The oak syngameon: more than the sum of its parts

Abstract

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.

Oaks: an evolutionary success story

“…The same general finding results from analysis of larger numbers of individuals in closely related species groups, for example the oaks of section Virentes (Cavender‐Bares et al , ; Eaton et al , ), section Protobalanus (Ortego et al , ), the eastern North American white oaks (Hipp et al , ), and the California scrub white oaks (Fitz‐Gibbon et al , ) and red oaks (Hauser et al , ). Macroevolutionary studies demonstrate with broad species sampling that regional assemblages of related oak species are true syngameons, ‘good species’ in spite of a long history of introgression (Hardin ; Cannon & Petit, ).…”

“…By the same token, macroevolution shapes microevolution, providing the backdrop of lineage diversity against which introgression, maintenance of genetic variation within species, adaptation, genetic drift and other population‐level processes play out. The high lineage diversity of oaks allows them to benefit from potentially adaptive multispecies introgression (Baranski, ; Hardin, ; Curtu et al , ; Peñaloza‐Ramírez et al , ; Lepais & Gerber, ; Eaton et al , ; Cannon & Petit, ). At the same time, trait divergence among species within clades enables close relatives to diverge ecologically and occupy a wide range of habitats, enabling high regional diversity among habitats (Cavender‐Bares et al , , ), while among‐clade convergence in habitat and climatic niche (Cavender‐Bares et al , ; Hipp et al , ) and differentiation in ecosystem functions among clades (González‐Rodríguez et al , ) allow distantly related oaks to co‐occur, enabling high local diversity.…”

Genomic landscape of the global oak phylogeny

“…The botanical and evolutionary literature is rife with case studies of localized gene flow (Hardin, ; Whittemore & Schaal, ; McVay et al ., 2017a; Kim et al ., ) and ancient introgression (McVay et al ., 2017b; Kim et al ., ; Crowl et al ., ) in oaks. Oaks have in fact been held up as a paradigmatic syngameon (Hardin, ; Van Valen, ; Dodd & Afzal‐Rafii, ; Cannon & Scher, ; Boecklen, ; Cannon & Petit, ), a system of interbreeding species in which incomplete reproductive isolation may facilitate adaptive gene flow and species migration (Petit et al ., ; Dodd & Afzal‐Rafii, ; Leroy et al ., ). The oak genome (Plomion et al ., ) consequently tracks numerous unique species‐level phylogenetic histories that result from lineage sorting and differential rates of introgression (Anderson, ; Eaton et al ., ; McVay et al ., 2017b; Edelman et al ., ).…”

Oak genomics is proving its worth

“…This contrast between the well‐defined phylogeny and the genomic heterogeneity of speciation strongly suggests that oaks have evolved through repeated hybridization in response to ecological opportunities. In light of this complex evolutionary history, more appropriate conservation strategies can be considered, as further discussed in the Viewpoint article by Cannon & Petit (in this issue of New Phytologist , pp. 978–983).…”

“…The forward‐looking Viewpoint featured in this issue by Cannon & Petit (pp. 978–983) lays out a roadmap for the development of ‘adaptive conservation strategies’ in oaks to help overcome the adaptive constraints of such long‐lived sessile organisms.…”