CHANGING DISTRIBUTION PATTERNS OF NORTHERN HEMISPHERE EUDICOT HOSTS OF ECTOEDEMIA S.S. DURING THE TERTIARY IN RELATION TO THEIR PHYLOGENY: SETTING THE SCENE FOR LEAFMINER EVOLUTION. LITERATURE THESIS June 2009 Author: Camiel Doorenweerd BSc. Supervision: Dr. Erik J. van Nieukerken (Naturalis) Prof. Dr. Gerard van der Velde (Radboud University) Front page image: “Oak Tree in Winter at Lacock Abbey” (Great Brittain) From: The Correspondence of William Henry Fox Talbot Project (http://foxtalbot.dmu.ac.uk/) 2 CONTENTS Introduction ............................................................................................................................................................ 5 Ectoedemia s. s. and hosts ................................................................................................................................. 5 Tertiary ................................................................................................................................................................ 8 Geographic changes ............................................................................................................................................ 8 Climate ................................................................................................................................................................ 8 APG II ................................................................................................................................................................... 9 Vicariance or dispersal ...................................................................................................................................... 10 Fossils ................................................................................................................................................................ 10 Fagaceae (Fagales) ................................................................................................................................................ 11 Betulaceae (Fagales) ............................................................................................................................................. 15 Salicaceae (Malpighiales) ...................................................................................................................................... 16 Salix ................................................................................................................................................................... 17 Populus .............................................................................................................................................................. 18 Rosaceae (Rosales) ................................................................................................................................................ 20 Platanaceae (Proteales) ........................................................................................................................................ 23 Discussion .............................................................................................................................................................. 25 References ............................................................................................................................................................ 26 3 4 INTRODUCTION Ectoedemia s.s. and hosts Ectoedemia Busck (Ectoedemia) in the family Nepticulidae is a subgenus of small moths of which the larvae are leaf‐ or petiole‐miners. Their distribution covers the temperate and tropic regions of the Northern Hemisphere, as well as South Africa and Indonesia, and they are always specialised on a single or several closely related host species. Ectoedemia sensu stricto are most speciose on Fagales, Rosales and Malpighiales, all Eurosid I (APGII, 2003), but also mine hosts that are only distantly related to those (see figure 1 and figure 2). The Ectoedemia species that have a current distribution throughout the northern hemisphere are all confined to Fagales, Rosales and a clade found on Malpighiales. Members of Proteales and Cornales are only hosts for species in North America, members of Ericales and Dipsacales only in Japan (van Nieukerken pers. comm.). If co‐evolution occurred in Ectoedemia s.s., in the sense that the evolution of the herbivores followed that of the hosts, it is expected that species currently mining on Platanus occidentalis (Proteales) are most basal. Platanus occidentalis is only found in North America and there are mid‐cretaceous ‘Ectoedemia’ fossil traces found in North America on an unidentified Platanoid (Labandeira et al., 1994). The larva of Ectoedemia, as all leaf‐miners, are dependent on their hosts. Although secondary evolution in leaf‐
mining moths has only been identified as one of multiple causes for speciation (Lopez‐Vaamonde et al., 2006), secondary distribution is inevitable. The host must be present before the dependent species can follow. Host shifts can complicate the interpretation of distribution patterns, as an intermediate host can be used to cross disjunctions in the distribution of the original host. Nonetheless the phylogeny of Ectoedemia s.s. seems relatively clear up to now, with most European species sampled and their molecular phylogeny reconstructed (van Nieukerken & Doorenweerd in prep., figure 1). The phylogenetic analysis shows two monophyletic clades with species mining Fagaceae (Fagales) and a weakly supported clade with Rosaceae (Rosales) miners that also includes a clade with Betulaceae miners (Fagales). Species that mine Salicaceae (Malpighiales) are all found on one strongly supported monophyletic clade. This conservatism within a host family suggests that host shifts to different families have been rare and the phylogenetic signal might be correlated with phylogenetic or distributional patterns of the hosts. The minimum age of each of the main host families has been estimated using reliable fossils to date a molecular phylogeny and gave the following results (Crepet et al., 2004): Fagaceae, Rosaceae and Salicaceae: 90 million years minimum age (myma), Betulaceae 83 myma and Platanaceae 100 myma. This paper aims to answer how the current distribution and host specificity of Ectoedemia s.s. is related to the radiation and distribution of hosts in the Tertiary by studying literature. The methods in literature include examining the fossil record, molecular phylogenies, molecular dating and the interpretations thereof for the main Ectoedemia s.s. host families or genera. 5 Figure 1: The current molecular phylogeny of Ectoedemia s.s. based on three genes, Zimmermannia (Ectoedemia) as outgroup (not shown) (Doorenweerd & van Nieukerken in prep.) Clades with more than one taxon are coloured to indicate different host families and mostly coincide with species groups: Dark blue = Albifasciella Group (Fagaceae ‐ Eurasian) Green = Populella Group (Salicaceae ‐ northern hemisphere) Pink = paraphyletic (Rosaceae ‐ northern hemisphere) Yellow = Occultella Group (Betulaceae mining ‐ European) Light blue = Suberis Group + Ornatella group (Fagaceae mining, Suberis group – European and Ornatella Group – Asian)
6 Figure 2: Angiosperm phylogeny at the order level from Soltis et al. 1999, which is equal to the order level phylogeny according to APG II. The numbers in brackets indicate the amount of specimens from that clade sampled. Orders that contain Ectoedemia s.s. hosts are marked yellow. 7 Tertiary Officially the term Tertiary was banned by the International Commission on Stratigraphy in 2003, but it is still commonly used in literature and discussions are ongoing if the ban should be undone1. It defines the period of 65,5 million years ago (mya) up to 2,588 mya, which is officially divided into two periods: Paleogene and Neogene, respectively 65,5 – 23,03 and 23,03 – 2,588 mya. In this paper the term Tertiary will also be used. Geographic and climate changes that occurred in the Tertiary will be shortly discussed to set a frame for the interpretation of Angiosperm evolution and distribution studies. Geographic changes Although all continents as we now know them are recognizable in the landmasses of the Tertiary, there were some differences and changes that occurred that are relevant to Angiosperm distribution. In the early Tertiary North America (NA) and Eurasia (EUA) were each separated into western and eastern sections by epicontinental seaways, the Turgai Strait in EUA and the Sundance Sea in NA (Tiffney and Manchester, 2001). Western NA was connected to Eastern Asia through the Bering Land Bridge (BLB)(figure 3) and eastern North America was connected via Greenland to north‐eastern Europe, a pathway known as the North Atlantic Land Bridge (NALB) (Milne, 2006). The epicontinental seaways and land bridges are likely to have played a key role in the distribution of at least some Angiosperm clades in the northern hemisphere (Milne, 2006). During the first period of the Tertiary the epicontinental seaways receded, uniting Western NA with Eastern NA and Europe with Asia. The breaking up of the NALB was a gradual process, the land separated into many islands and the connections between them are uncertain; making the precise time of the NALB breakup unknown. Biotic connections across the NALB were probably lost gradually up until the middle Tertiary, perhaps 25 or possibly even 15 mya (Milne and Abbott, 2002). The BLB broke down much later and is dated more precise at 5.4‐5.5 mya (Gladenkov et al., 2002). However, the availability of land bridges for range expansion is also dependent on the abiotic factors of these areas: climate. Climate After a relatively brief increase in temperature in the late Paleocene, known as the Paleocene‐Eocene Thermal Maximum (PETM)(figure 4), the climate cooled gently from 50 to 33 mya, then fluctuated until 15 mya, after which the climate cooled progressively, eventually reaching the Quarternary glaciations (Milne and Abbott, 2002). By then most extant plant orders had evolved and managed to distribute throughout the Northern Hemisphere in ‘boreotropical’ and later ‘mesophytic’ forest (Wolfe, 1975). The current disjunct distributions seen in many plant families and genera could be the result of isolation and subsequent speciation of ancestral species that were once found in these ancient forests. The number of disjunctions between Eastern Asia and NA is especially high, indicating that the BLB was more frequently used than the NALB (Donoghue and Smith, 2004). The NALB, existing in the Paleocene and early Eocene has been viewed as a principal route for the spread of thermophilic (including evergreen) taxa of the boreotropic flora in the early Tertiary (Tiffney and Manchester, 2001). During the Paleocene, migration of thermophilic plants across the BLB was likely limited by cool temperatures and long winter darkness due to its high latitude (Xiang et al., 2005). When the NALB started to break up in the Eocene the BLB region became warmer and may have served as an important route for evergreen, but also deciduous taxa (Tiffney and Manchester, 2001). 1
see http://www.stratigraphy.org/upload/ISChart2008.pdf for the most recent stratigraphic chart 8 Figure 3: from Milne (2006) indicating typical disjunct floral areas and the positions of the Tertiary NALB and BLB.
Although North America (NA) and Eurasia (EUA) were both continuous landmasses after the north‐south epicontinental seaways had disappeared, new biotic boundaries arised during the Tertiary as a north‐south belt of relatively arid conditions developed in the centres of NA and EUA. Next to that there was also an east‐west arid belt in Eastern Asia, which is likely to explain the typical north‐south disjunction in Eastern Asia (figure 3) (Milne, 2006). The fossil record was searched for traces of insect herbivory during the relatively brief increase in temperatures during the late Paleocene, the PETM (Wilf and Labandeira, 1999). It showed that there was a significant increase of insect herbivory during that period, according to the authors due to the warming of the climate. Aside from the fact if that actually was the cause, or that it was part of a larger successful evolutionary period of herbivores, it can be said that there was a trend of increased insect herbivory during the late Paleocene and early Eocene at higher latitudes. This is an interesting concept considering the availability of the NALB and BAB that disappeared shortly after: could this relatively short increase in temperature have mediated the distribution of hosts and herbivorous insects that specialized on deciduous hosts to different continents? APG II Plant phylogenetic knowledge has greatly increased in the last two decades and caused considerable shifts at all phylogenetic levels of Angiosperms (APGII, 2003). As a consequence, older interpretations of Angiosperm distributions sometimes have to be re‐evaluated. The most recent Angiosperm published classification and phylogeny was published in 2003 by the Angiosperm Phylogeny Group, titled APG II (APGII, 2003), but the APG website (Stevens, 2001 onwards) is continuously updated with new information from phylogenetic studies. In 9 contrast to previous classifications where morphology was always taken into account for classification, the latest APG classifications rely solely on genetic markers. Congruence with morphologic characters is not completely left out though and discussed in both the publication and website. Vicariance or dispersal There are two main population level processes to explain the existence of present day disjunctions in plant distribution. The first is vicariance; a wide distribution is separated into multiple smaller isolated areas in which allopatric speciation follows. The second is long distance seed dispersal; an ancestral population manages to disperse its seeds to a new area that is not connected genetically to the original population, allowing for rapid speciation (Milne, 2006). Vicariance is directional and to a certain extent even predictable, whereas long distance dispersal is random and unpredictable. For these reasons vicariance is the ‘usual suspect’ to explain current day distributions, but it is difficult to rule dispersal out (Milne, 2006). The general idea is that disjunct patterns found in the Northern Hemisphere are the result of Tertiary relict floras, whereas Southern Hemisphere disjunct patterns are more often the result of rare long distance dispersal events (Milne, 2006). An extensive fossil record is needed to prove which process facilitated distribution, and each family, genus, or even clade will have to be evaluated for vicariance or dispersal patterns. As Donoghue and Smith (2004) state: “the conservative thought that vicariance is the only reason for disjunct flora types is probably oversimplified and it is more likely that there were movements at different times.” Fossils Pollen (microfossils) are abundant in the fossil record of many locations, but mostly of wind pollinated plants and they do not always contain enough diagnostic characters to place them in the current tree of life. Bigger fossils only give a scarce representation of what was present at a certain point in history, but so do the extant species and their distribution. There is no telling in what may have gone extinct. Macrofossils that show coaled remnants of fruits, flowers and leaves, are the most reliable for determination but usually rare. Different studies use different kinds of fossils to add a molecular clock to their phylogenetic analysis which can result in widely diverging estimates (Crepet et al., 2004). Figure 4: Annual mean temperatures estimated in the Paleomap project (http://www.scotese.com/climate.htm) 10 FAGACEAE (FAGALES) Fagaceae are interesting not only because Ectoedemia s.s. are most speciose on this family, but also because their current distributions almost coincide completely. However, there are no Fagaceae mining Ectoedemia s.s. species described from North America even though oak diversity is especially high there. Oaks range from the montane tropics, where evergreen taxa are prominent, to near latitude 50°N, where they are deciduous. Quercus petraea and Q. robur, have the most northerly distributions, reaching 60°N in Scandinavia. Other oaks occur in most climates from tropical and temperate regions to the borders of deserts and in areas of very diverse seasonal distribution of precipitation (Axelrod, 1983). Of the currently recognised sections (see classification below) only members of the Quercus section Quercus are found throughout the entire distribution of Fagaceae, others are restricted to continents or even more local areas. Because hybridisation, cytoplasmic introgression and incomplete lineage sorting are common in Fagaceae the interspecific phylogeny is problematic (Manos et al., 1999), the sections however appear to have well developed sterile boundaries. Classification of Fagaceae with relevant genera for this paper following APG II (APGII, 2003; Manos et al., 1999; Nixon, 1993) : Fagaceae Fagoideae Fagus Quercoideae Quercus Quercus s.s. section Lobatae – red and black oaks [America] section Protobalanus – golden cup or intermediate oaks [America] section Quercus – white oaks [Northern Hemisphere] section Cerris – cerris oaks [Eurasia] Cyclobalanopsis – cycle‐cup oaks [Asia] Castanea Nothofagus Trigonobalanus Fossil analogs of modern Fagaceae are well represented in the Northern Hemisphere, indicating long‐term presence and speciation throughout the Tertiary and Quarternary (Manos et al., 2001). The minimum age of Fagaceae is placed at the Upper Paleocene to Lower Eocene based on fossil evidence (Nixon, 1993). Quercus appears to have achieved a widespread distribution during the Upper Eocene to Lower Oligocene, also based on fossil evidence. The widespread distribution of white oaks is suggestive of more recent connections between Asia and North America, perhaps involving the Bering Land Bridge. By the Eocene, all modern genera had been present (Zhou, 1999). The cooler, drier, and more variable climates that developed in the Oligocene are believed to have encouraged the evolution and migration of the oaks. The radiation into the modern sections that are present today in North America occurred during this time (Wolfe, 1980; Daghlian and Crepet, 1983). For Quercus s.s. section Quercus (white oaks) the fossil data generally support a NA origin during the Oligocene (Manos et al., 1999) with later appearance in Asia (China) in the Miocene (Zhou, 1999). A molecular clock analysis in a phylogenetic study resulted in an estimated time of divergence of the NA and EUA white oak clades approximately 17 mya (Manos et al., 2001); early Miocene, and thus corroborates the fossil record. This pattern follows that of BLB connections followed by vicariance during the Miocene. According to some authors only the deciduous ancestors of section Quercus were capable of migrating via land bridges during the Oligocene (Axelrod, 1983). In china the Paleocene fossils show the 11 appearance and diversification of Fagoidae and Castanea but Quercus sect. Quercus, does not appear until the Miocene (Zhou, 1999). Morphologic study suggested Q. sect. Protobalanus to be the evolutionary link between Q. sect. Lobotae and Q. sect. Quercus and molecular data supports that idea (Manos et al., 1999). Phylogenetic and paleobotanical evidence further suggests that Q. sect. Quercus, containing deciduous species, evolved at middle latitudes in NA and migrated to the EUA prior to the breakup of the land bridges (Manos et al., 1999). Other explanations would require the extinction of either Q. sect. Protobalanus or Q. sect. Lobatae in Eurasia, but this is unlikely because fossils of these sections have not been found there (Zhou, 1999). Quercus sections Lobatae and Protobalanus evolved at middle latitudes of NA and radiated into at least 300 species, with secondary radiations occurring in Mexico, Eastern NA and into EUA. In contrast, it appears that Q. sect. Cerris, comprising several subgroups totalling no more than 70 species, evolved at similar latitudes in Asia (figure 5) (Manos et al., 1999; Manos and Stanford, 2001). Figure 5: Left: phylogram based on parsimony analysis of ITS sequences of Quercus s.l. with bootstrap values. Right: phylogram of Quercus section Quercus indicating a monophyletic origin for all North American species and a monophyletic origin for all Eurasian species. From: Manos and Stanford 2001 12 The Suberis group is one of the two Ectoedemia s.s. Fagaceae mining groups and consists of five species that phylogeographical structure of the evergreen Quercus ilex from the Q. sect. Cerris was done by Lumaret et. al. in 2002. Q. ilex (holm oak) is mostly found in the Mediterranean area, but also extends along the Atlantic coast up to the north of France and has been introduced by humans in many other parts of Europe. There are two main morphological types of Q. ilex: the ‘ilex’ type and the ‘rotundifolia’ type. The two types differ in geographic distribution, humidity preference and morphology and have been regarded as different species, subspecies or even just two varieties by different authors (Lumaret et. al., 2002 for references). A chlorotype phylogram in a study by Lumaret et al. (2002) revealed several clades that did not show only the two types but also various intermediate chlorotypes which differentiated successively from the root (outgroup was Q. alnifoliae, a species endemic to Sicily) and indicated a post glacial migration pattern from east to west (Lumaret et al., 2002). Moreover, Lumaret et al. describes that the high amount of differentiation between the different chlorotypes indicates that the clades are indicative for ice‐age refugia, which would be in congruence with the fossil records that indicates the presence of Q. ilex (as well as other species from the Q. sect. Cerris ) in those areas since the late Tertiary (Carrión et al., 2000). A detailed analysis of geographic patterns in the Ectoedemia Suberis group and evergreen oaks of the Mediteranean area is beyond the scope of this study, but this example shows that speciation patterns of the deeper phylogeny of Ectoedemia s.s. and their hosts probably need more detailed study of distribution patterns and their relation with glacial refugia of the Quarternary. The oldest fossil acorns are from the Miocene, found in North America, from the extinct species Quercus hiholensis belonging to the Q. sect. Quercus (Borgardt and Pigg, 1999). Borghardt and Pigg describe that evidence of predation is present in many of the Q. hiholensis acorns: “The cotyledonary tissues are disrupted by what appears to be cavities or channels containing foreign material. ... Cotyledonary tissue is missing, and there appears to be frass (insect excrement) in the cavity and the surrounding tissue. In a second example, an unusual circular object is found within the seed that is not a normal developmental feature of oak cotyledons. This circular structure may represent a larval body or the cavity it formed in a cross‐sectional view. Several other seeds in the collection (not illustrated) appear to have been consumed entirely, for the seed cavity is completely filled with insect remains and/or frass. This suggests that plant–animal interactions among oaks and their predators in the Miocene were similar to those found today.” There is a subgenus within Ectoedemia, Etainia, known for mining the fruit of Aceraceae. It would a leap to suggest that this sistergenus was responsible for these fossil herbivorous traces, as herbivory of seeds is known from several insect orders, but it shows that intimate herbivore‐host habits per se already existed. The lack of Ectoedemia s.s. on Fagaceae in NA, even though that is the most likely location of origin of Fagaceae and also the most diverse area of Fagaceae, suggests that the origin of the Fagaceae mining Ectoedemia groups lies in Asia. The likely scenario is that the ancestor of Ectoedemia s.s. was present in Asia when the Fagaceae arrived there from NA through the BLB, early Miocene, and there was a host shift, either by Ectoedemia or their ancestor, towards this host family somewhere during the Miocene. As the climate cooled down however, the BLB broke up as a biotic bridge of Fagaceae and the road back to NA disappeared before Ectoedemia s.s. could distribute there. The separation of a NA and Eurasian clade of Quercus section Quercus is clearly visible in genetic result and indicates an ancient split that would coincide with the cooling of the climate and the loss of the BLB as a deciduous connection between NA and EUA during the miocene. The Fagaceae that had reached Asia, most likely species from Q. sect. Protobalanus, underwent a split into two Asian clades, one which would later become the Eurasian part of Q. sect. Quercus and one which would later become Q. section Cerris. Possibly this split coincides with the north Asia and south Asia typical plant disjunctions, but there is no hard evidence for that. The black and red oaks, very successful species in NA, appear to be derived from white oaks. Especially the 13 close relationship with Q. robur, a strictly EUA species that is found at high latitudes, leaves two options. Either the white oaks distributed throughout the EUA in a period of 23‐15 mya and crossed the atlantic through the NALB, during its gradual break up, or the red and black oaks are a result of a long distance dispersal event from European white oaks that reached NA. In case of the latter, the reason for absence of Ectoedemia, or Nepticulidae in general, on black and red oaks would be obvious. The current distribution of Ectoedemia s.s. goes to equal latitudes of the hosts and suggests that if the NALB was used to cross the Atlantic by Q. sect. Quercus, the miners had no reason not to follow. This scenario is corroborated by the second Ectoedemia s.s. Fagaceae mining group; the Suberis group. This group is specialised on oaks belonging to Q. sect. Cerris and Q. sect. Quercus oaks, and is only found in EUA, as is Q. sect. Cerris. The basal position of several eastern Russian Ectoedemia s.s. species to the Suberis group also indicate and Asian origin and westward distribution and radiation, possibly vicariance. A similar distribution and radiation seems likely for Q. sect. Cerris, leaving secondary evolution in this group possible. 14 BETULACEAE (FAGALES) Betulaceae are only mined by a small number of Ectoedemia s.s. species, but those species are found widespread, as are the hosts. Betulaceae mining is common in multiple Lepidoptera families, including Gracillariidae (Lopez‐Vaamonde et al., 2003) and Nepticulidae (van Nieukerken, pers. comm.) The Betulaceae classification following Chen et al. 1999): Betulaceae Betuloideae Betula Alnus Coryloideae Corylus Ostryopsis Carpinus Ostrya That Betulaceae have close relationships to some Gondwanaland groups, such as Nothofagus and Casuarinaceae, is strongly supported by molecular phylogenetic study (Chen et al., 1999). Nevertheless, the family appears to have originated in EUA during the Cretaceous, judging from distribution patterns of fossil and extant representatives (Chen et al., 1999). This is corroborated by a study that compared several fossil dating methods on phylogenetic results in Betulaceae (Forest et al., 2005) which showed that the diversification of the family started during the early or mid Cretaceous. Late Cretaceous and Early Tertiary fossil occurrences of Betulaceae fossils are almost exclusively from temperate latitudes of the Northern Hemisphere. Occording to fossil data, all six extant genera of Betulaceae had differentiated by the Oligocene. The greatest diversity in Betulaceae is in the moist temperate forests of East Asia, particularly in China, where all six genera are currently well represented. During the Cretaceous and Early Tertiary, migration between Eurasia and North America was possible via the NALB and BLB. The effect of these intercontinental migrations can still be observed among several genera of the family today, although the land connections have been severed (Chen et al., 1999). There was an overall increase of insect herbivory during the Paleocene to mid Eocene on dicot plants according to the fossil record in North America, but this increase was significantly higher for Betulaceae (Wilf and Labandeira, 1999). The increase was both in frequency and diversity, indicating that many insect herbivores migrated north, that there was a radiation of Betulaceae feeders, or many host shifts to Betulaceae, or a combination of those three. It appears that Betulaceae had diversified and spread throughout the northern hemisphere relatively early in time; possibly during the Cretaceous but definitely by the Oligocene. Their resistance to extreme cold (Sakai, 1971) can be a reason why they managed to distribute as far as they did. The wide distribution suggests that there was plenty of opportunity for leaf‐miners to make a host shift. 15 SALICACEAE (MALPIGHIALES) The Ectoedemia Populella group mines Salix spp. and Populus spp. (the tribe Saliceae in the family Salicaceae). The species in this group contain many genetic and morphological synapomorphies and apomorphies. Aside from a good representation of species from the Populella group in EU there are also several species known only from NA, species from AS exist but are more rare (van Nieukerken pers. comm.). The EU and NA species appear mixed in the phylogenetic tree and thus have no suggestion of a directional distribution and radiation. Malpighiales are strongly supported monophyletic, but relationships within them are still poorly understood and undergoing much change as phylogenetic knowledge increases (Chase et al., 2002). Like in Fagaceaee, species in Salicaceae are notorious for interspecific hybridization (Eckenwalder, 1996a). The original classification by Linnaeus in the 1750’s only recognised two genera in this family: Populus and Salix, and even in the year 2000 only 2‐4 genera were recognised (Azuma et al., 2000). The current APG II listing however includes 55 genera, mainly due to the inclusion of a large part of Flacourtiaceae , including the type genus of that family (APGII, 2003)(figure 6). Ectoedemia s.s. are only known to mine the original two genera though; Salix and Populus. Figure 6: Phylogeny of Salicaceae from Boucher 2003, also including the extinct genus Pseudosalix, which is described in that paper. Ectoedemia s.s. are only found on Saliceae.
16 Saliceae favour river banks and can withstand lower temperatures than Fagaceae. The frost resistance of buds and twigs of a number of plant species indigenous to Japan were tested for frost tolerance (Sakai, 1971), including Salix and Populus. The study showed that Salix, Populus and Betula were by far the most frost resistant and could even survive a liquid nitrogen treatment (<‐100 °C), Fagaceae could ‘only’ resist ‐30 °C. This indicates the first mentioned three genera were less affected by the cooling of the climate as the Miocene progressed, and were theoretically able to use the NALB and BLB for distribution longer than Fagaceae. There are no phylogenetic studies that include molecular dating for the origin and early distribution of Salicaceae as a whole. This is undoubtedly because of the recent increase of knowledge on the phylogeny and subsequent shifts in Salicaceae (Chase et al. 2002) but also major shifts within the genera Salix and Populus based on molecular data. For now the discussion of origin and distribution relies on fossil record alone. One particularly interesting fossil from the Eocene in NA (Utah) was studied by Boucher (2003), who describes a clear fossil with foliage and fruit that has characteristics of both Populus and Salix. He describes it as a new genus, Pseudoilex, and places it as sister to Saliceae (figure 6). In the same study they looked at the current distribution of Saliceae and outgroups and conclude the following: “This distribution pattern (all outroups of Saliceae only extant in Asia), together with the cladistically nested position of the tribe Saliceae relative to these genera in the tribe Flacourtieae would lead to the suggestion that Saliceae originated in eastern Asia prior to dispersing across North America and Europe. However, the early fossil occurrence of both Populus and Pseudosalix in the Eocene of North America introduces the possibility of a North American diversification of the Saliceae. If this were the case, we would expect to find other fossil representatives of the Flacourtieae in North America. If the group actually evolved in Asia and subsequently dispersed to North America, then we may expect to find fossils of Pseudosalix and/or other extinct Flacourtieae, such as Utkholokia Iljinskaya & Chelebaeva, in the early Tertiary of Asia.” Thus, currently both AS and NA are seen as options for the point of origin of Saliceae but the earliest known fossils are known only from North America. Those fossils are found from late Paleocene, but more reliable fossils of both fruits and foliage are dated from early middle Eocene. It is speculated however that the absence of Asian fossils could be due to a sampling bias and that there may be more fossils of Salicaceae to be found in Asia (Boucher et al., 2003). Salix Salix is a genus of about 400‐500 species, currently distributed mainly in the northern parts of NA and Europe and in the montane regions of China. It is absent from or uncommon in tropical regions, and only three species are native to Central and South America (Argus, 1980). Paleobotanical evidence from eastern North America indicates that the composition of communities changed over long periods of time as species migrated following glaciation. However, what exactly happened to Salix in the Tertiary has not been thoroughly studied. Salix appears later in the fossil record than Populus (in the early Eocene) and companioning fossils show that the early species also occupied riparian habitats. However, some modern Salix species may be of recent origin; on the grounds of their distribution many of the American Salix species may even have been derived during or after the last glaciation, which ended approximately 10 000 years ago (Brunsfeld et al., 2007). In contrast Skvortsoy (Skvortsov, 1999) finds it likely that most speciation in EUA Salix had already occurred in the Tertiary (Karrenberg et al., 2002). 17 Populus Most of the Ectoedemia s.s. species found on Saliceae are found on Populus, even though there are relatively few species of poplars compared to willows (Hamzeh and Dayanandan, 2004). Populus is divided into a number of sections, similar to the classification structure in Fagaceae. With a few exceptions, there is reasonable agreement in literature on the characteristics and species composition of the sections, and barriers of hybridization are known to exist between the sections from crossing experiments (Eckenwalder, 1996a; Eckenwalder, 1996b; Zsuffa, 1975). However, there is still no consensus on how many Populus species there are and even one of the sections does not appear to be monophyletic (Hamzeh and Dayanandan, 2004). Moreover, most studies have a NA‐EU bias and neglect the Populus diversity in Asia. Because of their fast growth rate and high productivity Populus spp. are especially well suited for plantations (Gielen and Ceulemans, 2001). Cultivated poplar species from NA easily hybridize with native EU species, making phylogenetic analysis even more difficult (Vanden Broeck et al., 2006). A study on the possible consequences of an increase of CO2 and increased global temperatures by Gielen and Ceulemans (2001) showed that Poplars would do exceedingly well in a warmer and CO2 richer climate. So besides the resistance to extreme cold (Sakai, 1971), Populus also manages to survive and even do better in extreme heat, indicating the enormous plasticity of this genus. Aside from a large plasticity, Populus spp. are also known for easily reproducing vegetatively, their small pollen can travel far by wind and their seeds can travel far by wind or water (Breen et al., 2009). Classification of Populus into six sections following Eckenwalder (Eckenwalder, 1996a): Populus section Tacamahaca (balsampoplars) section Aigeros (cottonwoods) section Leucoides Section Populus (aspens and white poplars) section Abaso section Turanga Species from Populus sections Tacamahaca and Aigeros are found in riparian areas, species from P. sect. Leucoides mostly in swamps. Species from P. sect. Populus are found in drier habitats, and the remaining two sections are restricted to warmer areas and are geographically separated. P. sect. Abaso with only member P. mexicana is only found in southern NA whilst P. sect. Turanga, with only members P. euphratica and P. ilicifolia are found in Africa. The latter two sections are morphologically most similar to Flacourtiaceae and therefore thought to be the most basal of the genus (Karrenberg et al., 2002). The earliest recognisable Salicaceae fossils are leaves of P. sect. Abaso from western NA, dating back to the Palaeocene, approximately 58 million years ago. These fossils are similar to the extant P. Mexicana that is common on flood plains in Mexico (Eckenwalder, 1996b). Hamzeh and Dyanadan (2004) speculate that most of the hybridisation and introgression events predate the beginning of the Miocene, before the breaking up of the NALB. They say this because in one of the more derived sections, P. sect. Aigeiros, they found a parental lineage native to NA as well as a parental lineage native to EUA. They deem cross‐oceanic hybridization unlikely due to the short lived pollen and seeds, but they cannot rule it out. Unfortunately they do not speculate about the possible use of the BLB but restrict themselves to the NALB. Their phylogenetic tree also shows a clear EUA clade of P. sect. Populus and a NA clade, but they do not draw any conclusions from that separation. In other papers, such as (Donoghue and Smith, 2004) such results are interpreted to coincide with vicariance; which would mean that the split between 18 the NA and EUA clade of P. sect. Populus is indicative of the closing of the NALB. That would mean that most of the hybridisation and introgression happened after the NALB opened up; during the Miocene or even later. The most primitive Populus sections are found in NA and Africa, and are adapted to tropic climate. The oldest fossils are found in NA, so the African section is probably the result of a long distance dispersal event, as is the likely cause of many southern hemisphere disjunct distributions (Donoghue and Smith, 2004). The phylogenetic reconstruction of Hamzeh and Dyanadan does not include these sections, but places P. sect. Populus most basal, with a distinct NA clade and a EUA clade. P. sect. populus is adapted to relatively drier and colder climate, which might explain why it is the only section that managed to disperse throughout the northern hemisphere. The many hiates in the early distribution as well as the frequent cultivation of Populus and introductions from NA to EU and vice versa make it difficult to be conclusive about distribution or vicariance of Saliceae. The restriction of certain Ectoedemia s.s. species from the Populella group to NA and the diversity suggest that most of their speciation happened in NA and the presence of these species in EU could be attributed to the frequent cultivation of Poplars; that they are actually anthropogenically introduced from NA to EU. Other scenarios include an earlier (early Miocene) introduction from NA into EU of P. sect. Populus with Ectoedemia, possibly using the NALB. To be conclusive more Ectoedemia species and specimens will have to be added to the phylogenetic reconstruction of the subgenus, right now many NA species are lacking. 19 ROSACEAE (ROSALES) There is a large group of Ectoedemia s.s. that mine Rosaceae, but their phylogenetic relationships are not clear throughout the group as of yet. This is reflected in low probabilities on several clades in the phylogram (figure 2) but was also noted by the lack of synapomorphies in morphologic study (van Nieukerken, 1986). Numerous species that mine Rosaceae are found in Asia, and many more species are expected to be found there, but they are also speciose in Europe and a number of species is described from NA. There are currently 90 genera recognised within Rosaceae, their distribution is worldwide but most abundant in the northern hemisphere. Rosaceae are a difficult family from a phylogenetic point of view, numerous different classifications have been proposed by different studies and even at present there are issues to be resolved (Potter et al., 2007). The most recent classification by Potter et al. (2007) combined the results of other studies with their own and recognises only three subfamilies instead of the more classical view of four subfamilies defined by the structure of the fruits. The classification of Rosaceae with the genera that are mined by Ectoedemia following Potter et al. (2007)( tabulated order: Family‐subfamily‐supertribe‐tribe‐subtribe‐
genus): Rosaceae Rosoideae Filipendula Rosodae Rosa Rubus Sanguisorbeae Agrimoniinae Argrimonia Aremonia Sanguisorbinae Sanguisorba Potentilleae Potentilla Fragariinae Fragaria Spiraeoideae Kerriodae Amygdaleae Prunus Spiraeeae Spiraea Pyrodae Pyreae Pyrinae Malus Sorbus Crataegus 20 Based on molecular dating of phylogenetic trees the crown group Rosales, including Rosaceae, originated ca 76 mya (late Cretaceous) (Wikstrom et al., 2001). Wang et al. (Wang et al., 2009) suggests rather older dates, and claim crown group Rosales divergence began 96‐85 mya (upper cretaceous). Most of the genera are subdivided into numerous subgenera and sections, their phylogenetic relationships are troublesome. Reasons for this complexity include rapid evolutionary radiation of lineages and reticulations among the ancestors of those lineages. According to Potter et al. (2007) the phylogenetic trees suggest a NA origin for the entire family and the subfamilies. Next to that they also say that more detailed study of the tribes will be needed to really sort out the complex geographic patterns. Some of the genera that have been studied at deeper phylogeny level include Crataegus, Rubus and Rosa. One of the recent studies to clarify the relationships of species within the genus Rosa state: “Our understanding of evolution and phylogenetics relationships within the genus Rosa is on the one hand contradictory, and on the other in its infancy” (Wissemann and Ritz, 2005). They do not go as far as to infer geographic distribution patterns, partly because many Asian species were lacking in their study. Something they do note is about Rosa sect. Caninae (dogroses); they quickly spread over the European landscape after the last glaciations (16kya) and due to their allopolyploid constitution and special type of meiosis they established different ecological types in different niches which explains the wide diversity seen today. Although many of the Rosa studies have a European bias the species diversity is highest in Asia (Stevens, 2001 onwards). The genus Rubus lists approximately 750 species and is found on all continents except Antarctica. An original thought was that Rubus originated in southwestern China, because of the high number of species, subgenera and morphological variation in that area. A phylogenetic analysis showed however that the most basal species are not Chinese (Alice and Campbell, 1999). Instead, one of the species has a western NA to Far Eastern Asia distribution, another species is circumpolar and the remaining species are restricted to Southern NA. This makes an origin of Rubus in Eastern Asia or western NA more likely. Much of the diversification could well have happened in Asia though. The existing classification of Crataegus divides species into 15 sections based on geographical distribution and morphology (Lo et al., 2009). More than 100 species representing 11 sections are found in NA, whereas 60 or more species representing four sections are known from EUA. Crataegus has a wide geographical distribution in the northern hemisphere and is a woody genus with its earliest fossils dating from the mid‐Tertiary (DeVore and Pigg, 2007) with 140‐200 species. However, the phylogenetic relationships between Eurasia and NA Crataegus are still unknown. Both DIVA and Mesquite analyses indicate instead that Eastern North America and Europe are probably the most recent common areas for all species. At least four dispersal events are inferred to explain its present distribution. Birds and small mammals are common dispersal vectors of Crataegus seeds (Lo et al., 2009) which might explain the current wide, and complicated, distribution. So, although Rosaceae and subfamilies appear to have originated in NA, the diversification of the tribes may have been in Asia. Reconstructions of the distribution patterns remain highly speculative due to the frequent hybridization, polyploidy and human cultivation that includes the crossing of many species from all over the world. Nonetheless, the current richness of species in Asia indicates this was probably at least one of the places where radiation occurred. 21 The lack of knowledge on Rosaceae in Asia is mirrored in the Rosaceae mining Ectoedemia spp. in Asia. Many more species are expected to be found there (van Nieukerken pers. comm.). That, combined with the known hiates in Rosaceae phylogeny and distribution patterns make it difficult to speculate about possible secondary distribution patterns, but also make this host family especially interesting for future research. As there is much interest in Rosaceae and as understanding of evolutionary mechanics increases the phylogenetic data on Rosaceae should rapidly increase in the coming years (Wissemann and Ritz, 2007). Although Ectoedemia are only found on a small subsection of the total genera in Rosaceae, the amount is still disproportiately large to the amount of the genera mined in other plant families, where there is a much stronger restriction to a few genera or even a few sections. The shallow diversification of Rosaceae is estimated to be in the upper Cretaceous, the relatively generalist position of Ectoedemia on Rosa spp. and Rubus spp. may be explained by relatively recent, possibly postglacial, diversification of these genera. 22 PLATANACEAE (PROTEALES) In North America there are two Ectoedemia s.s. species that mine Platanus occidentalis (E. clemensella and E. platanella). Also in North America there are fossils dated 94 mya from an unidentified platanoid with markings that resemble the current mines of E. clemensella. Unfortunately the mines do not contain diagnostic characters and the extant Ectoedemia species has not yet been included in the phylogenetic studies. Platanaceae are estimated to have originated 110‐119 mya; Albian (Anderson et al., 2005), making it the oldest modern host for Ectoedemia, but that does not necessarily say anything about the timing of host shift. A study on the fossil pollen record of Platanus revealed that the genus, which currently only lists seven species, was once much more diverse (Denk and Tekleva, 2006). Moreover, it revealed that P. kerrii, which is restricted to Vietnam and Laos, is rather distinct from the rest of the species and appears to be more derived rather than more primitive. In a phylogenetic study of six Platanus species two major clades were identified: one with species from Europe and Western NA (P. orientalis and P. racemosa), the other with species from eastern NA and Eastern Mexico (P. mexicana, P. occidentalis, and P. rzedowskii) (Feng et al., 2005)(figure 7). These two clades coincide with the typical plant disjunct areas as mentioned by Milne (2006). Figure 7: The phylogenetic tree of six Platanus species from Feng et al. (2005) including the results of two molecular clock analysis.
Although the oldest Platanaceae may be from the Albian, the molecular dating of abovementioned six species shows a diversification during the Miocene. The fossil record of Platanaceae generally is noted to be one of the richest of all angiosperms and is relatively continuous from mid cretaceous to early tertiary (Feng et al., 2005). The fossil record also shows that most diversification occurred in the early Tertiary, and that the current existing species are only a small portion of the original Platanaceae family. The disjunction in the molecular results of the six species (figure 7) between Europe and western NA is consistent with an ancient vicariance event when the epicontinental seaway in NA was still present during the upper cretaceous which made distribution between western NA and Europe possible, but blocked distribution between eastern NA and western NA. The other clade contains species from eastern Mexico and eastern NA. This disjunction was not 23 seen in the phylogenetics of the other families treated here, which may indicate that those families distributed after the epicontinental seaway had receeded during the Paleogene. Fossils from the early Tertiary of Kamchatka and Alaska are similar to the leaves in the P. occidentalis clade, suggesting that likely ancestors of this group dispersed at high latititudes across the BLB. However, long distance dispersal is a likely explanataion as well considering the small single‐seeded fruits of Platanus. In any case it seems that Platanus originated in NA and reached Asia possibly before the beginning of the Tertiary. 24 DISCUSSION As the early evolution and distribution of the hosts for Ectoedemia s.s. is at least in part speculative, it is dangerous to speculate about the early evolution and distribution of Ectoedemia s.s. in relation to their hosts. Nonetheless this paper showed there are some patterns that can already be noticed even with todays incomplete pictures of host and herbivore. Fagaceae is a fairly well examined family both phylogenetically and in the fossil record and shows clear distribution patterns that can be explained by vicariance. Including more NA and Asian Ectoedemia s.s. into phylogenetic study should lead to a reconstruction of what probably happened and could provide information on where more species are to be expected. This will probably condescend the Tertiary and the Quaternary and even later glaciations will have to be taken into account. For the Ectoedemia Suberis group this could probably already be done, as this group appears to be well known in at least the Mediterranean area and much is known about the refugial areas and different species there. The other families remain more difficult. Betulaceae and Salicaceae appear to have reached a widespread distribution relatively early in time. When and where different species may have originated is difficult to say, also because of the frequent hybridization, back crossing and cultivation. For these families it also seems likely that long distance dispersal has played a large role in speciation, something that is hard to track back. If the phylogeny of especially Salicaceae will reach more maturity in the coming years more information on early evolution and distribution can be expected as well. Rosaceae are at least as difficult as Salicaceae in terms of entangling the early evolution and distribution because even todays phylogeny is filled with hiates. When genera are viewed in detail some patterns emerge, such as with Crataegus. Hopefully studies will lose the European bias however and focus more on the Asian Rosaceae to reveal the more basal clades and possibly early distribution. The same goes for Ectoedemia s.s. of which the current Asian diversity is poorly known. Platanaceae are potentially very interesting for Ectoedemia. If the fossils from the Albian are indeed from Ectoedemia, and the present day Ectoedemia that feed on Platanaceae are most basal of the genus then they can probably be regarded as living fossils. Until these species are actually studied phylogenetically this is only speculation. The family, and genus Platanus, is probably mostly extinct and todays species are only few of what they once were. Their current day distribution is therefore also only a small portion of the distribution they once had, but the fossil record contains some clues. Although much is speculative, and will probably always remain at least partly speculative, close study of Ectoedemia s.s. and host species can shed light on what actually happened in the early days of Lepidoptera evolution and help to explain the distribution patterns and diversity we see today. 25 REFERENCES Alice, L. A., and C. S. Campbell. 1999. 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