Plant reproductive ecology and evolution in a changing Mediterranean climate
The Mediterranean region has long provided a fascinating setting to study and understand the natural history of plants. In terms of the human use of plants, the region has been at the heart of the origin and domestication of several major agricultural crops. In terms of our understanding of the natural world, naturalist systematics based on the biology of organisms began there, as Aristotle and others have shown us. Interestingly, the origin of western plant science is associated with an area of high biological diversity – the eastern Mediterranean. Now, it has become evident that the Mediterranean climate region is one of the important biodiversity hotspots in the world (Myers et al. 2000). Many scientists have contributed to knowledge on the high number of species in the Mediterranean flora and others have since explored the possible origins of such diversity. A number of factors have caused this high diversity, of which the intermediate location of the Mediterranean region between more temperate, desert and tropical climate regions (which have furnished many species of the flora), its geomorphological and landscape heterogeneity that provides for a mosaic of habitats, and a phased geological and climatic history are of major importance (Thompson 2005).
There has thus been much interest in the biological processes that promote divergence and/or contribute to population and lineage persistence in a region which has long undergone phased changes in climate, without having been physically directly touched by glaciations. Many of these processes are related to plant reproductive ecology. However, the Mediterranean climate region is also one of the most seriously threatened regions in terms of potential biodiversity loss in a future scenario of global change (Sala et al. 2000), in which increasing urbanisation, land development and climate change have already begun to impact many a landscape (Thirgood 1981).
All regions on Earth provide examples of environmental and historical constraints in the processes of plant evolution as populations adapt, survive and diversify. Thus, it is not surprising to see scientific papers, books and societies on tropical, polar or mountain biology. The Mediterranean region has been less successful in this aspect, despite the biological diversity that it represents. Two important landmarks for the Mediterranean region concern the comprehensive account of Thompson (2005) and the ISOMED society, which organises the MEDECOS conferences (Arista et al. 2017) to promote important contributions to unravel causes of diversity in the five Mediterranean regions (Cowling 1992; Hopper & Gioia 2004; Allsopp et al. 2014) and sometimes across them (Cowling et al. 1996; Rundel et al. 2016). In such comparative accounts, the Mediterranean Basin is however sometimes only partially represented, and to date no complete exhaustive review of reproductive ecology has been written.
In this Special Issue of Plant Biology we present a set of papers focused on different topics related to plant reproductive biology in a Mediterranean environment. For practical reasons, reproductive biology is here considered in a narrow sense, in relation to flower, fruit and seed biology and associated breeding and mating systems, rather than dispersal and establishment. Contributions are organised by topic and include review papers and empirical case studies, and sometimes a bit of both. Several papers attempt to unravel different mechanisms and strategies underlying reproductive systems in the Mediterranean. None of them are exclusive to the Mediterranean, but illustrate strategies that may be particularly functional in Mediterranean environments and thus at least partially explain biodiversity evolution. A small number of papers are devoted to the genetic aspects of plant reproduction, to throw light on how plants cope with harsh environments, typical of the Mediterranean. The evolutionary processes and strategies are examined in a historical context, by comparative analyses in some papers. Spatial variation in Mediterranean environments is analysed in contributions devoted to different typical Mediterranean communities. Theory-oriented studies lead to practical issues of high relevance in the Mediterranean, such as conservation, domestication and invasions. Finally, a view from Mediterranean climate regions in the Southern Hemisphere brings the opportunity to contrast with the rest of the issue devoted to the Mediterranean Basin. Needless to say, many of the contributions are transversal as they deal with several of the above-mentioned topics, indicative of the multi-faceted nature of research on plant reproduction.
Plant reproductive strategies
The diversity of plant breeding systems is well represented in the Mediterranean. Reciprocal style polymorphisms are particularly visible examples, such as heterostyly and related systems, for which outcrossing is promoted with efficient pollen transfer while maintaining hermaphroditism and avoiding self-interference between sex organs in a flower. These polymorphisms are usually maintained within populations through negative frequency-dependent selection. In the Mediterranean this polymorphism often illustrates a spatially dynamic system with variable morph ratios among populations and different stages in the evolution towards or loss of heterostyly (Thompson 2005).
Three papers in this issue deal with this topic. Comparative studies of the evolution of style polymorphism were made by Ruiz-Martín et al. (2018) in a phylogenetic study of the genus Linum, a group of plants that first attracted the attention of Darwin (1877). These authors show that the polymorphism is common in the Mediterranean Basin, and has independently evolved in the Mediterranean-type climate region of the Cape Floristic Region in South Africa. Pannell (2018) found that the morph ratio and seed production in a population of a style polymorphic species of low reciprocity between sex organs (Lithodora fruticosa) is associated with gender differentiation of morphs. Some of these style polymorphic plants show particular pollination systems that help explain how the polymorphism is maintained or lost, as Pérez-Barrales et al. (2018) illustrate in Narcissus papyraceus. These authors take advantage of the presence of different pollinators in different regions to experimentally test their pollination roles in relation to the flower architecture of each style morph.
For other flower polymorphisms selective processes can function in a different manner. Narbona et al. (2018) review the incidence of flower colour polymorphism in the Mediterranean flora in the light of available evidence, and explain in detail that the apparent lack of within-population polymorphism points to differentiation processes leading to speciation, via directional selection mediated by pollinators or other agents, or through stochastic processes.
Polyploidy and hybridisation are critical processes in plant evolution. They are the result of the wide promiscuity of plants in their reproduction, and their relevance is clear in the review of Marques et al. (2018). Polyploidy is a very frequent process, both among and within species. Despite the fact that this topic has been frequently investigated by plant taxonomists, the authors stress the lack of data in a region where spatial and temporal heterogeneity should promote these processes. Moving back to the population level, Thompson et al. (2018) insist on the importance of on-going hybridisation in plant populations, and provide an example of parallel evolution of hybrid forms from the same parental species on different Mediterranean islands in the genus Cyclamen. Muñoz-Pajares et al. (2018) focus on a single species, Erysimum mediohispanicum, which has diploid and tetraploid populations with different geographic ranges, abiotic niches and floral traits that are putatively associated with pollination biology and that may contribute to differentiation.
Genetic mechanisms
In addition to directional selective regimes or stochastic population differentiation, phenotypic divergence should be based on parent–offspring inheritance of the traits involved. The genetic and epigenetic basis for adaptation and differentiation is the focus of two papers. The study of Marcer et al. (2018) on a large population sample of genetic variation for two critical reproductive traits (seed dormancy and flowering time) in Arabidopsis thaliana in the Iberian Peninsula reports a spatial correlation with minimum temperature climate data. This work also provides sound information on sites of finer adjustment (those with the highest temperatures in the southwest) between phenological traits and response to global warming. In a companion paper, Balao et al. (2018) review the evidence which suggests that epigenetic variation contributes to the response of plants to stressful factors in the Mediterranean, such as drought, fire or poor soils.
Historical processes
In the last 10 years, understanding the historical factors that have contributed to plant diversification and endemism in the Mediterranean flora has become a major theme of research. The paper by Vargas et al. (2018) explores the timing of diversification in published phylogenies in order to examine whether there are correlations between historical climate conditions and the association of diversification with reproductive or vegetative traits. The association, when it does exist, is idiosyncratic, with no emergent pattern. However, the number of available phylogenies in which reproductive traits can be analysed limits interpretation. Interestingly, pollination ecology does not seem to play a dominant role in diversification, in contrast with that reported for the Mediterranean climate regions of South Africa and Australia. Vargas et al. (2018) stress the effect of geographic isolation in their review. Traits related to adaptation to dry climates before the onset of the Mediterranean climate and diversification before (Miocene or earlier) and after (Plio-Pleistocene) the onset of Mediterranean climate in the basin are both reported, making it difficult to disentangle the true effect of diversification and adaptation in relation to the onset of a Mediterranean climate. With a similar approach, Escudero et al. (2018) review the association between chromosome number and diversification. Although historical features of geological and climatic evolution in the region may have contributed to coupled karyotype change and diversification in some plant groups, there is no overall general pattern. But again, the number of available phylogenies may hinder the detection of such patterns.
Mountains and islands: focal points for ecology and evolution
One of the most characteristic community types of the Mediterranean is shrublands, which have long been studied in detail for their ecophysiology and ecomorphology, and in this issue plant reproductive aspects have finally received equivalent attention at the community level in the paper of Petanidou et al. (2018) on eastern Mediterranean islands along a climatic gradient. They show how structural aspects of plant–pollinator networks are closely associated with species richness, which is in turn affected by climate, implying that pollination network structure is indirectly affected by climate change.
Mediterranean mountains have a history of isolation that is at the heart of the high rates of endemism we see there (Médáil & Quézel 1997; Thompson 2005). They are also where the climate of the Mediterranean region is rapidly changing and thus the potential scene for dramatic effects on species distributions, particularly as habitat fragmentation continues. Three papers in this issue address this point. The first concerns the paper of Giménez-Benavides et al. (2018) who review the available evidence concerning whether climate is affecting the relationships between plants and their pollinators on high mountains, but due to the low number of studies, in comparison with post-dispersal ecology and regeneration, it is difficult to come to a conclusion. In addition, most studies are observational rather than experimental, which limits their prospective value.
In a study of how pollinator–plant networks are affected by landscape structure for species on gypsum outcrops, Santamaría et al. (2018) illustrate how high degrees of fragmentation in the landscape causes randomness in such networks, and identify a link between plant specialisation on soil characteristics and pollinator specialisation. Pollinators are more sensitive to fragmentation than plants (although this may be a temporal difference), and something very common in the Mediterranean region, inter-annual variation in meteorological factors, has a marked effect on plant–pollinator interactions. This is an important point for the maintenance of such interactions in a Mediterranean setting where fragmentation is likely to continue, and climate likely to vary more erratically.
Another type of habitat that is dotted around the Mediterranean landscape concerns localised temperate climate refugia. Such ancient refugia often harbour small populations of individual species, such as the stands of pedunculate oaks (Quercus robur) in Mediterranean Spain studied by Moracho et al. (2018). These authors report how reproduction is modulated by a combination of small-scale and landscape-scale drivers. As a result of short-distance mating, limited pollen flow is only observed at a landscape scale, and the intrinsic ability of populations to maintain their reproductive capacity may help explain their successful long-term persistence in refugia that occur in an otherwise adverse broader environment.
The islands in the Mediterranean Sea can be counted by the thousand, and are very different in size, substrate, distance to the mainland, age and geological origin. With the exception of a few small volcanic islands, all are of continental origin; hence their current flora is derived from an initial continental floristic set, differentiation since isolation, extinction and colonisation. This makes their study more complicated than on oceanic islands where evolution occurs following colonisation (Whittaker & Fernández-Palacios 2006). The challenge has been taken up by Traveset & Navarro (2018), who made an extensive literature review of what is known of the plant reproductive ecology on Mediterranean islands. They draw attention to biases in studies concentrated in particular areas and on work at the species level rather than on island communities. There is thus still a lot that we need to discover, despite the fact that some islands have been colonised by human populations since the birth and early development of Western civilisations and that many islands are seriously threatened by modern-day overexploitation of resources and massive tourism.
A centre of concern for conservation science
Understanding plant reproductive ecology has direct implications for conservation science, an interdisciplinary field, if ever there was one. Thompson et al. (2018), using their empirical work on sites of on-going hybridisation in western Mediterranean Cyclamen and a review of the literature on the occurrence of such sites, illustrate how natural hybridisation is an evolutionary process that has a major influence on the distribution of genetic variation and the appearance of new species. They argue that sites of on-going hybridisation should become a conservation priority for the preservation of evolutionary potential in the flora.
Some species represent an important target for conservation because they are typical of endangered habitats and thus provide an indicator of habitat changes that can have effects at the entire community scale. Malcomia littorea is a characteristic species of vulnerable coastal dune habitats for which critical information for conservation can be obtained in studies of local adaptation of isolated sub-populations and the genetic structure of the species in a given area (De Vitis et al. (2018).
Conservation also implies eradication of invasive species, which in some cases not only affect pristine habitats, but also productive agricultural land. Although the flora of the Mediterranean Basin is more an export source than a recipient of invasive plants (Thompson 2005), there is increasing concern about the introduction of exotic species. One of these is the cosmopolitan Datura stramonium, jimson weed, native to Central America and which began its colonisation of the Mediterranean in the mid 16th century, soon after the European colonisation of America. The annual life cycle of this species means that it has experienced many generations in the invaded range and thus probable evolution of invasiveness, perhaps in relation to release from invertebrate herbivores (Valverde et al. 2015) and increased selfing. Jiménez-Lobato et al. (2018) report a comparative study between Mexican and southern Spanish populations and found that phenotypic selection on stigma–anther separation is released in invaded populations, in comparison with native populations. The latter show some inbreeding depression, which is consistent with the hypothesis of evolution of invasiveness.
It is well known that the eastern Mediterranean formed one of the oldest centres of plant domestication due to the availability of wild species with useful traits upon which artificial selection was feasible. Most of these traits relate to plant reproduction, seed production was a target resource for Neolithic man and seed trait evolution is a major element in their diversification from wild relatives. Iriondo et al. (2018) review the available evidence on the artificial selection process imposed on reproductive traits, the traits that have facilitated or impeded selection, and once the lineage is domesticated and cultivated, the frequency of gene flow between crops and wild relatives. This paper illustrates how hybridisation and introgression have been of major importance for domesticated species and also in the opposite direction with the transfer of new genetic combinations into wild species. This opens a new avenue for research where the focus is put on the impact of agriculture, even traditional, on the genetic admixture of wild communities.
News from the southern hemisphere
The vast majority of papers in this Special Issue concern the Mediterranean Basin. A study of the comparative ecology and evolution of plant reproduction among the different Mediterranean-type climate regions remains to be undertaken, despite the immense investment in comparative studies of plant ecophysiology, community structure, species diversity and fire ecology. What appears for the moment is that the generalised pollination systems found in the Northern Hemisphere are not a prevalent feature of Southern Hemisphere Mediterranean ecosystems (Johnson & Steiner 2003; Johnson 2010). Two papers on Southern Hemisphere case studies throw some light on possible mechanisms here. Pauw & Johnson (2018) describe the reproductive biology of two co-occurring Cape shrubs that share pollinators and nectar thieves. The density of conspecific and co-occurring plants is directly related to higher reproductive success and lower nectar robbing, promoting coexistence in a species-rich community.
In their review of pollination ecology in the Chilean Mediterranean-type ecosystem Medel et al. (2018) illustrate the importance of studying pollination ecology where insects are scarce, and highlight the importance of isolation of Mediterranean-type ecosystems for our understanding of their diversity and functioning of plant–pollinator interactions. The lack of research on the impact of agricultural and other human activities on pollinators is stressed in their review.
The papers included in this Special Issue of Plant Biology thus cover a variety of topics on plant reproduction. Despite the range of themes, which are far from being exhaustive, the papers in this Special Issue identify a number of important priorities for future work, some of which are common to nearly all the papers in this issue.
First, it is clear that we need to construct common databases on the evolution of species diversity in the flora, on pollinator networks, community structure in relation to fragmentation, and changes in demography and life-cycle parameters under the influence of climate variation. Nearly all the papers in this Special Issue point to the need for more clear-cut experimental information that probes the causes of observed changes, and for long-term studies with proper temporal and spatial replication. Mediterranean-type ecosystems are sensitive to global changes, and we need such work to continue to help us understand how this sensitivity is translated into biodiversity evolution and change. As a result of its marked regional- and landscape-scale spatial heterogeneity, which has allowed for persistence and diversification during historical phases of climate change, and to the long-standing presence of humans to which plant populations and communities are resilient and have adapted, the Mediterranean Basin has a flora with the potential to cope with future anthropogenic-based environmental change. Monitoring this interaction is now necessary, as the treatment of the different themes in this Special Issue reveals.
Finally, the Mediterranean world is changing and we need research priorities that are not only adapted to these changes but which inform non-scientists on the objectives and strategies we need to identify and pursue to conserve the natural heritage of the Mediterranean flora. The evolution of the flora has often gone hand-in-hand with human activities; it must now do so in a way in which the processes that create diversity are preserved. We must insist on the processes identified in this Special Issue to inform the non-academic world of the need to preserve the interactions among plant species and with their biotic and abiotic environment that ultimately shape the evolution of plant diversity. Plant reproduction is at the heart of this concern.
