Quercus Genetics: Insights into the Past, Present, and Future of Oaks

A special issue of Forests (ISSN 1999-4907). This special issue belongs to the section "Forest Ecophysiology and Biology".

Deadline for manuscript submissions: closed (1 May 2021) | Viewed by 34483

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Guest Editor
Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USA
Interests: population and landscape genetics; conservation genetics; mating systems; science education

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Guest Editor
Department of Biological Sciences, University of Illinois at Chicago, Chicago, IL 60607, USA
Interests: quercus; conservation genetics; population genetics; landscape genetics

Special Issue Information

Dear Colleagues,

The genus Quercus (Quercus, Fagaceae) comprises more than 400 species distributed throughout the northern hemisphere. While the highest oak diversity occurs in American and Asia, European species are also widespread. Oaks are ecological dominants of many temperate forests, and evergreen species are major components of Mediterranean and subtropical woodlands. They provide important ecosystem services and valuable timber. Oak species exhibit high genetic diversity, and this diversity has provided a wealth of information regarding oak ecology and evolution. Recent genetic and genomic studies of oaks have unraveled their evolutionary origins, history, and past radiations. Genetic approaches have also been applied to learn about more recent events, such as range expansions and contractions occurring at northern latitudes.
Interest in hybridization between oaks species dates back at least as far as Darwin, and genetic tools have provided new insight into rates and patterns of hybridization, underlying ecological factors, and evolutionary consequences of genetic introgression. Further, we can now ask what genes or genomic regions are responsible for maintaining species barriers in oaks in the face of gene flow.
Genetic studies have also demonstrated widespread, long-distance pollen movement in oaks. Despite such extensive gene flow, evidence for divergent selection and local adaption has also emerged. The genes and genetic architecture underlying adaptive traits such as drought-tolerance and phenology may help us to make predictions regarding oak response to abiotic stress. Finally, many species of oaks are threatened by habitat loss and climate change, and understanding the genetic diversity and structure of these declining species is key for successful protection and recovery. This Special Issue focuses on what recent genetic studies have revealed about adaptation in oaks, their susceptibility to climate and other environmental stresses, and implications for management of both widespread and restricted species. We welcome submission of research reports and review papers that address these topics.

Dr. Mary Ashley
Dr. Janet R. Backs
Guest Editors

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Keywords

  • Oaks (Quercus)
  • Genetics of forest trees
  • Genetic diversity
  • Environmental stress (climate change, fragmentation)
  • Hybridization
  • Pollination and gene flow
  • Conservation genetics
  • Adaptive divergence

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Published Papers (9 papers)

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Editorial

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2 pages, 616 KiB  
Editorial
Quercus Genetics: Insights into the Past, Present, and Future of Oaks
by Janet R. Backs and Mary V. Ashley
Forests 2021, 12(12), 1628; https://doi.org/10.3390/f12121628 - 24 Nov 2021
Cited by 6 | Viewed by 1662
Abstract
The genus Quercus comprises over 400 species found across the Northern Hemisphere [...] Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)

Research

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12 pages, 2147 KiB  
Article
Geographical Structuring of Quercus robur (L.) Chloroplast DNA Haplotypes in Lithuania: Recolonization, Adaptation, or Overexploitation Effects?
by Darius Danusevičius, Virgilijus Baliuckas, Jurata Buchovska and Rūta Kembrytė
Forests 2021, 12(7), 831; https://doi.org/10.3390/f12070831 - 24 Jun 2021
Cited by 3 | Viewed by 2473
Abstract
We studied the maternally inherited chloroplast DNA polymorphism at three microsatellite loci of 157 Quercus robur trees from 38 native populations in Lithuania. We found high diversity of eight haplotypes from the Balkan lineage A (frequency 0.75) and the “German” subbranch of the [...] Read more.
We studied the maternally inherited chloroplast DNA polymorphism at three microsatellite loci of 157 Quercus robur trees from 38 native populations in Lithuania. We found high diversity of eight haplotypes from the Balkan lineage A (frequency 0.75) and the “German” subbranch of the Balkan lineage A (freq. 0.12), western and eastern Italian lineages C (freq. 0.05 and 0.06, respectively), and Iberian lineage B (freq. 0.03). The haplotypes were geographically well structured (among population differentiation index PhiPT = 0.30, the p-value < 0.001) that is unexpected for such a small territory as Lithuania. We raised a hypothesis on historical overexploitation of oaks by eliminating certain haplotypes in Lithuania, following a drastic felling of oak forests over the last few centuries. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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26 pages, 2888 KiB  
Article
An Updated Infrageneric Classification of the North American Oaks (Quercus Subgenus Quercus): Review of the Contribution of Phylogenomic Data to Biogeography and Species Diversity
by Paul S. Manos and Andrew L. Hipp
Forests 2021, 12(6), 786; https://doi.org/10.3390/f12060786 - 15 Jun 2021
Cited by 30 | Viewed by 7042
Abstract
The oak flora of North America north of Mexico is both phylogenetically diverse and species-rich, including 92 species placed in five sections of subgenus Quercus, the oak clade centered on the Americas. Despite phylogenetic and taxonomic progress on the genus over the [...] Read more.
The oak flora of North America north of Mexico is both phylogenetically diverse and species-rich, including 92 species placed in five sections of subgenus Quercus, the oak clade centered on the Americas. Despite phylogenetic and taxonomic progress on the genus over the past 45 years, classification of species at the subsectional level remains unchanged since the early treatments by WL Trelease, AA Camus, and CH Muller. In recent work, we used a RAD-seq based phylogeny including 250 species sampled from throughout the Americas and Eurasia to reconstruct the timing and biogeography of the North American oak radiation. This work demonstrates that the North American oak flora comprises mostly regional species radiations with limited phylogenetic affinities to Mexican clades, and two sister group connections to Eurasia. Using this framework, we describe the regional patterns of oak diversity within North America and formally classify 62 species into nine major North American subsections within sections Lobatae (the red oaks) and Quercus (the white oaks), the two largest sections of subgenus Quercus. We also distill emerging evolutionary and biogeographic patterns based on the impact of phylogenomic data on the systematics of multiple species complexes and instances of hybridization. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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14 pages, 1896 KiB  
Article
Genome-Wide Variation in DNA Methylation Predicts Variation in Leaf Traits in an Ecosystem-Foundational Oak Species
by Luke Browne, Brandon MacDonald, Sorel Fitz-Gibbon, Jessica W. Wright and Victoria L. Sork
Forests 2021, 12(5), 569; https://doi.org/10.3390/f12050569 - 1 May 2021
Cited by 8 | Viewed by 3126
Abstract
Epigenetic modifications such as DNA methylation are a potential mechanism for trees to respond to changing environments. However, it remains controversial the extent to which DNA methylation impacts ecologically important traits that influence fitness. In this study, we used reduced-representation bisulfite sequencing to [...] Read more.
Epigenetic modifications such as DNA methylation are a potential mechanism for trees to respond to changing environments. However, it remains controversial the extent to which DNA methylation impacts ecologically important traits that influence fitness. In this study, we used reduced-representation bisulfite sequencing to associate genomic and epigenomic variation with seven phenotypic traits related to growth, leaf function, and disease susceptibility in 160 valley oak (Quercus lobata) saplings planted across two common gardens in California. We found that DNA methylation was associated with a significant fraction of phenotypic variance in plant height, leaf lobedness, powdery mildew infection, and trichome density. Two of the seven traits were significantly associated with DNA methylation in the CG context, three traits were significantly associated with CHG methylation, and two traits were significantly associated with CHH methylation. Notably, controlling for genomic variation in SNPs generally reduced the amount of trait variation explained by DNA methylation. Our results suggest that DNA methylation may serve as a useful biomarker to predict phenotypic variation in trees, though it remains unclear the degree to which DNA methylation is a causal mechanism driving phenotypic variation in forest tree species. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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18 pages, 2566 KiB  
Article
Comparing Genetic Diversity in Three Threatened Oaks
by Emma Suzuki Spence, Jeremie B. Fant, Oliver Gailing, M. Patrick Griffith, Kayri Havens, Andrew L. Hipp, Priyanka Kadav, Andrea Kramer, Patrick Thompson, Raakel Toppila, Murphy Westwood, Jordan Wood, Bethany A. Zumwalde and Sean Hoban
Forests 2021, 12(5), 561; https://doi.org/10.3390/f12050561 - 29 Apr 2021
Cited by 12 | Viewed by 4471
Abstract
Genetic diversity is a critical resource for species’ survival during times of environmental change. Conserving and sustainably managing genetic diversity requires understanding the distribution and amount of genetic diversity (in situ and ex situ) across multiple species. This paper focuses on three emblematic [...] Read more.
Genetic diversity is a critical resource for species’ survival during times of environmental change. Conserving and sustainably managing genetic diversity requires understanding the distribution and amount of genetic diversity (in situ and ex situ) across multiple species. This paper focuses on three emblematic and IUCN Red List threatened oaks (Quercus, Fagaceae), a highly speciose tree genus that contains numerous rare species and poses challenges for ex situ conservation. We compare the genetic diversity of three rare oak species—Quercus georgiana, Q. oglethorpensis, and Q. boyntonii—to common oaks; investigate the correlation of range size, population size, and the abiotic environment with genetic diversity within and among populations in situ; and test how well genetic diversity preserved in botanic gardens correlates with geographic range size. Our main findings are: (1) these three rare species generally have lower genetic diversity than more abundant oaks; (2) in some cases, small population size and geographic range correlate with genetic diversity and differentiation; and (3) genetic diversity currently protected in botanic gardens is inadequately predicted by geographic range size and number of samples preserved, suggesting non-random sampling of populations for conservation collections. Our results highlight that most populations of these three rare oaks have managed to avoid severe genetic erosion, but their small size will likely necessitate genetic management going forward. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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25 pages, 4619 KiB  
Article
Genetic, Morphological, and Environmental Differentiation of an Arid-Adapted Oak with a Disjunct Distribution
by Bethany A. Zumwalde, Ross A. McCauley, Ian J. Fullinwider, Drew Duckett, Emma Spence and Sean Hoban
Forests 2021, 12(4), 465; https://doi.org/10.3390/f12040465 - 10 Apr 2021
Cited by 9 | Viewed by 3579
Abstract
The patterns of genetic and morphological diversity of a widespread species can be influenced by environmental heterogeneity and the degree of connectivity across its geographic distribution. Here, we studied Quercus havardii Rydb., a uniquely adapted desert oak endemic to the Southwest region of [...] Read more.
The patterns of genetic and morphological diversity of a widespread species can be influenced by environmental heterogeneity and the degree of connectivity across its geographic distribution. Here, we studied Quercus havardii Rydb., a uniquely adapted desert oak endemic to the Southwest region of the United States, using genetic, morphometric, and environmental datasets over various geographic scales to quantify differentiation and understand forces influencing population divergence. First, we quantified variation by analyzing 10 eastern and 13 western populations from the disjunct distribution of Q. havardii using 11 microsatellite loci, 17 morphological variables, and 19 bioclimatic variables. We then used regressions to examine local and regional correlations of climate with genetic variation. We found strong genetic, morphological and environmental differences corresponding with the large-scale disjunction of populations. Additionally, western populations had higher genetic diversity and lower relatedness than eastern populations. Levels of genetic variation in the eastern populations were found to be primarily associated with precipitation seasonality, while levels of genetic variation in western populations were associated with lower daily temperature fluctuations and higher winter precipitation. Finally, we found little to no observed environmental niche overlap between regions. Our results suggest that eastern and western populations likely represent two distinct taxonomic entities, each associated with a unique set of climatic variables potentially influencing local patterns of diversity. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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Review

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16 pages, 822 KiB  
Review
Quercus Conservation Genetics and Genomics: Past, Present, and Future
by Janet R. Backs and Mary V. Ashley
Forests 2021, 12(7), 882; https://doi.org/10.3390/f12070882 - 6 Jul 2021
Cited by 5 | Viewed by 3915
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
18 pages, 1409 KiB  
Review
Use of Genomic Resources to Assess Adaptive Divergence and Introgression in Oaks
by Desanka Lazic, Andrew L. Hipp, John E. Carlson and Oliver Gailing
Forests 2021, 12(6), 690; https://doi.org/10.3390/f12060690 - 27 May 2021
Cited by 21 | Viewed by 4135
Abstract
Adaptive divergence is widely accepted as a contributor to speciation and the maintenance of species integrity. However, the mechanisms leading to reproductive isolation, the genes involved in adaptive divergence, and the traits that shape the adaptation of wild species to changes in climate [...] Read more.
Adaptive divergence is widely accepted as a contributor to speciation and the maintenance of species integrity. However, the mechanisms leading to reproductive isolation, the genes involved in adaptive divergence, and the traits that shape the adaptation of wild species to changes in climate are still largely unknown. In studying the role of ecological interactions and environment-driven selection, trees have emerged as potential model organisms because of their longevity and large genetic diversity, especially in natural habitats. Due to recurrent gene flow among species with different ecological preferences, oaks arose as early as the 1970s as a model for understanding how speciation can occur in the face of interspecific gene flow, and what we mean by “species” when geographically and genomically heterogeneous introgression seems to undermine species’ genetic coherence. In this review, we provide an overview of recent research into the genomic underpinnings of adaptive divergence and maintenance of species integrity in oaks in the face of gene flow. We review genomic and analytical tools instrumental to better understanding mechanisms leading to reproductive isolation and environment-driven adaptive introgression in oaks. We review evidence that oak species are genomically coherent entities, focusing on sympatric populations with ongoing gene flow, and discuss evidence for and hypotheses regarding genetic mechanisms linking adaptive divergence and reproductive isolation. As the evolution of drought- and freezing-tolerance have been key to the parallel diversification of oaks, we investigate the question of whether the same or a similar set of genes are involved in adaptive divergence for drought and stress tolerance across different taxa and sections. Finally, we propose potential future research directions on the role of hybridization and adaptive introgression in adaptation to climate change. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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Other

6 pages, 666 KiB  
Viewpoint
Answers Blowing in the Wind: A Quarter Century of Genetic Studies of Pollination in Oaks
by Mary V. Ashley
Forests 2021, 12(5), 575; https://doi.org/10.3390/f12050575 - 5 May 2021
Cited by 6 | Viewed by 2589
Abstract
For the past 25 years, the twin tools of highly variable genetic markers (microsatellites) and paternity assignment have provided a powerful approach for investigating pollination patterns in trees, including many Quercus species. Early studies consistently demonstrated surprisingly abundant and extensive long-distance pollen movement [...] Read more.
For the past 25 years, the twin tools of highly variable genetic markers (microsatellites) and paternity assignment have provided a powerful approach for investigating pollination patterns in trees, including many Quercus species. Early studies consistently demonstrated surprisingly abundant and extensive long-distance pollen movement in oaks. Indeed, numerous studies showed high levels of pollen immigration (50% or more), even for relatively isolated stands of oaks. Research also characterized fertilization patterns within stands and between hybridizing species in mixed stands. More recent studies have expanded our knowledge of genetic exchange effected by successful pollen movement, identified even more remarkable examples of the distances Quercus pollen can travel, and examined pollination patterns in relictual populations as well as those at the leading edges of range expansion. While the paradigm of long distance pollination continues to hold, a few recent studies that have also revealed the limits of pollen movement, identifying cases of reproductive isolation in extreme situations, where populations are at risk. This review will highlight what has been learned about Quercus pollination, what questions remain, and propose implications for forest management in the face of changing landscapes and climates. Full article
(This article belongs to the Special Issue Quercus Genetics: Insights into the Past, Present, and Future of Oaks)
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