Patterns and Processes in Plant Phylogeography in the Mediterranean Basin. a Review

Patterns and Processes in Plant Phylogeography in the Mediterranean Basin. A Review

Gonzalo Nieto Feliner

Real Jardín Botánico, CSIC

Plaza de Murillo 2

28014 Madrid

Phone: +34 914203017

Mobile: +34 609446046

Running head: Plant phylogeography in the Mediterranean Basin

Key words: glacial refugia, hybridization, latitudinal patterns, Mediterranean Basin, phylogeography, plants, spatio-temporal concordance, straits

ABSTRACT

Phylogeography, born to bridge population genetics and phylogenetics in an explicit geographic context, has provided a successful platform for unveiling species evolutionary histories. The Mediterranean Basin, one of the earth’s 25 biodiversity hotspots, is known for its complex geological and palaeoclimatic history. Aiming to throw light on the causes and circumstances that underlie such a rich biota, a review of the phylogeographic literature on plant lineages from the Mediterranean Basin is presented focusing on two levels. First, phylogeographic patterns are examined, arranged by potential driving forces such as longitude, latitude—and its interaction with altitude—, straits or glacial refugia. Spatial coincidences in phylogeographic splits are found but, in comparison to other regions such as the Alps or North America, no largely common phylogeographic patterns across species are found in this region. Factors contributing to phylogeographic complexity and scarcity of common patterns include less drastic effects of Pleistocene glaciations than other temperate regions, environmental heterogeneity, the blurring of genetic footprints via admixing over time and, for older lineages, possibly a greater stochasticity due to the accumulation of responses to palaeoclimatic changes. At a second level, processes inferred in phylogeographically-framed studies that are potential drivers of evolution are examined. These include gradual range expansion, vicariance, long-distance dispersal, radiations, hybridization and introgression, changes in reproductive system, and determinants of successful colonization. Future phylogeographic studies have a great potential to help explaining biodiversity patterns of plant groups and understanding why the Basin has come to be one of the biodiversity hotspots on earth. This potential is based on the crucial questions that can be addressed when geographic gaps are adequately filled (mainly northern Africa and the eastern part of the region), on the important contribution of younger lineages—for which phylogeographic approaches are most useful—to the whole diversity of the Basin, and on the integration of new methods, particularly those that allow refining the search for spatio-temporal concordance across genealogies.

CONTENTS

I. Introduction

II. Patterns

(1) Large-scale spatial patterns

(a) Longitudinal patterns

(b) Latitudinal patterns

(d) Role of straits

(2) Spatio-temporal phylogeographic concordance

(3) Patterns and complexity

III. Processes

(a) Gradual range expansion

(b) Vicariance

(d) Radiations

(e) Hybridization and introgression

(f) Changes in reproductive systems

(g) Ecology determining success of colonization

IV. Perspectives

V. Acknowledgements

VI. References

I. INTRODUCTION

The Mediterranean Basin comprises a large territory around the Mediterranean Sea that is characterized by a Mediterranean climate, that is to say, mild rainy winters and hot dry summers. According to Quézel and Médail (2003) the Mediterranean region in a bioclimatic sense spans an area of 2,300,000 km2, whose limits have sometimes been suggested as coinciding with the natural distribution range of the olive tree (Olea europaea L.) (Fig. 1). It extends approx. 4000 km along an east-west axis and approx. 1600 km along a north-south axis.

This region is of considerable biological interest because of its rich biota compared to the surrounding areas and is considered one of the earth’s 25 biodiversity hot-spots (Myers et al., 2000). At the plant species level, i.e., in floristic terms, the Mediterranean region contains a flora that includes c. 24.000 species of which c. 60 % are endemics (Greuter 1991) whereas, for instance, all of tropical Africa has a comparable plant richness (30,000 taxa) in a surface area four times larger (Médail and Quezel, 1997). Compared to higher latitudes, 80% of all European plant endemics are Mediterranean (Comes, 2004). This richness is attributed to a number of factors including palaeogeologic and palaeoclimatic history, ecogeographical heterogeneity, human influence (Blondel and Aronson, 1999; Blondel et al., 2010) and a high percentage of species with narrow distribution ranges (Humphries et al., 1999; Thompson, 2005).

Geological and palaeoclimatic complexity is characteristic of the Mediterranean region. Its geological evolution involves complicated interactions between orogenic processes and widespread extensional tectonics (Rosenbaum et al., 2002). The area was formed during the Cenozoic simultaneously with the convergence of the African and Eurasian Plates and three associated smaller plates, Iberia, Apulia and Arabia (Dercourt et al., 1986; Krijgsman, 2002). The western Mediterranean was particularly active tectonically and consisted during the Oligocene of several small blocks that were remnants of a Paleozoic mountain chain, the Hercynian belt (Rosenbaum et al., 2002). Rotation, migration and collision processes along more than 30 Mya resulted in those small blocks located in the current territories of the Betic-Rif ranges, the Balearic Islands, the Kabylies, Corsica, Sardinia, and Calabria. The eastern Mediterranean region (Hellenic arc and Aegean basin) is more recent and its present configuration is the result of the collision of the Arabian plate with stable Eurasia in middle Miocene, which closed the connection between the Tethys Sea and the Indian Ocean (Krijgsman, 2002).

The palaeoclimatic history of the Mediterranean Basin included important long-term changes such as the gradual global cooling since the Oligocene (Zachos et al., 2008) and an aridification that started c. 9-8 Mya (Van Dam, 2006). During the Late Miocene, subduction processes in the westernmost Mediterranean caused the closure of the marine gateways that existed between the Atlantic Ocean and the Mediterranean Sea, leading to the desiccation of the Mediterranean Sea that is known as the Messinian Salinity Crisis (MSC) 5.96-5.33 Mya (Hsü, 1972; Krijgsman, 2002). This period was followed by the establishment of a Mediterranean type climate, around 3.2 Mya (Suc, 1984). In addition, the Basin has been influenced by cyclical climatic changes, driven by the Milankovitch oscillations, due to periodical shifts in the Earth's orbit and axial tilt that decreased their periodicity to 100 Ky during the Pleistocene (Imbrie et al., 1993; Jansson and Dynesius, 2002).

Phylogeography has shed light on the evolutionary history of current plant species by bridging population genetic approaches and phylogenetic focuses, or micro- and macroevolution, as the father of the discipline put it (Avise et al., 1987). The geographic coverage of phylogeographic investigations has been more intense in regions such as North America (Brunsfeld et al., 2001; Soltis et al., 2006) and the Alps (Schönswetter et al., 2005), but has reached most regions including the Arctic (Abbott and Comes, 2004), China (Qiu et al., 2011), the Southern Hemisphere (Beheregaray, 2008) and also the Mediterranean region, where a substantial increase in the number of studies has occurred over the last ten to twelve years.

The present paper reviews the topic of Mediterranean Plant Phylogeography aiming to throw light on the evolutionary history of plants in the Basin, finding clues for its biodiversity richness and complexity, and contributing to understand the whole puzzle of the history of European plants during the last 2 - 3 My. The review has a double focus, on patterns and process, and has been elaborated from studies published in over 130 papers.

A summary of the knowledge concerning a very significant part of the region, i.e., the three southern European peninsulas (Iberia, Italy, Balkans), and the role they have played in European biogeography during the last million years, has been recently published (Hewitt, 2011). The Balkans represent the main biodiversity hotspot and the major source for postglacial colonization of central and northern Europe and it was suggested that such richness could be related to opportunities for dispersal and vicariance along a complex geological history that included several land connections, disconnections and submergences, particularly during the Miocene and Pliocene (Griffiths et al., 2004; Tzedakis, 2004). However, its geographic position closer to Asian biotas probably also contributed to its richness (Mansion et al., 2008).

In the evolution of plant lineages in the Iberian Peninsula, on the other hand, determinant factors are the mountain ranges allowing multiple refugia and producing “a pulsating patchwork of allopatric to parapatric clades”, and the recurrent connections and disconnections with Northern Africa starting even before the MSC between 7 and 14 Mya (Hewitt, 2011).

The Italian Peninsula is a younger conglomerate that contributed less to postglacial colonization of central and northern Europe due to the strong geographic barrier represented by the Alps. However, multiple refugia have been identified corresponding to major mountain blocks, with a particular differentiation in the South both in animal (e.g., Joger et al., 2007; Canestrelli and Nascetti, 2008) and in plant groups (Cozzolino et al., 2003; Vettori et al., 2004; Heuertz et al., 2006; Španiel et al., 2011).

However, that work—one of the last by the late Godfrey Hewitt (Hewitt, 2011)—was almost exclusively based on studies of mammals, reptiles, amphibians and insects. Despite the common geological, climatic and environmental history for all organisms phylogeographic patterns might vary. Mechanisms such as polyploidization and hybridization, and ecogeographical concepts such as niche conservatism, are regarded as more significant in plants than in animal groups (Sanmartín, 2007; Donoghue, 2008).

This review is focused on the species level, i.e., within species or closely-related species, as was the original scope of Phylogeography (Avise et al., 1987). However, there is not a sharp border line between species and closely-related species and thus some works going beyond the species level that were important for the Mediterranean Basin have also been considered. On a geographic side, despite being traditionally considered a part or an extension of the Mediterranean region, the Macaronesian archipelagos have not been considered here because oceanic island biogeography (and phylogeography) is a specific field that has received much attention in recent years and a considerable part of the literature has been devoted to the Macaronesian region (Juan et al., 2000; Sanmartín et al., 2008; Fernández-Palacios et al., 2011).

II. PATTERNS

In this section, the main phylogeographic patterns detected in plant groups across the Mediterranean Basin are arranged following the inferred major driving forces or causal factors.

(1) Large-scale spatial patterns

Even if small scale factors and specific biological properties of the plant groups are important in driving differentiation in an environmentally heterogeneous region like this, large scale factors also have a role in contributing to gene flow interruption, and thus to phylogeographic splits. The patterns listed below (longitudinal, latitudinal, sea straits, refugia) are associated to longitude and latitude, spanning the size and shape of the region, and potentially contributed to create shared patterns across plant groups.

(a) Longitudinal patterns

East-west phylogeographical breaks, i.e, occurring along the longest axis of the Mediterranean Basin, have frequently been inferred, and sometimes dated, to have arisen as a consequence of pre-Pleistocene diversification of lineages. The most apparent cases are those in which there is a clear current geographical gap associated with a phylogeographic split, which might have resulted from contraction of formerly continuous ranges. These disjunctions or highly scattered ranges are seen in the lowland shrub Buxus balearica Lam. (Rosselló et al., 2007; Fig. 2), the salt-tolerant succulent Microcnemum coralloides (Loscos & J. Pardo) Buen (Kadereit and Yaprak, 2008) or the herbaceous legume Erophaca baetica (L.) Boiss. from evergreen oak forests (Casimiro-Soriguer et al., 2010). In the coastal subshrub Cephalaria squamiflora (Sieber) Greuter such gap is emphasized by its insular distribution ranging from the Balearics to the Aegean (Rosselló et al., 2009). When there is no current geographic gap, the location of the phylogeographic break or the secondary contact may still be detectable (e.g., in the perennial mountain herb Heliosperma pusillum (Waldst. & Kit.) Rchb., Frajman and Oxelman, 2007), particularly when the distribution range is linear as in the marsh sedge Carex extensa Gooden. (Escudero et al., 2010). It is however more frequent that events subsequent to the initial gene flow interruption, such as partial westwards colonization of genotypes originated in the East or vice versa, led to a more complex picture, as in the case of the submediterranean herbaceous Anthyllis montana L. (Kropf et al., 2002), the laurel trees Laurus nobilis L. and L. azorica (Seub.) Franco (Rodríguez-Sánchez et al., 2009) or the thermophilous lowland shrub Myrtus communis L. (Migliore et al., 2012). Westward or eastward waves of colonization, not only during the Pleistocene but at different times depending on the climatic conditions and the ecological requirements of the species in question, have been decisive in shaping the current species and genetic composition of the Mediterranean flora. Examples are found in Araceae, Carex extensa, Erica arborea L. or Myrtus communis (Mansion et al., 2008; Escudero et al., 2010; Désamoré et al., 2011; Migliore et al., 2012; respectively). Such expansions have been reported to be important during the Oligocene–Miocene, when microplates located between Paratethys and Tethys allowed land connections along the Mediterranean (Steininger and Rögl, 1984; Meulenkamp and Sissingh, 2003). However, other organisms expanded through the Southern rim of the Basin at different periods (North Africa – Arabia, Quézel, 1985) as the steppic herbaceous perennial Ferula loscosii (Willk.) Lange (Pérez-Collazos et al., 2009) or some thistles (Cardueae; Barres et al., 2013).

In addition to east-west phylogeographic splits, different levels in genetic diversity on a large scale in eastern vs. western areas of the Mediterranean Basin have been found too, particularly in trees. Some of those E-W differences have been related to the place of origin or major diversification of the group in question (e.g., in Quercus suber L., Lumaret et al., 2005), while for other groups decisive factors have occurred along their evolutionary history. For instance, among gymnosperm tree species from the genus Abies, Cedrus, Cupressus and Pinus, a decreasing trend in genetic diversity running east-west along the Basin has been detected and has been attributed to an east (warm/wet) – west (cold/dry) trend during the last glacial maximum (LGM) (Fady, 2005; Wu et al., 2007). Such a decreasing gradient of within-population genetic diversity from east to west has also been found in a meta-analysis based on different groups of living organisms, but it is stronger in the southern part (northern Africa) than in the northern Mediterranean, in low-land plants than in plants at higher elevations, in trees that in other life-forms, and in bi-parentally and paternally than in maternally inherited DNA markers (Conord et al., 2012). However, there is no overall correlation between genetic diversity and species diversity across the Basin (Fady and Conord, 2010) and different situations concerning richer eastern or western lineages are found at the species level (e.g., in Cistus, Guzmán and Vargas, 2005; Hordeum, Jakob et al., 2007; or Heliosperma, Frajman and Oxelman, 2007). Therefore, new evidence is necessary to understand the extent and causes for the prevailing idea that the Eastern Mediterranean is a reservoir for plant evolution or a cradle for lineages diversification (Mansion et al., 2009; Roquet et al., 2009; Barres et al., 2013).