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Review

Plant Conservation Practitioners Can Benefit from Neutral Genetic Diversity

by
Mi Yoon Chung
1,
Sungwon Son
2,
Jordi López-Pujol
3,
Kangshan Mao
4 and
Myong Gi Chung
5,*
1
Department of Biological Sciences, Chungnam National University, Daejeon 34134, Korea
2
Division of Plant Resources, Korea National Arboretum, Yangpyeong 12519, Korea
3
Botanical Institute of Barcelona (IBB, CSIC-Ajuntament de Barcelona), 08038 Barcelona, Spain
4
Key Laboratory for Bio-Resources and Eco-Environment of Ministry of Education, College of Life Science, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu 610065, China
5
Division of Life Science and the RINS, Gyeongsang National University, Jinju 52828, Korea
*
Author to whom correspondence should be addressed.
Diversity 2021, 13(11), 552; https://doi.org/10.3390/d13110552
Submission received: 21 September 2021 / Revised: 22 October 2021 / Accepted: 26 October 2021 / Published: 30 October 2021
(This article belongs to the Special Issue Conservation Genetics and Biogeography of Seed Plant Species)
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Abstract

:
Several papers deal with a conservation genetics gap in which plant conservation and restoration managers or practitioners do not soundly integrate population genetics information into conservation management. Authors concerned about this issue point out that practitioners perceive genetic research results to be impractical or unnecessary in the short term due to time and financial constraints. In addition, researchers often fail to translate research findings into comprehensive, jargon-free recommendations effectively. If possible, conservation-related or conservation-oriented articles should be easily written to bridge the research–implementation gap. Finally, based on a previously published prioritization framework for conservation genetics scenarios, we introduce four simple genetic categories by exemplifying each case. We hope that conservation practitioners could employ these suggested guidelines for the prioritization of population- and species-level management.

1. Introduction

Traditionally, neutral genetic variation (hereafter, NGV) surveys that use neutral (or nearly neutral) genetic markers (e.g., allozymes, RAPDs (random amplified polymorphic DNAs), AFLPs (amplified fragment length polymorphisms), ISSRs (inter simple sequence repeats), microsatellites or SSRs (simple sequence repeats) or STRs (short tandem repeats), and more recently, neutral single nucleotide polymorphisms (SNPs)) are cheaper and take much less time than adaptive genetic variation (hereafter, AGV). However, variation at any of the abovementioned genetic markers does not (usually) directly influence fitness. In other words, different alleles at a single locus would not provide higher or lower adaptability among the individuals of a given population. To date, the vast majority of studies on conservation genetics have been based on NGV. One of the reasons researchers use NGV is that a reservoir of genetic diversity in plant populations that is neutral now could become adaptive when the environmental conditions change in the future [1,2].
In plants, common garden and/or reciprocal transplant studies have traditionally been conducted to assess levels and degrees of AGV within and among populations, which require plenty of time and resources [3,4,5,6,7,8,9]. The most comprehensive studies in this regard are those conducted with commercially important timber-yielding tree species because their well-adapted genotypes are used to replant clear-cut areas [10,11,12,13,14,15]. Due to the advent of genomic tools by high throughput sequencing (HTS), researchers on population and landscape genomics have primarily studied model species on the adaptation of local populations, climate change adaptation, and conservation (or restoration) biology (reviewed in [16,17,18]). Furthermore, recent advances in computational methods and reduced HTS-related costs for using genetic data (e.g., SNPs) to identify adaptive loci through association with phenotypic traits or environmental factors have increased the number of published papers [19,20]. Recently, some conservation geneticists have suggested that policy makers integrate genomics into decision making for laws protecting endangered species [9,21].
In very recent times, a debate about the assumption that NGV would be considered a proxy for AGV has arisen [2,20,22,23,24]. In particular, Teixeira and Huber [24] claim that NGV does not predict adaptive potential (AGV). However, García-Dorado and Caballero [22] stress that NGV is “a useful tool for conservation biology.” In the era of HTS, it is important to understand AGV. Still, conservation geneticists and practitioners should appreciate that demography and many ecological and evolutionary processes relevant to conservation can only be understood (estimated) through neutral markers (NGV). In this light, it is clear that the study of AGV and NGV are very complementary.
In this short review, we briefly recommend bridging the gap between conservation geneticists and conservation practitioners. We further encourage researchers and managers to collaborate to bring together knowledge and experience to develop appropriate management strategies for individual species/populations. Finally, to make conservation practitioners easily employ population genetics information in conservation practice, we propose a series of simplified and expected scenarios according to levels of neutral genetic parameters (which originally were proposed by Ottewell et al. [25]), providing examples in detail.

2. Bridging the Gap between Conservation Geneticists and Conservation Practitioners: Some Examples

As of 2011, there were only 20 (8%) out of 249 plant species reintroductions worldwide with some knowledge on genetic diversity [26]; this ratio may be higher now, yet statistics are lacking. In addition, it may be challenging and crucial to know precisely how practitioners have used genetic information for conservation implementation because many data are either currently unpublished or included in technical reports with restricted access [26,27]. Taylor et al. [28] contended that these barriers to implementation or similar adverse situations for conservation practitioners exist internationally. Britt et al. [29], using a meta-analysis of published conservation studies that employed genetic and genomic data sets, found that only 38% of the studies could inform conservation or management through clearly stated recommendations for action or policy. Thus, conservation researchers should communicate better with practitioners to integrate genetic findings into conservation implementation [25,29,30,31,32,33,34,35].
Recently, there has been increasing interest in reducing the gap between conservation science and practice [27,28,29,33,34,36,37,38]. In New Zealand, Taylor et al. [28] interviewed 148 conservation practitioners from the Department of Conservation regarding their attitude to, knowledge of, and experiences employing population genetics for conservation. Several important results emerged from the survey. First, conservation practitioners want to use population genetics for conservation management, but they do not routinely do so. Second, funding and expertise are the main barriers to the use of genetics in conservation (practitioners want to work with geneticists at universities or other institutes but are unsure how to reach them and do not fully understand how genetics might benefit them). Recent advances in understanding the genomic basis of adaptation would have widened the gap in incorporating genomic knowledge into active management plans [21,39,40]. To bridge the conservation gap between researchers and managers/practitioners, Taylor et al. [28] proposed “a plan to address barriers to use of genetics by conservation practitioners”, aiming to improve understanding and the integration of population genetics into conservation management. Specifically, this plan had three main suggestions. First, the improvement of the communication between conservation geneticists and practitioners through “genetics surgery” (where researchers answer genetics-based queries), “speed dating” (practitioners are introduced to multiple conservation geneticists to identify overlapping interests), and sabbaticals/exchanges (practitioners work closely with conservation geneticists and vice versa). Second, the increase of expertise among practitioners via one-day workshops, a YouTube channel, and online self-taught courses. Third, the creation of conservation genetics “hubs” through contact points and large-scale funding opportunities. Initiatives such as surveys may improve the researcher’s understanding of the problems and obstacles faced by practitioners, paving the way for enhanced communication and partnerships that enable more effective conservation strategies and activities. Recently, Cook et al. [40] proposed a “hypothetical sequential scenario” for an isolated but important population of a threatened and declining plant or animal species: first, understanding of management context; second, generation of relevant evidence (e.g., population genetics and fitness data); third, supporting the use of appropriate evidence; finally, collaboration between researchers and practitioners. Considering suggestions by Taylor et al. [28] and Cook et al. [40], we believe that the practitioners’ clear understanding of NGV and AGV presented in the previous section will help bridge the “research–implementation gap”.
It would be meaningful to introduce an example where conservation/restoration managers have directly applied genetic information. To develop a model of integrated (neutral) genetic and demographic conservation for threatened plants, Izumi Washitani and his colleagues [41] conducted a long-term project on restoring the threatened aquatic plant Nymphoides peltata in Lake Kasumigaura, Japan. As a result of restoration efforts, increases in the number of local populations and genetic diversity in the Lake Kasumigaura metapopulation led to population recovery. Unfortunately, although the population increased in the early stages of reintroduction, more recently, N. peltata populations are declining in almost all the sites in the lake, including the introduced site, and the genetic diversity (measured using neutral markers) is also declining (J. Nishihiro, pers. comm. in 2019). This result may not be surprising, given that the expected survival rate for reintroduced native species is low (on average, 52%, 19%, and 16% for survival, flowering, and fruiting, respectively, for reintroduced plants, based on 249 plant species reintroductions worldwide [26]). However, at present, it may be premature to determine whether the reintroduction of N. peltata in Lake Kasumigaura has been successful or not. Thus, there is no choice but to wait for their long-term monitoring. Despite the fact that restoration efforts will not always be entirely successful, conservation researchers, managers, and practitioners should keep in mind that knowledge of the NGV of target species, if the information of AGV is unavailable, is one of the most important traits that positively influence plant reintroduction outcomes [26]. The total absence of data on species’ genetic variation has often condemned the actions of restoration to failure, e.g., the failed reintroduction attempts of Lysimachia minoricensis on Minorca Island, Spain, probably occurred because the seeds that were used came from a single collection and thus lacked genetic variability [42]. This stresses the importance of assessing overall, genome-wide genetic diversity for rare and endangered plant species [43].
As noted above, to put population genetics information into the field, conservation practitioners may need a simplified prioritization framework for conservation strategies that are easily used [25], which helps to bridge the research–implementation gap. In the following two sections, we discuss this issue.

3. Expected Scenarios According to Levels of Neutral Genetic Parameters: A Simplified Proposal

Thanks to the large body of plant allozyme literature, researchers have demonstrated that a series of life history and ecological traits account for considerable variance in within- and among-population genetic diversity [44,45,46]. These traits include life forms, breeding systems, geographic ranges, and seed dispersal mechanisms, which can be used, therefore, to predict the levels and distribution of genetic diversity in seed plant species.
Focusing on life forms, forest trees, on average, have more allozyme genetic diversity within their populations than annuals or herbaceous perennials as measured by HeP-N (0.144 versus 0.101 or 0.096; the subscript N refers to neutral), %PP-N (47.9 versus 29.4 or 27.5; Table 1), and AP-N (1.74 versus 1.45 or 1.38; Table 1). A similar pattern was also found in overall species-level genetic diversity across life forms as measured by HeS-N (0.170 versus 0.154 or 0.125; Table 1), %PS-N (62.7 versus 49.2 or 42.8; Table 1), and AS-N (2.16 versus 2.02 or 1.75; Table 1). Furthermore, the degree of among-population allozyme genetic diversity in trees is substantially lower than in herbaceous perennials or annuals as measured by GST-N (0.089 versus 0.256 or 0.355; Table 1). A similar pattern is found for DNA-based markers (Table 1). Several factors are suggested to explain the higher within-population genetic diversity and the lower among-population genetic divergence in trees. These include a predominantly outcrossing mating system, higher levels of gene flow, longevity, tall statures, low population densities, occurrence in late successional communities, polycarpic nature, larger Ne, low linkage disequilibrium, presumably high levels of AGV, a higher basic number of chromosomes, more diversifying selection, or delayed maturity [45,47,48].
As Ottewell et al. [25] emphasized, the GST-N (or FST-N) and He-N parameters are preferentially used to measure NGV because they could be, at least partly, proxies of ecological and evolutionary processes, such as random genetic drift, habitat fragmentation, founder effects, or gene flow. Four main scenarios can be delineated to provide a clear, general guide to implement genetic management (“LH” or low GST-N (L) and high He (H), “HL” or high GST-N and low He, “LL” or low GST-N and low He, and “HH” or high GST-N and high He [25]; Figure 1). As Ottewell et al. [25] proposed, if the parameter FIS (inbreeding coefficient) is also considered, then eight combinations are produced; however, here, we only deal with GST-N (or FST-N) and He-N because estimates of FIS are often sensitive to sampling strategies and the clonal structure of vegetatively reproducing plants.
Based on the mean values for allozymes reported in Table 1 (based on an extensive database of about 740 species), we proposed a classification of both the GST-N and HeP-N values into two levels (high (H) or low (L); see [48] for more details). For trees, GST-N and HeP-N values below 0.089 and 0.144, respectively, were considered as “L”, whereas values higher than these thresholds were regarded as “H”. For herbaceous perennials, using the same scheme, GST-N < 0.256 as L and GST > 0.256 as H, whereas HeP-N < 0.096 as L, and HeP-N > 0.096 as H. Compared with allozymes, mean values for SSRs and other DNA-based dominant markers were obtained from a much smaller body of studies [49]. Since Nybom [49] classified plants according to the life form category as annuals, short-lived perennials, and long-lived perennials, the categories “long-lived perennials” and “woody perennials” were considered as equivalent. As with allozymes, we took the means provided by Nybom [49] as threshold values (Table 1). For long-lived perennials, the threshold values of ΦST-N, GST-N, and HPOP for RAPDs were 0.25, 0.19, and 0.25, respectively, and GST-N and HeP-N values for SSRs were 0.19 and 0.68, respectively. For short-lived perennials, the threshold values of ΦST-N, GST-N, and HPOP for RAPDs were 0.41, 0.32, and 0.20, respectively, and GST-N and HeP-N values for SSRs were 0.31 and 0.55, respectively. Threshold values for annuals for each marker are also detailed in Table 1. As Nybom [49] only provides means of Hpop and ΦST-N (or GST-N) for RAPDs, for practical reasons we consider that these thresholds could also be applicable to other dominant markers such as AFLPs and ISSRs.
The first category (LH; low among-population differentiation (GST-N or FST-N) and high within-population diversity (HeP-N)) is expected to be found in many outcrossing and high dispersal species with regional or wide distributions. Populations of these species would have been historically connected, likely having kept large Ne (“healthy” populations [25]). In contrast, the HL (high differentiation and low diversity) type is often found for rare, endemic, or threatened tree and herbaceous species. This genetic pattern would result from populations with historically low Ne and disjunct distribution, traits that would have persisted for a long period of time. Compared to the LH and HL categories, the LL (low differentiation and low diversity) and the HH (high differentiation and high diversity) ones are less commonly found. The LL category is expected to be found fairly often in plant species with populations that have been historically connected but with low Ne and/or a signature of historical founder effects or bottlenecks. Species recovering from range contractions (e.g., post-glacial founder effects through post-glacial recolonizations) would show the LL pattern. The HH category would be expected in plant species with disjunct distribution but large Ne and little contemporary gene flow; examples may include species with special habitats or species contracted to refugial areas with historically large Ne [25].

4. A Prioritization Framework for Conservation Strategies Based on Neutral Genetic Diversity Scenarios

To be useful for conservation, however, the four genetic categories (LH, HL, LL, and HH) should be linked to specific recommendations and guidelines for the prioritization of population-level management [25,48]. As for the long-term management and conservation of those plant species under the LH scenario, Ottewell et al. [25] suggested that translocation between populations is a viable option to enhance Ne. Management of ecological and demographic threats at the species level is needed to maintain population size and gene flow. Facilitation of pollen and seed immigration would be necessary to minimize the effects of inbreeding and outbreeding depression. As for in situ restoration efforts (e.g., reinforcements), we suggest that seeds of these species could be sourced from a few populations with low pairwise GST values with the population to be restored. This strategy will improve the chances of successful restoration if adaptive traits are correlated with neutral marker loci. In addition, just a few populations would be needed to be protected in situ yet contrasting habitats should be taken into consideration. As for ex situ and in situ conservation efforts, populations with high HeP-N (and AR) should be targeted, assuming that these populations also harbor high genetic diversity (AGV) at phenotypically important traits.
Representative allozyme-based examples of the LH category are the trees Pinus rigida (GST-N = 0.023 and HeP-N = 0.146 [50]) and Fagus grandifolia (GST-N = 0.056 and HeP-N = 0.165 [51]) in the northeastern USA, and the herbaceous perennials Liatris helleri (GST-N = 0.159 and HeP-N = 0.219 [52]) and Asclepias exaltata (GST-N = 0.093 and HeP-N = 0.182 [53]) in the southeastern USA, and Cymbidium goeringii (GST-N = 0.098 and HeP-N = 0.240 [54]; Figure 1) in the Korean Peninsula. Except for C. goeringii, all four species occur in the old-growth forests of the Appalachians in the southeastern USA, which are considered refugia at the Last Glacial Maximum (21,000–18,000 years ago). We must keep in mind that many published papers using NGV belong to the LH scenario.
Under the HL scenario, conservation managers and practitioners should consider that the management activities for HL plants (e.g., ongoing translocations) are more expensive in terms of management intensity and cost than those for LH ones. Notably, many rare and threatened species fall into this category [44]. Translocation between populations is a recommended measure, but it should be done with special caution to minimize potential outbreeding depression. Ottewell et al. [25] also indicate that a means for recovering in situ presumed total genetic diversity from seed banks would be necessary and, since the small population sizes of these species make them susceptible to the loss of total genetic diversity, in situ conservation efforts should emphasize habitat protection. We suggest that ex situ seed conservation in HL plant species should also be a priority, and germplasm resources should be established from seeds collected from as many populations as possible with high HeP-N (and AR), rather than only from a few populations. The introduction of enough total genetic diversity is necessary so that natural selection can respond to the population’s environment being restored [55]. In addition, the planting of seedlings of these species in potential habitats that represent future climatic conditions could also be a successful conservation strategy [48].
The HL scenario is commonly found in rare herbaceous understory species. Examples include the herbaceous perennial Helonias bullata (allozymes, GST-N = 0.306 and HeP-N = 0.029 [56]) in the old-growth forests of the Appalachians, the herb Urophysa rockii (SSRs, ΦST-N = 0.669 and HeP-N = 0.341 [57]; Figure 1) in southwestern China, the narrow endemic perennial herb Clematis acerifolia (allozymes, GST-N = 0.273 and HeP-N = 0.072 [58]) in north-eastern China, and the rare small carnivorous plant Drosera rotundifolia in southern Korea (allozymes, GST-N = 0.817 and HeP-N = 0.005 [59]). However, this pattern has also been observed in some trees. Despite their current wide distributions, some woody species with a history of small and disjunct populations, smaller founder populations, or populations that have experienced past bottlenecks might harbor low HeP-N. This scenario has been observed for Pinus resinosa (SSRs, HeP-N = 0.078 [60]) in two populations in Virginia and West Virginia in the Southern Appalachians (eastern USA), and for Picea asperata (allozymes, GST-N = 0.311 and HeP-N = 0.096 [61]) in southwestern China.
Diversity 13 00552 g001 550
Figure 1. Flow chart on the applications of neutral genetic markers to conservation, restoration, and management strategies. We follow the four genetic scenarios according to levels and degree of neutral genetic diversity (i.e., LH or low GST-N (L) and high He (H), HL or high GST-N and low He, LL or low GST-N and low He, and HH or high GST-N and high He, where “L” and “H” stand for “low” and “high”, respectively; Ottewell et al. (2016)). For details of conservation management strategies for each genetic scenario, refer to the text. Reference for LH is from Chung et al. [54], HL from Xie et al. [57], LL from Chung et al. [62], and HH from Chung et al. [63]. Photo of Urophysa rockii was taken from Xie et al. [64], which is under license CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/ accessed on 21 September 2021)–no changes were made by us.
Figure 1. Flow chart on the applications of neutral genetic markers to conservation, restoration, and management strategies. We follow the four genetic scenarios according to levels and degree of neutral genetic diversity (i.e., LH or low GST-N (L) and high He (H), HL or high GST-N and low He, LL or low GST-N and low He, and HH or high GST-N and high He, where “L” and “H” stand for “low” and “high”, respectively; Ottewell et al. (2016)). For details of conservation management strategies for each genetic scenario, refer to the text. Reference for LH is from Chung et al. [54], HL from Xie et al. [57], LL from Chung et al. [62], and HH from Chung et al. [63]. Photo of Urophysa rockii was taken from Xie et al. [64], which is under license CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/ accessed on 21 September 2021)–no changes were made by us.
Diversity 13 00552 g001
Under the LL scenario, a few populations could be sampled, but seeds should be taken from a high number of individuals within each selected population for ex situ conservation. As for in situ restoration, management to increase recruitment and facilitate pollen and seed immigration, and the active translocation of individuals (by sourcing recruits from genetically diverse populations elsewhere) to increase population size, especially when remnant populations are highly inbred, would be suitable measures [25]. At the same time, conservation managers should employ a means for recovering total genetic diversity in situ (e.g., facilitating recoveries from seed banks). Examples fitting the LL scenario include the two terrestrial orchids Bletilla striata (allozymes, GST-N = 0.130 and HeP-N = 0.060 [62]; Figure 1) in southern Korea, a species of presumably post-glacial origin (immigrated from southern Japan), and Dendrobium officinale (AFLPs, ΦST-N = 0.263 and Hpop = 0.143 [65]) from six populations in refugia in southwestern China. Other allozyme-based examples are the rhizomatous evergreen small subshrub Chimaphila japonica (GST-N = 0.028 and HeP-N = 0.030 [66]) and the perennial herb Lycoris sanguinea var. koreana (GST-N = 0.092 and HeP-N = 0.052 [67]), both in southern Korea.
Finally, under the HH scenario, a large number of populations are needed, but with a small number of samples per population, for ex situ conservation because extant populations would be healthy but divergent, constituting individual management units [25]. Perhaps, ecological efforts, rather than genetic ones, have to be taken into account, e.g., by focusing on managing habitats and ecological threats to maintain as many populations as possible across the species range and to maintain large sizes for them. There are some allozyme-based examples of trees showing an HH pattern, including Pinus pungens, which occurs in several disjunct populations ranging from north Georgia to Pennsylvania in the eastern USA (GST-N = 0.135 and HeP-N = 0.242 [68]), the tree Manglietia patungensis (GST-N = 0.165 and HeP-N = 0.192 [69]) from southwestern China, and Hylotelephium (=Sedium) ussuriense (GST-N = 0.261 and HeP-N = 0.156 [63]; Figure 1), found in only one location in Juwangsan National Park in the southern Korean Peninsula region. This pattern has also been observed in the diploid populations of the perennial weed Turnera ulmifolia var. intermedia from Central and South America (allozymes, GST-N = 0.480 and HeP-N = 0.130 [70]), and in Trillium grandiflorum (allozymes, GST-N = 0.530 and HeP-N = 0.170 [71]) in the eastern USA, for which samples were included from both glaciated and non-glaciated regions.

5. Conclusions

What stands out in Ottewell et al. [25] is that they are proposing a prioritization framework that is, notably, very clearly defined and efficiently written, which makes the genetic management strategies for each scenario easy to be understood by non-experts. As an improvement of Ottewell et al.’s [25] treatment, we here provide representative examples for each of the four scenarios that are based on our proposal of genetic judgment as “H” or “L” using average values. We expect that such kinds of studies will help researchers and managers/practitioners to work in partnership to bring together knowledge, expertise, and experience, which is a mandatory step for developing appropriate synthetic management strategies for individual species. Indeed, the NGV information could still be useful for bridging the gap between researchers and practitioners developing and implementing appropriate conservation measures.

Author Contributions

Conceptualization, M.Y.C. and M.G.C.; writing—original draft preparation, M.G.C.; writing—review and editing, M.Y.C., S.S., J.L.-P., K.M. and M.G.C.; visualization, M.G.C. and M.Y.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Basic Science Research Program through the National Research Foundation (NRF), funded by the Ministry of Science and ICT of the Republic of Korea (NRF- 2020R1I1A3074635 to M.Y.C. and NRF-2017R1A2B4012215 to M.G.C.), and was partly carried out as part of the study on population characteristics and conservation management strategies of rare plants in the Korea National Arboretum (KNA1-2-37, 20-4), who supported M.G.C. in 2021. K.M. was supported by the National Natural Science Foundation of China (grant no. U20A2080, 31622015) while J.L.-P. is funded by the Spanish Ministerio de Ciencia e Innovación (PID2020-119163GB-I00).

Acknowledgments

We would like to thank J.L. Hamrick, J.D. Nason, J. Merilä, and A. Caballero for helps during writing.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Harrison, K.A.; Pavlova, A.; Telonis-Scott, M.; Sunnucks, P. Using Genomics to Characterize Evolutionary Potential for Conservation of Wild Populations. Evol. Appl. 2014, 7, 1008–1025. [Google Scholar] [CrossRef] [PubMed]
  2. DeWoody, J.A.; Harder, A.M.; Mathur, S.; Willoughby, J.R. The Long-Standing Significance of Genetic Diversity in Conservation. Mol. Ecol. 2021, 30, 4147–4154. [Google Scholar] [CrossRef]
  3. Campbell, R.K. Soils, Seed-Zone Maps, and Physiography: Guidelines for Seed Transfer of Douglas-Fir in South-Western Oregon. For. Sci. 1991, 37, 973–986. [Google Scholar]
  4. Rehfeldt, G.E. Genetic Variation, Climate Models and the Ecological Genetics of Larix occidentalis. For. Ecol. Manag. 1995, 78, 21–37. [Google Scholar] [CrossRef]
  5. Mazer, S.M.; LeBuhn, G. Genetic Variation in Life-History Traits: Heritability Estimates within and Genetic Differentiation among Populations. In Life History Evolution in Plants; Vuorisalo, T.O., Mutikainen, P.K., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands, 1999; pp. 86–171. [Google Scholar]
  6. Willi, Y.; Van Buskirk, J.; Hoffmann, A.A. Limits to the Adaptive Potential of Small Populations. Annu. Rev. Ecol. Evol. Syst. 2006, 37, 433–458. [Google Scholar] [CrossRef]
  7. Shirk, R.Y.; Hamrick, J.L. Multivariate Adaptation but no Increase in Competitive Ability in Invasive Geranium carolinianum L. (Geraniaceae). Evolution 2014, 68, 2945–2959. [Google Scholar] [CrossRef] [PubMed]
  8. Ye, Q.; Tang, F.; Wei, N.; Yao, X. Molecular and Quantitative Trait Variation within and among Small Fragmented Populations of the Endangered Plant Species Psilopeganum sinense. Ann. Bot. 2014, 113, 79–86. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Flanagan, S.P.; Forester, B.R.; Latch, E.K.; Aitken, S.N.; Hoban, S. Guidelines for Planning Genomic Assessment and Monitoring of Locally Adaptive Variation to Inform Species Conservation. Evol. Appl. 2018, 11, 1035–1052. [Google Scholar] [CrossRef] [PubMed]
  10. Vimmerstedt, J.P. Southern Appalachian White Pine Plantations Site, Volume, and Yield; USDA Forest Service, Southeastern Forest Experimental Station: Asheville, NC, USA, 1962; pp. 1–15.
  11. Anekonda, T.S.; Lomas, M.C.; Adams, W.T.; Kavanagh, K.L.; Aitken, S.N. Genetic Variation in Drought Hardiness of Coastal Douglas-Fir Seedlings from British Columbia. Can. J. For. Res. 2002, 32, 1701–1716. [Google Scholar] [CrossRef] [Green Version]
  12. Arend, M.; Kuster, T.; Günthardt-Goerg, M.S.; Dobbertin, M. Provenance-Specific Growth Responses to Drought and Air-Warming in Three European Oak Species (Quercus robur, Q. petraea and Q. pubescens). Tree Physiol. 2011, 31, 287–297. [Google Scholar] [CrossRef] [Green Version]
  13. Gary, L.A.; Grat, T.; Mbogga, M.S.; Chen, P.-Y.; Hamann, A. Assisted Migration to Address Climate Change: Recommendations for Aspen Reforestation in Western Canada. Ecol. Appl. 2011, 21, 1591–1603. [Google Scholar] [CrossRef] [PubMed]
  14. Alberto, F.J.; Aitken, S.N.; Alía, R.; González-Martínez, S.C.; Hänninen, H.; Kremer, A.; Lefévre, F.; Lenormand, T.; Yeaman, S.; Whetten, R. Potential for Evolutionary Responses to Climate Change-Evidence from Tree Populations. Glob. Chang. Biol. 2013, 19, 1645–1661. [Google Scholar] [CrossRef] [Green Version]
  15. George, J.; Grabner, M.; Karanitsch-Ackerl, S.; Mayer, K.; Weißenbacher, L.; Schueler, S. Genetic Variation, Phenotypic Stability, and Repeatability of Drought Response in European Larch Throughout 50 years in a Common Garden Experiment. Tree Physiol. 2017, 37, 33–46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  16. Sork, V.L. Genomic Studies of Local Adaptation in Natural Plant Populations. J. Hered. 2018, 109, 3–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Anderson, J.T.; Song, B.-H. Plant Adaptation to Climate Change—Where Are We? J. Syst. Evol. 2020, 58, 533–545. [Google Scholar] [CrossRef] [PubMed]
  18. Capblancq, T.; Fitzpatrick, M.C.; Bay, R.A.; Exposito-Alonso, M.; Keller, S.R. Genomic Prediction of (Mal)Adaptation Across Current and Future Climatic Landscapes. Annu. Rev. Ecol. Evol. Syst. 2020, 51, 245–269. [Google Scholar] [CrossRef]
  19. Mahony, C.R.; MacLachlan, I.R.; Lind, B.M.; Yoder, J.B.; Wang, T.; Aitken, S.N. Evaluating Genomic Data for Management of Local Adaptation in a Changing Climate: A lodgepole Pine Case Study. Evol. Appl. 2019, 13, 116–131. [Google Scholar] [CrossRef] [Green Version]
  20. Fernandez-Fournier, P.; Lewthwaite, J.M.M.; Mooers, A.Ø. Do We Need to Identify Adaptive Genetic Variation When Prioritizing Populations for Conservation? Conserv. Genet. 2021, 22, 205–216. [Google Scholar] [CrossRef]
  21. Funk, W.C.; Forester, B.R.; Converse, S.J.; Darst, C.; Morey, S. Improving Conservation Policy with Genomics: A Guide to Integrating Adaptive Potential into U.S. Endangered Species Act Decisions for Conservation Practitioners and Geneticists. Conserv. Genet. 2018, 20, 115–134. [Google Scholar] [CrossRef]
  22. García-Dorado, A.; Caballero, A. Neutral Genetic Diversity as a Useful Tool for Conservation Biology. Conserv. Genet. 2021, 22, 541–545. [Google Scholar] [CrossRef]
  23. Kardos, M.; Armstrong, E.; Fitzpatrick, S.; Hauser, S.; Hedrick, P.; Miller, J.; Tallmon, D.A.; Funk, W.C. The Crucial Role of Genome-Wide Genetic Variation in Conservation. bioRxiv 2021. [Google Scholar] [CrossRef]
  24. Teixeira, J.C.; Huber, C.D. The Inflated Significance of Neutral Genetic Diversity in Conservation Genetics. Proc. Natl. Acad. Sci. USA 2021, 118, e2015096118. [Google Scholar] [CrossRef]
  25. Ottewell, K.M.; Bickerton, D.C.; Byrne, M.; Lowe, A.J. Bridging the Gap: A genetic Assessment Framework for Population-Level Threatened Plant Conservation Prioritization and Decision-Making. Divers. Distrib. 2016, 22, 174–188. [Google Scholar] [CrossRef] [Green Version]
  26. Godefroid, S.; Piazza, C.; Rossi, G.; Buord, S.; Stevens, A.-D.; Aguraiuja, R.; Cowell, C.; Weekley, C.W.; Voggk, G.; Iriondo, J.M.; et al. How Successful are Plant Species Reintroductions? Biol. Conserv. 2011, 144, 672–682. [Google Scholar] [CrossRef]
  27. Hoban, S.M.; Hauffe, H.C.; Pérez-Espona, S.; Arntzen, J.W.; Bertorelle, G.; Bryja, J.; Frith, K.; Gaggiotti, O.; Galbusera, P.; Godoy, J.; et al. Bringing Genetic Diversity to the Forefront of Conservation Policy and Management. Conserv. Genet. Resour. 2013, 5, 593–598. [Google Scholar] [CrossRef] [Green Version]
  28. Taylor, H.R.; Dussex, N.; van Heezik, Y. Bridging the Conservation Genetics Gap by Identifying Barriers to Implementation for Conservation Practitioners. Glob. Ecol. Conserv. 2017, 10, 231–242. [Google Scholar] [CrossRef]
  29. Britt, M.; Haworth, S.E.; Johnson, J.B.; Martchenko, D.; Shafer, A.B. The Importance of Non-Academic Coauthors in Bridging the Conservation Genetics Gap. Biol. Conserv. 2018, 218, 118–123. [Google Scholar] [CrossRef]
  30. Hulme, P.E. Bridging the Knowing-Doing Gap: Know-Who, Know-What, Know-Why, Know-How and Know-When. J. Appl. Ecol. 2014, 51, 1131–1136. [Google Scholar] [CrossRef]
  31. Rivers, M.C.; Brummitt, N.A.; Lughadha, E.N.; Meagher, T.R. Do Species Conservation Assessments Capture Genetic Diversity? Glob. Ecol. Conserv. 2014, 2, 81–87. [Google Scholar] [CrossRef] [Green Version]
  32. Haig, S.M.; Miller, M.P.; Bellinger, R.; Draheim, H.M.; Mercer, D.M.; Mullins, T.D. The Conservation Genetics Juggling Act: Integrating Genetics and Ecology, Science and Policy. Evol. Appl. 2016, 9, 181–195. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Fabian, Y.; Bollmann, K.; Brang, P.; Hein, C.; Olschewski, R.; Rigling, A.; Stofer, S.; Holderegger, R. How to Close the Science-Practice Gap in Nature Conservation? Information Sources Used by Practitioners. Biol. Conserv. 2019, 235, 93–101. [Google Scholar] [CrossRef]
  34. Holderegger, R.; Balkenhol, N.; Bolliger, J.; Engler, J.O.; Gugerli, F.; Hochkirch, A.; Nowak, C.; Segelbacher, G.; Wider, A.; Zachos, F.E. Conservation Genetics: Linking Science with Practice. Mol. Ecol. 2019, 28, 3848–3856. [Google Scholar] [CrossRef] [Green Version]
  35. Hoban, S.; Bruford, M.; D’Urban Jackson, J.; Lopes-Fernandes, M.; Heuertz, M.; Hohenlohe, P.A.; Paz-Vinas, I.; Sjögren-Gulve, P.; Segelbacher, G.; Vernesi, C.; et al. Genetic Diversity Targets and Indicators in the CBD post-2020 Global Biodiversity Framework must be Improved. Biol. Conserv. 2020, 248, 108654. [Google Scholar] [CrossRef]
  36. Knight, A.T.; Cowling, R.M.; Rouget, M.; Balmford, A.; Lombard, A.T.; Campbell, B.M. Knowing but Not Doing: Selecting priority Conservation Areas and the Research–Implementation Gap. Conserv. Biol. 2008, 22, 610–617. [Google Scholar] [CrossRef]
  37. Dubois, N.S.; Gomez, A.; Carlson, S.; Russell, D. Bridging the Research-Implementation Gap Requires Engagement from Practitioners. Conserv. Sci. Pract. 2019, 2, e134. [Google Scholar] [CrossRef] [Green Version]
  38. Taft, H.R.; McCoskey, D.N.; Miller, J.M.; Pearson, S.K.; Coleman, M.A.; Fletcher, N.K.; Mittan, C.S.; Meek, M.H.; Barbosa, S. Research–Management Partnerships: An Opportunity to Integrate Genetics in Conservation Actions. Conserv. Sci. Pract. 2020, 2, e218. [Google Scholar] [CrossRef]
  39. Mable, B.K. Conservation of Adaptive Potential and Functional Diversity: Integrating Old and New Approaches. Conserv. Genet. 2019, 20, 89–100. [Google Scholar] [CrossRef] [Green Version]
  40. Cook, C.N.; Beever, E.A.; Thurman, L.L.; Thompson, L.M.; Gross, J.E.; Whiteley, A.R.; Nicotra, A.B.; Szymanski, J.A.; Botero, C.A.; Hall, K.R.; et al. Supporting the Adaptive Capacity of Species through more Effective Knowledge Exchange with Conservation Practitioners. Evol. Appl. 2021, 4, 1969–1979. [Google Scholar] [CrossRef]
  41. Nishihiro, J.; Uesugi, S.R.; Takagawa, I.; Washitani, I. Toward the Restoration of a Sustainable Population of a Threatened Aquatic Plant, Nymphoides peltata: Integrated Genetic/Demographic Studies and Practices. Biol. Conserv. 2009, 142, 1906–1912. [Google Scholar] [CrossRef]
  42. Ibáñez, O.; Calero, C.; Mayol, M.; Rosselló, J.A. Isozyme uniformity in a wild extinct insular plant, Lysimachia minoricensis J.J. Rodr. (Primulaceae). Mol. Ecol. 1999, 8, 813–817. [Google Scholar] [CrossRef]
  43. Laikre, L.; Hoban, S.; Bruford, M.W.; Segelbacher, G.; Allendorf, F.W.; Gajardo, G.; González Rodríguez, A.; Hedrick, P.W.; Heuertz, M.; Hohenlohe, P.A.; et al. Post-2020 Goals Overlook Genetic Diversity. Science 2020, 367, 1083–1085. [Google Scholar] [CrossRef] [Green Version]
  44. Hamrick, J.L.; Godt, M.J.W. Allozyme Diversity in Plant Species. In Plant Population Genetics, Breeding and Germplasm Resources; Brown, A.H.D., Clegg, M.T., Kahler, A.L., Weir, B.S., Eds.; Sinauer: Sunderland, MA, USA, 1989; pp. 43–63. [Google Scholar]
  45. Hamrick, J.L.; Godt, M.J.W. Effects of Life History Traits on Genetic Diversity in Plant Species. Philos. Trans. R. Soc. B 1996, 351, 1291–1298. [Google Scholar]
  46. Hamrick, J.L.; Godt, M.J.W. Sherman-Broyles, S.L. Factors Influencing Levels of Genetic Diversity in Woody Plant Species. New For. 1992, 6, 95–124. [Google Scholar] [CrossRef]
  47. Petit, R.; Hampe, A. Some Evolutionary Consequences of Being a Tree. Annu. Rev. Ecol. Evol. Syst. 2006, 37, 187–214. [Google Scholar] [CrossRef] [Green Version]
  48. Chung, M.Y.; Son, S.; Herrando-Moraira, S.; Tang, C.Q.; Maki, M.; Kim, Y.D.; López-Pujol, J.; Hamrick, J.L.; Chung, M.G. Incorporating Differences between Genetic Diversity of Trees and Herbaceous Plants in Conservation Strategies. Conserv. Biol. 2020, 34, 1142–1151. [Google Scholar] [CrossRef] [PubMed]
  49. Nybom, H. Comparison of Different Nuclear DNA Markers for Estimating Intraspecific Genetic Diversity in Plants. Mol. Ecol. 2004, 13, 1143–1155. [Google Scholar] [CrossRef]
  50. Guries, R.P.; Ledig, F.T. Genetic Diversity and Population Structure in pitch pine (Pinus rigida Mill.). Evolution 1982, 36, 387–402. [Google Scholar] [CrossRef]
  51. Houston, D.B.; Houston, D.R. Allozyme Genetic Diversity among Fagus grandifolia Trees Resistant or Susceptible to Beech Bark Disease in Natural Populations. Can. J. For. Res. 2000, 30, 778–789. [Google Scholar] [CrossRef]
  52. Godt, M.J.W.; Hamrick, J.L. Genetic Diversity and Morphological Differentiation in Liatris helleri (Asteraceae), a Threatened Plant Species. Biodiver. Conserv. 1996, 5, 461–471. [Google Scholar] [CrossRef]
  53. Broyles, S.B.; Wyatt, R. Allozyme Diversity and Genetic Structure in Southern Appalachian Populations of Asclepias exaltata. Syst. Bot. 1993, 18, 18–30. [Google Scholar] [CrossRef]
  54. Chung, M.Y.; Chung, M.G. Allozyme Diversity and Population Structure in Korean Populations of Cymbidium goeringii (Orchidaceae). J. Plant Res. 1999, 112, 139–144. [Google Scholar] [CrossRef]
  55. Bucharova, A.; Bossdorf, O.; Hölzel, N.; Kollman, J.; Prasse, R.; Durka, W. Mix and Match: Regional Admixture Provenancing Strikes a Balance among Different Seed-Searching Strategies for Ecological Restoration. Conserv. Genet. 2019, 20, 7–17. [Google Scholar] [CrossRef]
  56. Godt, M.J.W.; Hamrick, J.L.; Bratton, S. Genetic Diversity in a Threatened Wetland Species, Helonias bullata (Liliaceae). Conserv. Biol. 1995, 9, 596–604. [Google Scholar] [CrossRef]
  57. Xie, D.-F.; Li, M.-J.; Tan, J.-B.; Price, M.; Xiao, Q.-Y.; Zhou, S.-D.; Yu, Y.; He, X.J. Phylogeography and Genetic Effects of Habitat Fragmentation on Endemic Urophysa (Ranunculaceae) in Yungui Plateau and Adjacent Regions. PLoS ONE 2017, 12, e0186378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  58. López-Pujol, J.; Zhang, F.-M.; Ge, S. Population Genetics and Conservation of the Critically Endangered Clematis acerifolia (Ranunculaceae). Can. J. Bot. 2005, 83, 1248–1256. [Google Scholar] [CrossRef] [Green Version]
  59. Chung, M.Y.; López-Pujol, J.; Chung, M.G. Population History of the Two Carnivorous Plants Drosera peltata var. nipponica and Drosera rotundifolia (Droseraceae) in Korea. Am. J. Bot. 2013, 11, 2231–2239. [Google Scholar] [CrossRef]
  60. Boys, J.; Cherry, M.; Dayanandan, S. Microsatellite Analysis Reveals Genetically Disjunct Populations of Red Pine (Pinus resinosa, Pinaceae). Am. J. Bot. 2005, 92, 833–841. [Google Scholar] [CrossRef] [Green Version]
  61. Luo, J.; Wang, Y.; Korpelainen, H.; Li, C. Allozyme Variation in Natural Populations of Picea Asperata. Silva Fenn. 2005, 39, 167–176. [Google Scholar] [CrossRef] [Green Version]
  62. Chung, M.Y.; López-Pujol, J.; Chung, M.G. Low Genetic Diversity in Marginal Populations of Bletilla striata (Orchidaceae) in Southern Korea: Insights into Population History and Implications for Conservation. Biochem. Syst. Ecol. 2013, 46, 88–96. [Google Scholar] [CrossRef]
  63. Chung, M.Y.; López-Pujol, J.; Chung, M.G. Comparative Genetic Structure between Sedium ussuriense and S. kamtschaticum (Crassulaceae). Am. J. Bot. 2014, 101, 946–956. [Google Scholar] [CrossRef]
  64. Xie, D.-F.; Cheng, R.-Y.; Fu, X.; Zhang, X.-Y.; Price, M.; Lan, Y.-L.; Wang, C.-B.; He, X.-J. A Combined Morphological and Molecular Evolutionary Analysis of Karst-Environment Adaptation for the Genus Urophysa (Ranunculaceae). Front. Plant Sci. 2021, 12, 667988. [Google Scholar] [CrossRef]
  65. Li, X.; Ding, X.; Chu, B.; Zhou, Q.; Ding, G.; Gu, S. Genetic Diversity Analysis and Conservation of the Endangered Chinese Endemic Herb Dendrobium officinale Kimura et Migo (Orchidaceae) Based on AFLP. Genetica 2008, 133, 159–166. [Google Scholar] [CrossRef] [PubMed]
  66. Chung, M.G.; Kang, S.S. Allozyme Genetic and Clonal Diversity within Populations of Chimaphila japonica and Pyrola japonica (Pyrolaceae). Isr. J. Plant Sci. 1996, 44, 259–271. [Google Scholar] [CrossRef]
  67. Chung, M.G. Allozyme Diversity in the Endangered Herb Lycoris sanguinea Var. koreana (Amaryllidaceae). Ann. Bot. Fenn. 1999, 36, 1–7. [Google Scholar]
  68. Gibson, J.P.; Hamrick, J.L. Genetic Diversity and Structure in Pinus pungens (Table Mountain Pine) Populations. Can. J. For. Res. 1991, 21, 635–642. [Google Scholar] [CrossRef]
  69. He, J.S.; Li, Z.Z.; Huang, H.W. Allozymic Genetic Diversity in Manglietia patungensis, an Endangered Species, and Its Conservation Strategies. Biodivers. Sci. 2005, 13, 27–35, (In Chinese with English abstract). [Google Scholar] [CrossRef]
  70. Shore, J.S. Tetrasomic Inheritance and Isozyme Variation in Turnera ulmifolia vars. elegans Urb. and intermedia Urb. (Turneraceae). Heredity 1991, 66, 305–312. [Google Scholar] [CrossRef]
  71. Griffin, S.R.; Barrett, S.C.H. Post-Glacial History of Trillium grandiflorum (Melanthiaceae) in Eastern North America: Inferences from Phylogeography. Am. J. Bot. 2004, 91, 465–473. [Google Scholar] [CrossRef] [Green Version]
Table
Table 1. Mean levels and distribution of allozyme, RAPD, and SSR diversity of plant species representing different life forms (for allozymes from [48] and for RAPDs and SSRs from [49]) a.
Table 1. Mean levels and distribution of allozyme, RAPD, and SSR diversity of plant species representing different life forms (for allozymes from [48] and for RAPDs and SSRs from [49]) a.
ParameterAnnualsHerbaceous PerennialsWoody Perennials
Allozyme
NP, NS226, 226228, 215213/214
%PP-N29.4 b27.5 b47.9 a
%PS-N49.2 b42.8 b62.7 a
AP-N1.45 b1.38 b1.74 a
AS-N2.02 ab1.75 b2.16 a
HeP-N0.101 b0.096 b0.144 a
HeS-N0.154 b0.125 c0.170 a
GST-N0.355 a0.256 b0.089 c
ParameterAnnualsShort-lived perennialsLong-lived perennials b
RAPD c
N61737
Hpop0.13 b0.20 ab0.25 a
N104560
ΦST-N0.62 a0.41 b0.25 c
N21824
GST-N0.47 a0.32 ab0.19 b
SSR
N152959
HeP-N0.46 b0.55 b0.68 a
N41217
GST-N0.40 a0.31 ab0.19 b
aNP, NS, number of entries at population and species levels, respectively; N, number of entries; subscripts “P” and “S” indicate population and species levels, respectively, and subscript “N” indicates neutral. %P, the percentage of polymorphic loci; A, mean number alleles per locus; He, gene diversity or Hardy–Weinberg expected heterozygosity both at monomorphic and polymorphic loci; GST (or FST), among-population genetic differentiation; ΦST, fixation index among populations relative to the total genetic variation among individuals. Values sharing the same letter in a column are not significantly different at p < 0.05. The table was modified from Tables 2 and 3 of Chung et al. [48]. b To facilitate the comparisons between allozymes and other molecular markers, we equate “long-lived perennials” to “woody perennials”. c Nybom [49] provides the only means of Hpop and ΦST-N (or GST-N) for RAPDs, but for practical reasons these thresholds are also applicable to AFLPs and ISSRs.
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Chung, M.Y.; Son, S.; López-Pujol, J.; Mao, K.; Chung, M.G. Plant Conservation Practitioners Can Benefit from Neutral Genetic Diversity. Diversity 2021, 13, 552. https://doi.org/10.3390/d13110552

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Chung MY, Son S, López-Pujol J, Mao K, Chung MG. Plant Conservation Practitioners Can Benefit from Neutral Genetic Diversity. Diversity. 2021; 13(11):552. https://doi.org/10.3390/d13110552

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Chung, Mi Yoon, Sungwon Son, Jordi López-Pujol, Kangshan Mao, and Myong Gi Chung. 2021. "Plant Conservation Practitioners Can Benefit from Neutral Genetic Diversity" Diversity 13, no. 11: 552. https://doi.org/10.3390/d13110552

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Chung, M. Y., Son, S., López-Pujol, J., Mao, K., & Chung, M. G. (2021). Plant Conservation Practitioners Can Benefit from Neutral Genetic Diversity. Diversity, 13(11), 552. https://doi.org/10.3390/d13110552

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