REFERENCES
Aguilar, A., Roemer, G., Debenham, S., Binns, M., Garcelon, D., &
Wayne, R. K. (2004). High MHC diversity maintained by balancing
selection in an otherwise genetically monomorphic mammal.Proceedings of the National Academy of Sciences of the United
States of America , 101 , 3490–3494.
https//doi.org/10.1073/pnas.0306582101
Allendorf, F. W. (2017). Genetics and the conservation of natural
populations: allozymes to genomes. Molecular Ecology , 26 ,
420–430. https//doi.org/10.1111/mec.13948
Allendorf, F. W., Hohenlohe, P. A., & Luikart, G. (2010). Genomics and
the future of conservation genetics. Nature Reviews Genetics ,11 , 697–709. https//doi.org/10.1038/nrg2844
Bekessy, S. A., Ennos, R. A., Burgman, M. A., Newton, A. C., & Ades, P.
K. (2003). Neutral DNA markers fail to detect genetic divergence in an
ecologically important trait. Biological Conservation ,110 , 267–275. https//doi.org/S0006-3207(02)00225-2
Bell, G. (2010). Fluctuating selection: the perpetual renewal of
adaptation in variable environments. Philosophical Transactions of
the Royal Society B: Biological Sciences , 365 , 87–97.https://doi.org/10.1098/rstb.2009.0150
Bergland, A. O., Behrman, E. L., O’Brien, K. R., Schmidt, P. S., &
Petrov, D. A. (2014). Genomic evidence of rapid and stable adaptive
oscillations over seasonal time scales in Drosophila . PLoS
Genetics , 10 ,e1004775.
https//doi.org/10.1371/journal.pgen.1004775
Britt, M., Haworth, S. E., Johnson, J.B., Martchenko, D., & Shafer, A.
B. (2018). The importance of non-academic coauthors in bridging the
conservation genetics gap. Biological Conservation , 218 ,
118–123. https://doi.org/10.1016/j.biocon.2017.12.019
Capblancq, T., Fitzpatrick, M. C., Bay, R. A., Exposito-Alonso, M., &
Keller, S. R. (2020). Genomic prediction of (mal)adaptation across
current and future climatic landscapes. Annual Review of Ecology,
Evolution, and Systematics , 51 , 245–269.https://doi.org/10.1146/annurev-ecolsys-020720-042553
Ceska, J. F., Affolter, J. M., & Hamrick, J. L. (1997). Developing a
sampling strategy for Baptisia arachnifera based on allozyme
diversity. Conservation Biology , 11 , 1133–1139.https://doi.org/10.1046/j.1523-1739.1997.95527.x
Charlesworth, D. (2006). Balancing selection and its effects on
sequences in nearby genome regions. PLoS Genetics , 2(4) ,
e64. https//doi.org/10.1371/journal.pgen.0020064
Chun, Y. J., Nason, J. D., & Moloney, K. A. (2009). Comparison of
quantitative and molecular genetic variation of native vs. invasive
populations of purple loosestrife (Lythrum salicaria L.,
Lythraceae). Molecular Ecology , 18 , 3020–3035.
https//doi.org/10.1111/j.1365-294X.2009.04254.x
Chun, Y. J., Le Corre, V., & Bretagnolle, F. (2011). Adaptive
divergence for a fitness-related trait among invasive Ambrosia
artemisiifolia populations in France. Molecular Ecology ,20 , 1378–1388. https//doi.org/10.1111/j.1365-294X.2011.05013.x
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. (2020).
Incorporating differences between genetic diversity of trees and
herbaceous plants in conservation strategies. Conservation
Biology , 34 , 1142–1151. https//doi.org/10.1111/cobi.13467
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 , 552.
https://doi.org/10.3390/d13110552
Clausen, J., Keck, D. D., & Hiesey, W. M. (1941). Experimental
studies on the nature of species I. Effect of varied environments on
western North American plants . Carnegie Institution of Washington
Publication No. 520, pp. 1–452.
Colautti, R. I., Lee, C. R., & Mitchell-Olds, T. (2012). Origin, fate,
and architecture of ecologically relevant genetic variation. Current
Opinion in Plant Biology, 15,
199–204.
https//doi.org/10.1016/j.pbi.2012.01.016
De Kort, H., Vandepitte, K., & Honnay, O. (2013). A meta-analysis of
the effects of plant traits and geographical scale on the magnitude of
adaptive differentiation as measured by the difference betweenQ ST and F ST.Evolutionary Ecology , 27 , 1081–1097.
https//doi.org/10.1007/s10682-012-9624-9
Depardieu, C., Girardin, M. P., Nadeau, S., Lenz, P., Bousquet, J., &
Isabel, P. (2020). Adaptive genetic variation to drought in a widely
distributed conifer suggests a potential for increasing forest
resilience in a drying climate. New Phytologist , 227 ,
427–439. https//doi.org/10.1111/nph.16551
de Villemereuil, P., Gaggiotti, O. E., Mouterde, M., & Till-Bottraud,
I. (2016). Common garden experiments in the genomic era: new
perspectives and opportunities. Heredity , 116 , 249–254.https//dx.doi.org/10.1038/hdy.2015.93
DeWoody, J. A., Harder, A. M., Mathur, S., & Willoughby, J. R. (2021).
The long-standing significance of genetic diversity in conservation.Molecular Ecology , 30 , 4147–4154.
https//doi.org/10.1111/mec.16051
Dlugosch, K. M., & Parker, I. M. (2007). Molecular and quantitative
trait variation across the native range of the invasive speciesHypericum canariense : evidence for ancient patterns of
colonization via pre-adaptation? Molecular Ecology , 16 ,
4269–4283. https//doi.org/10.1111/j.1365-294X.2007.03508.x
Dubois, N.S., Gomez, A., Carlson, S., & Russell, D. (2019). Bridging
the research-implementation gap requires engagement from practitioners.Conservation Science and Practice , 2, e134. https//doi.org/
10.1111/csp2.134
Edelaar, P., Burraco, P., & Gomez-Mestre, I. (2011). Comparisons
between Q ST and F ST—how
wrong have we been? Molecular Ecology , 20 , 4830–4839.
https//doi.org/10.1111/j.1365-294X.2011.05333.x
Ehrlich, P. R., & Raven, P. H. (1969). Differentiation of populations.Science , 165 , 1228–1232.
https//doi.org/10.1126/science.165.3899.1228
Fabian, Y., Bollmann, K., Brang, P., Hein, C., Olschewski, R., Rigling,
A., Stofer, S., & Holderegger, R. (2019). How to close the
science-practice gap in nature conservation? information sources used by
practitioners. Biological Conservation , 235 , 93–101.https://doi.org/10.1016/j.biocon.2019.04.011
Fijarczyk, A., & Babik, W. (2015). Detecting balancing selection in
genomes: limits and prospects. Molecular Ecology , 24 ,
3529–3545. https//doi.org/10.1111/mec.13226
Flanagan, S. P., Forester, B. R., Latch, E. K., Aitken, S. N., & Hoban,
S. (2018). Guidelines for planning genomic assessment and monitoring of
locally adaptive variation to inform species conservation.Evolutionary Applications , 11 , 1035–1052.
https//doi.org/10.1111/eva.12569
Frankham, R. (2015). Genetic rescue of small inbred populations:
meta-analysis reveals large and consistent benefits of gene flow.Molecular Ecology , 24 , 2610–2618.
https//doi.org/10.1111/mec.13139
García-Dorado A, & Caballero A. (2021). Neutral genetic diversity as a
useful tool for conservation biology. Conservation Genetics ,22 , 541–545. https://doi.org/10.1007/s10592-021-01384-9-9
Gravuer, K., von Wettberg, E., & Schmitt, J. (2005). Population
differentiation and genetic variation inform translocation decisions forLiatris scariosa var. novae-angliae , a rare New England
grassland perennial. Biological Conservation , 124 ,
155–167. https//doi.org/10.1016/j.biocon.2005.01.021
Hall, M. C., Dworkin, I., Ungerer, M. C., & Purugganan, M. P. (2007).
Genetics of microenvironmental canalization in Arabidopsis
thaliana . Proceedings of the National Academy of Sciences of the
United States of America , 104 , 13717–13722.
https//doi.org/10.1073/pnas.0701936104
Hamrick, J. L., & Godt, M. J. W. (1996). Conservation genetics of
endemic plant species. In J. C. Avise, & J. L. Hamrick (Eds.),Conservation Genetics: Case Histories from Nature (pp. 281–304).
Chapman & Hall.
Hamrick, J. L., Godt, M. J. W., & Gonzales, E. (2006). Conservation of
genetic diversity in old-growth forest communities of the southeastern
United States. Applied Vegetation Science , 9 , 51–57.
https://doi.org/10.1111/j.1654-109X.2006.tb00655.x
Hendry, A. P. (2002). Q st > = \(\neq\ \)<F st? Trends in Ecology & Evolution , 17 , 502.https://doi.org/10.1016/S0169-5347(02)02603-4
Holderegger, R., Balkenhol, N., Bolliger, J., Engler, J. O., Gugerli,
F., Hochkirch, A., Nowak, C., Segelbacher, G., Wider, A., & Zachos, F.
E. (2019). Conservation genetics: linking science with practice.Molecular Ecology , 28 , 3848–3856.
https://doi.org/10.1111/mec.15202
Holsinger, K. E., & Weir B. S. (2010). Genetics in geographically
structured populations: defining, estimating and interpretingF ST. Nature Reviews Genetics , 10 ,
639–650. https://doi.org/10.1038/nrg2611
Jiménez-Ambriz, G., Petit, C., Bourrié, I., Dubois, S., Olivieri, I., &
Ronce, O. (2007). Life history variation in the heavy metal tolerant
plant Thlaspi caerulescens growing in a network of contaminated
and noncontaminated sites in southern France: role of gene flow,
selection and phenotypic plasticity. New Phytologist , 173 ,
199–215. https://doi.org/10.1111/j.1469-8137.2006.01923.x
Karhunen, M., Merilä, J.,
Leinonen, T., Cano, J. M., & Ovaskainen, O. (2013). DRIFTSEL: an R
package for detecting signals of natural selection in quantitative
traits. Molecular Ecology Resources , 13 , 746–754.https://doi.org/10.1111/1755-0998.12111
Karhunen, M., Ovaskainen, O., Herczeg, G., & Merilä, J. (2014).
Bringing habitat information into statistical tests of local adaptation
in quantitative traits: a case study of nine-spined sticklebacks.Evolution , 68 , 559–568. https://doi.org/10.1111/evo.12268
Kawakami, T., Morgan, T. J., Nippert, J. B., Ocheltree,T. W., Keith, R.,
Dhakal, P., & Ungerer, M. C. (2011). Natural selection drives clinal
life history patterns in the perennial sunflower species,Helianthus maximiliani . Molecular Ecology , 20 ,
2318–2328.
https://doi.org/10.1111/j.1365-294X.2011.05105.x
Keller, S. R., Soolanayakanahally, R. Y., Guy, R. D., Silim, S. N.,
Olson, M. S., & Tiffin, P. (2011). Climate-driven local adaptation of
ecophysiology and phenology in balsam poplar, Populus balsamiferaL. (Salicaceae). American Journal of Botany , 98 , 99–108.
https//doi.org/10.3732/ajb.1000317
Kreitman, M. (2001). “Selective sweep.” In S. Brenner, & J. H. Miller
(Eds.), Encyclopedia of Genetics (pp. 1803–1804). Academic
Press.
Kremer, A., Zanetto, A., & Ducousso, A. (1997). Multilocus and
multitrait measures of differentiation for gene markers and phenotypic
traits. Genetics , 14, 1229–1241.
https://doi.org/10.1093/genetics/145.4.1229
Lamy, J.-B., Plomion, C., Kremer, A., & Delzon, S. (2012).Q ST < F ST as a
signature of canalization. Molecular Ecology , 21 ,
5646–5655. https//doi.org/10.1111/mec.12017
Lamy, J.-B., Bouffier, L., Burlett, R., Plomion, C., Cochard, H., &
Delzon, S. (2011). Uniform selection as a primary force reducing
population genetic differentiation of cavitation resistance across a
species range. PLoS ONE , 6(8) , e23476.
https//doi.org/10.1371/journal.pone.0023476
Lande, R. (1992). Neutral theory of quantitative genetic variance in an
island model with local extinction and recolonization. Evolution ,46 , 381–389. https://doi.org/10.1111/j.1558-5646.1992.tb02046.x
Le Corre, V., & Kremer, A. (2012). The genetic differentiation at
quantitative trait loci under local adaptation. Molecular
Ecology , 21 , 1548–1566. https//doi.org/
10.1111/j.1365-294X.2012.05479.x
Leinonen, T., O’Hara, R. B., Cano, J. M., & Merilä, J. (2008).
Comparative studies of quantitative trait and neutral marker divergence:
a meta-analysis. Journal of Evolutionary Biology , 21 ,
1–17. https//doi.org/10.1111/j.1420-9101.2007.01445.x
Leinonen, T., McCairns, R. J. S., O’Hara, R. B., & Merilä, J. (2013).Q ST–F ST comparisons:
evolutionary and ecological insights from genomic heterogeneity.Nature Reviews Genetics , 14 , 179–190.
https//doi.org/10.1038/nrg3395
Li, Z., Löytynoja, A., Fraimout, A., & Merilä, J. (2019). Effects of
marker type and filtering criteria onQ ST-F ST comparisons.Royal Society Open Science , 6(11) , 190666.https://dx.doi.org/10.1098/rsos.190666
Machado, H. E., Bergland, A. O., Taylor, R., Tilk, S., Behrman, E.,
Dyer, K., Fabian, D. K., Flatt, T., González, J., Karasov, T., Kim, B.,
Kozeretska, I., Lazzaro, B. P., Merritt, T. J. S., Pool, J. E., O’Brien,
K., Rajpurohit, S., Roy, P. R., Schaeffer, S. W., Serga, S., Schmidt,
P., & Petrov, D. A. (2021). Broad geographic sampling reveals the
shared basis and environmental correlates of seasonal adaptation inDrosophila . eLife , 10 , e67577.
https//doi.org/10.7554/eLife.67577
Marin, S., Gibert, A., Archambeau, J., Bonhomme,V., Lascoste, M., &
Pujol, B. (2020). Potential adaptive divergence between subspecies and
populations of snapdragon plants inferred fromQ ST–F ST comparisons.Molecular Ecology , 29 , 3010-3021.
https://doi.org/10.1111/mec.15546
McKay, J. K., Bishop, J. G., Lin, J.-Z., Richards, J. H., Sala, A., &
Mitchell-Olds, T. (2001). Local adaptation across a climatic gradient
despite small effective population size in the rare Sapphire Rockcress.Proceedings of the Royal Society B: Biological Sciences , 268,
1715–1721. https//doi.org/10.1098/rspb.2001.1715
McKay, J. K., & Latta, R. G. (2002). Adaptive population divergence:
markers, QTL and traits. Trends in Ecology & Evolution ,17 , 285–291. https//doi.org/10.1016/S0169-5347(02)02478-3
Merilä, J., & Sheldon, B. C. (1999). Genetic architecture of fitness
and nonfitness traits: empirical patterns and development of ideas.Heredity , 83 , 103–109.
https://doi.org/10.1046/j.1365-2540.1999.00585.x.
Merilä, J., & Crnokrak, P. (2001). Comparison of genetic
differentiation at marker loci and quantitative traits. Journal of
Evolutionary Biology , 14 , 892–903.
https//doi.org/10.1046/j.1420-9101.2001.00348.x
Merimans, P., & Hedrick, P. W. (2010). Assessing population structure:F ST and related measures. Molecular
Ecology , 11 , 5–18.
http//doi.org/10.1111/j.1755-0998.2010.02927.x
Messer, P. W., Ellner, S. P., & Hairston, N. G. Jr. (2016). Can
population genetics adapt to rapid evolution? Trends in Genetics ,32 , 408-418. https//doi.org/10.1016/j.tig.2016.04.005.
Meyer, C. L., Kostecka, A. A., Saumitou-Laprade, P., Créach, A.,
Castric, V., Pauwels, M., & Frérot, H. (2010). Variability of zinc
tolerance among and within populations of the pseudometallophyte speciesArabidopsis halleri and possible role of directional selection.New Phytologist , 185 , 130–142.
https//doi.org/10.1111/j.1469-8137.2009.03062.x
Nielson, R. (2005). Molecular signatures of natural selection.Annual Review of Genetics , 39 , 197–218.
https://doi.org/10.1146/annurev.genet.39.073003.112420
Nosil, P., Egan, S. P., & Daniel, J. (2007). Heterogeneous genomic
differentiation between walking-stick ecotypes: “isolation by
adaptation” and multiple roles for divergent selection.Evolution , 62 , 316–336. https//doi.org/10.1 I
11/j.1558-5646.2007.00299
Oostermeijer, J. G. B., van Fijek, M. W., & den Nijs, J. C. M. (1994).
Offspring fitness in relation to population size and genetic variation
in the rare perennial plant species Gentiana pneumonanthe .Oecologia , 97 , 289–296. https//doi.org/10.1007/BF00317317
Ottewell, K. M., Bickerton, D. C., Byrne, M., & Lowe, A. J. (2016).
Bridging the gap: a genetic assessment framework for population-level
threatened plant conservation prioritization and decision-making.Diversity and Distributions , 22 , 174–188.
https//doi.org/10.1111/ddi.12387
Ovaskainen, O., Karhunen, M., Zheng, C. Z., Arias, J. M. C., & Merilä,
J. (2011). A new method to uncover signatures of divergent and
stabilizing selection in quantitative traits. Genetics ,189 , 621–632. https//doi.org/10.1534/genetics.111.129387
Petit, C., Fréville, H., Mignot, A., Colas, B., Riba, M., Imbert, E.,
Hurtrez-Boussés, I., Virevaire, M., & Olivieri, I. (2001). Gene flow
and local adaptation in two endemic plant species. Biological
Conservation , 100 , 21–34.
https//doi.org/10.1016/S0006-3207(00)00204-4
Podolsky, R. H. (2001). Genetic variation for morphological and allozyme
variation in relation to population size in Clarkia dudleyana , an
endemic annual. Conservation Biology , 15 , 412–423.
https//doi.org/10.1046/j.1523-1739.2001.015002412.x
Podolsky, R. H., & Holtsford, T. P. (1995). Population structure of
morphological traits in Clarkia dudleyana . I. Comparison ofF ST between allozymes and morphological traits.Genetics , 140 , 733–744.
https//doi.org/10.1093/genetics/140.2.733
Prendeville, H. R., Barnard-Kubow, K., Dai, C., Barringer, B. C., &
Galloway, L. F. (2013). Clinal variation for only some phenological
traits across a species range. Oecologia , 173 , 421–430.
https//doi.org/10.1007/s00442-013-2630-y
Pressoir, G., & Berthaud, J. (2004). Population structure and strong
divergent selection shape phenotypic diversification in maize landraces.Heredity , 92 , 95–101.
https//doi.org/10.1038/sj.hdy.6800388
Reed, D. H., & Frankham, R. (2001). How closely correlated are
molecular and quantitative measures of genetic variation? A
meta-analysis. Evolution , 55 , 1095–1103.
https://doi.org/10.1111/j.0014-3820.2001.tb00629.x
Reed, D. H., & Frankham, R. (2003). Correlation between fitness and
genetic diversity. Conservation Biology , 17 , 230–237.
https//doi.org/10.1046/j.1523-1739.2003.01236.x
Rodríguez-Quilón, I., Santos-del-Blanco, L., Serra-Varela, M. J.,
Koskela, J., González-Martínez, S. C., & Alía, R. (2016). Capturing
neutral and adaptive genetic diversity for conservation in a highly
structured tree species. Ecological Applications , 26 ,
2254–2266. https://doi.org/10.1002/eap.1361
Savolainen, O., Pyhäjärvi, T., & Knürr, T. (2007). Gene flow and local
adaptation in trees. Annual Review of Ecology, Evolution, and
Systematics , 38 , 595–619.
https//doi.org/10.1146/annurev.ecolsys.38.091206.095646
Savolainen, O. (2011). The genomic basis of local climatic adaptation.Science , 334 , 49–50.
https//doi.org/10.1126/science.1213788
Schwaegerle, K. E. K., Garbutt, K., & Bazzaz, F. A. (1986).
Differentiation among nine populations of Phlox . I.
Electrophoretic and quantitative variation. Evolution , 40 ,
506–517.
https//doi.org/10.1111/j.1558-5646.1986.tb00503.x
Shirk, R. Y., & Hamrick, J. L. (2014). Multivariate adaptation but no
increase in competitive ability in invasive Geranium carolinianumL. (Geraniaceae). Evolution , 68 , 2945–2959.
https//doi.org/10.1111/evo.12474
Slatkin, M. (1973). Gene flow and selection in a cline. Genetics ,75 , 733–756. https//doi.org/10.1093/genetics/75.4.733
Sork, V. L. (2018). Genomic studies of local adaptation in natural plant
populations. Journal of Heredity , 109 , 3–15.
https//doi.org/10.1093/jhered/esx091
Spitze, K. (1993). Population structure in Daphnia obtusa :
quantitative genetic and allozyme variation. Genetics ,135 , 67–374. https://doi.org/10.1093/genetics/135.2.367
Sreejayan, Kumar, U. S., Varghese, G., Jacob, T. M., P., & Thomas, G.
(2011). Stratification and population structure of the genetic resources
of ancient medicinal rice (Oryza sativa L.) landrace Njavara.Genetic Resources and Crop Evolution , 58 , 697–711.
https//doi.org/10.1007/s10722-010-9613-1
Steinger, T., Haldimann, P., Leiss, K., & Müller-Schärer, H. (2002).
Does natural selection promote population divergence? A comparative
analysis of population structure using amplified fragment length
polymorphism markers and quantitative traits. Molecular Ecology ,11 , 2583–2590.
https//doi.org/10.1046/j.1365-294x.2002.01653.x
Stephan, W. (2019). Selective sweeps. Genetics , 211 ,
5–13. https://doi.org/10.1534/genetics.118.301319
Szulkin, M., Bierne, N., & David, P. (2010). Heterozygosity-fitness
correlations: a time for reappraisal. Evolution , 64 ,
1202–1217. https//doi.org/10.1111/j.1558-5646.2010.00966.x
Taylor, H. R., Dussex, N., & van Heezik, Y. (2017). Bridging the
conservation genetics gap by identifying barriers to implementation for
conservation practitioners. Global Ecology and Conservation ,10 , 231–242. https://doi.org/10.1016/j.gecco.2017.04.001
Teixeira, J. C., & Huber, C. D. (2021). The inflated significance of
neutral genetic diversity in conservation genetics. Proceedings of
the National Academy of Sciences of the United States of America ,118(10) , e2015096118. https://doi.org/10.1073/pnas.2015096118
Turesson, G. (1922). The genotypical response of the plant species to
the habitat. Hereditas , 3 , 211-350.
https://doi.org/10.1111/j.1601-5223.1922.tb02734.x
Volis, S., Yakubov, B., Shulgina, I., Ward, D., & Mendlinger, S.
(2005). Distinguishing adaptive from nonadaptive genetic
differentiation: comparison of Q ST andF ST at two spatial scales. Heredity ,95 , 466–475. https://doi.org/10.1038/sj.hdy.6800745
Waldmann, P., & Andersson, S. (1998). Comparison of quantitative
genetic variation and allozyme diversity within and between populations
of Scabiosa canescens and S. columbaria . Heredity ,81 , 79–86. https://doi.org/10.1046/j.1365-2540.1998.00379.x
Whitlock, M. C. (2008). Evolutionary inference fromQ ST. Molecular Ecology , 17 ,
1885–1896. https//doi.org/10.1111/j.1365-294X.2008.03712.x
Wright, S. (1951). The genetical structure of populations. Annals
of Eugenics , 1 , 323–354.
https//doi.org/10.1111/j.1469-1809.1949.tb02451.x
Ye, Q., Tang, F., Wei, N., & Yao, X. (2014). Molecular and quantitative
trait variation within and among small fragmented populations of the
endangered plant species Psilopeganum sinense . Annals of
Botany , 113 , 79–86. https//doi.org/10.1093/aob/mct255
Yu, Q., Ellen, E. D., Wade, M. J., & Delph, L. F. (2011). Genetic
differences among populations in sexual dimorphism: evidence for
selection on males in a dioecious plant. Journal of Evolutionary
Biology , 24 , 1120–1127.
https//doi.org/10.1111/j.1420-9101.2011.02245.x
TABLE 1 Definitions of terms used in this mini review