EXTINCT TRANSITIONAL FAGACEAE FROM THE OLIGOCENE AND THEIR PHYLOGENETIC IMPLICATIONS

Fruits, catkins, and associated leaves of at least two extinct trigonobalanoid taxa have been discovered at an Oligocene fossil plant locality rich in fagaceous remains. These fossils exhibit a mosaic of fruit and pollen characters found in the two extant subfamilies Castaneoideae and Fagoideae of Fagaceae. Comparison with cladograms based on modern taxa suggests that these extinct taxa were similar to the ancestors of subfamily Fagoideae and may have been intermediate between Fagus and the modern trigonobalanoid genera. Pollen types isolated from the fossil staminate catkins provide unique character states that are transitional between modern pollen types in Fagaceae and are important in understanding the evolution of exine micromorphology within the family. This analysis provides a striking example of the use of character data from fossils to determine character-state adjacency prior to polarization of characters using outgroup comparison. Because of the mosaic nature of their character complexes, these fossils support monophyly in both the family Fagaceae and the subfamily Fagoideae. In addition, the occurrence of trigonobalanoid fossils in the Oligocene of North America has interesting biogeographic implications and provides insights into the nature of North American Fagaceae during the Tertiary.     

ATTACHED REPRODUCTIVE AND VEGETATIVE REMAINS OF THE EXTINCT AMERICAN-EUROPEAN GENUS CEDRELOSPERMUM (ULMACEAE) FROM THE EARLY TERTIARY OF UTAH AND COLORADO

Fossil twigs with attached foliage, fruits, and flowers from the middle Eocene of the Green River Formation in northeastern Utah and northwestern Colorado and from the early Oligocene Florissant beds of central Colorado provide a firm basis for reconstructing two species of an extinct ulmaceous genus that was widely distributed in the Tertiary of midlatitude western North America and Europe. The fruits are samaras of Cedrelospermum Saporta, a genus previously known only from isolated specimens. The distichously arranged, slender, pinnate-veined leaves vary from serrate with simple teeth to, less commonly, entire-margined. Corresponding isolated leaves in the Green River, Florissant, and other Eocene to Oligocene localities of western North America are now excluded from Zelkova and Myrica, to which they were previously misidentified. The anthers of the staminate flowers contain 3–5 porate pollen with rugulate sculpture. Based upon combined characters of phyllotaxy, and leaf, flower, fruit, and pollen morphology, Cedrelospermum can be referred to the extant subfamily Ulmoideae, and is similar to Phyllostylon, Zelkova, and Hemiptelea. The abundance of Cedrelospermum in lake sediments of volcanic areas, together with its production of numerous small winged fruits, suggest that it was an early successional colonizer of open habitats.     

Did gene family expansions during the Eocene–Oligocene boundary climate cooling play a role in Pooideae adaptation to cool climates?

Adaptation to cool environments is a common feature in the core group of the grass subfamily Pooideae (Triticeae and Poeae). This suggest an ancient evolutionary origin of low temperature stress tolerance dating back prior to the initiation of taxonomic divergence of core Pooideae species. Viewing the Pooideae evolution in a palaeo‐climatic perspective reveals that taxonomic divergence of the core Pooideae group initiated shortly after a global super‐cooling period at the Eocene–Oligocene boundary (～33.5–26 Ma). This global climate cooling altered distributions of plants and animals and must have imposed selection pressure for improved low temperature stress responses. Lineage‐specific gene family expansions are known to be involved in adaptation to new environmental stresses. In Pooideae, two gene families involved in low temperature stress response, the C‐repeat binding factor (CBF) and fructosyl transferase (FT) gene families, has undergone lineage‐specific expansions. We investigated the timing of these gene family expansions by molecular dating and found that Pooideae‐specific expansion events in CBF and FT gene families took place during Eocene–Oligocene super‐cooling period. We hypothesize that the E–O super‐cooling exerted selection pressure for improved low temperature stress response and frost tolerance in a core Pooideae ancestor, and that those individuals with multiple copies of CBF and FT genes were favoured.     

An efficient method for estimating vein density of Glossopteris and its application

Glossopteris-type leaves are the most abundant floristic element from the Gondwanan continent and are recorded throughout the Permian, which was a period of extreme icehouse-to-hothouse climatic global change. Fossil leaf traits can be useful for the reconstruction of palaeoenvironments and identification of climatic changes throughout geological time, but the conservative morphology of Glossopteris leaves has thus far made them difficult to use for this purpose. If the characters of Glossopteris can be better quantified then it should make them useful for tracking environmental changes over a wide geographical area and over a long time interval. Venation density is a highly variable leaf trait that might be useful for this purpose. This trait can be calculated, usually as vein length per centimetre squared, but this can be a time-consuming procedure. In this paper we propose a new rapid method to estimate venation density in a conical sector of Glossopteris leaf lamina using an accurate linear model whose predictors are three linear venation densities, measured as veins per centimetre. In addition to substantially reducing the data collection time, it is less biased and more reproducible than methods applied previously with this leaf type. Using this more robust method, preliminary results significantly distinguish the venation densities of leaves produced in wet and drier ecosystems, matching a pattern similar to modern plants. This is the first survey using a large sample size to reveal that environmental stress controlled the vein architecture of Palaeozoic plants, in a manner similar to plants in modern ecosystems.     

TRIGONOBALANUS (FAGACEAE): TAXONOMIC STATUS AND PHYLOGENETIC RELATIONSHIPS

The fagaceous genus Trigonobalanus as recently treated includes 3 species, two in Malaysia and Southeast Asia and a single species in Colombia, South America. Character analysis suggests that the genus as currently circumscribed is paraphyletic, without synapomorphies to unite the three species. Each of the three species is a morphologically distinct relict of a group that probably was ancestral to the modern genera Quercus and Fagus. Each of the three species also has at least one autapomorphy which is unique within Fagaceae. Analysis of cupule morphology in Fagaceae provides an interpretation of evolution in cupules which differs substantially from Forman's interpretation. We interpret trigonobalanoid cupules as indicative of an ancestral type of inflorescence within Fagaceae. This inflorescence type is a dichasial structure in which the outermost axes are cupular valves, but the degree of branching and subsequent number of fruits are variable. Following this model, a strict relationship exists between valve number and fruit number as seen in cupules of Trigonobalanus (valves = fruits + 1). Fossil evidence is consistent with our interpretation of the phylogenetic position of the trigonobalanoids. We propose to segregate the three species of Trigonobalanus as three monotypic genera; two of these require names which we provide here: Formanodendron and Colombobalanus.     

Warm–cold colonization: response of oaks to uplift of the Himalaya–Hengduan Mountains

Clarifying the relationship between distribution patterns of organisms and geological events is critical to understanding the impact of environmental changes on organismal evolution. Quercus sect. Heterobalanus is now distributed across the Himalaya–Hengduan Mountains (HHM) and warm lowland in East China, yet how the distribution patterns of this group changed in response to the HHM uplift remains largely unknown. This study examines the effect of tectonic events in the HHM region on the oaks, providing a biological perspective on the geological history of this region. Fifty‐six populations of Quercus sect. Heterobalanus were genotyped using four chloroplast DNA regions and nine nuclear simple sequence repeat loci to assess population structure and diversity, supplemented by molecular dating and ancestral area reconstructions. The underlying demographic dynamics were compared using ecological niche models of the species distributions during the last glacial maximum and the present. These analyses illustrate that Quercus sect. Heterobalanus diversified as the HHM uplifted and climatic cooling during the mid‐Miocene, colonizing the cold habitats from warm broadleaf mixed forests. Lineages in cold highlands and warm lowlands have diverged as a consequence of local adaptation to diverging climates since the late Miocene. Our results suggest that continuous uplift of the HHM in the late Miocene to early Pliocene accompanied by simultaneous cooling triggered the differentiation of oaks. The biogeography of Quercus sect. Heterobalanus illuminates the geological events responsible for the modern‐day HHM.     

Evolution of angiosperm seed disperser mutualisms: the timing of origins and their consequences for coevolutionary interactions between angiosperms and frugivores

The origins of interactions between angiosperms and fruit‐eating seed dispersers have attracted much attention following a seminal paper on this topic by Tiffney (1984). This review synthesizes evidence pertaining to key events during the evolution of angiosperm–frugivore interactions and suggests some implications of this evidence for interpretations of angiosperm–frugivore coevolution. The most important conclusions are: (i) the diversification of angiosperm seed size and fleshy fruits commenced around 80 million years ago (Mya). The diversity of seed sizes, fruit sizes and fruit types peaked in the Eocene around 55 to 50 Mya. During this first phase of the interaction, angiosperms and animals evolving frugivory expanded into niche space not previously utilized by these groups, as frugivores and previously not existing fruit traits appeared. From the Eocene until the present, angiosperm–frugivore interactions have occurred within a broad frame of existing niche space, as defined by fruit traits and frugivory, motivating a separation of the angiosperm–frugivore interactions into two phases, before and after the peak in the early Eocene. (ii) The extinct multituberculates were probably the most important frugivores during the early radiation phase of angiosperm seeds and fleshy fruits. Primates and rodents are likely to have been important in the latter part of this first phase. (iii) Flying frugivores, birds and bats, evolved during the second phase, mainly during the Oligocene and Miocene, thus exploiting an existing diversity of fleshy fruits. (iv) A drastic climate shift around the Eocene–Oligocene boundary (around 34 Mya) resulted in more semi‐open woodland vegetation, creating patchily occurring food resources for frugivores. This promoted evolution of a ‘flying frugivore niche’ exploited by birds and bats. In particular, passerines became a dominant frugivore group worldwide. (v) Fleshy fruits evolved at numerous occasions in many angiosperm families, and many of the originations of fleshy fruits occurred well after the peak in the early Eocene. (vi) During periods associated with environmental change altering coevolutionary networks and opening of niche space, reciprocal coevolution may result in strong directional selection formative for both fruit and frugivore evolution. Further evidence is needed to test this hypothesis. Based on the abundance of plant lineages with various forms of fleshy fruits, and the diversity of frugivores, it is suggested that periods of rapid coevolution in angiosperms and frugivores occurred numerous times during the 80 million years of angiosperm–frugivore evolution.     

Pollen morphology of Quercus sect. Ilex and its relevance for fossil pollen identification in southwest China

Pollen grains of 16 modern species of Quercus were examined by scanning electron microscopy (SEM) and light microscopy (LM). The focus of this investigation was on a small group (c. eight species) of alpine, sclerophyllous oaks that may form a monophyletic group within sect. Ilex. The data were combined with published data for Polar axis (P) and Equatorial diameter (E) for more than 80 species. Based on pollen morphology Quercus pollen grains were divided into three types: (1) The Cyclobalanopsis type is smallest (generally < 23 μm) in size, with P/E ratios of approximately 1.08 and a psilate or fine-grained surface; (2) Quercus sect. Ilex type is 23–29 μm, the P/E ratio is approximately 1.24 (prolate) and it has a rugulate pollen surface; (3) the Quercus sect. Quercus type is generally > 29 μm in size, has a P/E ratio of approximately 1.04, and a clearly verrucate pollen surface. Based on a comparison with modern pollen size and ornamentation, fossil pollen grains of the Quaternary Qinghai Lake core can be assigned to the Chinese southwest mountain oak group of Quercus sect. Ilex (in particular Quercus semecarpifolia). In addition, we show that the pollen percentages of Quercus rapidly increased to the highest level during the glacial period. Using SEM for the identification of fossil Quercus pollen grains is essential to ensure the accuracy of differentiating evergreen Quercus types (sect. Ilex versus sect. Cyclobalanopsis) during the last glacial period in southwest China.     

Evolution of rDNA FISH patterns in the Fagaceae

The Fagaceae is one of the most important plant families in European forest ecosystems, and it includes several genera distributed in the Northern hemisphere. In this work we studied the genome organization and evolution within the family, by karyotyping and physically mapping rDNA in ten European and Asian species of the genera Fagus, Quercus, and Castanea. All of the species studied had a chromosome number of 2n=2x=24, except for the first report of a single individual of Quercus suber which proved to be triploid (2n=3x=36). The rDNA physical mapping revealed several patterns: the dominant one is present in European and Asian Quercus subgenus Quercus, and in Castanea sativa and Castanea crenata, consisting of two 18S–25S rDNA loci (one subterminal major and one pericentromeric minor) and one 5S rDNA pericentromeric locus. In Fagus sylvatica and in Quercus sessilifolia, different patterns were observed: four terminal 18S–25S rDNA loci and two 5S rDNA pericentromeric loci in the former, and five 18S–25S rDNA loci (three terminal and two intercalary) and one 5S rDNA pericentromeric locus in the latter. In Castanea mollissima a distinct rDNA distribution pattern with two intercalary 18S–25S rDNA loci and two 5S rDNA was found. These findings suggest rDNA loci restructuring during Castanea evolution, and variability of 18S–25S loci between Quercus and Cyclobalanopsis subgenera.     

A new species of Zelkova (Ulmaceae,Ulmoideae) with leaves and fruits from the Oligocene of South China and its biogeographical implications

A new fossil species of Zelkova is described from the Oligocene Ningming Formation of Guangxi, South China. Zelkova ningmingensis sp. nov. is characterized by leaves with craspedodromous venation pattern and drupaceous fruit type. The new species possesses elliptical to ovate leaves, bearing 7–12 pairs of secondary and simple toothed margin, as well as epidermal cells with straight or rounded anticlinal walls. The species is compared with extant and other fossil species hitherto reported of the genus. It is most similar to the living Zelkova schneideriana in the leaf gross morphology and epidermal characters, which may be suggested to be the ancestral type of Zelkova schneideriana. The discovery of Zelkova ningmingensis sp. nov. in Guangxi indicates that Zelkova has already existed in southern China as early as the Oligocene. In combination with Zelkova material from the Oligocene of Europe, it can be inferred that Eurasian Zelkova had begun to diversify by at least the Oligocene. Because China is the biodiversity centre of modern Zelkova, the fossil herein provides new insights into Zelkova biogeography.     

Modern pollen and vegetation relationships in the mountains of southern California,USA

The relationship between modern pollen assemblages and modern vegetation along two elevational transects within the Transverse and Peninsular Ranges of southern California, USA, is demonstrated using cluster analysis of the pollen data. Cluster analysis separates the Sonora Desert vegetation, Valley grassland/agricultural land and chaparral vegetation types on the San Jacinto Mountains transect. Chaparral is not easily separated on the San Bernardino Mountains transect, probably due to the presence of Quercus dumosa (scrub oak) there. The lower montane Quercus – Pinus (oak – pine) community is distinct from other forest types, and can be subdivided palynologically based upon relative importance of Quercus, Pinus and Cupressaceae [primarily Calocedrus decurrens (incense cedar)] pollen. Subdivisions include Quercus – Pinus – Cupressaceae, Quercus – Cupressaceae – Pinus and Quercus – Pinus assemblages. Higher elevation Pinus – Abies (pine – fir) and Pinus-dominated communities are also differentiated from one another, although the subalpine vegetation type only occurs on the San Bernardino Mountains transect. Though the study area presently straddles a transition between winter-wet and summer-wet climatic regimes, differences between the pollen assemblages in the two mountain ranges are minimal. Pollen assemblages from lower elevations document the effects of human activities, primarily agriculture, on the modern pollen rain of the region, with the occurrence of introduced citrus (Citrus sp.) and shade (Eucalyptus sp.) trees and weedy disturbance indicators (e.g., Brassicaceae).     

Antagonistic selection and pleiotropy constrain the evolution of plant chemical defenses

When pleiotropy is present, genetic correlations may constrain the evolution of ecologically important traits. We used a quantitative genetics approach to investigate constraints on the evolution of secondary metabolites in a wild mustard, Boechera stricta. Much of the genetic variation in chemical composition of glucosinolates in B. stricta is controlled by a single locus, BCMA1/3. In a large‐scale common garden experiment under natural conditions, we quantified fitness and glucosinolate profile in two leaf types and in fruits. We estimated genetic variances and covariances (the G ‐matrix) and selection on chemical profile in each tissue. Chemical composition of defenses was strongly genetically correlated between tissues. We found antagonistic selection between defense composition in leaves and fruits: compounds that were favored in leaves were disadvantageous in fruits. The positive genetic correlations and antagonistic selection led to strong constraints on the evolution of defenses in leaves and fruits. In a hypothetical population with no genetic variation at BCMA1/3, we found no evidence for genetic constraints, indicating that pleiotropy affecting chemical profile in multiple tissues drives constraints on the evolution of secondary metabolites.     

ITS sequences from nuclear rDNA suggest unexpected phylogenetic relationships between Euro-Mediterranean, East Asiatic and North American taxa ofQuercus (Fagaceae)

Nucleotide sequences from the internal transcribed spacer (ITS) regions of the 18S–26S nuclear ribosomal DNA have been studied from ten species ofQuercus (representing four subgenera),Castanea sativa andFagus sylvatica, as a preliminary molecular contribution to the still poorly understood systematics and evolution ofFagaceae. The resulting matrix has been used to calculate pair-wise sequence divergence indices and to construct a maximum parsimony tree forQuercus coding indels as a fifth state. Divergence is greater forQuercus vs.Fagus than forQuercus vs.Castanea. The tree for theQuercus taxa studied reveals two clearly divergent clades. In clade I the evergreen W MediterraneanQ. suber appears in a basal position as sister to more distal deciduous taxa, i.e. the E MediterraneanQ. macrolepis and the E AsiaticQ. acutissima (all formerly united as different sections under the apparently polyphyletic subg.Cerris), andQ. rubra (a representative of the N American subg.Erythrobalanus), forming a pair withQ. acutissima. In clade II the evergreen southeastern N AmericanQ. virginiana is basal and sister to the remaining three branches, i.e. a pair of evergreen Mediterranean taxa withQ. ilex andQ. coccifera (subg.Sclerophyllodrys), the deciduous but otherwise plesiomorphic SE European/SW AsiaticQ. cerris (type species of subg.Cerris), and the related but more apomorphic European pairQ. petraea andQ. robur (subg.Quercus). These results partly conflict with current taxonomic classification but are supported by some anatomical and morphological characters. They document polyphyletic lines from evergreen to deciduous taxa and suggest Tertiary transcontinental connections within the genus.     

A SYNOPSIS OF NORTH AMERICAN ASTERS: THE SUBGENERA,SECTIONS AND SUBSECTIONS OF ASTER AND LASALLEA

Traditional treatments of Aster were found unsatisfactory in predicting cytological and morphological characteristics of members of various subgenera, sections and subsections of different authors. A realignment of species into these infrageneric categories is presented and is based on sets of shared morphological characteristics of roots or rhizomes, leaves, and phyllaries. Eight subgenera are recognised in Aster. Subgenus Aster is divided into five sections on morphological characteristics: three have X = 9, one has X = 8 and one has X = 7. Subgenus Aster section Dumosi has been redefined and contains all the X = 8 species. Ten X = 5 species and one X = 4 species previously classified in up to six sections of subgenus Aster were found to be morphologically and cytologically related to each other, but unrelated to the other species of Aster. These eleven species have been assigned to the genus Lasallea sensu Semple & Brouillet. Lasallea has been divided in sections and subsections with new combinations presented in this paper.     

THE PLATYCARYA PERPLEX AND THE EVOLUTION OF THE JUGLANDACEAE

We report on the leaves, fruits, inflorescences, and pollen of two fossil species in the genus Platycarya. The association of these dispersed organs has been established by their repeated co-occurrence at a large number of localities, and for two of the organs (fruit and pistillate inflorescence, and pollen and staminate inflorescence) by apparent organic attachment of compression fossils. Each of the two species can be distinguished by characteristics of all the known megafossil organs. We also review the fossil record of dispersed platycaryoid fruits and inflorescences, recognizing three additional species of Platycarya and two of Hooleya. Two of the fossil Platycarya species are morphologically very different from the living Platycarya strobilacea Sieb. et Zucc., but they show the diagnostic features of the genus. Hooleya is a generalized member of the Platycaryeae that is probably close to the ancestry of Platycarya. The two Platycarya species known from multiple organs provide a remarkable example of mosaic evolution in which fertile and foliar structures have attained different levels of morphological specialization. The leaves, often considered the most plastic of plant organs, retain several features that are otherwise seen only in the Engelhardieae. These similarities in leaf architecture between the fossil Platycarya species and Engelhardieae are advanced features for the Juglandaceae, and thus indicate a sister-group relationship between the two lines. In contrast to the leaves, the fruits, inflorescences, and pollen of the fossil Platycarya species are almost as specialized as those of the extant P. strobilacea and bear little resemblance to the same structures in other genera of the family. The morphology, taphonomy, sedimentary setting, and geographic and stratigraphic distribution of three of the fossil platycaryoid species suggest that they were wind-dispersed, early successional plants that grew in thickets. This habit is retained by Platycarya strobilacea and is typical of many of the amentiferae (e.g. Myricaceae, Betulaceae). The r-selected life-history pattern of the Platycarya line may well have contributed to its low diversity through geologic time.     

Latitudinal cline of flowering and fruiting phenology in Fagaceae in Asia

The seasonal timing of flowering and fruiting is crucial for the reproductive success of plants and for resource availability to animals. Although plants synchronize their reproductive timing to coincide with appropriate seasons by responding to environmental cues, seasonal variations in temperature and precipitation vary minimally in very wet tropical environments. To explore the latitudinal cline in the reproductive phenology of the Fagaceae in Asia, we analyzed phenology data for a total of 94, 121, and 219 species from Thailand, Malesia, and China, respectively, in the three genera of Fagaceae, Quercus, Castanopsis, and Lithocarpus. We found that Quercus and Castanopsis showed flowering peaks in April in China. In Thailand, the peak shifted to an earlier month, and the peak disappeared in Malesia. The flowering period lengthened with decreasing latitude in the animal-pollinated genera Castanopsis and Lithocarpus. However, this was not the case for the wind-pollinated genus Quercus. The fruiting period lengthened with decreasing latitude in all three genera. We examined the relationship between reproductive phenology and climatic factors. The combination of monthly temperature and precipitation best explained the monthly change in the proportion of flowering and fruiting species in China in all three genera. However, climatic factors had almost no impact on the predictive ability of the model in Malesia. Our results on phenological shifts in the family Fagaceae, from the temperate climates and seasonal tropics to the humid tropics, provide valuable information for predicting phenological changes in future climate change.     

Distribution of isoprenoid emitters in the Quercus genus around the world: chemo-taxonomical implications and evolutionary considerations based on the ecological function of the trait

Isoprenoid (isoprene and monoterpenes) emission is widespread among oak species. A number of studies investigating the emission by oak species around the world are here compiled. These studies indicate that isoprenoids are reliable taxonomical markers at subgenera level. Isoprene-emitters belong to the subgenera Lobateae, Quercus sensu strictu, and Protobalanus and are therefore found in every continent of the northern hemisphere. Non-emitters and monoterpene-emitters belong to Cerris and Ilex (= Schlerophyllodris) subgenus, respectively, and are particularly, if not solely, diffused in the Mediterranean area. The results suggest that the taxonomical assignment of some species should be reviewed. Experimental data indicate that isoprenoids have a protective role against environmental stresses and a strong antioxidant action. On the basis of the present knowledge I speculate that in oaks the ancestral trait is the emission of isoprene, and that the other traits evolved as adaptive response to the environment.     

ATTACHED LEAVES,INFLORESCENCES, AND FRUITS OF FAGOPSIS,AN EXTINCT GENUS OF FAGACEOUS AFFINITY FROM THE OLIGOCENE FLORISSANT FLORA OF COLORADO,U.S.A.

Specimens showing staminate and pistillate inflorescences attached to branches bearing Fagopsis longifolia (Lesq.) Hollick foliage, from the Oligocene Florissant flora of Colorado, permit a relatively complete characterization of the extinct Fagopsis plant. The alternately arranged simple leaves have pinnate craspedodromous venation and prominent simple teeth. Staminate inflorescences are globose on a stout peduncle and contain anthers with tricolporate pollen. Pistillate inflorescences are ovoid heads with compact, helically arranged three-flower units and are interpreted to have three styles per flower. The infructescence consists of small wedge-shaped cupules, each containing three tiny fruits, and subtended by a persistent bract. The cupules unravel from the swollen peduncle at maturity and are often dispersed as strings of adhering fruit-wedges which frequently take on a regular, more or less circular appearance. Fagopsis is unlike any living genus but has characters which support a relationship to the Fagaceae. Unlike extant members of the family, which typically have fruits adapted for animal dispersal, Fagopsis is less obviously specialized and perhaps adapted for wind dispersal. The striking differences in fruiting structures between Fagopsis and extant Fagaceae parallel the differences between the extant genera Platycarya and Juglans in the Juglandaceae, and Alnus and Corylus in the Betulaceae.