Next Article in Journal
Characteristic Value of the Modulus of Elasticity (MOE) for Natural and Planted Larch in Northeast China
Next Article in Special Issue
Quercus Genetics: Insights into the Past, Present, and Future of Oaks
Previous Article in Journal
How to Evaluate Downed Fine Woody Debris Including Logging Residues?
Previous Article in Special Issue
Geographical Structuring of Quercus robur (L.) Chloroplast DNA Haplotypes in Lithuania: Recolonization, Adaptation, or Overexploitation Effects?
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 12
Issue 7
10.3390/f12070882
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Quercus Conservation Genetics and Genomics: Past, Present, and Future

by
Janet R. Backs
* and
Mary V. Ashley
Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USA
*
Author to whom correspondence should be addressed.
Forests 2021, 12(7), 882; https://0-doi-org.brum.beds.ac.uk/10.3390/f12070882
Submission received: 1 May 2021 / Revised: 15 June 2021 / Accepted: 30 June 2021 / Published: 6 July 2021
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
Versions Notes

Abstract

:
Quercus species (oaks) have been an integral part of the landscape in the northern hemisphere for millions of years. Their ability to adapt and spread across different environments and their contributions to many ecosystem services is well documented. Human activity has placed many oak species in peril by eliminating or adversely modifying habitats through exploitative land usage and by practices that have exacerbated climate change. The goal of this review is to compile a list of oak species of conservation concern, evaluate the genetic data that is available for these species, and to highlight the gaps that exist. We compiled a list of 124 Oaks of Concern based on the Red List of Oaks 2020 and the Conservation Gap Analysis for Native U.S. Oaks and their evaluations of each species. Of these, 57% have been the subject of some genetic analysis, but for most threatened species (72%), the only genetic analysis was done as part of a phylogenetic study. While nearly half (49%) of published genetic studies involved population genetic analysis, only 16 species of concern (13%) have been the subject of these studies. This is a critical gap considering that analysis of intraspecific genetic variability and genetic structure are essential for designing conservation management strategies. We review the published population genetic studies to highlight their application to conservation. Finally, we discuss future directions in Quercus conservation genetics and genomics.

1. Introduction

Oaks have evolved and adapted over the past 56 million years [1]. Their success has been attributed to high genetic diversity, rapid migration and adaptability, and their propensity for hybridization and introgression [2]. While the ecosystem services oaks provide support a multitude of species, humans in particular have interacted and benefited directly from oaks over many millennia. Acorns of Quercus ithaburensis and Q. caliprinos, identified by charcoal analysis, have been associated with early humans from 65,000–48,000 years ago and were likely included in their diet [3]. Oak wood, bark, leaves, and roots, as well as acorns, are part of traditional medicine in many parts of the world, and continue to be used as medicinal remedies [4,5,6,7]. Oaks figure in human folklore and culture [8] and have been perceived as sacred in numerous human societies [9]. Because of their abundance and high biomass they sequester carbon and so contribute to climate regulation [10]. Genomic studies are now illuminating the genetic basis behind humans’ representation of oaks as symbolic of ‘longevity, cohesiveness, and robustness’ [11]. While this paper focuses on the species that have been adversely impacted by humans, the long relationship between humans and oaks has also had a positive effect on many species [2]. For example, fire regimes that have been used over human history to control undergrowth and enhance hunting areas have benefited oaks through reduced competition with understory vegetation and more shade-tolerant trees in the open areas maintained by such fires [12,13,14]. However, we are currently living in a time when many oak species are in danger.
The exact number of species in the genus Quercus is still open to clarification, as new species continue to be discovered in oak hot-spots such as Mexico/Central America and China/Southeast Asia. Recent estimates are that approximately 430–435 differentiated species exist [2,15,16]. Oaks occur across the Northern Hemisphere from the equator to boreal regions and thrive in elevations from sea level to 4000 m on various soil types from alkaline to acidic. Species richness is especially high in North America and Asia, where oaks have adapted (and speciated) in response to varying ecological niches [2]. Some oaks, such as Q. hinckleyi, are as small as one meter at maturity and grow as clumps of long-lived clones. More familiar to most are large trees that dominate the landscape and live for hundreds of years, such as Quercus macrocarpa, Q. petraea and Q. robur. They can also be extremely rare and critically threatened (Q. hinckleyi [17,18]) or abundant with wide-spread distributions, like the other species just mentioned.
Effective conservation management benefits from genetic data to clarify species’ identity and adaptations and to provide information on intraspecific diversity and population structure. Unfortunately, missing or incomplete genetic information limits comprehensive planning for many threatened oak species. A survey of conservation actions conducted as part of the Conservation Gap Analysis of Native U.S. Oaks [19] (hereafter Gap Analysis) found that genetic research was one of the least reported efforts, highlighting the need for genetic investigations for many oak species. Specific genetic gaps are seen for phylogenetics/taxonomy to clarify evolutionary significant units (ESU) and for population genetics to address diversity, gene flow, and hybridization/introgression. These findings motivated our effort here to evaluate the state of Quercus conservation genetics.

2. Developing a List of Oaks of Concern

For our review of the status of oak conservation genetics, we combine findings from The Red List of Oaks 2020 [16] (hereafter Red List) and the Gap Analysis to create a list of global species of concern. The Red List assessed 430 Quercus species. Species were evaluated based on current and projected population sizes, geographic range/endemism, population decline, and fragmentation. While the majority of oak species are not threatened, the study found that 41% are ‘species of conservation concern’ with 112 falling into the IUCN Threatened Categories: Critically Endangered (CR), Endangered (EN), or Vulnerable (VU) (see p. 9 and Appendix A in [16]) for descriptions and criteria of the IUCN categories. We use this list of species in our review. An additional 105 species are categorized as Near Threatened (NT) or Data Deficient (DD). If DD species are included in the analysis’ calculations, the report estimates that globally 31% of oaks are in danger of extinction [16]; we did not include these additional 105 species in our literature review since few have been the subject of genetic studies.
The Red List identifies the U.S. as one of the areas with the highest number of threatened oaks, so we incorporated additional information from a detailed report on U.S. oaks, the Gap Analysis [19]. The Gap Analysis found that 31% of native U.S. oak species are ‘species of concern’ based on an assessment of data reported in The Red List of Oaks 2017 [20], the NatureServe conservation rankings [21], the USDA Forest Service risk assessment of vulnerability to climate change [22], and a survey of ex situ collections conducted as part of the gap report itself. Evaluation focused on risks of extinction, susceptibility to the effects of climate change, and presence of species in ex situ collections and considered both current and near-term threats. In addition to the criteria used in the Red List, the Gap Analysis looked at regeneration/recruitment and genetic variation/species integrity. Based on these criteria, it scored each species’ level of vulnerability. Results show 28 U.S. oak species are ‘species of concern’, including 12 species not included in the Red List that we added to our list of ‘Oaks of Concern’. Our combined list of threatened species is shown in Table 1 and contains 124 species.
The countries with the highest numbers of threatened oak species are China with 36, Mexico with 32, and the United States with 28. Not surprisingly these are the three countries with the highest oak species richness. Other regions of concern are Viet Nam with 20 threatened oak species and Malaysia with nine. Chinese, Mexican, and Vietnamese oaks are mainly threatened by loss of habitat due to logging, agriculture, and urbanization, while in the United States, climate change and invasive species are the major concerns [16].

3. Genetic Research on Oaks of Concern

We used citations in the Red List, the Gap Analysis, Google Scholar Searches (filtering on species name and the word ‘genetics’ for a date range of 2000 to present), and citations contained within these studies, to identify genetic studies that have been conducted on the species on our list, with the caveat that the results represent a ‘point in time’ and that new research is constantly being added, may not yet be published, or was not found by this search protocol. Citations to genetic studies are included in Table 1.
We found a total of 78 references that included analysis of one or more species on the list. We classified each of the cited papers by the main focus of the research: phylogeny/taxonomy (PT), population genetics (PG), conservation (CON), genome assembly (G), and genomic methods (GENOM). Of the 124 species, 71 (57%) had one or more published research papers involving a genetic study. Quercus sections with the highest numbers of listed species are Cyclobalanopsis, Lobatae, and Quercus. Of the Oaks of Concern in each of these sections, 24 of 55 (44%) of Cyclobalanopsis, 15 of 30 (50%) of Lobatae, and 16 of 21 (76%) of Quercus taxa have cited genetic research.
Of the published genetic papers, 24 of 78 (31%) are phylogeny/taxonomy related (PT) with a number dealing with macroevolution of the Quercus genus (such as [1,28]), while others focus on phylogenies within Quercus sections (such as [23,40,41,61]), and still others look at regional phylogenies (such as [30,33,34,46,47,48,56,58,59,88,91]). It is notable that for 51 of the 71 (72%) species with cited works, the only genetic research was phylogeny/taxonomy related (see Table 1). The rise of genomic analysis in phylogenetics over the last few years (phylogenomics [99]) has provided better tools for clarifying enigmatic relationships within Quercus. In particular, with the application of RAD-seq methods, it has been possible to use tens of thousands of genetic markers to get good phylogenetic signal and provide insights into the evolutionary diversification of the Quercus genus [1,2]. Phylogenetic research is important in delineating conservation units (ESUs), a critical component in establishing a starting point for conservation planning. Phylogenetics/phylogenomics has been used to answer many questions about Oaks of Concern, such as confirming species’ identity and addressing introgression. Additionally, many of these papers include other pertinent data relating to conservation, for example, to hybridization and biogeography. While elucidating the evolutionary history of oaks is certainly an important endeavor, direct implications of phylogenetic reconstruction for conservation management are limited. Most phylogenetic studies include only one or a very few representatives of each species, so provide little insight into many issues most pertinent to conservation management.

4. Population Genetics for Oaks of Concern

We found that a critical area of conservation research, population genetics studies (PG), are missing for the vast majority of Oaks of Concern. Population genetics studies assess intraspecific genetic diversity and population structure and form the foundation of the field of conservation genetics. While we found 39 of 78 (50%) papers focused on population genetic (PG) questions, only 16 different species were investigated in these papers (Table 2), leaving 87% of the species with no information on intraspecific diversity. Five papers examined specific conservation (CON) questions, such as ex situ conservation [100], habitat destruction [93], and genetics as input to conservation planning in response to climate change [73,76,85]. Five dealt with genomic methods (GENOM) such as epigenetics [79,80,86], ecological niche modeling [84], and landscape genomics [81].
While it is discouraging that only 16 Oaks of Concern have population genetics (PG) related citations (Table 2), these studies provide important examples of the work that has been done, as well as highlighting the somewhat limited breadth of the population genetics research for endangered oaks to date. Of those species that have been studied using population genetic approaches, twelve are in Mexico or the U.S., three in China or Southeast Asia, and one in North Africa. China has the largest number of threatened species on our Oaks of Concern list (36), but only a handful of species have been studied (Table 1) and only three have been the subject of population genetic research (Table 2). These three species are members of the Cyclobalanopsis section occurring in Southeast Asia. Quercus arbutifolia is an Endangered species found in the mountain cloud forests of southern China and Viet Nam. Xu et al. [29], used chloroplast (cpDNA) and nuclear (ITS) DNA sequences to examine Q. arbutifolia’s genetic diversity, phylogeographic structure, and evolutionary history. The authors acknowledge the highly threatened status of this species, but highlight how their findings on genetic diversity, which they found to be unexpectedly high, and population dynamics are critical to developing effective conservation plans. Quercus austrocochinchinensis is a Vulnerable species found in China, The Lao People’s Democratic Republic, Thailand, and Viet Nam. It is referenced in six genetic research papers, but only one population genetics paper. Possible hybridization between Q. austrocochinchinensis and a sympatric species, Q. kerrii, was investigated using AFLP markers and nu-SSRs, providing information for long-term conservation and restoration of the tropical ravine rainforest environment in the Indo-China area [31]. Quercus bambusifolia is an Endangered species found in China, Hong Kong, and Viet Nam. Using population genetics analyses of nu-SSR data, Zeng et al. [35,36] examined inbreeding, genetic diversity, and population structure, and provide data applicable to restoration of severely fragmented tropical landscapes.
The only North African species on our list of Oaks of Concern is Q. afares, the African Oak, a Vulnerable species with a limited distribution in the coastal mountains of Algeria and Tunisia. With genetic analysis using nuclear allozymes and chloroplast markers, Mir et al. [24] confirmed its identity as a stable hybrid of two sympatric but phylogenetically distant species, Q. suber and Q. canariensis. Q. afarensis combines traits of these two species, suggesting one or more hybridization events.
Quercus mulleri (section Lobatae) is a microendemic oak found in the Sierra Sur de Oaxaca of Mexico. In the first report on this species since it was identified 60 years ago, a population genetics study (PG) examined genetic diversity and population structure using nu-SSRs with the goal of providing information to enhance conservation strategies [87].
The western United Sates, particularly California, has been the focus of numerous studies of oak population genetics, including several studies of Oaks of Concern. Quercus dumosa is an endangered oak (section Quercus) found in Baja California, Mexico, and California. Three population genetics studies (PG) examined genetic exchange between this species and its close relatives. One study focused on the influence of environmental gradients using RAD-seq [42], another examined introgression and species’ integrity related to neighboring species using nu-SSR [43], and a third examined genetic differentiation and population structure to examine evolutionary history of sympatric species using nu-SSR [45]. Quercus engelmanii is also an endangered species distributed in Baja California, Mexico and southern California, US. Population genetic studies have examined responses to geography and climate [49], ecological niche modeling [50], and hybridization/introgression using RNA-seq [51].
Valley oak, Q. lobata, a California endemic listed as Near Threatened, is by far the most thoroughly investigated species on our list. Seven papers report on phylogeny/taxonomy [1,28,44,61,62,71,83], one paper reports on genome assembly [62], and five (including one in this special edition [86]) investigate new genomic methods 79–81,84,86]. A number of population genetic papers have also focused on Q. lobata. Several studies have investigated gene flow, hybridization, and population structure [46,65,67,68,69,70,72,74,75,77,78]. One study used whole-transcriptome sequencing (mRNA-Seq) to investigate sequence variation with climate gradients [60] and another looked at geographic patterns of genetic variation in relation to climate change using chloroplast and nu-SSRs [63]. Drought response was measured using ecophysiological traits and gene expression (RNA-seq) [64]. A common garden experiment and genome-wide sequencing were used to examine adaptational lag to temperature, with potential application to identifying genotypes preadapted to future climate change conditions [66]. Valley oak provides a model of how different genetic approaches can be used to investigate the ecological and evolutionary genetics of a threatened tree species, predict future trends, and assist in developing strategies to manage the risks a species is facing.
Two species of oaks on our list are endemic to the California Channel Islands, Q. pacifica and Q. tomentella. Quercus pacifica is an Endangered species, and researchers have investigated gene flow, population structure, and relationships to two mainland oaks using nu-SSRs [43] and evolutionary history and demographics using nu-SSRs and cpSSRs [45]. Quercus tomentella, also listed as Endangered, is a member of the small section Protobalanus. Population genetics papers cover genetic variation and population structure [94], landscape and conservation genetics [95] and genetic variation and population structure [96] all using nu-SSRs. Another species, Quercus parvula is found on Santa Cruz Island and in the California Coast Ranges and is classified as Near Threatened. Two population genetics papers report on genetic differentiation and introgression [89] and species differentiation [90], both using AFLP genetic markers.
Quercus hinckleyi is a Critically Endangered species with an extremely limited distribution in Texas, USA. Population genetic studies have examined clonality, diversity and population structure [18], hybridization [55], and genetic diversity assessment of in situ and ex situ populations [54]. Important for conservation, Backs et al. [18] reported a high level of clonality at some sites, with the number of genetically unique individuals being substantially lower than previously assumed from population counts.
The other Oaks of Concern that have had population genetic studies are primarily in the Eastern United States. One paper in this Special Issue examines genetic diversity and population structure in the Endangered Q. havardii [53]. Another paper in this Special Issue conducted population assessments of three Oaks of Concern, Q. georgiana, Q. oglethorpensis, and Q. boyntonii, and reports that these species have lower genetic diversity than more abundant oaks [39]. Another paper covers genetic diversity and population structure of Q. georgiana using EST-SSRs [52].
One question recently explored for several North America species is how well the genetic diversity of the species is captured in ex situ collections. Oak seeds (acorns) are not candidates for seed banks; they lose viability when desiccated. Desiccation is part of the standard protocol of conventional seed-banking [101,102,103,104]. Conservation of living oaks in ex situ collections can be constrained by space limitations, long generation times, and their proclivity to hybridize [54]. A recent paper by Backs et al. [54] reported that ex situ collections of Q. hinckleyi were likely sampled from only one of the remaining in situ genetic clusters and missed much of the in situ diversity. The study of Quercus georgiana, Q. oglethorpensis, and Q. boyntonii mentioned above reports that while common alleles are well preserved in ex situ collection, low frequency and rare alleles are not [39].
For many other species on our Oaks of Concern list, there are immediate questions that can be addressed through genetic and/or genomic analysis, such as confirming taxa, identifying clones, examining levels of diversity, and measuring gene flow [105]. Quercus tardifolia, is a good example. It is described as Data Deficient, requiring both field research and taxonomic clarification and lacking demographic data and diversity information [19]. Other species of concern are not so lacking in information, but still have genetic gaps in their conservation portfolios. Quercus robusta needs research to distinguish spontaneous hybrids from historic hybrids that have evolved into true species [106]. For Q. acerifolia, there is a need to identify genetic structure of populations [107] and for Q. carmenensis there is a need to verify species integrity and/or levels of introgression [108].
To summarize, our survey of genetic studies shows that while some Oaks of Concern have benefited from population genetic research, most are lacking basic conservation-focused data. This need can be addressed through population genetic analysis looking at species integrity, intraspecific diversity, population structure, gene flow, hybridization levels, and diversity capture in ex situ collections. Only with this information can comprehensive conservation strategies be developed.

5. Future Directions

Some exciting new genetic methods that have application to conservation questions can be characterized as ‘genomic research’. The ability to look across an entire oak genome or use ‘reduced representation’ genome sampling has been made possible in recent years by advances in DNA sequencing as well as through better ‘big data’ manipulation due to increased computing power, storage capabilities, and robust analytic applications. A sampling of genomic research that has been directed toward oak conservation includes phylogenomics [83], epigenetics [80], QTL (quantitative trait loci) [109], and landscape genomics [110]. While phylogenomics provides a broad evolutionary picture of oaks and helps define ESU’s, epigenetics, QTL, and landscape genomics have the potential to investigate the genomic basis of adaptive traits and apply this knowledge to developing conservation strategies for Oaks of Concern. These new genomic research methods will provide information on plant and species adaptive responses, data needed for flexible conservation efforts that may include plant migration and/or reintroduction.
Epigenetics is the study of heritable phenotypic changes in an organism that do not involve alterations in the DNA code itself. It is emerging as an important field of research for understanding plant adaptability and plasticity and for identifying the ‘ecological background’ of individuals [111]. The shortfall in oak-related research in these areas is exemplified by a survey of epigenetic research which found of approximately 20,000 epigenetic studies published in 2019, only 3% of the papers were plant-related, and of those only 5% focused on forest species [112]. Of tree-related papers, only a handful reference Quercus species, for example, [80,113,114].
Epigenetic modification can be created by biotic or abiotic environmental stresses, stochastic “epigenetic mutations” [111,115] or natural processes such as hybridization [116]. They can be reset when a stress is relieved or may result in heritable epigenetic marks that can be passed on as ‘molecular memory’ persisting through several subsequent generations and potentially becoming evolutionarily viable [116,117,118]. Oaks as long lived organisms have the time to enhance their epigenetic responses through a number of stressful events before passing along these responses through their germlines [119]. Some work has been done with oaks and epigenetics [114,120] including a paper in this Special Issue that examines experimental DNA methylation using the Near Threatened Q. lobata [86]. This is an area of conservation interest that should be explored both for planning conservation strategies and basic research into underlying adaptive mechanisms.
Current data processing capabilities have also made it possible to search genome-wide for QTL (quantitative trait loci) [109]. QTL mapping seeks to identify the relationship between various genomic locations and a set of quantitative traits, leading to a chromosomal location and ultimately to identification of gene(s) with the final goal of looking at gene expression. Among other things, this will lead to a better understanding of genetic mechanisms of variation and adaptation [121]. Results can then be applied to adjust conservation measures in response to rapid change, for example, by identifying the genetic adaptability potential of individuals to be used in assisted migration or reintroduction [122,123].
Landscape genomics examines the relationship and interaction between adaptive genetic loci on genomes and landscape variations across which natural populations exist [110]. It seeks to identify the aspects of the environment that affect genetic variation and how that variation in turn affects adaptation [124,125]. It is a valuable tool in understanding oaks’ responses to environmental stresses and evaluating alleles that occur under certain climate and habitat conditions. These correlations will aid in conservation planning for plant migration or restoration by identifying populations or individuals that are currently responding favorably to conditions that are anticipated in the climatic future [81,126,127].
These emerging genomic tools as well as more traditional population genetic analyses can and should provide vital input to developing effective oak conservation strategies. Our review highlighted important gaps in our knowledge of many species that are or may soon be facing extinction. For geneticists, there is much work and many opportunities to address conservation needs of the Oaks of Concern.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hipp, A.L.; Manos, P.S.; Hahn, M.; Avishai, M.; Bodénès, C.; Cavender-Bares, J.; Crowl, A.A.; Deng, M.; Denk, T.; Fitz-Gibbon, S.; et al. Genomic landscape of the global oak phylogeny. New Phytol. 2020, 226, 1198–1212. [Google Scholar] [CrossRef]
  2. Kremer, A.; Hipp, A.L. Oaks: An evolutionary success story. New Phytol. 2020, 226, 987–1011. [Google Scholar] [CrossRef]
  3. Lev, E.; Kislev, M.E.; Bar-Yosef, O. Mousterian vegetal food in Kebara Cave, Mt. Carmel. J. Archaeol. Sci. 2005, 32, 475–484. [Google Scholar] [CrossRef]
  4. Morales, D. Oak trees (Quercus spp.) as a source of extracts with biological activities: A narrative review. Trends Food Sci. Technol. 2021, 109, 116–125. [Google Scholar] [CrossRef]
  5. Lev, E.; Amar, Z. Ethnopharmacological survey of traditional drugs sold in Israel at the end of the 20th century. J. Ethnopharmacol. 2000, 72, 191–205. [Google Scholar] [CrossRef]
  6. Guha, B.; Arman, M.; Islam, M.N.; Tareq, S.M.; Rahman, M.M.; Sakib, S.A.; Mutsuddy, R.; Tareq, A.M.; Emran, T.B.; Alqahtani, A.M. Unveiling pharmacological studies provide new insights on Mangifera longipes and Quercus gomeziana. Saudi J. Biol. Sci. 2021, 28, 183–190. [Google Scholar] [CrossRef] [PubMed]
  7. Xu, J.; Fu, C.; Li, T.; Xia, X.; Zhang, H.; Wang, X.; Zhao, Y. Protective effect of acorn (Quercus liaotungensis Koidz) on streptozotocin-damaged MIN6 cells and type 2 diabetic rats via p38 MAPK/Nrf2/HO-1 pathway. J. Ethnopharmacol. 2021, 266, 113444. [Google Scholar] [CrossRef] [PubMed]
  8. Logan, W.B. Oak: The Frame of Civilization; WW Norton & Company: New York, NY, USA, 2005. [Google Scholar]
  9. Altman, N. Sacred Trees; Sierra Club Books: San Francisco, CA, USA, 1994. [Google Scholar]
  10. Cavender-Bares, J. Diversity, distribution and ecosystem services of the North American oaks. Int. Oaks 2016, 27, 37–48. [Google Scholar]
  11. Leroy, T.; Plomion, C.; Kremer, A. Oak symbolism in the light of genomics. New Phytol. 2020, 226, 1012–1017. [Google Scholar] [CrossRef]
  12. Keeley, J.E. Native American impacts on fire regimes of the California coastal ranges. J. Biogeogr. 2002, 29, 303–320. [Google Scholar] [CrossRef]
  13. Barrett, R.D.; Schluter, D. Adaptation from standing genetic variation. Trends Ecol. Evol. 2008, 23, 38–44. [Google Scholar] [CrossRef]
  14. Dey, D.C.; Guyette, R.P. Anthropogenic fire history and red oak forests in south-central Ontario. For. Chron. 2000, 76, 339–347. [Google Scholar] [CrossRef] [Green Version]
  15. Denk, T.; Grimm, G.W.; Manos, P.S.; Deng, M.; Hipp, A.L. An updated infrageneric classification of the oaks: Review of previous taxonomic schemes and synthesis of evolutionary patterns. In Oaks Physiological Ecology. Exploring the Functional Diversity of Genus Quercus L.; Springer: Cham, Switzerland, 2017; pp. 13–38. [Google Scholar]
  16. Carrero, C.; Jerome, D.; Beckman, E.; Byrne, A.; Coombes, A.J.; Deng, M.; González-Rodríguez, A.; Hoang, V.S.; Khoo, E.; Nguyen, N.; et al. The Red List of Oaks; The Morton Arboretum: Lisle, IL, USA, 2020. [Google Scholar]
  17. Muller, C.H. The signigicance of vegetative reproduction in Quercus. Madroño 1951, 11, 129–137. [Google Scholar]
  18. Backs, J.R.; Terry, M.; Klein, M.; Ashley, M. V Genetic analysis of a rare isolated species: A tough little West Texas oak, Quercus hinckleyi CH Mull. J. Torrey Bot. Soc. 2015, 142, 302–313. [Google Scholar] [CrossRef]
  19. Beckman, E.; Meyer, A.; Denvir, A.; Gill, D.; Man, G.; Pivorunas, D.; Shaw, K.; Westwood, M. Conservation Gap Analysis of Native U.S. Oaks.; The Morton Arboretum: Lisle, IL, USA, 2019. [Google Scholar]
  20. Jerome, D.; Beckman, E.; Kenny, L.; Wenzell, K.; Kua, C.; Westwood, M. The Red List of US Oaks; Morton Arboretum: Lisle, IL, USA, 2017. [Google Scholar]
  21. Frances, A. NatureServe and Native Plant Conservation in North America; Ormsby, A., Leopold, S., Eds.; NatureServe: Arlington, VA, USA, 2017. [Google Scholar]
  22. Potter, K.M.; Crane, B.S.; Hargrove, W.W. A United States national prioritization framework for tree species vulnerability to climate change. New For. 2017, 48, 275–300. [Google Scholar] [CrossRef]
  23. Vázquez, M.L. Molecular evolution of the internal transcribed spacers in red oaks (Quercus sect. Lobatae). Comput. Biol. Chem. 2019, 83, 107117. [Google Scholar] [CrossRef]
  24. Mir, C.; Toumi, L.; Jarne, P.; Sarda, V.; Di Giusto, F.; Lumaret, R. Endemic North African Quercus afares Pomel originates from hybridisation between two genetically very distant oak species (Q. suber L. and Q. canariensis Willd.): Evidence from nuclear and cytoplasmic markers. Heredity 2006, 96, 175–184. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Denk, T.; Grimm, G.W. The oaks of western Eurasia: Traditional classifications and evidence from two nuclear markers. Taxon 2010, 59, 351–366. [Google Scholar] [CrossRef]
  26. Sakka, H.; Baraket, G.; Abdessemad, A.; Tounsi, K.; Ksontini, M.; Salhi-Hannachi, A. Molecular phylogeny and genetic diversity of Tunisian Quercus species using chloroplast DNA CAPS markers. Biochem. Syst. Ecol. 2015, 60, 258–265. [Google Scholar] [CrossRef]
  27. Simeone, M.C.; Cardoni, S.; Piredda, R.; Imperatori, F.; Avishai, M.; Grimm, G.W.; Denk, T. Comparative systematics and phylogeography of Quercus Section Cerris in western Eurasia: Inferences from plastid and nuclear DNA variation. PeerJ 2018, 6, e5793. [Google Scholar] [CrossRef] [Green Version]
  28. McVay, J.D.; Hipp, A.L.; Manos, P.S. A genetic legacy of introgression confounds phylogeny and biogeography in oaks. Proc. R. Soc. Lond. B Biol. Sci. 2017, 284, 20170300. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  29. Xu, J.; Jiang, X.-L.; Deng, M.; Westwood, M.; Song, Y.-G.; Zheng, S.-S. Conservation genetics of rare trees restricted to subtropical montane cloud forests in southern China: A case study from Quercus arbutifolia (Fagaceae). Tree Genet. Genomes 2016, 12, 1. [Google Scholar] [CrossRef]
  30. Deng, M.; Jiang, X.L.; Hipp, A.L.; Manos, P.S.; Hahn, M. Phylogeny and biogeography of East Asian evergreen oaks (Quercus section Cyclobalanopsis; Fagaceae): Insights into the Cenozoic history of evergreen broad-leaved forests in subtropical Asia. Mol. Phylogenet. Evol. 2018, 119, 170–181. [Google Scholar] [CrossRef] [PubMed]
  31. An, M.; Deng, M.; Zheng, S.-S.; Jiang, X.-L.; Song, Y.-G. Introgression Threatens the Genetic Diversity of Quercus austrocochinchinensis (Fagaceae), an Endangered Oak: A Case Inferred by Molecular Markers. Front. Plant Sci. 2017, 8, 229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. An, M.; Deng, M.; Zheng, S.-S.; Song, Y.-G. De novo transcriptome assembly and development of SSR markers of oaks Quercus austrocochinchinensis and Q. kerrii (Fagaceae). Tree Genet. Genomes 2016, 12, 1. [Google Scholar] [CrossRef]
  33. Binh, H.T.; Ngoc, N.V.; Bon, T.N.; Tagane, S.; Suyama, Y.; Yahara, T. A new species and two new records of Quercus (Fagaceae) from northern Vietnam. PhytoKeys 2018, 92, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Binh, H.T.; Ngoc, N.V.; Tagane, S.; Toyama, H.; Mase, K.; Mitsuyuki, C.; Strijk, J.S.; Suyama, Y.; Yahara, T. A taxonomic study of Quercus langbianensis complex based on morphology and DNA barcodes of classic and next generation sequences. PhytoKeys 2018, 95, 37–70. [Google Scholar] [CrossRef] [Green Version]
  35. Zeng, X.; Fischer, G.A. Using multiple seedlots in restoration planting enhances genetic diversity compared to natural regeneration in fragmented tropical forests. For. Ecol. Manag. 2021, 482, 118819. [Google Scholar] [CrossRef]
  36. Zeng, X.; Fischer, G.A. Wind pollination over 70 years reduces the negative genetic effects of severe forest fragmentation in the tropical oak Quercus bambusifolia. Heredity 2020, 124, 156–169. [Google Scholar] [CrossRef] [PubMed]
  37. Liu, X.; Chang, E.-M.; Liu, J.-F.; Huang, Y.-N.; Wang, Y.; Yao, N.; Jiang, Z.-P. Complete chloroplast genome sequence and phylogenetic analysis of Quercus bawanglingensis Huang, Li et Xing, a vulnerable oak tree in China. Forests 2019, 10, 587. [Google Scholar] [CrossRef] [Green Version]
  38. Hoban, S.; Callicrate, T.; Clark, J.; Deans, S.; Dosman, M.; Fant, J.; Gailing, O.; Havens, K.; Hipp, A.L.; Kadav, P.; et al. Taxonomic similarity does not predict necessary sample size for ex situ conservation: A comparison among five genera. Proc. R. Soc. B 2020, 287, 20200102. [Google Scholar] [CrossRef]
  39. Spence, E.S.; Fant, J.; Gailing, O.; Griffith, M.P.; Havens, K.; Hipp, A.L.; Kadav, P.; Kramer, A.; Thompson, P.; Toppila, R.; et al. Comparing genetic diversity in three threatened oaks. Forests 2021, 12, 561. [Google Scholar] [CrossRef]
  40. Cavender-Bares, J.; González-Rodríguez, A.; Eaton, D.A.R.; Hipp, A.A.L.; Beulke, A.; Manos, P.S. Phylogeny and biogeography of the American live oaks (Quercus subsection Virentes): A genomic and population genetics approach. Mol. Ecol. 2015, 24, 3668–3687. [Google Scholar] [CrossRef] [PubMed]
  41. Manos, P.S.; Doyle, J.J.; Nixon, K.C. Phylogeny, Biogeography, and Processes of Molecular Differentiation in Quercus Subgenus Quercus (Fagaceae). Mol. Phylogenet. Evol. 1999, 12, 333–349. [Google Scholar] [CrossRef] [Green Version]
  42. Burge, D.O.; Parker, V.T.; Mulligan, M.; Sork, V.L. Influence of a climatic gradient on genetic exchange between two oak species. Am. J. Bot. 2019, 106, 864–878. [Google Scholar] [CrossRef] [PubMed]
  43. Backs, J.R.; Ashley, M.V. Evolutionary history and gene flow of an endemic island oak: Quercus pacifica. Am. J. Bot. 2016, 103, 2115–2125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Kim, B.Y.; Wei, X.; Fitz-Gibbon, S.; Lohmueller, K.E.; Ortego, J.; Gugger, P.F.; Sork, V.L. RADseq data reveal ancient, but not pervasive, introgression between Californian tree and scrub oak species (Quercus Fagaceae). Mol. Ecol. 2018, 27, 4556–4571. [Google Scholar] [CrossRef]
  45. Ortego, J.; Noguerales, V.; Gugger, P.F.; Sork, V.L. Evolutionary and demographic history of the Californian scrub white oak species complex: An integrative approach. Mol. Ecol. 2015, 24, 6188–6208. [Google Scholar] [CrossRef] [Green Version]
  46. Sork, V.L.; Riordan, E.; Gugger, P.F.; Fitz-Gibbon, S.; Wei, X.; Ortego, J. Phylogeny and introgression of California scrub white oaks (Quercus section Quercus). Int. Oaks 2016, 27, 61–74. [Google Scholar]
  47. Yang, Y.; Zhu, J.; Feng, L.; Zhou, T.; Bai, G.; Yang, J.; Zhao, G. Plastid genome comparative and phylogenetic analyses of the key genera in Fagaceae: Highlighting the effect of codon composition bias in phylogenetic inference. Front. Plant Sci. 2018, 9, 82. [Google Scholar] [CrossRef]
  48. Yang, Y.; Zhou, T.; Qian, Z.; Zhao, G. Phylogenetic relationships in Chinese oaks (Fagaceae, Quercus): Evidence from plastid genome using low-coverage whole genome sequencing. Genomics 2021, 113, 1438–1447. [Google Scholar] [CrossRef] [PubMed]
  49. Riordan, E.C.; Gugger, P.F.; Ortego, J.; Smith, C.; Gaddis, K.; Thompson, P.; Sork, V.L. Association of genetic and phenotypic variability with geography and climate in three southern California oaks. Am. J. Bot. 2016, 103, 73–85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  50. Ortego, J.; Riordan, E.C.; Gugger, P.F.; Sork, V.L. Influence of environmental heterogeneity on genetic diversity and structure in an endemic southern Californian oak. Mol. Ecol. 2012, 21, 3210–3223. [Google Scholar] [CrossRef] [PubMed]
  51. Oney-Birol, S.; Fitz-Gibbon, S.; Chen, J.-M.; Gugger, P.F.; Sork, V.L. Assessment of shared alleles in drought-associated candidate genes among southern California white oak species (Quercus Quercus). BMC Genet. 2018, 19, 1. [Google Scholar] [CrossRef] [PubMed]
  52. Kadav, P.D. Characterization of Genic Microsatellite Markers (EST-SSRSs) in the Endangered Oak Species Quercus georgiana M.A. Curtis; Michigan Technological University: Houghton, MI, USA, 2017. [Google Scholar]
  53. Zumwalde, B.A.; McCauley, R.A.; Fullinwider, I.J.; Ducket, D.; Spence, E.S.; Hoban, S. Genetic, morphological, and environmental differentiation of an arid-adapted oak with a disjunct distribution. Forests 2021, 12, 465. [Google Scholar] [CrossRef]
  54. Backs, J.R.; Hoban, S.; Ashley, M.V. Genetic diversity assessment of ex situ collections of endangered Quercus hinckleyi. Int. J. Plant Sci. 2021, 182, 220–228. [Google Scholar] [CrossRef]
  55. Backs, J.R.; Terry, M.; Ashley, M.V. Using genetic analysis to evaluate hybridization as a conservation concern for the threatened species Quercus hinckleyi C.H. Muller (Fagaceae). Int. J. Plant Sci. 2016, 177, 122–131. [Google Scholar] [CrossRef]
  56. Kamiya, K.; Harada, K.; Ogino, K.; Clyde, M.M.; Latiff, A.M. Phylogeny and genetic variation of Fagaceae in tropical montane forests. Tropics 2003, 13, 119–125. [Google Scholar] [CrossRef] [Green Version]
  57. Rodríguez-Correa, H.; Oyama, K.; Quesada, M.; Fuchs, E.J.; Quezada, M.; Ferrufino, L.; Valencia-Ávalos, S.; Cascante-Marín, A.; González-Rodríguez, A. Complex phylogeographic patterns indicate Central American origin of two widespread Mesoamerican Quercus (Fagaceae) species. Tree Genet. Genomes 2017, 13, 62. [Google Scholar] [CrossRef]
  58. Jiang, X.; Hipp, A.L.; Deng, M.; Su, T.; Zhou, Z.; Yan, M. East Asian origins of European holly oaks (Quercus section Ilex Loudon) via the Tibet-Himalaya. J. Biogeogr. 2019, 46, 2203–2214. [Google Scholar] [CrossRef]
  59. Douaihy, B.; Saliba, C.; Stephan, J.; Simeone, M.C.; Cardoni, S.; Farhat, P.; Kharrat, M.B.D. Tracking diversity and evolutionary pathways of Lebanese oak taxa through plastome analyses. Bot. Lett. 2020, 167, 315–330. [Google Scholar] [CrossRef]
  60. Gugger, P.F.; Cokus, S.J.; Sork, V.L. Association of transcriptome-wide sequence variation with climate gradients in valley oak (Quercus lobata). Tree Genet. Genomes 2016, 12, 15. [Google Scholar] [CrossRef]
  61. Crowl, A.A.; Manos, P.S.; McVay, J.D.; Lemmon, A.R.; Lemmon, E.M.; Hipp, A.L. Uncovering the genomic signature of ancient introgression between white oak lineages (Quercus). New Phytol. 2020, 226, 1158–1170. [Google Scholar] [CrossRef]
  62. Sork, V.L.; Fitz-Gibbon, S.T.; Puiu, D.; Crepeau, M.; Gugger, P.F.; Sherman, R.; Stevens, K.; Langley, C.H.; Pellegrini, M.; Salzberg, S.L. First draft assembly and annotation of the genome of a California endemic oak Quercus lobata Née (Fagaceae). G3 Genes Genomes Genet. 2016, 6, 3485–3495. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Sork, V.L.; Davis, F.W.; Westfall, R.; Flint, A.; Ikegami, M.; Wang, H.; Grivet, D. Gene movement and genetic association with regional climate gradients in California valley oak (Quercus lobata Née) in the face of climate change. Mol. Ecol. 2010, 19, 3806–3823. [Google Scholar] [CrossRef] [PubMed]
  64. Mead, A.; Peñaloza Ramirez, J.; Bartlett, M.K.; Wright, J.W.; Sack, L.; Sork, V.L. Seedling response to water stress in valley oak (Quercus lobata) is shaped by different gene networks across populations. Mol. Ecol. 2019, 28, 5248–5264. [Google Scholar] [CrossRef]
  65. Ashley, M.V.; Abraham, S.T.; Backs, J.R.; Koenig, W.D. Landscape genetics and population structure in Valley Oak (Quercus lobata Née). Am. J. Bot. 2015, 102, 2124–2131. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Browne, L.; Wright, J.W.; Fitz-Gibbon, S.; Gugger, P.F.; Sork, V.L. Adaptational lag to temperature in valley oak (Quercus lobata) can be mitigated by genome-informed assisted gene flow. Proc. Natl. Acad. Sci. USA 2019, 116, 25179–25185. [Google Scholar] [CrossRef] [Green Version]
  67. Dutech, C.; Sork, V.L.; Irwin, A.J.; Smouse, P.E.; Davis, F.W. Gene flow and fine-scale genetic structure in a wind-pollinated tree species, Quercus lobata (Fagaceaee). Am. J. Bot. 2005, 92, 252–261. [Google Scholar] [CrossRef]
  68. Abraham, S.; Zaya, D.; Koenig, W.; Ashley, M. Interspecific and intraspecific pollination patterns of Valley Oak, Quercus lobata, in a mixed stand in coastal central California. Int. J. Plant Sci. 2011, 172, 691–699. [Google Scholar] [CrossRef] [Green Version]
  69. Craft, K.J.; Ashley, M.V.; Koenig, W.D. Limited hybridization between Quercus lobata and Quercus douglasii (Fagaceae) in a mixed stand in central coastal California. Am. J. Bot. 2002, 89, 1792–1798. [Google Scholar] [CrossRef] [Green Version]
  70. Gharehaghaji, M.; Minor, E.S.; Ashley, M.V.; Abraham, S.T.; Koenig, W.D. Effects of landscape features on gene flow of valley oaks (Quercus lobata). Plant Ecol. 2017, 218, 487–499. [Google Scholar] [CrossRef]
  71. Grivet, D.; Deguilloux, M.-F.; Petit, R.J.; Sork, V.L. Contrasting patterns of historical colonization in white oaks (Quercus spp.) in California and Europe. Mol. Ecol. 2006, 15, 4085–4093. [Google Scholar] [CrossRef]
  72. Grivet, D.; Robledo-Arnuncio, J.J.; Smouse, P.E.; Sork, V.L. Relative contribution of contemporary pollen and seed dispersal to the effective parental size of seedling population of California valley oak (Quercus lobata, Née). Mol. Ecol. 2009, 18, 3967–3979. [Google Scholar] [CrossRef]
  73. Grivet, D.; Sork, V.L.; Westfall, R.D.; Davis, F.W. Conserving the evolutionary potential of California valley oak (Quercus lobata Née): A multivariate genetic approach to conservation planning. Mol. Ecol. 2008, 17, 139–156. [Google Scholar] [CrossRef]
  74. Pluess, A.R.; Sork, V.L.; Dolan, B.; Davis, F.W.; Grivet, D.; Merg, K.; Papp, J.; Smouse, P.E. Short distance pollen movement in a wind-pollinated tree, Quercus lobata (Fagaceae). For. Ecol. Manag. 2009, 258, 735–744. [Google Scholar] [CrossRef]
  75. Scofield, D.G.; Alfaro, V.R.; Sork, V.L.; Grivet, D.; Martinez, E.; Papp, J.; Pluess, A.R.; Koenig, W.D.; Smouse, P.E. Foraging patterns of acorn woodpeckers (Melanerpes formicivorus) on valley oak (Quercus lobata Née) in two California oak savanna-woodlands. Oecologia 2011, 166, 187–196. [Google Scholar] [CrossRef]
  76. Sork, V.L.; Davis, F.W.; Grivet, D. Incorporating Genetic Information into Conservation Planning for California Valley Oak. In Proceedings of the Sixth Symposium on Oak Woodlands: Today’s Challenges, Tomorrow’s Opportunities, Rohnert Park, CA, USA, 9–12 October 2006; pp. 497–509. [Google Scholar]
  77. Sork, V.L.; Davis, F.W.; Smouse, P.E.; Apsit, V.J.; Dyer, R.J.; Fernandez-M, J.F.; Kuhn, B. Pollen movement in declining populations of California Valley oak, Quercus lobata: Where have all the fathers gone? Mol. Ecol. 2002, 11, 1657–1668. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  78. Sork, V.L.; Smouse, P.E.; Grivet, D.; Scofield, D.G. Impact of asymmetric male and female gamete dispersal on allelic diversity and spatial genetic structure in valley oak (Quercus lobata Née). Evol. Ecol. 2015, 29, 927–945. [Google Scholar] [CrossRef]
  79. Browne, L.; Mead, A.; Horn, C.; Chang, K.; Celikkol, Z.A.; Henriquez, C.L.; Ma, F.; Beraut, E.; Meyer, R.S.; Sork, V.L. Experimental DNA demethylation associates with changes in growth and gene expression of oak tree seedlings. G3 Genes Genomes Genet. 2020, 10, 1019–1028. [Google Scholar] [CrossRef] [Green Version]
  80. Gugger, P.F.; Fitz-Gibbon, S.; Pellegrini, M.; Sork, V.L. Species-wide patterns of DNA methylation variation in Quercus lobata and its association with climate gradients. Mol. Ecol. 2016, 25, 1665–1680. [Google Scholar] [CrossRef] [PubMed]
  81. Gugger, P.F.; Fitz-Gibbon, S.T.; Albarrán-Lara, A.; Wright, J.W.; Sork, V.L. Landscape genomics of Quercus lobata reveals genes involved in local climate adaptation at multiple spatial scales. Mol. Ecol. 2021, 30, 406–423. [Google Scholar] [CrossRef] [PubMed]
  82. Gugger, P.F.; Peñaloza-Ramírez, J.M.; Wright, J.W.; Sork, V.L.; Schnitzler, J.-P. Whole-transcriptome response to water stress in a California endemic oak, Quercus lobata. Tree Physiol. 2016, 37, 632. [Google Scholar] [CrossRef] [PubMed]
  83. Fitz-Gibbon, S.; Hipp, A.L.; Pham, K.K.; Manos, P.S.; Sork, V.L.; Jaramillo-Correa, J.P. Phylogenomic inferences from reference-mapped and de novo assembled short-read sequence data using RADseq sequencing of California white oaks (Quercus section Quercus). Genome 2017, 60, 743–755. [Google Scholar] [CrossRef] [Green Version]
  84. Gugger, P.F.; Ikegami, M.; Sork, V.L. Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata Née. Mol. Ecol. 2013, 22, 3598–3612. [Google Scholar] [CrossRef]
  85. Sork, V.L.; Squire, K.; Gugger, P.F.; Steele, S.E.; Levy, E.D.; Eckert, A.J. Landscape genomic analysis of candidate genes for climate adaptation in a California endemic oak, Quercus lobata. Am. J. Bot. 2016, 103, 33–46. [Google Scholar] [CrossRef] [Green Version]
  86. Browne, L.; MacDonald, B.; Fitz-Gibbon, S.; Wright, J.W.; Sork, V.L. Genome-wide variation in DNA methylation predicts variation in leaf traits in an ecosystem-foundational oak species. Forests 2021, 12, 569. [Google Scholar] [CrossRef]
  87. Pingarroni, A.; Molina-Garay, C.; Rosas-Osorio, C.; Alfonso-Corrado, C.; Clark-Tapia, R.; Monsalvo-Reyes, A.; Campos, J.E. Abundancia y diversidad genética de Quercus mulleri, especie microendémica amenazada de Oaxaca. Madera Bosques 2020, 26. [Google Scholar] [CrossRef]
  88. Hauser, D.A.; Keuter, A.; McVay, J.D.; Hipp, A.L.; Manos, P.S. The evolution and diversification of the red oaks of the California Floristic Province (Quercus section Lobatae, series Agrifoliae). Am. J. Bot. 2017, 104, 1581–1595. [Google Scholar] [CrossRef] [Green Version]
  89. Kashani, N.; Dodd, R.S. Genetic differentiation of two California red oak species, Quercus parvula var. shreveii and Q. wislizeni, based on AFLP genetic markers. In Proceedings of the Fifth Symposium on Oak Woodlands: Oaks in California’s Challenging Landscape; San Diego, CA, USA, 22–25 October 2001, pp. 417–426.
  90. Dodd, R.S.; Kashani, N. Molecular differentiation and diversity among the California red oaks (Fagaceae; Quercus section Lobatae). Theor. Appl. Genet. Theor. Angew. Genet. TAG. 2003, 107, 884–892. [Google Scholar] [CrossRef]
  91. McCauley, R.A.; Cortés-Palomec, A.C.; Oyama, K. Species diversification in a lineage of Mexican red oak (Quercus section Lobatae subsection Racemiflorae)—The interplay between distance, habitat, and hybridization. Tree Genet. Genomes 2019, 15, 1. [Google Scholar] [CrossRef]
  92. Su, H.; Yang, Y.; Ju, M.; Li, H.; Zhao, G. Characterization of the complete plastid genome of Quercus sichourensis. Conserv. Genet. Resour. 2019, 11, 129–131. [Google Scholar] [CrossRef]
  93. Zheng, J.-W.; An, S.-Q.; Chen, L.; Leng, X.; Wang, Z.-S.; Xiang, H.-J. Effects of logging on the genetic diversity of Quercus tiaoloshanica Chun et Ko in a tropical montane forest of Hainan Island, Southern China. J. Integr. Plant Biol. 2005, 47, 1184–1192. [Google Scholar] [CrossRef]
  94. Ashley, M.V.; Abraham, S.; Kindsvater, L.C.; Knapp, D.; Craft, K. Population structure and genetic variation of Island. In Oak Ecosystem Restoration Research on Catalina Island, California; Knapp, D.A., Ed.; Catalina Island Conservancy: Avalon, CA, USA, 2010; pp. 125–135. [Google Scholar]
  95. Ashley, M.V.; Backs, J.R.; Abraham, S.T. Landscape and conservation genetics of the Island Oak, Quercus tomentella. Int. Oaks 2016, 27, 83–90. [Google Scholar]
  96. Ashley, M.V.; Backs, J.R.; Kindsvater, L.; Abraham, S.T. Genetic variation and structure in an endemic island oak, Quercus tomentella, and mainland canyon oak, Quercus chrysolepis. Int. J. Plant Sci. 2018, 179, 151–161. [Google Scholar] [CrossRef]
  97. Ortego, J.; Gugger, P.F.; Sork, V.L. Genomic data reveal cryptic lineage diversification and introgression in Californian golden cup oaks (section Protobalanus). New Phytol. 2018, 218, 804–818. [Google Scholar] [CrossRef] [Green Version]
  98. Yang, Y.; Zhang, H.; Ren, T.; Zhao, G. Characterization of the complete plastid genome of Quercus tungmaiensis. Conserv. Genet. Resour. 2018, 10, 457–460. [Google Scholar] [CrossRef]
  99. Philippe, H.; Delsuc, F.; Brinkmann, H.; Lartillot, N. Phylogenomics. Annu. Rev. Ecol. Evol. Syst. 2005, 36, 541–562. [Google Scholar] [CrossRef]
  100. Hoban, S. New guidance for ex situ gene conservation: Sampling realistic population systems and accounting for collection attrition. Biol. Conserv. 2019, 235, 199–208. [Google Scholar] [CrossRef]
  101. Wallace, S.H. Development of an Informational Resource to Inform Global Prioritization of Efforts to Conserve Threatened, Exceptional Plant Taxa. Ph.D. Thesis, University of Delaware, Newark, Delaware, 2015. [Google Scholar]
  102. Wyse, S.V.; Dickie, J.B. Predicting the global incidence of seed desiccation sensitivity. J. Ecol. 2017, 105, 1082–1093. [Google Scholar] [CrossRef] [Green Version]
  103. Wyse, S.V.; Dickie, J.B.; Willis, K.J. Seed banking not an option for many threatened plants. Nat. Plants 2018, 4, 848–850. [Google Scholar] [CrossRef] [PubMed]
  104. Pence, V.C. Evaluating costs for the in vitro propagation and preservation of endangered plants. In Vitro Cell. Dev. Biol. Plant 2011, 47, 176–187. [Google Scholar] [CrossRef]
  105. Van Dyke, F.; Lamb, R.L. Conservation Genetics. In Conservation Biology: Foundations, Concepts, Applications; Springer International Publishing: Cham, Switzerland, 2020; pp. 171–210. ISBN 978-3-030-39534-6. [Google Scholar]
  106. Beckman, E.; McNeil-Marshall, A.; Still, S.M.; Meyer, A.; Westwood, M. Quercus robusta C.H.Müll. Conservation Gap Analysis of Native U.S. Oaks; The Morton Arboretum: Lisle, IL, USA, 2019; pp. 184–189. [Google Scholar]
  107. Beckman, E.; Baker, B.; Lobdell, M.; Meyer, A.; Westwood, M. Conservation Gap Analysis of Native U.S. Oaks; The Morton Arboretum: Lisle, IL, USA, 2019; pp. 50–55. [Google Scholar]
  108. Beckman, E.; Still, S.M.; Meyer, A.; Westwood, M. Quercus carmenensis C.H.Müll. Conservation Gap Analysis of Native U.S. Oaks; The Morton Arboretum: Lisle, IL, USA, 2019; pp. 80–85. [Google Scholar]
  109. Borevitz, J.O.; Chory, J. Genomics tools for QTL analysis and gene discovery. Curr. Opin. Plant Biol. 2004, 7, 132–136. [Google Scholar] [CrossRef]
  110. Storfer, A.; Patton, A.; Fraik, A.K. Navigating the Interface Between Landscape Genetics and Landscape Genomics. Front. Genet. 2018, 9, 68. [Google Scholar] [CrossRef] [Green Version]
  111. Rey, O.; Eizaguirre, C.; Angers, B.; Baltazar-Soares, M.; Sagonas, K.; Prunier, J.G.; Blanchet, S.; Herrel, A. Linking epigenetics and biological conservation: Towards a conservation epigenetics perspective. Funct. Ecol. 2020, 34, 414–427. [Google Scholar] [CrossRef] [Green Version]
  112. Amaral, J.; Ribeyre, Z.; Vigneaud, J.; Sow, M.D.; Fichot, R.; Messier, C.; Pinto, G.; Nolet, P.; Maury, S. Advances and promises of epigenetics for forest trees. Forests 2020, 11, 976. [Google Scholar] [CrossRef]
  113. Rico, L.; Ogaya, R.; Barbeta, A.; Peñuelas, J.; Rennenberg, H. Changes in DNA methylation fingerprint of Quercus ilex trees in response to experimental field drought simulating projected climate change. Plant Biol. 2014, 16, 419–427. [Google Scholar] [CrossRef] [PubMed]
  114. Silva, H.G.; Sobral, R.S.; Magalhães, A.P.; Morais-Cecílio, L.; Costa, M.M.R. Genome-wide identification of epigenetic regulators in Quercus suber L. Int. J. Mol. Sci. 2020, 21, 3783. [Google Scholar] [CrossRef]
  115. Verhoeven, K.J.F.; Preite, V. Epigenetic variation in asexually reproducing organisms. Evol. Int. J. Org. Evol. 2013, 68, 644–655. [Google Scholar] [CrossRef]
  116. Bräutigam, K.; Vining, K.J.; Lafon-Placette, C.; Fossdal, C.G.; Mirouze, M.; Marcos, J.G.; Fluch, S.; Fraga, M.F.; Guevara, M.Á.; Abarca, D.; et al. Epigenetic regulation of adaptive responses of forest tree species to the environment. Ecol. Evol. 2013, 3, 399–415. [Google Scholar] [CrossRef]
  117. Bossdorf, O.; Richards, C.L.; Pigliucci, M. Epigenetics for ecologists. Ecol. Lett. 2008, 11, 106–115. [Google Scholar] [CrossRef]
  118. Chinnusamy, V.; Zhu, J.-K. Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 2009, 12, 133–139. [Google Scholar] [CrossRef] [Green Version]
  119. Boyko, A.; Kovalchuk, I. Epigenetic control of plant stress response. Environ. Mol. Mutagen. 2008, 49, 61–72. [Google Scholar] [CrossRef] [PubMed]
  120. Inácio, V.; Barros, P.M.; Costa, A.; Roussado, C.; Gonçalves, E.; Costa, R.; Graça, J.; Oliveira, M.M.; Morais-Cecílio, L.; Fu, B. Differential DNA Methylation Patterns Are Related to Phellogen Origin and Quality of Quercus suber Cork. PLoS ONE 2017, 12, e0169018. [Google Scholar] [CrossRef]
  121. Saintagne, C.; Bodénès, C.; Barreneche, T.; Pot, D.; Plomion, C.; Kremer, A. Distribution of genomic regions differentiating oak species assessed by QTL detection. Heredity 2004, 92, 20–30. [Google Scholar] [CrossRef] [Green Version]
  122. Aitken, S.N.; Whitlock, M.C. Assisted gene flow to facilitate local adaptation to climate change. Annu. Rev. Ecol. Evol. Syst. 2013, 44, 367–388. [Google Scholar] [CrossRef]
  123. Gonzalez, A.; Ronce, O.; Ferriere, R.; Hochberg, M.E. Evolutionary rescue: An emerging focus at the intersection between ecology and evolution. Philos. Trans. R. Soc. London 2013, 368, 20120404. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  124. Rellstab, C.; Gugerli, F.; Eckert, A.J.; Hancock, A.M.; Holderegger, R. A practical guide to environmental association analysis in landscape genomics. Mol. Ecol. 2015, 24, 4348–4370. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  125. Li, Y.; Zhang, X.-X.; Mao, R.-L.; Yang, J.; Miao, C.-Y.; Li, Z.; Qiu, Y.-X. Ten years of landscape genomics: Challenges and opportunities. Front. Plant Sci. 2017, 8, 2136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  126. Rellstab, C.; Zoller, S.; Walthert, L.; Lesur, I.; Pluess, A.R.; Graf, R.; Bodénès, C.; Sperisen, C.; Kremer, A.; Gugerli, F. Signatures of local adaptation in candidate genes of oaks (Quercus spp.) with respect to present and future climatic conditions. Mol. Ecol. 2016, 25, 5907–5924. [Google Scholar] [CrossRef]
  127. Martins, K.; Gugger, P.F.; Llanderal-Mendoza, J.; González-Rodríguez, A.; Fitz-Gibbon, S.T.; Zhao, J.-L.; Rodríguez-Correa, H.; Oyama, K.; Sork, V.L. Landscape genomics provides evidence of climate-associated genetic variation in Mexican populations of Quercus rugosa. Evol. Appl. 2018, 11, 1842–1858. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Table
Table 1. Species of Concern and genetic research focus.
Table 1. Species of Concern and genetic research focus.
Species of Concern
[Cited Research]		Conservation
Classification		Country
Distribution		Number of
Ex Situ
Collections		Quercus SectionCitation
Focus
Quercus acerifolia [1]EN US 44LobataePT
Quercus acutifolia [1,23] VU BZ, GT, HN, MX 34LobataePT
Quercus afares [1,24,25,26,27] VU DZ, TN 18CerrisPT, PG
Quercus ajoensis [1,28] VU MX, US 5QuercusPT
Quercus albicaulis CR CN 0Cyclobalanopsis
Quercus arbutifolia [1,29,30] EN CN, VN 0CyclobalanopsisPT, PG
Quercus argyrotricha CR N 4Cyclobalanopsis
Quercus arkansana [1] VU US 48LobataePT
Quercus asymmetrica EN CN, VN 0 Cyclobalanopsis
Quercus austrina [1,28] VU US 25QuercusPT
Quercus austrocochinchinensis [1,30,31,32,33,34] VU CN, LA, TH, VN 0CyclobalanopsisPT, PG, G
Quercus bambusifolia [35,36] EN CN, HK, VN 4CyclobalanopsisPG
Quercus baniensis [33,34] CR VN 0CyclobalanopsisPT
Quercus baolamensis [34] CR VN 0CyclobalanopsisPT
Quercus bawanglingensis [37] CR CN 0 Ilex PT, G
Quercus bidoupensis [34] CR VN 0 Cyclobalanopsis PT
Quercus blaoensis [33,34] CR VN 0 Cyclobalanopsis PT
Quercus boyntonii [1,28,38,39] CR US 21 Quercus PT, PG, CON
Quercus braianensis [33,34] VU LA, VN 0 Cyclobalanopsis PT
Quercus brandegeei [28,40] EN MX 9 Virentes PT
Quercus cambodiensis [34] CR KH 0 Cyclobalanopsis PT
Quercus camusiae [33,34] CR VN 0 Cyclobalanopsis PT
Quercus carmenensis EN MX, US 3 Quercus
Quercus cedrosensis [25,41] VU MX, US 2 Protobalanus PT
Quercus chapmanii [1,28] * LC US 8 Quercus PT
Quercus chrysotricha EN MY 0 Cyclobalanopsis
Quercus costaricensis [1] VU CR, HN, PA 2 Lobatae PT
Quercus cualensis EN MX 1 Lobatae
Quercus cupreata EN MX 4 Lobatae
Quercus daimingshanensis (damingshanensis) [1,30] EN CN 0 Cyclobalanopsis PT
Quercus dankiaensis CR VN 0 Cyclobalanopsis
Quercus delgadoana [1] EN MX 9 Lobatae PT
Quercus delicatula EN CN 0 Cyclobalanopsis
Quercus devia EN MX 0 Lobatae
Quercus dilacerata [34] CR VN 0 Cyclobalanopsis PT
Quercus dinghuensis CR CN 1 Cyclobalanopsis
Quercus disciformis [33] EN CN 2 Cyclobalanopsis PT
Quercus diversifolia [1] EN MX 3 Quercus PT
Quercus donnaiensis [33,34] CR VN 0 Cyclobalanopsis PT
Quercus dumosa [1,28,42,43,44,45,46] EN MX, US 30 Quercus PT, PG
Quercus edithiae [33,47,48] EN CN, HK, VN 0 Cyclobalanopsis PT
Quercus engelmannii [1,28,41,44,49,50,51] EN MX, US 36 Quercus PT, PG
Quercus fimbriata CR CN 0 Ilex
Quercus flocculenta EN MX 3 Lobatae
Quercus furfuracea VU MX 5 Lobatae
Quercus gaharuensis VU ID, MY 0 Cyclobalanopsis
Quercus galeanensis EN MX 8 Lobatae
Quercus georgiana [1,39,52] EN US 55 Lobatae PT, PG
Quercus graciliformis CR MX, US 21 Lobatae
Quercus gulielmi-treleasei [23] VU CR, PA 2 Lobatae PT
Quercus havardii [1,28,53] EN US 19 Quercus PT, PG
Quercus hinckleyi [1,18,54,55] CR MX, US 12 Quercus PT, PG, CON
Quercus hintonii [23] EN MX 3 Lobatae PT
Quercus hintoniorum [23] VU MX 6 Lobatae PT
Quercus hirtifolia EN MX 7 Lobatae
Quercus honbaensis [34] CR VN 0 Cyclobalanopsis PT
Quercus hondae [56] VU JP 2 Cyclobalanopsis PT
Quercus inopina [1] * LC US 5 Lobatae PT
Quercus insignis [1,28,57] EN BZ, CR, GT, HN, MX, NI, PA 27 Quercus PT
Quercus kerangasensis VU BN, ID, MY 0 Cyclobalanopsis
Quercus kinabaluensis EN MY 0 Cyclobalanopsis
Quercus kingiana [58] EN CN, LA, MM, TH 0 Ilex PT
Quercus kiukiangensis [30] EN CN 4 Cyclobalanopsis PT
Quercus kotschyana [1,59] EN LB 0 Quercus PT
Quercus kouangsiensis [1] EN CN 0 Cyclobalanopsis PT
Quercus laceyi [1,28] * LC MX, US 16 Quercus PT
Quercus lenticellata EN TH 0 Cyclobalanopsis
Quercus liboensis EN CN 2 Cyclobalanopsis
Quercus litseoides VU CN, HK 1 Cyclobalanopsis
Quercus lobata [1,28,41,44,49,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86] * NT US 41 Quercus PT, PG, G, CON, GENOM
Quercus lobbii EN BD, CN, IN 0 Cyclobalanopsis
Quercus lodicosa EN CN, IN, MM 0 Ilex
Quercus look [1,59] EN LB, SY 16 Cerris PT
Quercus lungmaiensis CR CN 1 Cyclobalanopsis
Quercus macdougallii EN MX 0 Quercus
Quercus marlipoensis CR CN 1 Ilex
Quercus meavei VU MX 1 Lobatae
Quercus merrillii VU ID, MY, PH 0 Cyclobalanopsis
Quercus miquihuanensis [23] EN MX 12 Lobatae PT
Quercus monnula CR CN 0 Quercus
Quercus motuoensis CR CN 0 Cyclobalanopsis
Quercus mulleri [87] CR MX 0 Lobatae PG
Quercus nivea EN MY 0 Cyclobalanopsis
Quercus nixoniana EN MX 0 Lobatae
Quercus obconicus EN CN 0 Cyclobalanopsis
Quercus oglethorpensis [1,28,39] EN US 47 Quercus PT, PG
Quercus pacifica [1,28,43,44,45,46] EN US 22 Quercus PT, PG
Quercus palmeri [1,28,41] * NT MX, US 18 Protobalanus PT
Quercus parvula [1,88,89,90] * NT US 15 Lobatae PT, PG
Quercus percoriacea EN MY 0 Cyclobalanopsis
Quercus petelotii EN VN 0 Cyclobalanopsis
Quercus phanera [1] EN CN 1 Cyclobalanopsis PT
Quercus pinbianensis CR CN 0 Cyclobalanopsis
Quercus pontica [1,25,28,61] EN GE, TR 91 Ponticae PT
Quercus pseudosetulosa [58] CR CN 0 Ilex PT
Quercus pseudoverticillata CR MY 0 Cyclobalanopsis
Quercus pumila [23] * LC US 15 Lobatae PT
Quercus quangtriensis [33] VU CN, LA, MM, TH, VN 0 Cyclobalanopsis PT
Quercus radiata [1,91] EN MX 0 Lobatae PT
Quercus ramsbottomii EN MM, TH 0 Cyclobalanopsis
Quercus robusta * DD US 2 Lobatae
Quercus rubramenta VU MX 0 Lobatae
Quercus runcinatifolia EN MX 1 Lobatae
Quercus rupestris EN VN 0 Cyclobalanopsis
Quercus sadleriana [1,28,61] * NT US 14 Ponticae PT
Quercus sagrana (sagraeana) [28] EN CU 1 Virentes PT
Quercus semiserratoides CR CN 2 Cyclobalanopsis
Quercus sichourensis [30,48,92] CR CN 1 Cyclobalanopsis PT, G
Quercus similis [1,28] * LC US 2 Quercus PT
Quercus steenisii EN ID 0 Cyclobalanopsis
Quercus tardifolia * DD MX, US 0 Lobatae
Quercus thomsoniana CR BD, BT, IN 0 Cyclobalanopsis
Quercus tiaoloshanica [93] EN CN 0 Cyclobalanopsis CON
Quercus tomentella [1,28,41,61,94,95,96,97] EN MX, US 33 Protobalanus PT, PG
Quercus tomentosinervis CR CN 0 Cyclobalanopsis
Quercus toumeyi [1,28] * DD MX, US 3 Quercus PT
Quercus treubiana VU ID, MY 0 Cyclobalanopsis
Quercus trungkhanhensis [33] CR VN 0 Ilex PT
Quercus tuitensis VU MX 0 Lobatae
Quercus tungmaiensis [58,98] EN CN, IN 3 Ilex PT, G
Quercus utilis [1,48,58] EN CN 2 Ilex PT
Quercus vicentensis VU MX, SV 1 Quercus
Quercus xanthotricha EN CN, LA 0 Cyclobalanopsis
Quercus xuanlienensis [33] CR VN 0 Cyclobalanopsis PT
Conservation classification: CR—Critically Endangered, EN—Endangered, VU—Vulnerable, * NT—Near Threatened, * LC—Least Concern, * DD—Data Deficient (* Gap Analysis). (see [16] for descriptions and criteria of IUCN categories). Country distribution: BD—Bangladesh, BT—Bhutan, BZ—Belize, CN—China, CR—Costa Rica, CU—Cuba, DZ—Algeria, GE—Georgia, GT—Guatemala, HK—Hong Kong, HN—Honduras, ID—Indonesia, IN—India, JP—Japan, KH—Cambodia, LA—Lao People’s Dem. Republic, LB—Lebanon, MM—Myanmar, MX—Mexico, MY—Malaysia, NI—Nicaragua, PA—Panama, PH—Philippines, SV—El Salvador, SY—Syrian Arab Republic, TH—Thailand, TN—Tunisia, TR—Turkey, US—United States, VN—Viet Nam. Citation focus: PT—phylogeny/taxonomy, PG—population genetics, CON—conservation, G—genome assembly, GENOM—genomic methods.
Table
Table 2. Population genetics studies involving Oaks of Concern.
Table 2. Population genetics studies involving Oaks of Concern.
Species of ConcernCitationFocus of StudyMethod Used
Q. afaresMir et al. [24]hybridizationnuclear allozymes, chloroplast markers
Q. arbutifoliaXu et al. [29]genetic diversitychloroplast (cpDNA), nuclear (ITS) DNA sequences
Q. austrocochinchinensisAn et al. [31]introgressionAFLP markers, nu-SSRs
Q. bambusifoliaZeng et al. [35,36]inbreeding, genetic diversity, population structurenu-SSRs
Q. boyntoniiSpence et al. [39]fragmentation, ex situ collections, inbreeding, heterozygositynu-SSRs and EST-SRRs
Q. dumosaBacks et al. [43]introgression nu-SSR
Burge et al. [42]gene flow/environmental gradientsRAD-seq
Ortego et al. [45]genetic differentiation, population structurenu-SSR
Q. engelmanniiOney-Birol et al. [51]hybridization/introgressionRNA-seq
Ortego et al. [50]ecological niche modelingnu-SSR
Riordan et al. [49]responses to geography and climatenu-SSR
Q. georgianaKadav [52]genetic diversity, population structureEST-SSRs
Spence et al. [39]fragmentation, ex situ collections, inbreeding, heterozygosity nu-SSRs and EST-SRRs
Q. havardiiZumwalde et al. [53]genetic diversity, population structure nu-SSRs
Q. hinckleyiBacks et al. [18]genetic diversity, population structurenu-SSRs
Backs et al. [55]hybridizationnu-SSRs
Backs et al. [54] genetic diversity, in situ/ex situnu-SSRs
Q. lobataAbraham et al. [68]hybridizationnu-SSRs
Ashley et al. [65]landscape genetics, population structurenu-SSRs
Browne at al. [66]adaptational lag/temperaturegenome-wide sequencing
Craft et al. [69]hybridizationnu-SSRs
Dutech et al. [67]gene flow, genetic diversity, population structurenu-SSRs
Gharehaghaji et al. [70]gene flownu-SSRs
Grivet et al. [73]gene flownu-SSRs
Gugger et al. [60]sequence variation/climate gradientswhole-transcriptome sequencing (mRNA-Seq)
Mead et al. [64]ecophysiological traits/gene expressionRNA-seq
Pluess et al. [74]gene flownu-SSRs
Scofield et al. [75]gene flownu-SSRs
Sork et al. [77]gene flow, pollen movementallozymes, nu-SSRs
Sork et al. [78]gene flow, population structurenu-SSRs
Sork et al. [63]gene flow, environmental gradientschloroplast and nuclear microsatellite
Sork et al. [46]hybridization, introgressionnu-SSRs, RADseq-based sequences
Q. mulleriPingarroni et al. [87] genetic diversitynu-SSRs
Q. oglethorpensisSpence et al. [39]fragmentation, ex situ collections, inbreeding, heterozygositynu-SSRs and EST-SRRs
Q. pacificaBacks et al. [43]gene flow, population structure, introgressionnu-SSRs
Ortego et al. [45]evolutionary history, demographicsnu-SSRs, cpSSRs
Q. parvulaDodd et al. [90]species differentiationAFLP genetic markers
Kashani et al. [89]genetic differentiation, introgressionAFLP genetic markers
Q. tomentellaAshley et al. [94,95]genetic variation, population structurenu-SSRs
Ashley et al. [95]landscape and conservation geneticsnu-SSRs
Ashley et al. [96]genetic variation, population structurenu-SSRs
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Backs, J.R.; Ashley, M.V. Quercus Conservation Genetics and Genomics: Past, Present, and Future. Forests 2021, 12, 882. https://0-doi-org.brum.beds.ac.uk/10.3390/f12070882

AMA Style

Backs JR, Ashley MV. Quercus Conservation Genetics and Genomics: Past, Present, and Future. Forests. 2021; 12(7):882. https://0-doi-org.brum.beds.ac.uk/10.3390/f12070882

Chicago/Turabian Style

Backs, Janet R., and Mary V. Ashley. 2021. "Quercus Conservation Genetics and Genomics: Past, Present, and Future" Forests 12, no. 7: 882. https://0-doi-org.brum.beds.ac.uk/10.3390/f12070882

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop