Advertisement

Alpine Botany

, Volume 127, Issue 2, pp 171–183 | Cite as

Intraspecific haplotype diversity in Cherleria sedoides L. (Caryophyllaceae) is best explained by chloroplast capture from an extinct species

  • Abigail J. MooreEmail author
  • Francisco J. Valtueña
  • Markus S. Dillenberger
  • Joachim W. Kadereit
  • Chris D. Preston
Original Article
  • 227 Downloads

Abstract

Cherleria sedoides, a plant species widespread in alpine areas of the major European mountain ranges and in Scotland, contains two highly divergent chloroplast haplotype groups, one widespread (WH) and one present only in some populations in the Alps (AH). We investigated whether this haplotype diversity is the result of (1) intraspecific differentiation, (2) retention of an ancestral polymorphism or (3) hybridisation. For this purpose, 106 matK sequences from throughout the Caryophyllaceae and 80 trnQ-rps16 and psbD-trnT sequences of C. sedoides (51) and other species of Cherleria (29) were used for the construction of phylogenies and haplotype networks. As the two haplotype groups were never each other’s closest relatives, haplotype diversity as a result of intraspecific differentiation is unlikely. Patterns of genetic differentiation within the WH and AH groups are very different. Whereas WH shows a radial pattern typical of rapid expansion, AH is divided into two divergent subgroups each containing more variation than the WH group. This suggests that the two haplotype groups have dissimilar histories and are therefore unlikely to represent an ancestral polymorphism. Instead, we conclude that the polymorphism is best interpreted as the result of hybridisation. As the WH and AH haplotype groups fall into Cherleria, but do not group with any extant species, we conclude that the rare AH group represents the original C. sedoides, and that the WH group was captured from another, now extinct, species of Cherleria.

Keywords

Alps cpDNA Hybridisation Minuartia s.l. Range expansion 

Notes

Acknowledgements

We thank Stephen Bungard, Jim McIntosh and Gordon Rothero for advice about suitable collection sites in Scotland, the staff of Scottish Natural Heritage (especially John Burrow, Tamara Lawton, Alexander Macdonald and Alex Turner) for approval to collect material in SSSIs and John Burton of Cononish farmhouse for facilitating our access to Ben Oss. FJV’s visit to Britain was made possible by a grant from the BSBI Science and Research Committee, and a stay of 4 months at the Institut für Spezielle Botanik und Botanischer Garten (Mainz, Germany) was supported by Ministerio de Educación, Cultura y Deporte (Programa de movilidad Jose Castillejo). For permission to collect in the Alps we thank Delphine Morandeau and Christine Lagarenne of the Ministère de l’Écologie, du Développement durable et de l’Énergie of France and Andrej Arih and Peter Skoberne of the Triglav National Park. For permission to collect in the northern Carpathians we thank Antoni Zięba of the Tatra National Park. We gratefully acknowledge Sulisława Borzyszkowska for helping us to obtain the permission to collect samples in Tatra National Park, Prof. Mária Höhn for her help in finding populations in the southern Carpathians, Prof. Vladimir Stevanović for information about localities of Cherleria sedoides in Balkans, Carmen G. Relinque for her assistance and company on collecting trips to Scotland and the Pyrenees and Natalie Schmalz for her company on the collecting trip to the northern Carpathians. We thank Maria Geyer (Mainz, Germany) for optimising the figures and four anonymous reviewers for their suggestions that improved the manuscript.

Funding

This study was funded by grants from the BSBI Science and Research Committee and the Ministerio de Educación, Cultura y Deporte (Programa de movilidad Jose Castillejo) to Francisco J. Valtueña.

Declaration of authorship

CDP, JWK and FJV designed the study. FJV (with CDP in Scotland) and MSD collected samples in the field and FJV performed the research. FJV, MSD and AJM analysed the data. All authors wrote the manuscript. FJV and AJM contributed equally to this publication.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

35_2017_190_MOESM1_ESM.txt (19 kb)
Supplementary material 1: Taxa used in the analyses, together with voucher information and GenBank accession numbers. Abbreviations for the Cherleria sedoides samples correspond to populations as in Table 1 (TXT 18 kb)
35_2017_190_MOESM2_ESM.pdf (2.7 mb)
Supplementary material 2: Cladogram of core Minuartia obtained with BEAST and based on chloroplast matK sequence variation. Posterior probability values (only PP ≥0.90)/maximum likelihood bootstrap values (only BS ≥70) are indicated above/below the branches (PDF 2777 kb)
35_2017_190_MOESM3_ESM.pdf (69 kb)
Supplementary material 3: Number of studied individuals (N) in alpine populations of Cherleria sedoides with widespread (WH) and alpine haplotype groups (AH) considering only the chloroplast region psbD-trnT. Population codes as in Table 1 (PDF 69 kb)

References

  1. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  2. Belahbib N, Pemonge M-H, Ouassou A, Sbay H, Kremer A, Petit RJ (2001) Frequent cytoplasmic exchanges between oak species that are not closely related: Quercus suber and Q. ilex in Morocco. Mol Ecol 10:2003–2012CrossRefPubMedGoogle Scholar
  3. Canestrelli D, Porretta D, Lowe WH, Bisconti R, Carere C, Nascetti G (2016) The tangled evolutionary legacies of range expansion and hybridization. Trends Ecol Evol 31:677–688CrossRefPubMedGoogle Scholar
  4. Cinget B, de Lafontaine G, Gérardi S, Bousquet J (2015) Integrating phylogeography and paleoecology to investigate the origin and dynamics of hybrid zones: insights from two widespread North American firs. Mol Ecol 24:2856–2870CrossRefPubMedGoogle Scholar
  5. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  6. Coleman M, Liston A, Kadereit JW, Abbott RJ (2003) Repeat intercontinental dispersal and Pleistocene speciation in disjunct Mediterranean and desert Senecio (Asteraceae). Am J Bot 90:1446–1454CrossRefPubMedGoogle Scholar
  7. Cottam WP, Tucker JM, Drobnick R (1959) Some clues to Great Basin postpluvial climates provided by oak distributions. Ecology 40:361–377CrossRefGoogle Scholar
  8. Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62:1908–1920PubMedGoogle Scholar
  9. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2, more models, new heuristics and parallel computing. Nat Methods 9:772CrossRefPubMedPubMedCentralGoogle Scholar
  10. De La Torre AR, Wang T, Jaquish B, Aitken SN (2013) Adaptation and exogenous selection in a Picea glauca × Picea engelmannii hybrid zone: implications for forest management under climate change. New Phytol 201:687–699CrossRefGoogle Scholar
  11. Dillenberger MS, Kadereit JW (2014) Maximum polyphyly: multiple origins and delimitation with plesiomorphic characters require a new circumscription of Minuartia (Caryophyllaceae). Taxon 63:64–88CrossRefGoogle Scholar
  12. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214CrossRefPubMedPubMedCentralGoogle Scholar
  13. Drummond AJ, Nicholls GK, Rodrigo AG, Solomon W (2002) Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161:1307–1320PubMedPubMedCentralGoogle Scholar
  14. Drummond AJ, Ho SYW, Rawlence N, Rambaut A (2007) A rough guide to BEAST 1.4. University of Auckland, New ZealandGoogle Scholar
  15. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973CrossRefPubMedPubMedCentralGoogle Scholar
  16. Endler JA (1977) Geographic variation, speciation, and clines. Princeton University Press, PrincetonGoogle Scholar
  17. Excoffier L, Ray N (2008) Surfing during population expansions promotes genetic revolutions and structuration. Trends Ecol Evol 23:347–351CrossRefPubMedGoogle Scholar
  18. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  19. Freeman DC, Turner WA, McArthur ED, Graham JH (1991) Characterization of a narrow hybrid zone between two species of big sagebrush (Artemisia tridentata: Asteraceae). Am J Bot 78:805–815CrossRefGoogle Scholar
  20. Hooper DU, Dukes JS (2010) Functional composition controls invasion success in a California serpentine grassland. J Ecol 98:764–777CrossRefGoogle Scholar
  21. Huang DI, Hefer CA, Kolosova N, Douglas CJ, Cronk QCB (2014) Whole plastome sequencing reveals deep plastid divergence and cytonuclear discordance between closely related balsam populars, Populus balsamifera and P. trichocarpa (Salicaceae). New Phytol 204:693–703CrossRefPubMedGoogle Scholar
  22. Kadereit JW, Uribe-Covers S, Westberg E, Comes HP (2006) Reciprocal hybridization at different times between Senecio flavus and Senecio glaucus gave rise to two polyploid species in north Africa and south-west Asia. New Phytol 169:431–441CrossRefPubMedGoogle Scholar
  23. Larkin DJ (2012) Lengths and correlates of lag phases in upper-Midwest plant invasions. Biol Invasions 14:827–838CrossRefGoogle Scholar
  24. Luo X, Hu Q, Zhou P, Zhang D, Wang Q, Abbot RJ, Liu J (2017) Chasing ghosts: allopolyploid origin of Oxyria sinensis (Polygonaceae) from its only diploid congener and an unknown ancestor. Mol Ecol 26:3037–3049CrossRefPubMedGoogle Scholar
  25. Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536CrossRefGoogle Scholar
  26. Miller MA, Pfeiffer W, Schwartz T (2012) The CIPRES science gateway: a community resource for phylogenetic analyses. In: TG’11, Proceedings of the 2011 TeraGrid conference, Salt Lake CityGoogle Scholar
  27. Moore AJ, Dillenberger MS (2017) A conspectus of the genus Cherleria (Minuartia s.l., Caryophyllaceae). Willdenowia 47:5–14CrossRefGoogle Scholar
  28. Moore AJ, Kadereit JW (2013) The evolution of substrate differentiation in Minuartia series Laricifoliae (Caryophyllaceae) in the European Alps: in situ origin or repeated colonization? Am J Bot 100:2412–2425CrossRefPubMedGoogle Scholar
  29. Moore AJ, Merges D, Kadereit JW (2013) The origin of the serpentine endemic Minuartia laricifolia subsp. Ophiolitica by vicariance and competitive exclusion. Mol Ecol 22:2218–2231CrossRefPubMedGoogle Scholar
  30. Pelser PB, Abbot RJ, Comes HP, Milton JJ, Möller M, Looseley ME, Cron GV, Barcelona JF, Kennedy AH, Watson LE, Barone R, Hernández F, Kadereit JW (2012) The genetic ghost of an invasion past: colonization and extinction revealed by historical hybridization in Senecio. Mol Ecol 21:369–387CrossRefPubMedGoogle Scholar
  31. Petit RJ, Bodénès C, Ducousso A, Rousell G, Kremer A (2003) Hybridization as a mechanism of invasion in oaks. New Phytol 161:151–164CrossRefGoogle Scholar
  32. Premoli AC, Mathiasen P, Acosta MC, Ramos VA (2012) Phylogeographically concordant chloroplast DNA divergence in sympatric Nothofagus s.s. How deep can it be? New Phytol 193:261–275CrossRefPubMedGoogle Scholar
  33. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.5. http://beast.bio.ed.ac.uk/Tracer. Accessed 11 Dec 2013
  34. Rieseberg LH, Soltis DE (1991) Phylogenetic consequences of cytoplasmic gene flow in plants. Evol Trends Plant 5:65–84Google Scholar
  35. Schönswetter P, Stehlik I, Holderegger R, Tribsch A (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Mol Ecol 14:3547–3555CrossRefPubMedGoogle Scholar
  36. Stamatakis A (2014) RAxML version 8, a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313CrossRefPubMedPubMedCentralGoogle Scholar
  37. Streicher JW, McEntee JP, Drzich LC, Card DC, Schield DR, Smart U, Parkinson CL, Jezkova T, Smith EN, Castoe TA (2016) Genetic surfing, not allopatric divergence, explains spatial sorting of mitochondrial haplotypes in venomous coralsnakes. Evolution 70:1435–1449CrossRefPubMedGoogle Scholar
  38. Václavík T, Meentemeyer RK (2012) Equilibrium or not? Modelling potential distribution of invasive species in different stages of invasion. Div Dist 18:73–83CrossRefGoogle Scholar
  39. Valtueña FJ, Dillenberger MS, Kadereit JW, Moore AJ, Preston CD (2015) What is the origin of the Scottish populations of the European endemic Cherleria sedoides L. (Caryophyllaceae)? New J Bot 5:13–25CrossRefGoogle Scholar
  40. Wendel JF (1989) New World tetraploid cottons contain Old World cytoplasm. Proc Natl Acad Sci USA 86:4132–4136CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wendel JF, Brubaker CL, Seelanan T (2010) The origin and evolution of Gossypium. In: Stewart JM, Oosterhuis D, Heitholt JJ, Mauney JR (eds) Physiology of cotton. Springer, Dordrecht, pp 1–18Google Scholar

Copyright information

© Swiss Botanical Society 2017

Authors and Affiliations

  • Abigail J. Moore
    • 1
    • 2
    Email author
  • Francisco J. Valtueña
    • 3
  • Markus S. Dillenberger
    • 1
    • 4
  • Joachim W. Kadereit
    • 5
  • Chris D. Preston
    • 6
  1. 1.Institut für Spezielle Botanik und Botanischer GartenJohannes Gutenberg-UniversitätMainzGermany
  2. 2.Department of Microbiology and Plant Biology and Oklahoma Biological SurveyUniversity of OklahomaNormanUSA
  3. 3.Área de Botánica, Facultad de CienciasUniversidad de ExtremaduraBadajozSpain
  4. 4.Department of Botany and Plant PathologyOregon State UniversityCorvallisUSA
  5. 5.Institut für Organismische und Molekulare EvolutionsbiologieJohannes Gutenberg-UniversitätMainzGermany
  6. 6.CambridgeUK

Personalised recommendations