Abstract
San Diego thornmint Acanthomintha ilicifolia (Gray) Gray (Lamiaceae) is a winter herb restricted to San Diego county in the United States and Baja California Norte in Mexico. Historic records document 80 occurrences of this species, with 55 extant occurrences in San Diego County currently known. We compared three measures of genetic variation to inform ongoing conservation efforts: putatively neutral genetic structure revealed from isozyme markers, apparent cytogenetic variation confirmed using flow cytometry, and potentially adaptive morphological variation quantified in a common-garden study. Together, these data indicated that this rare endemic is genetically complex, revealing significant differentiation of neutral and potentially adaptive genetic variation among populations, and possessing at least two cytotypes, sometimes even within the same population. While additional study is required to resolve the extent of potential local adaptation in this species, conservation plans should limit the movement of germplasm among occurrences and monitor populations in order to limit potential long-term impacts to population viability. Given that these findings challenge the canonical model of genetic structure in rare plants (low genetic variation and limited genetic structure), we recommend guidelines to apply genetic information to conservation strategies.
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References
Ægisdóttir HH, Kuss P, Stöcklin J (2009) Isolated populations of a rare alpine plant show high genetic diversity and considerable population differentiation. Ann Bot 104:1313–1322
Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188
Aronson J, Kigel J, Shmida A (1993) Reproductive allocation strategies in desert and Mediterranean populations of annual plants grown with and without water stress. Oecologia 93:336–342
Bauder ET, Sakrison J (1997) Autecology of San Diego thornmint (Acanthomintha ilicifolia). California Department of Fish and Game, Region 5 Natural Heritage Program, Borrego Springs
Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678
Bowen BW (1999) Preserving genes, species, or ecosystems? Healing the fractured foundations of conservation policy. Mol Ecol 8:S5-S10
Casler MD, Vogel KP, Taliaferro CM, Wynia RL (2004) Latitudinal adaptation of switchgrass populations. Crop Sci 44:293–303
Cole CT (2003) Genetic variation in rare and common plants. Annu Rev Ecol Evol Syst 34:213–237
Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Genet 6:836–846
DeWoody J, Trewin H, Taylor G (2015) Genetic and morphological differentiation in Populus nigra L.: isolation by colonization or isolation by adaptation? Mol Ecol 24:2641–2655
Etterson JR (2004) Evolutionary potential of Chamaecrista fasciculate in relation to climate change. II. Genetic architecture of three populations reciprocally planted along an environmental gradent in the great plains. Evolution 58:1459–1471
Farris MA, Lechowicz MJ (1990) Functional interactions among traits that determine reproductive success in a native annual plant. Ecology 71:548–557
Fehlberg SD, Ferguson CJ (2012) Intraspecific cytotypic variation and complicated genetic structure in the Phlox amabilis-P. woodhousei (Polemoniaceae) complex. Am J Bot 99:865–874
Godfrey S, Spiegelberg M (2015) Manchester habitat conservation area annual report. Center for Natural Lands Management, Fallbrook
Godt MJW, Walker J, Hamrick JL (2004) Allozyme diversity in Macbridea alba (Lamiaceae), and endemic Florida mint. J Hered 95:244–249
Grant JE, Brown AHD, Grace JP (1984) Cytological and isozyme diversity in Glycine tomentella Hayata (Leguminosae). Aust J Bot 32:665–677
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc B 351:1291–1298
Hardion L, Verlaque R, Rosato M, Rosselló JA, Vila B (2015) Impact of polyploidy on fertility variation of Mediterranean Arundo L. (Poaceae). CR Biol 338:298–306
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Hegarty MJ, Hiscock SJ (2008) Genomic clues to the evolutionary success of polyploid plants. Curr Biol 18:R435-R444
Hörandl E, Greilhuber J (2002) Diploid and autotetraploid sexuals and their relationships to apomicts in the Ranunculus cassubicus group: insights from DNA content and isozyme variation. Plant Syst Evol 234:85–100
Huck RB, Chambers HL (1997) Polyploidy: a factor in the evolution of Dicerandra Benth (Labiatae). Edinburgh J Bot 54:217–229
Kalisz S, Nason JD, Hanzawa FM, Tonsor SJ (2001) Spatial population genetic structure in Trillium grandiflorum: the roles of dispersal, mating, history and selection. Evol Biol 55:1560–1568
Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241
Kohn MH, Murphy WJ, Ostrander EA, Wayne RK (2006) Genomics and conservation genetics. Trends Ecol Evol 21:629–637
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952
Loiselle BA, Sork VL, Nason JD, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425
López-Pujol J, Orellana MR, Bosch M, Simon J, Blanché C (2003) Effects of habitat fragmentation on allozyme diversity and conservation status of the coastal sand dune plant Stachys maritima (Lamiaceae) in the Iberian Peninsula. Plant Biol 5:504–512
López-Pujol J, Bosch M, Simon J, Blanché C (2004) Allozyme diversity in the tetraploid endemic Thymus loscosii (Lamiaceae). Ann Bot 93:323–332
Martin SL, Husband BC (2009) Influence o fphylogeny and ploidy on species ranges of North American angiosperms. J Ecol 97:913–922
Messner S, Miranda SC, Green K, Philips C, Dudley J, Cayan D, Young E (2009) Climate change-related impacts in the San Diego region by 2050. California Climate Change Center, Sacramento
Nei M (1978) Estimation of average heterozygosity and genetic distances for small number of individuals. Genetics 89:583–590
Ottewell KM, Bickerton DC, Byrne M, Lowe AJ (2016) Bridging the gap: a genetic assessment framework for population-level threatened plant conservation prioritization and decision-making. Divers Distrib 22:174–188
Ouborg NJ, Vergeer P, Mix C (2006) The rough edges of the conservation genetics paradigm for plants. J Ecol 94:1233–1248
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Ramsey J, Schemske DW (1998) Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu Rev Ecol Syst 29:467–501
Ramsey J, Robertson A, Husband B (2008) Rapid adaptive divergence in New World Achillea, an autopolyploid complex of ecological races. Evolution 62–63:639–653
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
San Diego County (2017) MSP: a strategic habitat conservation roadmap. Goals Object 2:1–3
Schoenwald-Cox CM, Chambers SM, MacBryde B, Thomas L (eds) (1983) Genetics and conservation. Benjamin-Cummings, Menlo Park
Soltis DE, Rieseberg L (1986) Autopolyploidy in Tolmiea menziesii (Saxifragaceae): genetic insights from enzyme electrophoresis. Am J Bot 73:310–318
Soltis DE, Visger CJ, Soltis PS (2014) The polyploidy revolution then… and now: Stebbins revisited. Am J Bot 101:1057–1078
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci 101:15261–15264
Stebbins GL (1947) Types of polyploids: their classification and significance. Adv Genet 1:403–429
Steeck DM (1995) Reproductive biology of a rare California annual, Acanthomintha duttonii, and its congener, Acanthomintha obovata ssp. cordata. University of California, Davis
Thornton PE, Thornton MM, Mayer BW, Wilhelmi N, Wei Y, Devarakonda R, Cook RB (2014) Daymet: daily surface weather data on a 1-km grid for North America; version 2. Data set. Oak Ridge National Laboratory Distributed Active Archive Center, Oak Ridge. http://www.daac.ornl.gov. Accessed 14 May 2016
Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, dePamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, de Peer YV, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science (Washington, DC) 313:1596–1604
USDA Forest Service (2012) National forest genetics lab standard operating procedures for starch gel electrophoresis. USDA Forest Service, Placerville, p 103
Visser V, Molosfski J (2015) Ecological niche differentiation of polyploidization is not supported by environmental differences among species in a cosmopolitan grass genus. Am J Bot 102:36–49
Warner DA, Edwards GE (1989) Effects of polyploidy on photosynthetic rates, photosynthetic enzymes, contents of DNA, chlorophyll, and sizes and numbers of photosynthetic cells in the C4 dicot Atiplex confertifolia. Plant Physiol 91:1143–1151
Acknowledgements
The authors acknowledge and appreciate funding provided by the San Diego Association of Governments’ Environmental Mitigation Program (Grant Agreement #5001964), by the Center for Natural Lands Management, and by a donation from Dr. Hans and Elisabeth Spiegelberg. We thank Markus Spiegelberg, Sarah Godfrey, Patrick McConnell, and Jessie Vinje for their leadership in thornmint conservation and assistance in collecting foliage and seed samples from natural populations; Courtney Owens, Rosanna Hanson, Jody Mello, Randy Meyer, and James Boom for their assistance with laboratory technical work; and Laurie Lippitt and Stacy Anderson for managing the nursery common-garden activities. We thank Erin Conlisk, Kelly Anderson, and Burak Pekin for their for their assistance with data management and analyses of the common-garden research. We thank Michelle Labbé and Benjamin Janes for technical support in acquiring permits and property access permissions and other documents and data. We appreciate the conservation managers and regulatory agencies for protecting the wild populations of thornmint and for allowing us access and permission to sample them for this study. This paper is more robust in its content and eloquent in its presentation as a result of comments from the anonymous reviewers.
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DeWoody, J., Rogers, D.L., Hipkins, V.D. et al. Spatially explicit and multi-sourced genetic information is critical for conservation of an endangered plant species, San Diego thornmint (Acanthomintha ilicifolia). Conserv Genet 19, 893–907 (2018). https://doi.org/10.1007/s10592-018-1062-y
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DOI: https://doi.org/10.1007/s10592-018-1062-y