe 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; profoundclimatic event of the Tertiary (Burchardt, Stockey, 1983, 1984), Washington (Wolfe & 1978; Wolfe, 1978; Parrish, 1987; McGowran, TABLE 3. Distributionand affinitiesof fossilpines fromEocene depositslisted in approximateorder of age (old to young).Paleocoordinates from Smith et al. (1981).

Latitude/longitude Age Identification Affinity Location Current Paleo (Ma) Reference Pinus pollen genus Alaska, Nenana 64?N 148?W 77?N 128?W 54 Wahrhaftiget al. (1969) Pinus pollen genus Alaska, Colville 70?N 151?W 80?N 127?W Early Frederiksenet al. (1988) Pinus ? pollen genus Alaska, Death Valley 65?N 162?W 80?N 143?W Early Dickinsonet al. (1987) (bisaccate grains) Pinus pollen genus Canada, EllsmereIsland 77?N 84?W 75?N 18?W Early Manum (1962) Pinus pollen genus Greenland 70?N 52?W 60?N 8?W Early Manum (1962) Pinus pollen genus Iceland 65?N 21?W 50?N 80E Early Manum (1962) Pinus pollen genus Spitsbergen 79?N 140E 70?N 200E Early Manum (1962), Schweitzer(1974) Pinus pollen genus NorthDakota, Dunn 47?N 103?W 56?N 70?W Early Leopold & MacGinite(1972) Pinus pollen genus NorthwesternBorneo 2?N 110?E 2?N 110?E Late Early Muller(1966) P. delmnarensis subg. Strobus SouthernCalifornia 33?N 117?W 42?N 92?W 47-48 Axelrod(1986) Pinus pollen Cembroides SouthernCalifornia 33?N 117?W 4 1?N 92?W 47-48 Axelrod& Raven (1985) Pinus pollen Ponderosae SouthernCalifornia 33?N 117?W 41?N 92?W 47-48 Axelrod& Raven (1985) Pinus pollen genus NortheasternChina, 42?N 1240E 45?N 1180E Mid and Late Sung & Liu (1976), Hsu | Fushun (1983) P. ballji Cembroides Colorado,Green River 41?N 109?W 50?N 80?W 47 Wodehouse(1933), | Brown (1934) = P. driftwoodensis Sylvestres/ BritishColumbia, Smithers 55?N 127?W 66?N 97?W 46-47 Stockey(1983) Ponderosae/ (D Australes P. arnoldii Sylvestres BritishColumbia, 50?N 120?W 61?N 90?W 46-47 Miller(1973), Stockey Princeton (1984) P. slinilkaineensis subg. Strobus BritishColumbia, 50?N 120?W 61?N 90?W 46-47 Miller(1973) Princeton P. princetonensis Sylvestres BritishColumbia, 50?N 120?W 61?N 90?W 46-47 Stockey(1984) Princeton P. andersonji Ponderosae BritishColumbia, 50?N 120?W 61?N 90?W 46-47 Stockey(1984) Princeton Pinus pollen genus Washington,Republic 49?N 118?W 60?N 87?W 46-47 Wolfe & Wehr (1987) P. balfouroides Balfourianae Idaho, ThunderMountain 45?N 114?W 55?N 84?W 46-47 Brown(1937), Axelrod (1986) C o CD-B TABLE 3. Continued. 2CD Co Latitude/longitude Age Identification Affinity Location Current Paleo (Ma) Reference 2 Pinus pollen genus Canada, MacKenzie Delta 69?N 134?W 80?N 80?W Mid-Late Norris(1982) Pinus pollen genus Alabama,Claiborne Bluffs 31?N 88?W 36?N 62?W Middle Gray (1960) P. wheeleri Strobi Nevada, Elko 41?N 116?W 50?N 90?W 42 Axelrod(1968) P. crossii Balfourianae Nevada, Copper Basin 42?N 115?W 51?N 89?W 40-44 Axelrod(1966) P. wolfei SYlvestres/ Washington,Little Falls 47?N 123?W 60?N 93?W Early Late Miller(1974) Contortae P. alvordensis Contortae Nevada, Bull Run 41?N 117?W 50?N 91?W 38 Axelrod(1968) Pinus pollen genus New Mexico, Bernalillo 35?N 107?W 44?N 80?W 38 Leopold & MacGinite (1972) Pinus sp. genus SouthwesternJapan, Ube 34?N 1300E 40?N 1300E Early Late Huzioka & Takahashi (1970) Pinus sp. genus Japan,Kushiro 43?N 144?W 50?N 1350E Early Late Tanai (1972) Pinus pollen genus Colorado,Chaffee 39?N 105?W 49?N 76?W 36-37 Leopold & MacGinite (1972) mn< Pinus pollen genus BritishColumbia, Parsnip 55?N 122?W 66?N 90?W 35 Hopkinset al. (1972) River Pinus sp. genus Siberia,Tavda River 58?N 650E 52?N 580E Late Dorofeev(1963) Pinus sp. genus Siberia,Ob River 57?N 850E 54?N 750E Late Dorofeev(1963) Pinus sp. genus Siberia,Tym River 60?N 820E 55?N 730E Late Dorofeev(1963) P. spinosa Sylvestres/ Siberia,Irtysch River 57?N 750E 52?N 670E Late Dorofeev(1963) Ponderosae Pinus pollen genus Ukraine,River Don 47?N 400E 35?N 380E Late Chiguriaeva(1952) P. sturgisii Strobi Colorado,Florrissant 39?N 105?W 48?N 76?W 34-35 MacGinite(1953), Axelrod (1986) P. florrissantii Strobi Colorado,Florrissant 39?N 105?W 48?N 76?W 34-35 MacGinite(1953), Axelrod (1986) P. wheeleri Strobi Colorado,Florrissant 39?N 105?W 48?N 76?W 34-35 MacGinite(1953), Axelrod (1986) Pinus pollen genus SoutheasternChina 25-35?N 1200E 28-34?N 1180E Late Hsu (1983)

Co Co

180 120 60 0 60 120 180

A A A

A 60 + + 0 '

Boreo - Tropical Flora

-A A~~~~~~~~~~~~~~~~~~~~~~~~~~(l A,~~ + + + A~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~

,. I l l l.lA l l

FIGURE 5. Distributionof pine fossilsfrom Eocene deposits,mapped by estimatedpaleocoordinates on map of the Paleocene world.Base map? CambridgeUniversity Press 1981, takenfrom Smith, Hurley & Briden,Phanerozoic paleocontinentalworld maps. Volume80, Number2 Millar 485 1993 Evolutionof Pinus

100 ~ / 7 //,7y77 7, 7/~ /// //7>~'/7/777>//''>77

90 ~ / 7'77 7 307/~ 7

/ '/7/7 7/ CO 25~~~/~ ' / / /7 .CD/ / //4 70 ~ ~ ''~~'' CD ~ ~ 4 7~"/< / '4 -a ~ ~ ~ ~ ~ ~ ~ ///4 / /

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60 co/// ~ J~~ 777 / a)300 ~/4/f//J ~74 /~E

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,4~~/7Q/7777/ $/4/// 7 C~~~~ON7 - FIUR 6 Etiaedtepeatrs ro furlaiuds n orhAmriathe/ urn Tertiary.$V(bae o ecetg

ofetr lae) iniaigtewr n cool episode 7i7 the Eoen7 an /h rpi eprtr tteedo h Eocne teminl ocee ven).Fro W lfe(1 777. 7'rntdb pemsso eia/cetsjunloofA Siga i, heScintf/ /esar/ /So/c7iety. ~ /77747 , 7 ;~~/7

1990). The fluctuationsfrom 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 upliftedplateaus in southern Asia and the American Eocene. Average annual temperatures dropped ap- West led to accelerated chemical weathering, a proximately 10?-13IC, 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 30-50C, in the angiosperm taxa frommany middle latitudes world- early Oligocene it is estimated as 250C 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- many parts of the world, complex continental cli- tinctions of boreotropical floras were mirrored by mate patterns developed, possibly forthe firsttime, great expansion of pines and other cool-adapted and continental ice sheets first occurred in the taxa into many middle-latitudelocations. Many of Oligocene (McGowran, 1990). Extensive volca- the same fossil-bearingsites that contained boreo- nism and mountain-buildingin the Rocky Moun- tropical taxa in their late 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 millionyears (Axelrod, 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 180 120 60 0 60 120 180

60

01 ? + f. 0

0 ~ ~ ~

FIGURE 7. Distributionof pine fossilsfrom Oligocene and selectedMiocene deposits,mapped by estimatedpaleocoordinates on map of the early Miocene world.Base map ?) CambridgeUniversity Press 1981, takenfrom Smith, Hurley & Briden,Phanerozoic paleocontinentalworld maps. TABLE 4. Distributionand affinitiesof fossilpines fromOligocene deposits listed in approximateorder of age (old to young).Paleocoordinates from Smith et al. | C (1981). 2

Latitude/longitude Age 0 Identification Affinity Location Current Paleo (Ma) Reference Z Pinus pollen genus Oregon,Bridge Creek 44?N 118?W 47?N 105?W 31 Wolfe (1981), Mason (1927) 2 Pinus pollen genus Oregon,Lyons 45?N 123?W 49?N 110?W 31 Wolfe(1981) 1) Pinus pollen genus NorthDakota, Dunn County 47?N 103?W 48?N 88?W Early Leopold & MacGinite(1972) Pinus pollen genus Montana,Ruby Basin 45?N 1 12?W 46?N 100?W 32-36 Becker (1961), Wolfe (1977) P. crossii Balfourianae New Mexico, Hillsboro 33?N 108?W 34?N 98?W 32 Axelrod& Bailey (1976) Pinus pollen genus BritishColumbia, 56?N 126?W 60?N 110?W Early Piel (1971), Rouse & Matthews AustralianCreek (1979) P. escalatensis Contortae BritishColumbia, 50?N 127?W 56?N 115?W Early-Late Banks et al. (1981) Escalante Island Pinus pollen genus NorthwesternBorneo 2?N 110?E 5?N 110?E Early-Late Muller(1966) Pinus pollen genus Gulfof Alaska 60?N 145?W 68?N 128?W Late Wolfe (1972, 1977) P. buchananii Ponderosae Washington,Olympic 48?N 123?W 52?N 1100W Late Underwood& Miller(1980) P. avonensis Ponderosae Montana,Avon 47?N 1 13?W 50?N 100?W Late? Miller(1969) P. anthrarivus Strobi Idaho, Coal Creek 45?N 114?W 47?N 103?W 29 Axelrod(1986) P. balfouroides Balfourianae Idaho, Coal Creek 45?N 114?W 47?N 103?W 29 Axelrod(1986) | Pinus pollen genus Montana,Beaverhead Basin 45?N 113?W 47?N 102?W Late Becker (1961), Leopold & | MacGinite(1972) Pinus pollen genus Colorado,Chaffee 39?N 105?W 40?N 93?W Late Leopold & MacGinite(1972) P. crossii Balfourianae Colorado,Creede 38?N 105?W 39?N 93?W 27 Schorn & Wolfe (1989) P. riogrande Ponderosae Colorado,Creede 38?N 105?W 39?N 93?W 27 Schorn & Wolfe (1989) - P. sanjuanensis Cembroides Colorado,Creede 38?N 105?W 39?N 93?W 27 Axelrod(1986), Schorn& Wolfe (1989) Pinus sp. Contortae Colorado,Creede 38?N 105?W 39?N 93?W 27 Axelrod(1986), Schorn& Wolfe (cf. alvordensis) (1989) Pinus pollen genus Mexico, Chiapas 16?N 92?W 14?N 83?W Late Langenheimet al. (1967) (1 grain) Pinus pollen genus NorthwesternChina, 43?N 960E 44?N 920E Late? Hsu (1983) Quidam Pinus pollen genus NorthwesternChina, 42?N 950E 43?N 900E Late Sung (1958) NorthwesternGansu P. prepityusa Sylvestres WesternTranscaucasia 42?N 420E 35?N 400E Late? Czeczott(1954) P. maikopiae Sylvestres/ EasternTranscaucasia 40?N 500E 35?N 450E Late? Palibin(1935) Contortae 488 Annalsof the MissouriBotanical Garden

in the Mesozoic. Pines are known from Oligocene lations (1) occurred throughout middle latitudes in deposits that range in North America fromthe Gulf the Mesozoic, (2) were fragmented and displaced of Alaska (Wolfe, 1972), British Columbia (Banks to high and low latitudes and to middle-latitude et al., 1981), Washington (Underwood & Miller, uplands in the Eocene, and then (3) reappeared 1980), Montana (Miller, 1969; Leopold & widely throughoutmiddle 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 & Wolfe, 1989), to a single spec- The Mesozoic origin and spread of pines east imen from Chiapas, Mexico (Langenheim et al., and west throughoutLaurasia 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 littlelatitudinal 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 angiosperm 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). Al- 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 shiftin global climates toward warm humid where boreotropical florahad flourishedin previous conditions of middle latitudes in the early Tertiary epochs. appears to have favored the migrationand radiation The climatic deteriorationof the early Oligocene of angiosperms at the expense of pines. Although was followedby 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 throughoutmiddle latitudesin North America height growth, and reproduction. Conifers domi- (Axelrod, 1986), Europe (van der Burgh, 1973; nate in areas where angiosperm competition is re- Klaus, 1989), and Asia (Hsu, 1983) in the Mio- duced, for example, by fire,cold, or nutrientshort- cene; the direct ancestors of many 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 forestsat 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, 85?N, Ritchie, 1984), and Wrangell Mountains, humid periods of the Paleogene. Alaska (680N, 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- (1 70N, Graham, 1976) indicate the continued pres- latitude zone originallythought by Mirov to be the ence of pines in mountainous low latitudes, despite cradle of Pinus emerges not as a primaryMesozoic the fact that lowlands in these latitudes were dom- center of origin but as an important Eocene re- inated by boreotropical flora. fugium. Although many Mesozoic fossils from the polar region that had been identifiedas pine were later discredited, credible new records, mostly pol- IMPACT OF EARLY TERTIARY len, confirm abundant pine at many high-latitude CLIMATE ON PINE EVOLUTION locations in North America and Eurasia during the warm periods of the Eocene (Table 3). Pines may EOCENE PINE REFUGIA 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 shiftedlatitudinally 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 fromthe 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, Number2 Millar 489 1993 Evolutionof Pinus

connections between North America and Eurasia in the North Atlantic (Tiffney, 1985a, b) would have provided high-latitudecorridors for east-west a.) migration of pines during the Eocene (Tiffney, -d 1985a, b). The major limiting condition for plant growth 0~~~~~~0 poleward now is light.The suggestion that the Earth o = ON ON WW UUU may have had a lower angle of inclination in the early Tertiary (Wolfe, 1978), which would allow o ~~ ~ ~ C _Cd Cd EOEsd O OC ca ? >. 0'N ON 0' ON more light at high latitudes, has been discredited o 0 (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 N -- 0 N LO c -; photosynthesizeunder light regimes that were pro- 0 = 0 hibitive under conditions of lower carbon dioxide concentrations that apparently followed the end of U) .Y > X > n > ?_.) a. _ _ _ the Eocene (Berner et al., 1983; Creber & Chalo- . Q ner, 1984; Ruddiman & Kutzbach, 1989, 1991; 7= o ,o 40 N Kerr, 1991). 4 - M LO 5 ,Z u -!xzoU- U- o - Low latitudes in North America and Eurasia also -4 appear to have been refugia for pines during the 4> o ~~~~~~~~~~~~~~~~~~>> > > warm humid periods of the Eocene. There is ample evidence that conditions in general were warmer 0 Wkn-W4= and drier at low latitudes than at middle latitudes 0 in the Eocene. These conditions have been docu- mented for the southeastern United States, Central -a 2 0N 0 I Z 0 0 America, Taiwan (Wolfe, 1975), southern China and southeastern Asia (Guo, 1980; Hsu, 1983), ._ C0 1o Co o o 0 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 C I ~~~~~~~~~~~~~~~C circumpolar regions,the low-latitudedry areas were S 0 0 0 0 0 disjunct and disconnected, even between the south- oJd) . co X1; =:: ON eastern United States and Central America, and

2 a) refugial populations were unlikely to have been U a) ) cn N -~~~~~~~~~. 0 _ - ~_ ~ ~ ~_ ~_ _ c ) . connected by broad migrationroutes (Wolfe, 1975). C d There is less abundant fossil evidence for pines Cd Cd Cd s at low latitudes than at high latitudes during the = 1D cd Q Q > > > Q4-> > Q Q Eocene. There are few early Tertiary plant-bearing Q deposits in the areas of special interest, such as Mexico, Central America, and the Mediterranean, primarilydue 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- bU bOW)b W) ) C U) U) Uf) eastern and southwestern United States, and in HS areas of southeastern Europe that were at low 0- latitudes during the Eocene (Table 3). In Mexico, the single specimen of pine at Chiapas (14'N) from the Oligocene (one of the earliest Tertiary plant records in Mexico), and the abundance of pines in 490 Annals of the MissouriBotanical Garden

Veracruz (1 70N) from the Miocene suggest that SECONDARY CENTERS OF pines may have been present in Mexico and Central PINE DIVERSITY America earlier (Table 4). Similarly, pines were The widespread extirpation of pine populations present in the Oligocene and abundant in Miocene from middle latitudes at the end of the Mesozoic 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 frommiddle 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 frominterior western North America testifies Of two closely related pinaceous genera of the to the presence of mid-latitude refugia. Pines in Mesozoic, Pseudoaraucaria 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 refugialareas where conditions were favorable. related to Pinus, represents major extinctions in During warm humid periods, pines in interiorwest- the pine farrrilyduring the early Tertiary. ern North America may have been fragmentedinto 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 the evolution of new areas and centers of volcanism. Several of the pine- centers of pine diversity and 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 were generally low across the con- been documented for angiosperm floraas being one land elevations tinents, by the late Eocene several regions were of the firstareas at middle latitudes in North Amer- active tectonically. In subsequent epochs, volca- ica where climatic conditions became temperate nism and mountain-building became increasingly duringthe Paleogene. Widespread volcanism along important locally and globally. to the the cordillera added many cubic meters The upliftof 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-buildingcoincided 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-latitudeareas 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, withmany areas America is known to have had important upland having newly disturbed sites followingvolcanic 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 fragmentedand isolated. All these conditions must middle-latitudelocations in the Eocene. In Japan, have favored divergence and speciation in pines. the firstTertiary 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 farthernorth and expanded Although pines expanded and contracted from southward during the cool periods. Boreotropical refugialareas during the fluctuatingwarm and cool angiosperms occurred throughoutAsia 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 middlelatitudes. These Volume 80, Number2 Millar 491 1993 Evolutionof Pinus

migrations provided further opportunities for di- the lineages leading to P. contorta and P. banksi- vergence. As new environmentswere 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 driftby founder effects arose, as P. virginiana had southeastern affinities.Eocene well as for hybridizationwith formerlyisolated lin- fossils with affinitiesto Contortae have been found eages. in northern Washington, and Oligocene fossils in British Columbia, corroborating a northern refug- ium (Tables 3, 4). EVOLUTION WITHIN PINUS IN Subsection Ponderosae also may have had both RELATION TO EOCENE REFUGIA northern and southern refugia. There are 10-17 to Mexico and By the end of the Paleogene, all subsections of species endemic or nearly endemic whereas wide-rangingPinus pon- Pinus, withthe possible exception of Cembrae, had Central America, distribution and northern evolved (Axelrod, 1986; Millar & Kinloch, 1991). derosa has a northern in its habitat preference and The events of the early Tertiary probably gave rise ecological affinities vegetation associates. Early Tertiary pines most to at least two subsections, speciation of lineages to Ponderosae have been found in within several subsections, and the current bioge- closely allied British Columbia (Eocene, Table 3), northern ography of many subsections and groups within and Montana (Oligocene, Table 4). several subsections. Washington, 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 of pines at low and high latitudes (see diversity of evolutionary patterns in Ponderosae also indi- In Axelrod, 1986, for maps of pine subsections). cates northern and southern division in the sub- North America three subsections, Cembroides, 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 distinctphylads had southern originsin 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 monticola and P. strobus would have mi- trales may have had refugial areas with a broader grated fromnorthern refugia, and those of P. stro- southern distribution,including the Gulf Coast (Ta- biformis,P. ayacahuite, and P. chiapensis (Mar- bles 3, 4). The current distributionof 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 Australes may 1966) would have migrated fromsouthern refugia. have had refugia in both regions. Although not Northern refugia are corroborated by Eocene fossil identifiableto 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 fragmentedinto 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. flexilis and possibly P. strobifor- (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 Balfourianae is an ancient Four subsections in North America appear to lineage (Kossack, 1989; Strauss & Doerksen, 1991; have been fragmentedby 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 Sylvestres is indi- Mountain refugia during the early Tertiary. Pres- cated by the extant lineages of P. resinosa (40- ent distributionof the three closely related species 52?N) and P. cubensis (restricted to Cuba, 220N). is in the Rocky Mountain/Great Basin/Sierra- Eocene fossilswith affinitiesto Sylvestres that sup- Cascades Ranges of the western United States be- port a northernrefugium have been found in British tween 350N and 41'N latitude. Early Tertiary fos- Columbia and northern Washington (Table 3). sils with probable affinitiesto 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). 492 Annals of the MissouriBotanical Garden

In Eurasia, sequences of conifer-bearingdepos- as represented by extant P. bungeana, and by its from the early Tertiary are not as widely dis- early Tertiary deposits containing pine pollen in tributedas in North America, but evidence for pine China (Tables 3, 4). evolution in relation to refugia exists. Three ancient Refugia for subsection Strobi in Eurasia were subsections, Canarienses, Pineae, and Krempfi- mostly along the Tethys. Of the eight extant Eur- ani, have extant species restricted to regions that asian species in the subsection, only P. parviflora were along the Tethys seaway. 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. krempfiinow occurs. species are all distributedalong the formerTethys Pine was recorded in abundance throughout early region. No early Tertiary fossilsfrom Eurasia have Tertiary strata and in coastal southeast China and been specifically allied with subsection Strobi, al- in northwest Borneo (Tables 3, 4). Other fossil though Miocene fossils of the subsection testifyto floras for southeast Asia include temperate taxa, their presence in that region (Klipper, 1968). suggesting that pines would have found favorable The consequence of certain Eocene refugia be- habitats. coming secondary centers of pine diversityis best In western Europe, the boreotropical angio- described for Mexico and Central America. Al- sperm flora was recorded abundantly from 450N though parts of the Mexican and Central American to 560N (Chaney, 1940). Although there are no isthmuses were transientlyunder water during the fossil records from currently low latitudes in Eu- Mesozoic (Kellum, 1944; Eguiluz Piedra, 1985), rope, pine fossilsare known fromareas 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 Oligocene/ 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. Upliftin 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 distributionsfor 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, 21 varieties, and 14 forms(Eguiluz Piedra, sections appear to have been divided by Eocene 1985). Within many subsections, extensive radi- events into northernand southern refugia. In Syl- ation and speciation are ongoing, which has been vestres, lineages represented by extant P. sylves- attributed to active mountain-buildingthat 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 refugiumin Eurasia. The remaining 14 extant spe- related species clusters, with subsections Ponde- cies in Sylvestres, excluding P. densiflora, 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 Sylvestres The difficultyof 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-latituderefugia, as Parrya, including subsection Cembroides, is an- documented by fossil pollen of unknown affinity cient (Kossack, 1989; Strauss & Doerksen, 1991). fromthe Eocene and Oligocene of Japan and north- Ancestral Cembroides lineages would have been ern China (Tables 3, 4). Subsection Gerardianae concentrated in Mexican/Central 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-latituderefugium in northern China, have begun in the early Tertiary. Volume 80, Number2 Millar 493 1993 Evolutionof Pinus

Two subsections may have originated in Mexi- ways the Pleistocene was analogous to the Eocene. can/Central American refugia (Axelrod, 1980, The Pleistocene was also an epoch with fluctuating 1986). Unlike other subsections, Oocarpae and climates, but the deviation fromtemperate climates Sabinianae have no Mesozoic 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 mor- isodes. The amplitude in average temperature be- phological adaptations (Shaw, 1914, 1924; Little tween glacial and interglacial periods of the Pleis- & Critchfield,1969; Klaus, 1980; van der Burgh, tocene (5?-100C, Bowen, 1979) was about the 1984), these subsections have long been considered same as estimated for the cool and warm periods to have originated recently. Phylogenetic analysis of the Eocene. The Pleistocene differedin 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 floristicevidence, 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 terglacials. to mainland Mexico/Central America prior to the The events of the Pleistocene had enormous Miocene. The northern lineages appear to have effectson vegetation, including pines. In northern diverged by the time they reached California (Millar latitudes, pine distributionswere displaced by con- et al., 1988), indicating that the radiation events tinental ice sheets (e.g., Pinus contorta/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 & Spaulding, 1979). genetic relationships of some Latin American spe- Along coasts and in other lowlands, pine popula- cies link Oocarpae withAustrales 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; fossilrecords, appear to have had Mexican/Central Millar, 1983). Concomitant to the shiftsin distri- American Paleogene refugia, and may have been bution of pines were major changes in the genetic ancestral to Oocarpae. 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 confinedto southern California(Axelrod, of genetic variation withinspecies and allowed some 1986). Fossils are known only from 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 relationshipsof ex- appear to have completely reshuffledthe 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- primarilyaffected Pinus in a gradient from north nianae from early Tertiary Ponderosae lines. to south, with the effect that species and popula- tions shiftedsouth then north (or down then up in elevation) following the cycle of the glacial and PLEISTOCENE VERSUS EOCENE IMPACTS 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 distributionsand evolution. had the effectof dissecting the genus and concen- The question may arise whether the effectsof the tratingpines 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 offerlocal 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 extinctionsin North Amer- unprecedented in the historyof the Earth. In some ica are attributed to the Pleistocene (Critchfield, 494 Annals of the MissouriBotanical Garden

1984), although western Europe suffereda signif- ANDRESEN, J. W. 1964. The taxonomicstatus of Pinus icant impoverishmentof pine flora(Klipper, 1968). chiapensis. Phytologia10: 417-421. * 1966. A multivariateanalysis of Pinus chia- Some speciation, for example, in Balfourianae, pensis-monticola-strobusphylad. Rhodora 68: 1- Cembroides, and Oocarpae, seems to have been 24. triggered by the Pleistocene, but no major new AXELROD, D. I. 1965. A methodfor determiningthe trends have emerged. altitudesof Tertiaryfloras. Palaeobotanist 14: 144- Insufficienttime has elapsed since the close of 171. . 1966. The Eocene Copper Basin Flora of the Pleistocene for its full impact to be felt on northeasternNevada. Univ. Calif. Publ. Geol. Sci. evolution in Pinus. Patterns initiated by the Pleis- 59. tocene appear minor compared to the effects of . 1968. Tertiaryfloras and topographichistory the Eocene and are insufficientto erase the evo- of the Snake River basin, Idaho. Bull. Geol. Soc. Amer.79: 713-734. lutionaryimpacts of the early Tertiary. Thus, many . 1979. Desert vegetation,its age and origin. of the major evolutionary patterns of the early Pp. 1-72 in 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. Centerfor Arid and Semi-AridLand Studies,Lub- bock, Texas. VALIDATION OF THE HYPOTHESIS . 1980. Historyof the maritimeclosed-cone The arguments developed in this paper result in pines, Alta and Baja California.Univ. Calif. Publ. Geol. Sci. 120: 1-143. a workinghypothesis about the effectof the Eocene 1981. Holocene climaticchanges in relation on pine evolution. The hypothesis is a reconstruc- to vegetationdisjunction and speciation.Amer. Nat- tion of pine historybased on available information uralist117: 847-870. from the fossil record, climatic and tectonic evi- - 1986. Cenozoichistory of some western Amer- dence, and biogeographic record of angiosperms ican pines. Ann. MissouriBot. Gard. 73: 565-641. & H. P. BAILEY. 1976. Tertiaryvegetation, and conifers. Many gaps in informationexist that, climateand altitudeof 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. RAVEN. 1985. Originsof the Cordil- panded fossil records are urgently needed, es- leran flora.J. Biogeogr.12: 21-47. BANKS, H. P., A. ORTIZ-SOTOMAYOR& C. M. HARTMAN. pecially in regions hypothesized as Eocene pine 1981. Pinus escalantensis,sp. nov. a new permi- refugia that currently have meager fossil docu- neralizedcone fromthe Oligoceneof BritishColum- mentation. These include Paleogene records for bia. Bot. Gaz. (Crawfordsville)142: 286-293. Central America and Mexico, low latitudes along BARRON, E. J. 1984. Climaticimplications of the vari- the European Tethys, and high latitudes in eastern able obliquityexplanation of Cretaceous-Paleogene highlatitude floras. Geology 12: 595-597. Asia. Technologies that allow more accurate iden- 1985. Estimationsof the Tertiary global cool- tificationof fossilaffinities 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. Oligoceneplants from the upper Ruby River Basin, southwestMontana. Mem. Geo. groups. These technologies need to be applied to Soc. Amer.82. published fossil floras, with revised taxonomic lists. BERNER, R. A., A. LASAGA & R. M. CARRELS. 1983. Certain pine lineages have especially meager fossil The carbonate-silicategeochemical cycle and its ef- records, including Cretaceous records of sections fecton atmosphericcarbon-dioxide over the past 100 million Parrya, especially Gerardianae and Balfouria- years. Amer.J. Sci. 283: 641-683. BLACKWELL, W. H. 1984. Fossil Ponderosa-likepine nae, and Cretaceous/early Tertiary records of sec- wood fromthe Upper Cretaceousof northeastMis- tion Pinea. Accurate dating of fossils and corre- sissippi.Ann. Bot. (London) 53: 133-136. lation withpaleoclimatic and paleogeological events BOND, W. J. 1989. The tortoiseand the hare: ecology will also help to track the fine scale paths of these of angiospermdominance and gymnospermpersis- tence. J. Linn. Soc. Biol. 36: 227-249. pines. Finally, existing and emerging genetic and BOWEN, D. Q. 1979. Geographicalperspective 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 PotomacGroup of Maryland. Dept. Geol. MinesWa- allow tests of the hypothesized times of geographic ter Res. Bull. 27. BROWN, R. W. 1934. The recognizablespecies of the isolation. GreenRiver flora. U.S. Geol. Surv. Prof.Paper 185- C: 45-77. LITERATURE CITED . 1937. Additionsto some fossilfloras of the ALVIN, K. L. 1960. Furtherconifers of the Pinaceae westernUnited States. U.S. Geol. Surv. Prof.Paper fromthe Wealden Formationof Belgium.Mem. Inst. 186-J: 163-206. Roy. Sci. Nat. Belgique. 146: 1-39. BURCHARDT, B. 1978. Oxygenisotope palaeotempera- Volume 80, Number2 Millar 495 1993 Evolutionof Pinus

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