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Tragopogon comprises approximately 150 described species distributed throughout Eurasia from Ireland and the UK to India and China with a few species in North Africa. Most of the species diversity is found in Eastern Europe to Western Asia. Previous phylogenetic analyses identified several major clades, generally corresponding to recognized taxonomic sections, although relationships both among these clades and among species within clades remain largely unresolved. These patterns are consistent with rapid diversification following the origin of Tragopogon, and this study addresses the timing and rate of diversification in Tragopogon. Using BEAST to simultaneously estimate a phylogeny and divergence times, we estimate the age of a major split and subsequent rapid divergence within Tragopogon to be ~2.6 Ma (and 1.7–5.4 Ma using various clock estimates). Based on the age estimates obtained with BEAST (HPD 1.7–5.4 Ma) for the origin of crown group Tragopogon and 200 estimated species (to accommodate a large number of cryptic species), the diversification rate of Tragopogon is approximately 0.84–2.71 species/Myr for the crown group, assuming low levels of extinction. This estimate is comparable in rate to a rapid Eurasian radiation in Dianthus (0.66–3.89 species/Myr), which occurs in the same or similar habitats. Using available data, we show that subclades of various plant taxa that occur in the same semi-arid habitats of Eurasia also represent rapid radiations occurring during roughly the same window of time (1.7–5.4 Ma), suggesting similar causal events. However, not all species-rich plant genera from the same habitats diverged at the same time, or at the same tempo. Radiations of several other clades in this same habitat (e.g. Campanula, Knautia, Scabiosa) occurred at earlier dates (45–4.28 Ma). Existing phylogenetic data and diversification estimates therefore indicate that, although some elements of these semi-arid communities radiated during the Plio-Pleistocene period, other clades sharing the same habitat appear to have diversified earlier.
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The most rapid plant radiations have been shown to have occurred in well-known diversification hot spots, including the Andes, Canary Islands, Hawaiian Islands, South Africa and certain regions with Mediterranean climates (Paun et al., 2005; Linder, 2008; Sauquet et al., 2009). Valente et al. (2010) recently documented an exceptionally rapid rate of diversification in Dianthus (carnation; Caryophyllaceae) in temperate Eurasia; Dianthus comprises over 300 species, with over 100 species involved in the radiation examined. With this exception, rapid, recent radiations have not been well documented in the Mediterranean or other north-temperate Eurasian floras. In addition, the rapid diversification of Dianthus appears to coincide with an increase in aridity and seasonality in the region, mostly during the Plio-Pleistocene [1.2–7.0 million years ago (Ma)], marking the onset of the typical Mediterranean climate (Suc, 1984).
Species of Dianthus commonly occur in semi-arid, steppe-like communities in frequent association with species of Tragopogon (Asteraceae) (Carni, 1997; Fekete et al., 2002; Safronova, 2008). Based on several published treatments, Tragopogon comprises up to 150 species (reviewed in Mavrodiev et al., 2004, 2005); however, this number may well be an underestimate due to the proposed presence and recent detection of many cryptic species (see also Mavrodiev et al., 2007, 2008a,b). Tragopogon occurs throughout Eurasia from Ireland and the UK to India and China with a few species in North Africa. Most species occur in Iran, Iraq, Afghanistan and neighbouring areas of the Caucasus, Turkey, Eastern Europe and Central Asia. Although many species of Tragopogon occur in and near the Mediterranean, the distribution of Tragopogon corresponds more accurately to the Paratethys region, an ancient basin that covered 3 million km2 and that is represented today by the Mediterranean, Black, Caspian and Aral Seas (reviewed in Sprovieri et al., 2003), and the adjacent mountainous areas (Tzvelev, 1985). Thus, although the large number of Mediterranean species of Tragopogon may initially suggest a diversification in response to the onset of Mediterranean climate with wet, mildly cool winters and long, dry summers, the diversification may have actually occurred in semi-arid steppe vegetation further east and north-east, where winters are colder and precipitation is more evenly distributed throughout the year. These different climates naturally harbour quite different vegetation with sclerophyllous shrublands and low-growing forests occurring in the Mediterranean and grasslands with interspersed forest islands farther east.
Despite extensive sampling of genes and species, the phylogeny of Tragopogon is not yet fully resolved (Mavrodiev et al., 2005, 2008a,b). Poorly resolved phylogenies in many groups of organisms, including diverse insect lineages, birds, turtles, mammals and angiosperms, have been interpreted as the result of rapid radiations (reviewed in Whitfield & Lockhart, 2007). We therefore hypothesize that the species-rich Tragopogon may similarly represent a rapid radiation that perhaps occurred in response to the same drying trends that are proposed to have prompted rapid diversification in Dianthus. Indeed, we postulate that other floristic elements of these same communities may have similarly diversified during this same time period, potentially brought on by similar climatic, ecological and/or geological factors. To test this hypothesis, we estimated divergence times to compute absolute rates of diversification for Tragopogon. In addition, we investigated the variability in diversification rate through time using a variety of methods and simulations. Results for Tragopogon are congruent with those for Dianthus. Thus, we propose that rapid diversification may be characteristic of many lineages from semi-arid grassland communities in Eurasia. We therefore searched the literature for further possible examples of rapid diversification in this habitat. We tried to control for the place of diversification to distinguish between hypotheses that the Mediterranean climate is responsible for the diversification versus diversification in response to environmental changes farther east.
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The estimated rate of diversification for Tragopogon is 0.84–2.71 species/Myr (assuming 200 extant species and little to no extinction during the age of the clade), which overlaps with the rate estimated for Dianthus (0.66–3.89 species/Myr; Valente et al., 2010). Therefore, Tragopogon appears to provide a second clear example of a rapid Eurasian radiation during the Plio-Pleistocene.
Significantly, the rate of Tragopogon radiation is also close to many other examples of rapid plant radiations from around the world (reviewed in Valente et al., 2010). For example, Tragopogon radiated at rates comparable with Mediterranean Cistus (Guzmán & Vargas, 2009; speciation rate of 1.46–2.44 species/Myr), alpine Soldanella (Kadereit et al., 2004: 1;.64–2.55 species/Myr), South American Lupinus (Hughes & Eastwood, 2006: 1;.30–3.78 species/Myr), South American Valeriana (Bell & Donoghue, 2005: 1;.71–3.2 species/Myr) and Neotropical Gentianella (von Hagen & Kadereit, 2001: 1.64–2.55 species/Myr).
In Eurasia, different species of Tragopogon occur in various types of open habitats, often with Dianthus species (Vicherek, 1972; Karpov et al., 1987; Golub & Saveljeva, 1991; Golub, 1994; Carni, 1997; Tyschenko, 1998; Umanets & Solomakha, 1998; Fekete et al., 2002; Golub et al., 2002, 2009; Chytrý & Rafajová, 2003; Dubina et al., 2003, 2004; Voityuk, 2005; Safronova, 2008), as well as with species of other clades thought to represent rapid radiations. Such communities commonly include species of Artemisia, Astragalus, Campanula, Centaurea, Dianthus, Knautia, Scabiosa, Scorzonera, Silene and Veronica, in addition to Tragopogon (Carni, 1997; Fekete et al., 2002; Noroozi et al., 2008; Safronova, 2008). Thus, these genera may represent other cases of rapid diversification. Our analyses of diversification rates for some of these genera (Table 2) demonstrate that Dianthus and Tragopogon may be extreme cases of diversification in this region.
Table 2. Comparison of diversification rates among Mediterranean plant clades. Rates were calculated using methods described by Magallón & Sanderson (2001). When ranges in the number of species were given, we used the maximum value to calculate rate values. In addition, we assumed the proportion of extinction parameter (ε) to be equal to zero in all cases. Ages of clades were taken from reference supplied in last column
|Taxon||Age of crown group (Myr)||Diversification rate (crown group, sp/Myr)||Number of species||Distribution||References|
| Anthemis ||8.83||0.50||170||E Mediterranean||Lo Presti & Oberprieler (2009)|
| Antirrhinum ||4.1||0.62||25||W Mediterranean||Vargas et al. (2009)|
|Arum sect. Dioscorides||3.9||0.61||22||Mediterranean||Linz et al. (2010)|
| Campanula ||45–80||0.07–0.12||500||Mediterranean||Cellinese et al. (2009)|
|Centaurea (behen + involucrata Group)||7.68||0.55||150||Mediterranean||Barres et al., unpub. data|
|Centaurea (depressa + lingulata Group)||6.03||0.47||30||Eurasia||Barres et al., unpub. data|
|Centaurea sect. Acrocentron||2.13||1.95||100||Mediterranean||Barres et al., unpub. data|
| Cistus ||4.25||0.55||21||W Mediterranean||Fernández-Mazuecos & Vargas (2010)|
|Cistus-Halimium||5.2||0.54||33||Europe||Guzmán & Vargas (2009)|
|Cousinia – cousinioid clade||3.4–16.9||0.34–1.68||200–600||SW Asia||López-Vinyallonga et al. (2009)|
| Dianthus ||1.2–7.0||0.66–3.84||200||Mediterranean||Valente et al. (2010)|
|‘eu-Scorzonera’||3.8||0.89||50–60||Mediterranean and Irano-Turanian||This study|
|European Aquilegia||2.54||0.93||21||Asia||Bastida et al. (2010)|
| Tragopogon ||2.6||0.84–2.71||150–200||Eurasia||This study|
The diversification dates for Tragopogon, Dianthus and other examples from the Mediterranean coincide with marked climatic and topographic changes in this area. The inferred diversification time follows the Messinian Salinity Crisis (MSC), one of the most dramatic geological events that occurred in this area in the late Miocene, between 5.3 and 5.96 Ma (Hsü et al., 1977; Krijgsman et al., 1999). During this time, the Mediterranean Sea became temporarily isolated from the Atlantic Ocean, resulting in the gradual drying of the basin. The cause of the closure of the Strait of Gibraltar is not completely clear, and a large body of literature documents that the MSC was driven by a complex combination of tectonic and glacio-eustatic processes that progressively isolated the Mediterranean Sea from the open ocean (Clauzon et al., 1996; Krijgsman et al., 1999; Duggen et al., 2003; Fauquette et al., 2006; Jolivet et al., 2006; Rouchy et al., 2006; Gargani & Rigollet, 2007). Following the MSC, the warm, humid climate of the Miocene further deteriorated and shifted to clear seasonality with summer droughts and cold, humid winters (Valente et al., 2010). These Pliocene changes may not have happened simultaneously but seem to have started in the eastern Mediterranean (Thompson, 2005). Glaciations in the north led to a sharper climatic differentiation between the northern and southern sides of the Mediterranean (Pons et al., 1995). Furthermore, significant tectonic uplift from Turkey to the Iberian Peninsula (Güldali, 1979; Meulenkamp & Sissingh, 2003) led to an increased altitudinal differentiation in the vegetation (Combourieu-Nebout, 1993; Valente et al., 2010).
Although many species of Tragopogon (and Dianthus and other co-occurring floristic elements) occur in the Mediterranean region, diversification may in fact have been greater in the areas bordering the current Mediterranean and corresponding to the ancient Paratethys. The latter was a series of inland seaways, brackish lakes and wetlands that developed from the Tethys Ocean during the Oligocene–Neogene. The Paratethys had ongoing connections with the Mediterranean Sea both before and after the MSC (Clauzon et al., 2005; Popov et al., 2006; Krijgsman et al., 2010). Climatic interactions across the broad Paratethys basin had long-term geological and biological consequences (Sprovieri et al., 2003), with much of this basin now corresponding to meadow steppe, steppe, dry steppe and semi-desert regions. These areas – beyond the bounds of the current Mediterranean basin – were formed post-MSC (Krijgsman et al., 2010) at a time that seems to coincide with the origin of Tragopogon and other key elements of the steppe vegetation in this region.
Only an in-depth biogeographic analysis requiring a comprehensively sampled, well-supported and well-resolved phylogeny is actually able to discern between a Mediterranean centre of diversification and a Paratethyan centre. However, because approximately one-third of all species of Dianthus are endemic to the Mediterranean region but only 5–10% of the species of Tragopogon are, different centres of diversification for the two genera are possible. Furthermore, such biogeographic analyses of plants from this region are scarce (Lo Presti & Oberprieler, 2009; Mansion et al., 2009; Roquet et al., 2009), and we can therefore only provide preliminary insights from studies on other species-rich Eurasian lineages occurring in the same dry steppe habitats as Dianthus and Tragopogon. It is also noteworthy that the pattern reported here even extends to insects from these habitats (Esseghir et al., 2000).
A few lineages within Eurasian Campanula may have diversified before the onset of drier climates, but a large number of species appear to be the product of more recent diversification events that may have occurred during the Plio-Pleistocene (Cellinese et al., 2009; Roquet et al., 2009). However, as with Tragopogon and Dianthus, species-rich lineages may be susceptible to bias due to poor taxon sampling, clearly the case so far with Campanula and related taxa.
Centaurea sect. Acrocentron (100 species) may have diversified c. 5 Ma (Font et al., 2009) with a crown group in the western Mediterranean that was dated at c. 2 Ma (L. Barres, I. Sanmartín, C.-L. Anderson, A. Susanna, S. Buerki, M. Galbany-Casals, & R. Vilatersana, unpubl. data); this latter group is similar in age to Tragopogon and Dianthus (Table 2). One well-supported subclade (‘eu-Scorzonera’) of the former genus Scorzonera may be another example of a rapid radiation during the same general time frame, although it may have originated a little earlier. We estimate that this radiation occurred about 3.8 Ma (Table 2) and generated at least 50–60 species (Lipschiz, 1964; Kamelin & Tagaev, 1986; reviewed in Mavrodiev et al., 2004), mostly in Western Asia. Note that based on Mavrodiev et al. (2004), Scorzonera is not monophyletic (see also Fig. S1) and remains in need of more comprehensive study and revision. Therefore, the actual number of species in this well-supported subset of Scorzonera is unclear (Kilian et al., 2009), but may be at least twice as high as the estimate used previously.
Allopolyploidy is a common mode of speciation in Tragopogon; at least 12 Eurasian species are of polyploid origin or are reported to comprise diploid and polyploid cytotypes (Mavrodiev et al., 2008b). Through the union of divergent parental genomes, allopolyploids exhibit novel genetic combinations and may display novel phenotypes. Such phenotypic novelty may be manifested in adaptation to new habitats, such as those resulting from the climatic and topographic changes that followed the MSC. At least some of the diversification in Tragopogon during the past 2 + Ma can be attributed to polyploid speciation rather than to cladogenic events.
Other species-rich clades occurring in the same basic habitats with Tragopogon apparently radiated somewhat earlier (45–4.28 Ma) than Tragopogon (e.g. Campanula, Scabiosa, Knautia, Cousinia subgenus Cousinia, a few subgroups within Centaurea, and notably the major meadow grasses of the area; Table 2). Such temporal differences are not surprising, not just for methodological reasons, but also because diversification may have occurred not only at different places and at different times, but also with different causes. Given that the MSC coincided with a time of increasing aridity and was followed by a time of increasing seasonality, it is possible that plant taxa already present in the Mediterranean diversified first in response to aridity and later to increased seasonality, as demonstrated in Anthemis (Lo Presti & Oberprieler, 2009). Moreover, diversification may already have happened earlier in response to increased salinity during the MSC. Studies of pollen records suggest no significant climatic changes during this period and show that plant migration and regional extinction were driven exclusively by the increased salinity caused by the desiccation of the Mediterranean basin (Fauquette et al., 2006).
Taxa already adapted to aridity before the late Miocene, such as those in the mountains of Central Asia, may show a different pattern. The closest relatives found in Central Asia may not have undergone radiation events and habitat change before the late Miocene; rather, they may have radiated subsequently in the Mediterranean during the late Pliocene in response to increased seasonality and the development of dry meadow communities. For example, this pattern of Mediterranean species with closest relatives in mountainous areas is found in Veronica (Albach et al., 2004). However, not all taxa native to Asia necessarily underwent habitat shifts before migrating to Europe, as illustrated by Aquilegia, which evolved from forest species in Asia (e.g. Bastida et al., 2010) and exhibits only a late Pliocene radiation in the meadows of Western Europe. The east-to-west migration was favoured by the earlier onset of the climatic events in the east. Consequently, plant radiations in the western Mediterranean seem to have started later than those in the east (e.g. Vargas et al., 2009).
Thus, our comparisons reveal three potential cases of ‘pseudocongruence’ – that is, common spatial patterns that originated at different times through different causes (Cunningham & Collins, 1994) – in these clades that radiated in the same habitat. First, the place of diversification may have differed as semi-arid grasslands formed in parallel over a large area from Western Europe to Central Asia. This parallel formation subsequently allowed migration across the region, blurring patterns of initial diversification. Second, different factors, such as aridification, changes in seasonality or increasing salinity, responsible for the formation of semi-arid grasslands may have initiated diversification in different taxa. Third, differences in the timing of diversification may be reflected in analyses of diversification patterns in taxa from these habitats.
The late Pliocene has been inferred as the time frame for a major east–west vicariance event in Microcnemum (Kadereit & Yaprak, 2008) and Campylanthus (Thiv et al., 2010). Superficially, it may therefore seem as if the subclades of such taxa radiated in the late Pliocene, but in fact, they are more likely remnants of larger extinctions. This emphasizes that the same climatic and tectonic events can lead to rapid radiations in some groups but to extinction in others.
In summary, our comparison of diversification rates and patterns in Tragopogon with those of other clades from dry meadow communities of the Mediterranean and surrounding regions indicates that these plant communities did not evolve all at once but represent more malleable assemblages, with different components originating and diversifying at different times. These results also demonstrate the fairly rapid evolution of modern plant communities themselves. Detailed studies so far suggest that these speciation events occurred in allopatry and as a consequence of habitat shifts (Lo Presti & Oberprieler, 2009; Bastida et al., 2010) rather than in response to pollinator shifts. Thus, our data for Tragopogon and results summarized in Table 2 support the recent hypothesis that nonadaptive allopatric diversification can proceed remarkably rapidly (Kozak & Wiens, 2006; Valente et al., 2010). However, we also stress that other modes of speciation, such as hybridization and polyploidy, have ultimately generated additional species of Tragopogon (reviewed in Mavrodiev et al., 2004, 2007, 2008a,b), Veronica (summarized in Albach et al., 2008) and other clades represented in these meadow communities.
Many other clades may have similarly radiated rapidly throughout this region, but have not yet been investigated in detail. Examples include Acantholimon (Plumbaginaceae, 120 species), Silene (Caryophyllaceae, 194 species), Acanthophyllum (Caryophyllaceae, 70 species) and perhaps Eremurus (Asphodelaceae, 50 species). Hence, future studies should focus on these and other species-rich Eurasian lineages.