Origin and diversification

Fossil remains of oaks are common and have been discovered on the three continents. Earliest remains found in North America (Bones, 1979; Manchester, 1994), China (Jiang, 1993), and Europe (Kvaček & Walther,1989) are from the Eocene. The almost simultaneous appearance of the genus on the three continents, as witnessed by today’s detected fossil remains, has raised the question of the geographic origin and radiation of the genus. Two scenarios were proposed to reconstruct the history of the species. In the first scenario (Zhou, 1992), the genus appeared in South East Asia deriving from a sister genus Trigonobalanus during the Palaeocene, and migrated into two directions: to Europe and America via the North Altlantic Land Brigde before the Eocene, and via the Bering strait after the Miocene.

Scenario of Zhou (1992)

In the second scenario (Manos and Stanford, 2001 and Trelease, 1924), the genus Quercus derived from the widely distributed boreal-tropical deciduous forest that extended throughout the northern hemisphere at the beginning of the Tertiary. The genus further differentiated as the separation between the continents became more pronounced. As a result oak species occurred on the different continents as a vicariance between Asia and North America of an ancestral group composing the boreal-tropical forest.
- In Asia the “ancestral group” differentiated into the sub genus Cyclobalanopsis and the section Cerris of the genus Quercus. And species of the Cerris group migrated later westwards to Europe.
- In America, the “ancestral group” differentiated into section Lepidobalanus (white oaks), section Protobalanus and section Erythrobalanus (red oaks) with subsequent migration of white oaks from North America to Asia and further Europe

Scenario of Manos et al. (2001)

Despite the disagreement on the origin of the genus, paleobotanists agree on the extremely rapid diversification of the genus during the Oligocene and Miocene as a response to important climatic changes. Most fossil remains of that period are similar to extant samples. Hence it is believed that most of the extant species existed already at the mid Miocene (Trelease, 1924; Axelrod,1983).

Postglacial migration
During the quaternary era, oaks in the northern hemisphere were subjected to important migrations in response to climatic changes. There were about 17 Milankovitch climate oscillations (alternation of glacial-interglacial periods) during which oak species were subjected to successive restrictions and expansions of their distributions. A glacial period lasted from 50 to 100 thousand years whereas interglacial periods were much shorter and lasted between 10 to 20 thousand years. Climatic oscillations were strong selective forces favouring species that were vagile enough to track their moving habitats (Dynesius and Jansson, 2000). They were most likely responsible for the reduced number of species that occupy large continental distribution (Q. robur in Europe, Q. alba in America, or Q. acutissima in Asia). These movements have profoundly influenced the genetic diversity of the species, but in rather different ways between North America and Europe (Grivet et al., 2006; Kremer et al., 2010)

In Europe
A large survey conducted in Europe confronting the remaining historical footprints (pollen deposits) to genetic fingerprints (chloroplast DNA (cpDNA) polymorphisms) demonstrated how the extant distribution of genetic diversity was shaped by the dynamics of postglacial colonisation (Kremer, 2002). At the end of the last glaciations, European oaks were restricted to three major refugia (Southern Iberian Peninsula, Central Italy, and Southern Balkan Peninsula). As glacial periods lasted more than 100 000 years, species were most likely genetically differentiated among these refugial zones as shown by the completely different haplotype lineages (=cpDNA variant) occupying these regions. In less than 7000 years (from 13 000 to
6 000 BP), oaks recolonized the majority of their modern ranges starting from the refugial areas (Petit et al., 2002a and b; Brewer et al., 2002). Between 13,000 and 10,000 BP oaks increased in abundance in mountainous areas (Pyrénées, South-eastern Alps and Carpathian). The cooling of temperatures during 11,000 BP to 10,000 BP stopped this expansion and resulted in reductions of existing populations. After 10,000 BP, oaks spread throughout Europe and reached their extant distribution at about 6,000 BP. The expansion was more rapid in the west and was reduced in the centre and east due to the Alps and the Carpathian mountains.
On average the migration was extremely rapid (between 300 to 500 meters per year) (Brewer et al., 2002). Rare long dispersion events at long distances contributed significantly to the rapid expansion of the species (Le Corre et al, 1997; Davies et al, 2004). These dynamics had contrasting consequences on the diversity of the species. Despite the strong founder effects that accompanied the recolonization, oaks were able to maintain their genetic diversity. Although the highest neutral diversity is restricted to the southern areas of Europe, the level of diversity is still important in the central part of Europe, where the different migration fronts originating from the refugial zones merged (Petit et al., 2002a). However the today’s distribution of adaptive diversity is not correlated to neutral diversity; there is no footprint left by the maternal origin on the variation of adaptive traits (Kremer et al., 2002). Geographic variation for adaptive traits resulted from more recent local selection pressures. Interspecific hybridization was a key migration mechanism as it facilitated the dispersion of late successionnal species (Q. petraea) into pioneer species (Q. robur). The systematic sharing of the same cpDNA haplotype by different white oak species occupying the same stands indicates that hybridization was extensive during postglacial recolonization (Petit et al., 1997).

In North America
Post glacial colonisation dynamics in North America was quite different from Europe. On the Eastern side species were not restricted to genetically separated refugial zones. Furthermore, oak stands persisted as low density populations close to the Laurentide Ice Sheet, reducing opportunities for long distance dispersion and founder events. Hence postglacial recolonisation was more diffuse than in Europe and restricted (Schlarbaum et al., 1982). As a result, oaks of eastern North America show less cpDNA differentiation among populations (Magni et al., 2005)
    On the western side, oaks were also more stable in response to climatic oscillations. Californian oaks did not become totally extinct during the last glacial period. Populations declined in size, and expanded during the warming periods but by migrating locally, resulting in a patchy distribution of cpDNA diversity, and maintaining larger levels of diversity in comparison to European oaks (Grivet et al., 2006; Dodd and Kashani, 2003). A somewhat similar picture was described in the case of Mediterranean oaks in Spain, suggesting the maintenance of many refugial populations that still persisted today and retain large level of diversity (De Heredia et al, 2007).


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