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Genetic and fitness consequences of interpopulation mating in Dianthus guliae Janka: conservation implications for severely depleted and isolated plant populations

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Abstract

Genetic constraints may increase the extinction risk in small and isolated plant populations. Introducing foreign genes may restore their genetic variability and fitness, but it could also be harmful, especially when recipient and donor populations have diverged. In such cases, data on genetic relationships and the possible consequences of different patterns of gene flow are essential for effective conservation. We examined five microsatellite loci to study the genetic relationships among three core populations and an isolated peripheral one of the threatened endemic Dianthus guliae Janka. This provided a base for further genetic analyses and experimental pollinations illustrating links between genetic richness and fitness, and the effects of inter-population mating in two contrasting populations (a large core vs. a small peripheral). Microsatellite loci did not show significant deviations from Hardy–Weinberg expectations. However, the peripheral population had lower heterozygosity, a higher inbreeding coefficient, and significant divergence from core units. Fitness and genetic data indicated an enhanced fitness, along with an improved capacity to rebound heterozygosity deficit after occasional selfing, in the core-population compared to the peripheral one. Crossing within-population did not enhance genetic diversity and fitness in the small peripheral unit, while between-population crossing improved its heterozygosity and fitness. Finally, in the study system, current genetic divergence did not preclude heterosis in the small and isolated population after mating with a larger donor unit.

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References

  • Abeli T, Gentili R, Mondoni A, Orsenigo S, Rossi G (2014) Effects of marginality on plant population performance. J Biogeogr 41:239–249

    Article  Google Scholar 

  • Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242

    Article  CAS  PubMed  Google Scholar 

  • Ball SJ, Adams M, Possingham HP, Keller MA (2000) The genetic contribution of single male immigrants to small, inbred populations: a laboratory study using Drosophila melanogaster. Heredity 84:677–684

    Article  CAS  PubMed  Google Scholar 

  • Bataillon T, Kirkpatrick M (2000) Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter. Genet Res 75:75–81

    Article  CAS  PubMed  Google Scholar 

  • Becker U, Colling G, Dostal P, Jakobsson A, Matthies D (2006) Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe. Oecologia 150:506–518

    Article  PubMed  Google Scholar 

  • Becker U, Dostal P, Jorritsma-Wienk LD, Matthies D (2008) The spatial scale of adaptive population differentiation in a wide-spread, well-dispersed plant species. Oikos 117:1865–1873

    Article  Google Scholar 

  • Busch JW (2006) Heterosis in an isolated, effectively small, and self-fertilizing population of the flowering plant Leavenworthia alabamica. Evolution 60:184–191

    Article  PubMed  Google Scholar 

  • Channell R, Lomolino MV (2000) Dynamic biogeography and conservation of endangered species. Nature 403:84–86  

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Evol Syst 18: 237–268

  • Collin CL, Penet L, Shykoff JA (2009) Early inbreeding depression in the sexually dimorphic polymorphic plant Dianthus sylvestris (Caryophyllaceae): effects of selfing and biparental inbreeding among sex morphs. Am J Bot 96:2279–2287

    Article  PubMed  Google Scholar 

  • Colling G, Reckinger C, Matthies D (2004) Effects of pollen quantity and quality on reproduction and offspring vigor in the rare plant Scorzonera humilis (Asteraceae). Am J Bot 91:1774–1782

    Article  PubMed  Google Scholar 

  • Coombs JS, Letcher BH, Nislow KH (2008) Create: a software to create input files from diploid genotypic data for 52 genetic software programs. Mol Ecol Resour 8:578–580

    Article  CAS  PubMed  Google Scholar 

  • Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and evaluation of two tests for detecting recent bottlenecks. Genetics 144:2001–2014

    CAS  PubMed Central  PubMed  Google Scholar 

  • Donohue K (1998) Effects of inbreeding on traits that influence dispersal and progeny density in Cakile edentula var. lacustris (Brassicaceae). Am J Bot 85:661–668

    Article  CAS  PubMed  Google Scholar 

  • Dudash MR (1990) Relative fitness of selfed and crossed progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44:1129–1139

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188

    Article  CAS  PubMed  Google Scholar 

  • Ezard THG, Travis JMJ (2006) The impact of habitat loss and fragmentation on genetic drift and fixation time. Oikos 114:367–375

  • Finger A, Kettle CJ, Kaiser-Bunbury CN, Valentin T, Doudee D, Matatiken D, Ghazoul J (2011) Back from the brink: potential for genetic rescue in a critically endangered tree. Mol Ecol 20:3773–3784

    Article  CAS  PubMed  Google Scholar 

  • Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475

    Article  PubMed  Google Scholar 

  • Gargano D (2011) Population biology and conservation of Mediterranean endemics: studies on the rare Dianthus guliae Janka. Fitosociologia 48(s1):163–169

    Google Scholar 

  • Gargano D, Fenu G, Medagli P, Sciandrello S, Bernardo L (2007) The status of Sarcopoterium spinosum (Rosaceae) at the western periphery of its range: ecological constraints lead to conservation concerns. Isr J Plant Sci 55:1–13

    Article  Google Scholar 

  • Gargano D, Gullo T, Bernardo L (2009) Do inefficient selfing and inbreeding depression challenge the persistence of the rare Dianthus guliae Janka (Caryophyllaceae)? Influence of reproductive traits on a plant’s proneness to extinction. Plant Species Biol 24:69–76

    Article  Google Scholar 

  • Gargano D, Gullo T, Bernardo L (2011) Fitness drivers in the threatened Dianthus guliae Janka (Caryophyllaceae): disentangling effect of growth context, maternal influence and inbreeding depression. Plant Biol 13(s1):96–103

    Article  PubMed  Google Scholar 

  • Gerst KL, Angert AL, Venable LD (2011) The effect of geographic range position on demographic variability in annual plants. J Ecol 99:591–599

    Google Scholar 

  • Godefroid S, Piazza C, Rossi G, Buord S, Stevens A-D, Aguraiuja R, Cowell C, Weekley CW, Vogg G, Iriondo JM, Johnson I, Dixon B, Gordon D, Magnanon S, Valentin B, Bjureke K, Koopman R, Vicens M, Virevaire M, Vanderborght T (2011) How successful are plant species reintroductions? Biol Conserv 144:672–682

    Article  Google Scholar 

  • Goodman SJ (1997) RST CALC: a collection of computer programs for calculating unbiased estimates of genetic differentiation and determining their significance for microsatellite data. Mol Ecol 6:881–885

    Article  CAS  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

  • Ingvarsson PK (2001) Restoration of genetic variation lost—the genetic rescue hypothesis. Trends Ecol Evol 16:62–63

    Article  PubMed  Google Scholar 

  • Kanda LL, Fuller TK, Sievert PR, Kellogg RL (2009) Seasonal source-sink dynamics at the edge of a species’ range. Ecology 90:1574–1585

    Article  PubMed  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Lammi A, Siikamäki P, Mustajärvi K (1999) Genetic diversity, population size, and fitness in central and peripheral populations of a rare plant Lychnis viscaria. Conserv Biol 13:1069–1078

  • Lande R (1995) Mutation and conservation. Conserv Biol 9:782–791

    Article  Google Scholar 

  • Leimu R, Mutikainen P, Koricheva J, Fisher M (2006) How general are positive relationships between plant population size, fitness, and genetic variation? J Ecol 94:942–952

    Article  Google Scholar 

  • Leinonen PH, Remington DL, Savolainen O (2011) Local adaptation, phenotypic differentiation, and hybrid fitness in diverged natural populations of Arabidopsis lyrata. Evolution 65:90–107

    Article  PubMed  Google Scholar 

  • Lienert J (2004) Habitat fragmentation effects on fitness of plant populations—a review. J Nat Conserv 12:53–72

    Article  Google Scholar 

  • Lienert J, Fischer M, Diemer M (2002) Local extinctions of the wetland specialist Swertia perennis L. (Gentianaceae) in Switzerland: a revisitation study based on herbarium records. Biol Conserv 103:65–76

    Article  Google Scholar 

  • Lofflin DL, Kephart SR (2005) Outbreding, seedling establishment, and maladaptation in natural and reintroduced populations of rare and common Silene douglasii (Caryophyllaceae). Am J Bot 92:1691–1700

    Article  PubMed  Google Scholar 

  • Lönn M, Prentice HC (2002) Gene diversity and demographic turnover in central and peripheral populations of the perennial herb Gypsophila fastigiata. Oikos 99:489–498

    Article  Google Scholar 

  • Lopez S, Rousset F, Shaw FH, Shaw RG, Ronce O (2009) Joint effects of inbreeding and local adaptation on the evolution of genetic load after fragmentation. Conserv Biol 23:1618–1627

    Article  PubMed  Google Scholar 

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Lynch M (1995) A quantitative-genetic perspective on conservation issues. In: Avise J, Hamrick J (eds) Conservation genetics: case histories from nature. Chapman and Hall, New York, pp 471–501

    Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and non equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    CAS  PubMed Central  PubMed  Google Scholar 

  • McCoy EE, Jones AG, Avise JC (2001) The genetic mating system and tests for cuckoldry in a pipefish species in which males fertilize eggs and brood offspring externally. Mol Ecol 10:1793–1800

    Article  CAS  PubMed  Google Scholar 

  • Miller JM, Coltman DW (2014) Assessment of identity disequilibrium and its relation to empirical heterozygosity fitness correlations: a meta-analysis. Mol Ecol 23:1899–1909

    Article  PubMed  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Bot 51:238–254

    Google Scholar 

  • Oakley CG, Winn AA (2012) Effects of population size and isolation on heterosis, mean fitness, and inbreeding depression in a perennial plant. New Phytol 196:261–270

    Article  PubMed  Google Scholar 

  • Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447

    Article  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Pekkala N, Knott KE, Kotiaho JS, Nissinen K, Puurtinen M (2012) The benefits of interpopulation hybridization diminish with increasing divergence of small populations. J Evol Biol 25:2181–2193

    Article  PubMed  Google Scholar 

  • Peruzzi L, Gargano D (2006) Dianthus ferrugineus Mill. vs. D. guliae Janka: nomenclatural considerations on the Italian yellow carnation. Taxon 55:781–784

    Article  Google Scholar 

  • Pickup M, Field D (2013) Source population characteristics affect heterosis following genetic rescue of fragmented plant populations. Proc R Soc B 280:20122058

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237

    Article  Google Scholar 

  • Richards CM (2000) Inbreeding depression and genetic rescue in a plant metapopulation. Am Nat 155:383–394

    Article  PubMed  Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Shea KL, Furnier GR (2002) Genetic variation and population structure in central and isolated populations of balsam fir, Abies balsamea (Pinaceae). Am J Bot 89:783–791

    Article  PubMed  Google Scholar 

  • Sheridan PM, Karowe DN (2000) Inbreeding, outbreding, and heterosis in the yellow pitcher plant, Sarracenia flava (Sarraceniaceae), in Virginia. Am J Bot 87:1628–1633

    Article  CAS  PubMed  Google Scholar 

  • Smulders MJM, Rus-Kortekaas W, Vosman B (2000) Microsatellite markers useful throughout the genus Dianthus. Genome 43:208–210

    Article  CAS  PubMed  Google Scholar 

  • Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19:489–496

    Article  PubMed  Google Scholar 

  • Thompson JD (2005) Plant evolution in the Mediterranean. Oxford University Press, Oxford

    Book  Google Scholar 

  • Tutin TG, Walters SM (1993) Dianthus L. In: Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (eds) Flora Europaea 1, 2nd edn. Cambridge University Press, Cambridge, pp 227–246

    Google Scholar 

  • Walker D, Porter BA, Avise JC (2002) Genetic parentage assessment in the crayfish Orconectes placidus, a highfecundity invertebrate with extended maternal brood care. Mol Ecol 11:2115–2122

    Article  CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49

    Article  PubMed  Google Scholar 

  • Willi Y, Fischer M (2005) Genetic rescue in interconnected populations of small and large size of the self-incompatible Ranunculus reptans. Heredity 95:437–443

    Article  CAS  PubMed  Google Scholar 

  • Willi Y, Van Kleunen M, Dietrich S, Fischer M (2007) Genetic rescue persists beyond first-generation outbreeding in small populations of a rare plant. Proc R Soc B 274:2357–2364

    Article  PubMed Central  PubMed  Google Scholar 

  • Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2002) Rapid genetic deterioration in captive populations: causes and conservation implications. Conserv Genet 3:277–288

    Article  CAS  Google Scholar 

  • Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:833–843

    Article  Google Scholar 

  • Young AG, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–41418

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to Teresa Gullo, Vittoria Tropea, Giovanni Borda and Luigi Spina for support in experimental pollinations, and Antonio de Giuseppe for help in cultivating plants. The researches the paper refers to are part of the project ‘Sistematica e conservazione della flora della Calabria: indagini su diversità, ecologia, e rischio d’estinzione in popolazioni, specie e comunità vegetali’ supported by Ministero dell’Istruzione, dell’Università e della Ricerca (ex MURST 60 %). Finally, we thank Kevin O’Connell (O’Connell’s School) for linguistic improvements.

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Correspondence to Domenico Gargano.

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Gargano, D., Pellegrino, G. & Bernardo, L. Genetic and fitness consequences of interpopulation mating in Dianthus guliae Janka: conservation implications for severely depleted and isolated plant populations. Conserv Genet 16, 1127–1138 (2015). https://doi.org/10.1007/s10592-015-0727-z

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