Abstract
The mechanisms generating narrow endemism have long been of interest to biologists, with a variety of underlying causes proposed. This study investigates the origins of narrow endemism of two imperiled Florida endemics, Helianthus carnosus and Phoebanthus tenuifolius, in relation to a widespread sympatric close relative, Helianthus radula, as well as other members of the genus Helianthus. Using a combination of population genetics and environmental niche modeling, this study compares evidence in support of potential mechanisms underlying the origin of narrow endemism, including environmental specialization versus inbreeding, loss of diversity, or other predominantly genetic factors. The two narrow endemics were found to be comparable in genetic diversity to H. radula as well as other widespread Helianthus species, with little to no evidence of inbreeding. Environmental niche modeling indicates that distributions of both narrow endemics are strongly related to temperature and precipitation patterns, and that both endemics are threatened with severe reductions in habitat suitability under projected climate change. Evidence indicates that genetic factors likely are not the cause of narrow endemism in these species, suggesting that these species are likely ecological specialists and thus historical narrow endemics. This makes both species vulnerable to climate change, and of immediate conservation concern.
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Anderson RP, Raza A (2010) The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J Biogeogr 37:1378–1393
Araújo MB, Peterson AT (2012) Uses and misuses of bioclimatic envelope modeling. Ecology 93:1527–1539
Araújo MB, Ferri-Yanez F, Bozinovic F, Marquet PA, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol Lett 16:1206–1219
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Harvard
Beekman M, Ratnieks FLW (2000) Long-range foraging by the honey-bee, Apis mellifera L. Funct Ecol 14:490–496
Busch JW, Joly S, Schoen DJ (2010) Does mate limitation in self-incompatible species promote the evolution of selfing? The case of Leavenworthia alabamica. Evolution 64:1657–1670
Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Earl D, vonHoldt B (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57
Ellis JR, Pashley CH, Burke JM, McCauley DE (2006) High genetic diversity in a rare and endangered sunflower as compared to a common congener. Mol Ecol 15:2345–2355
Estill JC, Cruzan MB (2001) Phytogeography of rare plant species endemic to the southeastern United States. Castanea 66:3–23
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Foré SA, Guttman SI (1999) Genetic structure of Helianthus occidentalis (Asteraceae) in a preserve with fragmented habitat. Am J Bot 86:988–995
Fry J, Xian G, Jin S, Dewitz J, Homer C, Yang L, Barnes C, Herold N, Wickham J (2011) Completion of the 2006 national land cover database for the conterminous United States. Photogramm Eng Remote Sens 77:858–864
Gevaert SD, Mandel JR, Burke JM, Donovan LA (2013) High genetic diversity and low population structure in Porter’s sunflower (Helianthus porteri). J Hered 104:407–415
Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792
Hale ML, Burg TM, Steeves TE (2012) Sampling for microsatellite-based population genetic studies: 25 to 30 individuals per population is enough to accurately estimate allele frequencies. PLoS One 7:e45170
Hamrick JL, Godt MJW (1996) Conservation genetics of endemic plant species. In: Conservation genetics (pp 281–304). Springer, New York
Heiser CBJ, Smith DM, Clevenger SB, Martin WCJ (1969) The North American sunflowers: Helianthus. Mem Torrey Bot Club 22:1–218
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Kruckeberg AR, Rabinowitz D (1985) Biological aspects of endemism in higher plants. Annu Rev Ecol Syst 16:447–479
Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158
Le Quéré C, Peters GP, Andres RJ, Andrew RM, Boden TA, Ciais P, Friedlingstein P, Houghton RA, Marland G, Moriarty R, Sitch S, Tans P, Arneth A, Arvanitis A, Bakker DCE, Bopp L, Canadell JG, Chini LP, Doney SC, Harper A, Harris I, House JI, Jain AK, Jones SD, Kato E, Keeling RF, Klein Goldewijk K, Körtzinger A, Koven C, Lefèvre N, Maignan F, Omar A, Ono T, Park GH, Pfeil B, Poulter B, Raupach MR, Regnier P, Rödenbeck C, Saito S, Schwinger J, Segschneider J, Stocker BD, Takahashi T, Tilbrook B, van Heuven S, Viovy N, Wanninkhof R, Wiltshire A, Zaehle S (2014) Global carbon budget 2013. Earth Syst Sci Data 6:235–263
Mandel JR, Dechaine JM, Marek LF, Burke JM (2011) Genetic diversity and population structure in cultivated sunflower and a comparison to its wild progenitor, Helianthus annuus L. Theor Appl Genet 123:693–704
Mandel J, Milton E, Donovan L, Knapp S, Burke J (2013) Genetic diversity and population structure in the rare Algodones sunflower (Helianthus niveus ssp. tephrodes). Conserv Genet 14:31–40
Mandel JR, Dikow RB, Funk VA, Masalia RR, Staton SE, Kozik A, Michelmore RW, Rieseberg LH, Burke JM (2014) A target enrichment method for gathering phylogenetic information from hundreds of loci: an example from the compositae. Appl Plant Sci 2:1300085
Manni F, Guérard E, Heyer E (2004) Geographic patterns of (genetic, morphologic, linguistic) variation: how barriers can be detected by using Monmonier’s algorithm. Hum Biol 76:173–190
Milanovich JR, Peterman WE, Nibbelink NP, Maerz JC (2010) Projected loss of a salamander diversity hotspot as a consequence of projected global climate change. PLoS One 5:e12189
Natural Resources Conservation Service, United States Department of Agriculture. Web Soil Survey. Available online at http://websoilsurvey.nrcs.usda.gov/
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Nybom H (2004) Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Mol Ecol 13:1143–1155
Pashley CH, Ellis JR, McCauley DE, Burke JM (2006) EST databases as a source for molecular markers: lessons from Helianthus. J Hered 97:381–388
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259
Povilitis A, Suckling K (2010) Addressing climate change threats to endangered species in US recovery plans. Conserv Biol 24:372–376
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pruett CL, Winker K (2008) The effects of sample size on population genetic diversity estimates in song sparrows Melospiza melodia. J Avian Biol 39:252–256
Rius M, Darling JA (2014) How important is intraspecific genetic admixture to the success of colonising populations? Trends Ecol Evol 29:233–242
Sax DF, Early R, Bellemare J (2013) Niche syndromes, species extinction risks, and management under climate change. Trends Ecol Evol 28:517–523
Schilling EE (2001) Phylogeny of Helianthus and related genera. OCL-Ol Corps Gras Lipides 8:22–25
Schilling EE (2006a) Helianthus carnosus. In: Flora of North America Editorial Committee (ed) 1993+. Flora of North America North of Mexico. 16+ vols, vol 21. Flora of North America, New York, p 156
Schilling EE (2006b) Helianthus radula. In: Flora of North America Editorial Committee (ed) 1993+. Flora of North America North of Mexico. 16+ vols, vol 21. Flora of North America, New York, p 155
Schilling EE (2006c) Phoebanthus tenuifolius. In: Flora of North America Editorial Committee (ed) 1993+. Flora of North America North of Mexico. 16+ vols, vol 21. Flora of North America, New York, p 114
Schilling EE, Panero JL (2002) A revised classification of subtribe Helianthinae (Asteraceae: Heliantheae). I. Basal lineages. Bot J Linn Soc 140:65–76
Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234
Soltis DE, Morris AB, McLachlan JS, Manos PS, Soltis PS (2006) Comparative phylogeography of unglaciated eastern North America. Mol Ecol 15:4261–4293
Sorrie BA, Weakley AS (2001) Coastal plain vascular plant endemics: phytogeographic patterns. Castanea 66:50–82
Stebbins GL Jr (1942) The genetic approach to problems of rare and endemic species. Madroño 6:241–258
Steffan-Dewenter I, Kuhn A (2003) Honeybee foraging in differentially structured landscapes. Proc: Biol Sci 270:569–575
Stephens JD, Rogers WL, Mason CM, Donovan LA, Malmberg RL (2015) Species tree estimation of diploid Helianthus (Asteraceae) using target enrichment. Am J Bot (in press)
Štorchová H, Hrdličková R, Chrtek J Jr, Tetera M, Fitze D, Fehrer J (2000) An improved method of DNA isolation from plants collected in the field and conserved in saturated NaCl/CTAB solution. Taxon 49:79–84
Timme RE, Simpson BB, Linder CR (2007) High-resolution phylogeny for Helianthus (Asteraceae) using the 18 s–26 s ribosomal DNA external transcribed spacer. Am J Bot 94:1837–1852
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wahlund S (1928) The combination of populations and the appearance of correlation examined from the standpoint of the study of heredity. Hereditas 11:65–106
Warren DL (2012) In defense of ‘niche modeling’. Trends Ecol Evol 27:497–500
White GM, Boshier DH, Powell W (2002) Increased pollen flow counteracts fragmentation in a tropical dry forest: an example from Swietenia humilis Zuccarini. Proc Natl Acad Sci 99:2038–2042
Willi Y (2009) Evolution towards self-compatibility when mates are limited. J Evol Biol 22:1967–1973
Wills D, Hester M, Liu A, Burke J (2005) Chloroplast SSR polymorphisms in the compositae and the mode of organellar inheritance in Helianthus annuus. Theor Appl Genet 110:941–947
Yackulic CB, Chandler R, Zipkin EF, Royle JA, Nichols JD, Campbell Grant EH, Veran S (2013) Presence-only modelling using MAXENT: when can we trust the inferences? Methods Ecol Evol 4:236–243
Acknowledgments
Financial support for this research was provided by a Society for the Study of Evolution Rosemary Grant Award to CMM, a Florida Native Plant Society Conservation Grant to CMM, a University of Georgia Innovative and Interdisciplinary Research Grant to CMM, a University of Georgia Department of Plant Biology Palfrey Research Grant to CMM, a Plant Biology Graduate Student Association Research Assistance Award to CMM, and National Science Foundation Grant IOS 1122842 to LAD and DBI 0820451 to JMB. The authors thank Eric Goolsby and Elise Wygant for assistance with field collections, Kirsten Scofield, Charmaine Woody, and Kristi Haisler for assistance with DNA extraction, Charlotte Carrigan Quigley for assistance with PCR and genotyping protocols, and the Donovan lab group for helpful comments on earlier versions of this manuscript. The authors also thank the Florida State Park Service, the Florida Department of Agriculture and Consumer Services, the Florida Department of Transportation, the Florida Fish and Wildlife Commission, the Flagler Estates Road and Water Control District, Morningside Nature Center, Crystal River Preserve, Apalachicola National Forest, Tate’s Hell State Forest, St. Joseph’s Bay State Buffer Preserve, and Box-R Wildlife Management Area for assistance with collection permits for both H. carnosus and P. tenuifolius. In addition, the authors thank Dr. Louisa Carter Staton for aggregated soil layers and helpful advice on niche modeling, as well as Dr. Loren Anderson for tissue samples of P. tenuifolius from herbarium records at Florida State University.
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Mason, C.M., Ishibashi, C.D.A., Rea, A.M. et al. Environmental requirements trump genetic factors in explaining narrow endemism in two imperiled Florida sunflowers. Conserv Genet 16, 1277–1293 (2015). https://doi.org/10.1007/s10592-015-0739-8
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DOI: https://doi.org/10.1007/s10592-015-0739-8