The oak syngameon: more than the sum of its parts
See also the Editorial on this article by Plomion & Martin, 226: 943–946.
Summary
One of Anthropocene's most daunting challenges for conservation biology is habitat extinction, caused by rapid global change. Tree diversity has persisted through previous episodes of rapid change, even global extinctions. Given the pace of current change, our management of extant diversity needs to facilitate and even enhance the natural ability of trees to adapt and diversify. Numerous processes contribute to this evolutionary flexibility, including introgression, a widespread yet under-studied process. Reproductive networks, in which species remain distinct despite interspecific gene flow, are called syngameons, a concept largely inspired from work focusing on Quercus. Delineating and analyzing such species groups, empirically and theoretically, will provide insights into the nonadditive effects on evolution of numerous partially interfertile species exchanging genetic material episodically under changing environmental conditions. To conserve tree diversity, crossing experiments designed with an empirical and theoretical understanding of the constituent syngameon should be set up to assist diversification and adaptation in the Anthropocene. Our increasingly detailed knowledge of the oak genome and of oak interspecific and intraspecific phenotypic variation will improve our ability to sustain the diversity of this tree through an unpredictable and unprecedented future.
More than the sum of its parts
The species, defined as being reproductively isolated from other species, remains the primary currency of discussion in ecology, evolution and conservation and is based upon the biological species concept (Mayr, 1942), a confusing and arguably inappropriate term. Mayr's view has been widely adopted despite difficulties in diagnosing species on reproductive isolation (Rieseberg et al., 2006; Lagache et al., 2013). Early evolutionary botanists, like Johannes Lotsy, Verne Grant and James W. Hardin, have already demonstrated that closely related plant species are able to cross under certain circumstances and that interfertility varies among suites of species. They adopted the term ‘syngameon’ to describe the basic fact that these species are not reproductively isolated and yet largely behave as ‘good’ species, that is, form morphologically distinct groups in sympatry. Hence, a working definition for a syngameon is that of a group of otherwise distinct species interconnected by limited gene exchange, that is the most inclusive interbreeding evolutionary unit (Suarez-Gonzalez et al., 2018). Other terms are used to describe similar but not exactly overlapping concepts. For instance, the idea of ‘complexe d'espèces’ was introduced in France in 1984 by the agronomist Jean Pernès, who led research on gene flow between cultivated plants and their wild relatives (Pernès et al., 1984). The notion of species complex, as well as that of related concepts, evoke taxa that can be difficult to delimit taxonomically due to blurred species boundaries. By contrast, the concept of syngameon explicitly addresses the persistence of interfertile species that remain largely distinct despite living in sympatry and having numerous opportunities for hybridization.
Species in the tree genus Quercus are probably the most famous example of a syngameon (Cronk & Suarez-Gonzalez, 2018). Numerous lines of evidence, ranging from the discovery of morphological intermediates (Tucker, 1990) to genome-wide investigations of macroevolution (Eaton et al., 2015; McVay et al., 2017), indicate that hybridization and introgression are persistent and widespread phenomena among closely related oak species. Whereas Darwin argued in The Origin of Species (1872) that additional studies of oaks in Britain had not resulted in greater taxonomic clarity but rather in greater confusion, Burger (1975), who also struggled with the phenotypic patterns observed in oaks, focusing on Quercus macrocarpa and its relatives in North America, arrived at a more positive conclusion. He stated that ‘the classical species-concept in Quercus defines a very real population system and that it evolves on two fronts. One is that of continuing to adapt to a niche that differs slightly from its close relations. The second is in sharing the broader evolutionary advances of these same close relationships that together comprise the genetically isolated biological species. In other words, while species participating in a syngameon retain some level of interfertility, thereby helping them maintain a large effective population size, potential for gene flow among species is greatly reduced in comparison to gene flow within species, allowing each constituent species to persist.
Oaks are not unusual among trees for this behavior and have achieved their notoriety simply because they are one of the few well-studied northern temperate tree groups with sufficient levels of sympatric species richness to allow hybridization and introgression. Many of the most diverse genera of trees, particularly in the tropics, probably function as syngameons, given the similarity in ecological and evolutionary characteristics, including pervasive levels of sympatry, evolutionarily stable genomic structure, low levels of polyploidization, generalized pollination systems, and prodigious reproductive output (Momose et al., 1998; Petit & Hampe, 2006; Kremer et al., 2012; Chen et al., 2014; Cannon & Lerdau, 2015; Abbott, 2017; Beech et al., 2017; Caron et al., 2019). In fact, according to many botanists (Stebbins, 1950; Grant, 1957), long-lived woody perennials should engage more readily in interspecific matings than other plants. Interestingly, coral reef species, also interpreted as belonging to syngameons, share many ecological characteristics with trees, such as longevity, indefinite growth, lack of differentiated germline, and a sessile habit (Kenyon, 1997; van Oppen et al., 2001). However, the syngameon concept is likely to be of even broader relevance, as at least 25% of plant species and 10% of animal species are involved in hybridization and potential introgression with other species (Mallet, 2005). Therefore, lessons learned about oak syngameons will likely be generally applicable to the evolution of many other organisms.
Most conservation biologists view hybridization solely as a threat to species conservation, because of potential outbreeding depression and genetic extinction (Jackiw et al., 2015). Other evolutionary biologists have emphasized the potential advantages of participating in a syngameon as a creative source of novel phenotypic innovation and overall genetic diversity (reviewed in Arnold, 2004; Abbott et al., 2013; Hamilton & Miller, 2016; Suarez-Gonzalez et al., 2018). Participation in a syngameon could dampen local population extinction by expanding effective population sizes (Cannon & Lerdau, 2015). The genetic recovery of tree species, virtually wiped out by invasive diseases and pests, through the production of resistant cultivars, like in the case of the American chestnut (Clark et al., 2014) and elm (Sniezko & Koch, 2017), have been achieved through interspecific crosses and adaptive introgression. We argue here that the syngameon is more than the sum of the pairwise interactions between species but instead represents a dynamic network of species, acting over large periods of time and at continental scales. Like most networks, the syngameon should exhibit synergistic and emergent properties not seen in the constituent parts, as found in the application of circuit theory in ecology and conservation (McRae et al., 2008; Dickson et al., 2019). For instance, some species could act as a genetic conduit among otherwise disjunct species, with feedback loops of gene flow acting over millennial cycles. These new properties should be explored to best incorporate them into species conservation and management.
One of the more perplexing aspects of the syngameon is how species retain their cohesiveness and distinctiveness despite occasional hybridization. To solve this paradox, it is important to recall that hybridization is both frequency- and density-dependent: hybrids are produced in large numbers only episodically under conditions of extreme demographic imbalance among species, a process called Hubb's effect or the rare-species effect (reviewed and modeled in Klein et al., 2017). Such conditions are highly unstable. First, the rarest species can be genetically swamped and eliminated locally, resulting in the dominance of one species. Second, species can persist locally, each in sufficient number to limit hybridization, as a consequence of processes such as reinforcement, assortative mating, divergent selection, and selection against hybrids. To identify the most important factors affecting species cohesiveness and distinctiveness, additional spatially-explicit analyses of hybridization among co-distributed species are needed (Klein et al., 2017), focusing not only on species pairs but on the entire species network. Frequency of hybridization is often associated with rapid environmental change (Chunco, 2014). In particular, anthropogenic disturbances have long been known to increase hybridization rates (Abbott, 2017). Given environmental and temporal heterogeneity, fluctuating population sizes and prodigious gametic production, hybrids can function as genetic bridges allowing rapid introgression among species participating in the syngameon (Arnold et al., 1999; Cannon & Scher, 2017). However, introgression does not affect all genomic regions indiscriminately. Rather, it is known to filter interspecific gene flow to a small fraction of the genome (Martinsen et al., 2001; Leroy et al., 2020).
Ultimately, we would argue that the syngameon is not necessarily a transitional or incipient phase of a process towards complete speciation among the participant species. To explain the persistence of syngameons, two non-exclusive hypotheses can be proposed. First, low rates of hybridization might not be strongly counter selected, so that the evolution of complete reproductive isolation evolves only exceedingly slowly. Alternatively, hybridization could be selected for during critical episodes of environmental change. This would be the case if individuals retaining the ability to participate in a syngameon have an evolutionary advantage over those that that are fully genetically isolated. Regardless of the mechanisms involved, this implies that whenever ecological adaptation pressures and assortative mating mechanisms that first drove divergence among species remain in place, each species will retain its cohesiveness and distinctiveness, despite occasional episodes of introgression resulting in low differentiation for some traits. Future studies into the dynamics of the syngameon will need to explore how a syngameon is initiated and what is the impact of the number of participant species on its stability, and how to integrate the cumulative network effect of all interfertile species. We emphasize that the network of species, interacting over time and space and responding to periods of enduring stasis and rapid change, may create a synergistic evolutionary process that generates resilience and flexibility beyond the ability of any of its constituent parts.
Trees in the Anthropocene
Earth is entering a period of environmental change that outpaces records over the past five million years and pushes our global ecosystems into uncharted territory (Moritz & Agudo, 2013; Ellis, 2015). These changes, caused by humans profoundly altering basic Earth processes, has prompted the recognition of a new geological era, the Anthropocene (Steffen et al., 2007; Finney, 2014). The concept of a human-dominated Earth is compelling (Steffen et al., 2011; Williams et al., 2016). It presents a challenge to how we think about evolutionary and ecological forces and how we should manage them in the future (Caro et al., 2012; Dirzo et al., 2014; Malhi et al., 2014; Lugo, 2015; Hamilton & Miller, 2016). As many native wild populations are pushed into marginal and remote areas, the ability of plant and animal species to adapt becomes increasingly challenged. This has led to the prediction of an ongoing sixth major extinction (Leakey & Lewin, 1995; Millennium Ecosystem Assessment, 2005; Kolbert, 2014). Simultaneously, the Anthropocene generates new opportunities, in the form of the appearance of ‘hybrid’ new habitats as a consequence of shifting climate patterns and the introduction of new species (Woodruff, 2001). For instance, in a clade of partially-interfertile red oak species arranged parapatrically across an environmental gradient (shown in Cavender-Bares, 2019), the aboveground and belowground selection pressures will likely differ following climate change: a much more direct and immediate impact is expected on aboveground traits while belowground traits, particularly those largely dependent on soil structure and fertility and not drainage, would change more slowly (Fig. 1). These dynamics would generate novel combinations and varying pressures for gene flow among the species. The profound modification of extant habitats over the coming decades, along with the appearance of novel anthropogenic and spatially-heterogeneous habitats, will present both planted and spontaneous vegetation with a wide range of challenging environmental conditions.
What will tree species become in the Anthropocene? Given the prospects of rapid, unpredictable and unprecedented change, the attempt to preserve current genetic and phenotypic composition and integrity of species has its risks (McLachlan et al., 2007; Richards & Hobbs, 2015). Examination of species extinction patterns during previous major extinction events indicate that plants experience these massive global events differently than animals (Cascales-Miñana & Cleal, 2014). While Earth lost the vast majority of the dominant lineage of terrestrial vertebrates, the dinosaur, at the last major extinction, no major lineage of plants became extinct. In fact, extinction rates in flowering plants did not significantly change at the Cretaceous–Paleogene boundary and speciation may have actually accelerated (Silvestro et al., 2015). At first sight, trees would seem particularly vulnerable to sudden shifts in climate, given their slow macro-evolutionary dynamics and protracted life history strategies (Petit & Hampe, 2006; Webb et al., 2008; Alberto et al., 2013), but this could be balanced by their large population sizes and prodigious reproductive capacity, allowing rapid adaptation and great plasticity. In fact, the dramatic glacial cycles over the past two millions years have had relatively little impact on biogeographic distribution of diversity in trees (Lumibao et al., 2017), particularly in the tropics (Cannon & Manos, 2003). However, over the past few decades, fire and introduced pests and diseases have caused dieback among some tree species, suggesting that trees may be facing a unique set of evolutionary circumstances in the Anthropocene (Karnosky, 1979; Anagnostakis, 1987; Anderson et al., 2004; Guarín & Taylor, 2005; BenDor et al., 2006; Dolanc et al., 2014). More generally, the Anthropocene will involve a global biotic homogenization of habitats and communities (McKinney & Lockwood, 1999), which will likely drive similar homogenization effects on biological diversity.
Assisted diversification
Given the rather daunting future presented by the trends and predictions for the Anthropocene, we need to consider all of the tools and resources at our disposal to maintain the adaptive capacity of our ecosystems and their biological diversity (Ralls et al., 2018). As argued by Hamilton & Miller (2016) and Suarez-Gonzalez et al. (2018), interspecific gene flow represents an underutilized management option to conserve evolutionary potential in a changing environment. Placing introgression in the context of networks of genetically interacting species will provide insight into how the multi-dimensionality of these exchanges might lead to broad adaptations during periods of rapid change. Specifically, the acceleration of the rate of environmental changes in the Anthropocene suggests that organisms will require a concomitant acceleration of diversification, despite general trends towards homogenization. Detailed knowledge, empirical and theoretical, about genetic exchanges among large suites of tree species would facilitate the maintenance of overall diversity through controlled crossing programs. We need to adopt a systems approach to understand the full potential of the syngameon and the potential emergent nonadditive effects generated by a network of multiple species linked by gene flow. Such species can be said to co-evolve, not only because they come to occupy different complementary ecological niches but also because each can be a source of innovations for the others through introgression so that their fate is intimately linked.
The genomic resources now available for the oaks and for other tree groups will allow us to gain the high-resolution and detailed knowledge of genomic evolution necessary to understand and potentially utilize the evolutionary flexibility offered by the syngameon (Grabenstein & Taylor, 2018). We know that genes which resist introgression in the European white oak complex belong to three main categories: (1) those relating to ecological preferences of each species, namely drought and cold tolerance and adaptation to alkaline soils; (2) those involved in biotic interactions, such as immune response, resistance to biotic stress, and ecto-mycorrhizal associations; and (3) those related to intrinsic barriers, relating to phenology, pollen recognition and growth, and embryo development (Leroy et al., 2020). We are likely to learn that the current genome is not a faithful reflection of current environmental pressures but much more of a palimpsest with faint impressions of past histories and partially legible mysteries (McVay et al., 2017). The oaks provide an ideal model system for detailed study of these questions (Cavender-Bares, 2019).
The question will be how to strike the balance between assisting species to accelerate their diversification with the threats of outbreeding depression (Frankham et al., 2011) and genetic erosion (Rhymer & Simberloff, 1996). We would first propose to revise regulations enforcing species purity of forest reproductive material, to preserve and even increase intraspecific and interspecific variation in future tree communities. Second, we suggest that carefully controlled and managed crossing experiments be conducted for well-studied groups of trees, like the oaks, that naturally participate in syngameons. Using genomic tools and markers like those now available for the oak genome, a targeted approach to introgression can be pursued and the resulting offspring could be screened before planting, especially in existing novel nonanalog environments of the Anthropocene, such as in urban environments. This would allow us to select the widest variety of genotypes with careful monitoring and observation of the resulting phenotypes to understand the genomic interaction among the parental species. While the identification of gene–trait associations for specific characteristics like drought tolerance will be important, our ability to choose the specific winners in the future will be limited, given our inability to predict the ultimate outcome in environmental conditions. Hence allowing local natural selection pressures to choose among successful phenotypes appears as a more effective approach. Such a strategy could be compared with the traditional one where selection within species for material adapted to the new expected environmental conditions is performed.
These types of experiments would allow us to determine which traits are particularly conducive to introgression and to adaptation to the new conditions. Endangered species could be exposed to hybridization and introgression through controlled and episodic programs to assess the tradeoffs between outbreeding depression and adaptive introgression. While controversial, the assisted diversification idea has fewer risks, is easier to control, and has fewer collateral effects than assisted migration (Camacho et al., 2010). Botanic gardens are an ideal place for these controlled experiments, as they are well-positioned to build on past experiences with invasive species and are prepared to explore the risks of releasing new genotypes in nature. The oaks, and more broadly the Fagaceae, are an excellent model system to study the action of the syngameon and its potential uses for conservation and management purposes across continents and biomes (Cannon et al., 2018). Although many questions remain to be addressed, the evidence summarized throughout this article suggests that focusing on the syngameon and developing an understanding of how networks of species interact genetically, rather than focusing on each species independently, could help understand and promote adaption to the rapidly changing environments of the Anthropocene. Research focused on detangling the many possible implications will provide insight and potentially the ability to utilize the syngameon for conservation and management purposes.
Acknowledgements
CHC was funded by the Center for Tree Science at the Morton Arboretum with support from the Hamill Family Foundation. RJP was funded by INRA, by Agence Nationale de la Recherche, Grant/Award Number: ANR-10-LABX-25-01, and by Région Nouvelle Aquitaine (project TrackNat 2015-1R20301-00005174). Jeannine Cavender-Bares, Christian Lexer and two anonymous reviewers contributed valuable improvements for this article.
Author contributions
CHC formulated the concept for the article. CHC and RJP developed the interpretation and wrote the manuscript.
