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 STF 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 STF 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