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Original article access may require subscription. This method simultaneously features the characteristics of the constant-rates birth-death model with a three-state Markov model [57] and is implemented in the R package diversitree [58]. This likelihood-based approach allows the estimation of region-dependant rates of speciation, extinction and range evolution based on a fully resolved dated phylogenetic tree here the PL-dated allcompat tree. A strong advantage of this model lies in its ability to account for incomplete taxon sampling within areas [59].

To take into account incomplete taxon sampling within areas, a list of all Hyacinthaceae species and their respective distribution according to the eight areas was obtained from the WCSPF website [20] to determine the number of endemic and non-endemic species per area and the percentage of missing taxa for each area see Fig. S1 for more details. For each area, a ML parameter estimation and model comparison was conducted followed by Bayesian parameter estimation through MCMC [57].

To reduce the complexity of the analysis, two GeoSSE models — the full model and the model without between region speciation sAB — were estimated under a ML framework and compared using a likelihood ratio test as implemented in diversitree [58]. For all analyses, the model without sAB always better fitted the data suggesting that there are regional differences in diversification. The MCMC was run for 20, generations with a burn-in period of 5, generations.

Mediterranean‐Type Ecosystems

Finally, posterior probability distributions for the GeoSSE parameters were summarized using functions implemented in diversitree [58]. These analyses were not applied to the South America and Madagascar areas because they harbour only endemic species and thus are not suitable for GeoSSE analyses. Species richness in Hyacinthaceae is highest in sub-Saharan Africa spp. S1 for taxon sampling per area. All other areas have less than species.

Mediterranean-Type Ecosystems: The Function of Biodiversity by George Whitefield Davis

All species occurring in South America and Madagascar are restricted to these areas. Despite the fact that the topology was fixed in the BEAST analyses, the effective sample sizes of several parameters remain low i. Thus, the estimates obtained from the PL analyses are used for subsequent analyses. Since we will not be giving detailed consideration to the historical biogeography of Hyacinthaceae in light of the current classification we provide detailed, dated phylogenetic trees with ancestral area reconstructions for the family and the subfamilies in Figure S3.

The Bayesian and ML analyses produced very similar results and no significant discordance was noted between them; a comparison of support values Bayesian posterior probabilities and bootstrap supports for selected nodes is presented in Table S3. Figure 2 depicts the general dispersal pattern within Hyacinthaceae through time together with a LTT plot and the curve of O 18 variation in the last 60 Ma see Fig. S4 for extinction estimates.

Although based on a fraction of the total number of taxa comprised in the family, one could extrapolate from this LTT plot that species in Hyacinthaceae have accumulated relatively constantly throughout the history of the group Fig 2. A shift in the number of estimated dispersal and extinction events occurs shortly after the MMCO, with the highest number of dispersals estimated at the boundary between the Miocene and the Pliocene Fig.

The lineage through time plot shown in red and based on the PL-dated consensus tree is displayed with an estimation of climatic oscillations in blue estimated from the variation of O 18 concentration through time [54]. The dispersal and extinction events inferred by Lagrange are reported in two time slices: from 70 Ma to 16 Ma, and from 16 Ma to present Fig. It is not possible to make further inference on this optimization without a denser sampling of closely related families and a better supported sister relationship to Hyacinthaceae, so we concentrate hereafter on the ancestral area reconstruction within the clade comprising the Old World species of the family i.

Arrows depict dispersal events, whereas circles represent extinction events as estimated by the DEC model. See Fig. The deeper nodes in the family have been assigned sub-Saharan Africa as the ancestral area, thus inferring several dispersal events from this area to all other regions except Northern Europe before 16 Ma, with the Cape and Mediterranean Basin receiving by far the most migrants six and four, respectively; Fig.

Dispersals also occurred between the Mediterranean Basin and the Middle East and Asia, but these were only minor events one each. Extinction events in this first time slice are few and mostly concentrated in sub-Saharan Africa and the Mediterranean Basin. The scenario inferred in the second time slice 16 Ma to present; Fig. The number of dispersals increases sharply shortly after the MMCO, which coincides with the onset of conditions favourable for the establishment of Mediterranean conditions Fig. Sub-Saharan Africa remains an important contributor to the diversity of neighbouring areas, although three main aspects are particularly noteworthy in comparison with observations over the first time slice.

First, and most significantly, there is no dispersal event inferred between sub-Saharan Africa and the Mediterranean Basin, although all other areas continue to benefit as recipients from sub-Saharan Africa except Northern Europe. Secondly, the Cape region remains by far the principal recipient from sub-Saharan Africa 39 out of 99 dispersal events. Thirdly, the only dispersals towards sub-Saharan Africa are from the Cape and they are few three dispersals.

Sub-Saharan Africa was not a recipient during the first time slice Fig. The Mediterranean Basin is now also a major contributor to the diversity of its neighbours, particularly Northern Europe F and the Middle East, with 21 and 18 dispersal events respectively. The Middle East can be viewed as a major crossroad, acting as an important contributor as well as serving as a recipient; it has no equivalent among the other areas in that respect. The importance of sub-Saharan Africa as a contributor is balanced by the number of extinction events inferred for this region 22 extinctions inferred by Lagrange , by far the largest among all areas.

The Mediterranean Basin and Middle East regions also demonstrate significant numbers of extinction events, with 11 and 12 inferred extinctions respectively Fig. The GeoSSE analyses demonstrated higher speciation rates in the two Mediterranean climate regions Mediterranean Basin and the Cape than in the other regions i.

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Moreover, the Cape region has the highest speciation rate of all regions Fig. Similar patterns are retrieved for extinction rates, with the Mediterranean Basin and Cape regions both showing higher extinction rates, together with sub-Saharan Africa, than the other areas studied Fig. Speciation and extinction shown within a given region sA and xA, respectively and the remainder of the distributional range of Hyacinthaceae sB and xB, respectively for each area estimated by the GeoSSE analyses for the Hyacinthaceae dataset see text for more details. The biogeographical reconstruction presented here indicates that Hyacinthaceae originated in sub-Saharan Africa and began to diversify in the region around the Paleocene-Eocene boundary Fig.

S3 ; the deepest nodes in the Old World clade all received this single area as their most likely optimization.

Mediterranean-Type Ecosystems: the function of biodiversity

This scenario has been previously suggested by others, based either on a molecular phylogenetic analysis without an explicit biogeographical analysis [27] or with a less comprehensive taxonomic sampling and a single molecular marker [25]. Sub-Saharan Africa is the richest of all areas defined in the present study for Hyacinthaceae, with more than half of the species in the family found in the region spp out of ; Fig. In addition of being the cradle of the family and the centre of species richness, sub-Saharan Africa is also the primary source of the species occurring in the two Mediterranean areas Cape and Mediterranean Basin and in Madagascar, and has contributed to the diversity found in the Middle East and Asia Fig.

One of the main differences in the subsequent history of the family in two Mediterranean regions lies in the disruption of the link between sub-Saharan Africa and the Mediterranean Basin sometime before the MMCO; all the dispersals from sub-Saharan Africa to the Mediterranean Basin took place before 20 Ma Fig. This disruption coincides with the aridification of northern Africa, which took place from the Late Miocene onwards [18] and eventually led to the formation of the Sahara Desert.

This arid region acts as a physical barrier to dispersal events between sub-Saharan Africa and the Mediterranean Basin Figs. This period coincides with the intensification of aridity in western South Africa and the development of a Mediterranean climate in the Cape e. Although the current species richness in the two Mediterranean regions is similar and both exhibit the highest diversification rates among the regions examined here Fig. The high diversification rate found in the Mediterranean Basin is mainly the result of in situ speciation processes [61] Fig.

This area was only colonized prior to the MMCO and further large-scale immigration events were prevented by physical barriers, notably the Sahara Desert with the exception of three dispersals from the Middle East and one from Asia, all by widespread species; Fig. The most obvious triggers of this diversification are the establishment of the Mediterranean climate and concomitant fire regimes, as well as the Messinian salinity crisis and associated drier climates [1] , [15] , [55]. Several studies have reported increased diversification rates in herbaceous Mediterranean groups during this period e.

However, the influence of Quaternary climatic oscillations on the evolutionary processes responsible for the current species diversity should not be disregarded, especially in this region. It has been widely reported that these climatic fluctuations greatly influenced the speciation processes in most plants groups found in the region. The impact of the insular system in the Mediterranean on the diversification of bulbous plants, including Hyacinthaceae, remains to be fully explored, as has been done in other groups of the region [16] , [63].

Although there is no evidence of dispersal events from the Mediterranean Basin into sub-Saharan Africa after the MMCO, the Mediterranean area is an important source area for colonization of Northern Europe 21 out of 24 dispersal events to this region and has also contributed greatly to the diversity in the Middle East and, to a lesser extent, Asia Fig. Most of the dispersals from the Mediterranean Basin to Northern Europe occurred within the last two million years, suggesting that the colonization of Northern Europe took place gradually through the Quaternary Figs.

This is consistent with a role of the Mediterranean Basin as a refugium during the Quaternary glaciations, as suggested by several authors e. In the southern Hemisphere, the high diversification rate found in the Cape is most likely linked to both the establishment of the Mediterranean climate in the region and a high immigration rate from sub-Saharan Africa. Just six dispersals were inferred from sub-Saharan Africa to the Cape before 16 Ma, whereas 39 dispersals were recorded by the Lagrange analysis in the last 16 Ma. The mean date of these latter dispersals is 5.

Unsurprisingly, given its position at the tip of the continent, the Cape represents a biogeographical cul-de-sac, and the region has not contributed significantly to the diversity of Hyacinthaceae in other areas, with the exception of a few dispersal events into sub-Saharan Africa, all by widespread species that originated in the Cape.


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  • Its geographic isolation probably also ensured that the Cape was not enriched by emigrants from areas other than sub-Saharan Africa Fig. High diversification rate of Hyacinthaceae in the Cape Fig. Commonly proposed drivers of this diversification include adaptation to frequent fires and nutrient-poor soils, low vagility, geographic isolation and edaphic specialisation, and relatively muted climatic oscillations. The relative frequency of extinction events in the flora is far less clear. Our analysis shows that the extinction rate in Hyacinthaceae is higher in the Cape than elsewhere, implying that species turnover is relatively high in the family compared to other regions.

    This contrasts with the recent tendency to link high species diversity in the region with low rates of extinction, ostensibly due to reduced competition from other lineages [68].


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    • Lineage accumulation in the southwest corner of the African continent has been shown to be gradual in several groups e. Heliophila [72]. Although we show that speciation rates in the Cape are undeniably higher than elsewhere, we also show the region is characterised by the highest extinction rate of all six regions. This result is difficult to reconcile with the proposition that the rich plant diversity of the Cape is due to a combination of high speciation rates and low extinction rates e.

      Paradoxically, the large proportion of narrowly endemic species that characterises the Cape flora [70] is consistent with this pattern: narrow endemics are at greater risk of extinction from stochastic events than more widespread taxa. High rates of extinction are thus an inevitable corollary of high rates of evolution of narrow endemics.

      The Middle East area seems to have been a significant evolutionary crossroad between the northern hemisphere areas Mediterranean Basin, Northern Europe and Asia; Fig. The Hyacinthaceae of the Middle East area, contrary to that of most of the other areas, shows a complex biogeographical history involving immigrations from various areas sub-Saharan Africa, the Mediterranean Basin and Asia and emigrations to several neighbouring areas Fig. No other area has as many interactions with its neighbours. The region harbours several lineages of different ages and geographic origins and may have played a key role as a refugium of phylogenetic diversity in the northern Hemisphere representatives, especially during periods of drastic climatic fluctuations.

      The combined approach of parametric biogeographic reconstruction, which factors in paleogeographic history and phylogenetic uncertainty, and the joint assessment of the effect of geographic range evolution and diversification, provides powerful tools to examine the patterns and processes responsible for the evolution of biodiversity. We have used these tools to shed light on the evolution of plant diversity in two of the most species-rich Mediterranean ecosystems, the Cape of South Africa and the Mediterranean Basin.

      Our analysis is based on a single family with a good representation in both Mediterranean ecosystems and a complete representation at the generic level. Thus, conclusions drawn from the analyses presented here should be viewed cautiously, but provide nevertheless a valuable insight into the diversification of these unique biodiversity hotspots.

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      Similar studies in additional groups are necessary to assess the general validity of the patterns uncovered here before they can be generalized to the diversification processes in these species-rich regions. Significantly, however, rates of extinction in the Cape are shown to be commensurate with rates of speciation, suggesting that the two processes may represent two sides of the same evolutionary coin in a region that is well known for its biological riches.

      Histogram summarising the Hyacinthaceae species sampling per area. Regression lines in grey are provided for each tree. Biogeographical reconstruction of Hyacinthaceae using Lagrange and displayed on the PL-dated allcompat tree. MTEG will work to develop funding resources to support hands-on training for reserve managers in California and the four other Mediterranean regions to use the best available science to inform how they preserve and protect the ecosystems for which they are responsible, and develop proactive management plans to anticipate potential threats such as invasive species, non-native pathogens, climate change, human population pressures on protected areas e.

      The protection of MTE biodiversity requires the broad dissemination of scientific and technological knowledge, to foster a greater global understanding of these unique, critical ecosystems. Commission on Ecosystem Management. Our work. Photo: Lobsang Wangdu. Role of Biological Field Stations Biological field stations throughout the world have significant potential for addressing the most pressing environmental challenges facing science and society today by actively engaging in research collaborations and the development of environmental observatory networks and such field stations have particular relevance for Mediterranean-climate regions.

      Scientific Research, Best Practices, Information Sharing Mediterranean-climate regions provide many opportunities for comparative studies of the controlling factors in the evolution of biodiversity. Education and Training MTEG will work to develop funding resources to support hands-on training for reserve managers in California and the four other Mediterranean regions to use the best available science to inform how they preserve and protect the ecosystems for which they are responsible, and develop proactive management plans to anticipate potential threats such as invasive species, non-native pathogens, climate change, human population pressures on protected areas e.

      Public Outreach The protection of MTE biodiversity requires the broad dissemination of scientific and technological knowledge, to foster a greater global understanding of these unique, critical ecosystems. Follow us.