Skip to main content

Advertisement

Log in

Resolving neutral and deterministic contributions to genomic structure in Syntrichia ruralis (Bryophyta, Pottiaceae) informs propagule sourcing for dryland restoration

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Syntrichia ruralis is a cosmopolitan moss that occupies steep environmental gradients. In arid to semi-arid regions of the world it is a key component of biological soil crusts, which are fundamental to healthy dryland ecosystem processes. As such, S. ruralis has attracted the attention of conservationists seeking to restore degraded biological soil crust communities and their associated vascular flora. Here, we generate genomic data for S. ruralis populations that span climatic gradients across the Colorado Plateau of the southwestern USA to investigate the contributions of neutral and deterministic processes to the partitioning of genomic structure. Although S. ruralis appears to be highly dispersible, geographic proximity significantly predicts genomic similarity. In addition, even when taking into account apparently high migration rates among populations and spatial autocorrelation of allele frequencies, some genomic variation is explained by environmental gradients correlated with elevation and latitude. Consequently, efforts to restore dryland ecosystems by establishing S. ruralis as a foundation should include strategies to ensure that propagule sources of this moss are environmentally stratified and targeted to the current/future climates of restoration sites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Anderson CD, Epperson BK, Fortin MJ, Holderegger R, James P, Rosenberg MS, Scribner KT, Spear S (2010) Considering spatial and temporal scale in landscape-genetic studies of gene flow. Mol Ecol 19:3565–3575

    Article  PubMed  Google Scholar 

  • Antoninka A, Bowker MA, Reed SC, Doherty K (2016) Production of greenhouse-grown biocrust mosses and associated cyanobacteria to rehabilitate dryland soil function. Restor Ecol 2:324–335

    Article  Google Scholar 

  • Bemmels JB, Ortego J, Knowles LL (2016) Tests of species-specific models reveal the importance of drought in postglacial range shifts of a Mediterranean-climate tree: insights from integrative distributional, demographic and coalescent modelling and ABC model selection. Mol Ecol 25:4889–4906

    Article  CAS  PubMed  Google Scholar 

  • Bowker MA, Stark LR, McLetchie DN, Mishler BD (2000) Sex expression, skewed sex ratios, and microhabitat distribution in the dioecious desert moss Syntrichia caninervis (Pottiaceae). Am J Bot 87:517–526

    Article  CAS  PubMed  Google Scholar 

  • Brieuc MS, Ono K, Drinan DP, Naish KA (2015) Integration of Random Forest with population-based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha). Mol Ecol 24:2729–2746

    Article  PubMed  Google Scholar 

  • Broadhurst LM, Lowe A, Coates DJ, Cunningham SA, McDonald M, Vesk PA, Yates C (2008) Seed supply for broadscale restoration: maximizing evolutionary potential. Evol Appl 1:587–597

    PubMed  PubMed Central  Google Scholar 

  • Brunsfeld SJ, Miller TR, Carstens BC (2007) Insights into the biogeography of the Pacific Northwest of North America: evidence from the phylogeography of Salix melanopsis. Syst Bot 32:129–139

    Article  Google Scholar 

  • Cavender-Bares J, Ackerly DD, Baum DA, Bazzaz FA (2004) Phylogenetic overdispersion in Floridian oak communities. Am Nat 163:823–843

    Article  CAS  PubMed  Google Scholar 

  • Colosimo PF, Hosemann KE, Balabhadra S, Villarreal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928–1933

    Article  CAS  PubMed  Google Scholar 

  • Condon LA, Pyke DA (2016) Filling the interspace—restoring arid land mosses: source populations, organic matter, and overwintering govern success. Ecol Evol 6:7623–7632

    Article  Google Scholar 

  • DeChaine EG, Martin AP (2005) Marked genetic divergence among sky island populations of Sedum lanceolatum (Crassulaceae) in the Rocky Mountains. Am J Bot 92:477–486

    Article  CAS  PubMed  Google Scholar 

  • Désamoré A, Patiño J, Mardulyn P, Mcdaniel SF, Zanatta F, Laenen B, Vanderpoorten A (2016) High migration rates shape the postglacial history of amphi-Atlantic bryophytes. Mol Ecol 25:5568–5584

    Article  PubMed  Google Scholar 

  • Doherty KD, Bowker MA, Antoninka AJ, Johnson NC, Wood TE (2017) Biocrust moss populations differ in growth rates, stress response, and microbial associates. Plant Soil. https://doi.org/10.1007/s11104-017-3389-4

    Google Scholar 

  • Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361

    Article  Google Scholar 

  • Eaton DA (2014) PyRAD: assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics 30:1844–1849

    Article  CAS  PubMed  Google Scholar 

  • Eaton DA, Ree RH (2013) Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Syst Biol 62:689–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, González-Martínez SC, Neale DB (2010) Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda L., Pinaceae). Genetics 185:969–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107:1–5

    Article  CAS  PubMed  Google Scholar 

  • Eppley SM, Taylor PJ, Jesson LK (2007) Self-fertilization in mosses: a comparison of heterozygote deficiency between species with combined versus separate sexes. Heredity 98:38–44

    Article  CAS  PubMed  Google Scholar 

  • Escudero M, Eaton DA, Hahn M, Hipp AL (2014) Genotyping-by-sequencing as a tool to infer phylogeny and ancestral hybridization: a case study in Carex (Cyperaceae). Mol Phylogenet Evol 79:359–367

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Excoffier L, Dupanloup I, Huerta-Sánchez E, Sousa VC, Foll M (2013) Robust demographic inference from genomic and SNP data. PLOS Genet 9:e1003905

    Article  PubMed  PubMed Central  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frantz AC, Cellina S, Krier A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Galbreath KE, Hafner DJ, Zamudio KR, Agnew K (2010) Isolation and introgression in the Intermountain West: contrasting gene genealogies reveal the complex biogeographic history of the American pika (Ochotona princeps). J Biogeogr 37:344–362

    Article  Google Scholar 

  • Gompert Z, Lucas LK, Fordyce JA, Forister ML, Nice CC (2010) Secondary contact between Lycaeides idas and L. melissa in the Rocky Mountains: extensive admixture and a patchy hybrid zone. Mol Ecol 19:3171–3192

    Article  CAS  PubMed  Google Scholar 

  • Guillot G, Rousset F (2013) Dismantling the Mantel tests. Methods Ecol Evol 4:336–344

    Article  Google Scholar 

  • Hafner JC, Upham NS, Reddington E, Torres CW (2008) Phylogeography of the pallid kangaroo mouse, Microdipodops pallidus: a sand-obligate endemic of the Great Basin, western North America. J Biogeogr 35:2102–2118

    Article  PubMed  PubMed Central  Google Scholar 

  • Havens K, Vitt P, Still S, Kramer AT, Fant JB, Schatz K (2015) Seed sourcing for restoration in an era of climate change. Nat Area J 35:122–133

    Article  Google Scholar 

  • He Q, Edwards DL, Knowles LL (2013) Integrative testing of how environments from the past to the present shape genetic structure across landscapes. Evol Int J org Evol 67:3386–3402

    Article  Google Scholar 

  • Hedrick PW (1987) Genetic load and the mating system in homosporous ferns. Evol Int J org Evol 41:1282–1289

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hipp AL, Eaton DA, Cavender-Bares J, Fitzek E, Nipper R, Manos PS (2014) A framework phylogeny of the American oak clade based on sequenced RAD data. PLOS One 9:e93975

    Article  PubMed  PubMed Central  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103

    Article  CAS  PubMed  Google Scholar 

  • Knowles LL, Massatti R (2017) Distributional shifts–not geographic isolation–as a probable driver of montane species divergence. Ecography. https://doi.org/10.1111/ecog.02893

    Google Scholar 

  • Knowles LL, Massatti R, He Q, Olson LE, Lanier HC (2016) Quantifying the similarity between genes and geography across Alaska’s alpine small mammals. J Biogeogr 43:1464–1476

    Article  Google Scholar 

  • Kool JT, Moilanen A, Treml EA (2013) Population connectivity: recent advances and new perspectives. Landsc Ecol 28:165–185

    Article  Google Scholar 

  • Korpelainen H, Jägerbrand A, von Cräutlein M (2012) Genetic structure of mosses Pleurozium schreberi (Willd. ex Brid.) Mitt. and Racomitrium lanuginosum (Hedw.) Brid. along altitude gradients in Hokkaido. Jpn J Bryol 4:309–312

    Article  Google Scholar 

  • Lee CR, Mitchell-Olds TH (2011) Quantifying effects of environmental and geographical factors on patterns of genetic differentiation. Mol Ecol 20:4631–4642

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis LR, Rozzi R, Goffinet B (2014) Direct long-distance dispersal shapes a New World amphitropical disjunction in the dispersal-limited dung moss Tetraplodon (Bryopsida: Splachnaceae). J Biogeogr 41:2385–2395

    Article  Google Scholar 

  • Lönnell N, Hylander K, Jonsson BG, Sundberg S (2012) The fate of the missing spores—patterns of realized dispersal beyond the closest vicinity of a sporulating moss. PLOS One 7:e41987

    Article  PubMed  PubMed Central  Google Scholar 

  • Lotterhos KE, Whitlock MC (2015) The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Mol Ecol 24:1031–1046

    Article  PubMed  Google Scholar 

  • Lynch M (2008) Estimation of nucleotide diversity, disequilibrium coefficients, and mutation rates from high-coverage genome-sequencing projects. Mol Biol Evol 25:2409–2419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magdy M, Werner O, McDaniel SF, Goffinet B, Ros RM (2016) Genomic scanning using AFLP to detect loci under selection in the moss Funaria hygrometrica along a cliate gradient in the Sierra Nevada Mountains, Spain. Plant Biol 18:280–288

    Article  CAS  PubMed  Google Scholar 

  • Manel S, Poncet BN, Legendre P, Gugerli F, Holderegger R (2010) Common factors drive adaptive genetic variation at different spatial scales in Arabis alpina. Mol Ecol 19:3824–3835

    Article  PubMed  Google Scholar 

  • Massatti R, Knowles LL (2014) Microhabitat differences impact phylogeographic concordance of codistributed species: genomic evidence in montane sedges (Carex L.) from the Rocky Mountains. Evol Int J org Evol 68:2833–2846

    Article  Google Scholar 

  • Massatti R, Knowles LL (2016) Contrasting support for alternative models of genomic variation based on microhabitat preference: species-specific effects of climate change in alpine sedges. Mol Ecol 25:3974–3986

    Article  CAS  PubMed  Google Scholar 

  • Massatti R, Reznicek AA, Knowles LL (2016) Utilizing RADseq data for phylogenetic analysis of challenging taxonomic groups: a case study in Carex sect. Racemosae. Am J Bot 103:337–347

    Article  CAS  PubMed  Google Scholar 

  • McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT (2013) Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogenet Evol 66:526–538

    Article  CAS  PubMed  Google Scholar 

  • Merwe M, McPherson H, Siow J, Rossetto M (2014) Next-Gen phylogeography of rainforest trees: exploring landscape-level cpDNA variation from whole-genome sequencing. Mol Ecol Res 14:199–208

    Article  Google Scholar 

  • Miles CJ, Longton RE (1990) The role of spores in reproduction in mosses. Bot J Linean Soc 104:149–173

    Article  Google Scholar 

  • Mishler BD (1990) Reproductive biology and species distinctions in the moss genus Tortula, as represented in Mexico. Syst Bot 1:86–97

    Article  Google Scholar 

  • Mishler BD (2007) Syntrichia. In: Flora of North America Editorial Committee (eds) 1993 + Flora of North America North of Mexico, 20 + vols. New York and Oxford. vol 27, p 618-

  • Mitchell VL (1976) The regionalization of climate in the western United States. J Appl Meteorol 15:920–927

    Article  Google Scholar 

  • Moran PA (1948) The interpretation of statistical maps. J R Stat Soc Series B Methodol 10:243–251

    Google Scholar 

  • Moran PA (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23

    Article  CAS  PubMed  Google Scholar 

  • Narum SR, Buerkle CA, Davey JW, Miller MR, Hohenlohe PA (2013) Genotyping-by-sequencing in ecological and conservation genomics. Mol Ecol 22:2841–2847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nath V, Asthana AK (2001) Reproductive Biology of Bryophytes. In: Reproductive Biology of plants, Springer, Berlin, pp. 148–174

  • Nosil P (2007) Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. Am Nat 169:151–162

    Article  PubMed  Google Scholar 

  • Nosil P, Egan SP, Funk DJ (2008) Heterogeneous genomic differentiation between walking-stick ecotypes: ‘isolation by adaptation’ and multiple roles for divergent selection. Evolution Int J org Evolution 62:316–336

    Article  Google Scholar 

  • Nosil P, Funk DJ, Ortiz-Barrientos D (2009) Divergent selecation and heterogeneous genomic divergence. Mol Ecol 18:375–402

    Article  PubMed  Google Scholar 

  • Oldfield S, Olwell P (2015) The right seed in the right place at the right time. Bioscience 65:955–956

    Article  Google Scholar 

  • Orsini L, Vanoverbeke J, Swillen I, Mergeay J, de Meester L (2013) Drivers of population genetic differentiation in the wild: isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Mol Ecol 22:5983–5999

    Article  PubMed  Google Scholar 

  • Paasch AE, Mishler BD, Nosratinia S, Stark LR, Fisher KM (2015) Decoupling of sexual reproduction and genetic diversity in the female-biased Mojave Desert moss Syntrichia caninervis (Pottiaceae). Int J Plant Sci 176:751–761

    Article  Google Scholar 

  • Papadopoulou A, Knowles LL (2015a) Genomic tests of the species-pump hypothesis: recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands. Evolution Int J org Evolution 69:1501–1517

    Article  Google Scholar 

  • Papadopoulou A, Knowles LL (2015b) Species-specific responses to island connectivity cycles: refined models for testing phylogeographic concordance across a Mediterranean Pleistocene Aggregate Island Complex. Mol Ecol 24:4252–4268

    Article  PubMed  Google Scholar 

  • Peterson BK, Weber JN, Kay EH, Fisher HS, Hoekstra HE (2012) Double digest RADseq: an inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLOS One 7:e37135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinheiro F, Cozzolino S, Draper D, de Barros F, Felix LP, Fay MF, Palma-Silva C (2014) Rock outcrop orchids reveal the genetic connectivity and diversity of inselbergs of northeastern Brazil. BMC Evol Biol:1–15

    Google Scholar 

  • Pisa S, Werner O, Vanderpoorten A, Magdy M, Ros RM (2013) Elevational patterns of genetic variation in the cosmopolitan moss Bryum argenteum (Bryaceae). Am J Bot 100:2000–2008

    Article  PubMed  Google Scholar 

  • Plant Conservation Alliance (2015) National seed strategy for rehabilitation and restoration 2015–2020. US Department of the Interior, Bureau of Land Management. https://www.blm.gov/programs/natural-resources/native-plant-communities/national-seed-strategy. Accessed 30 June 2017

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 3 March 2017

  • Raufaste N, Rousset F (2001) Are partial mantel tests adequate? Evolution Int J org Evolution 55:1703–1705

    Article  CAS  Google Scholar 

  • Rellstab C, Gugerli F, Eckert AJ, Hancock AM, Holderegger R (2015) A practical guide to environmental association analysis in landscape genomics. Mol Ecol 24:4348–4370

    Article  PubMed  Google Scholar 

  • Richardson BA, Brunsfeld SJ, Klopfenstein NB (2002) DNA from bird dispersed seed and wind disseminated pollen provides insights into postglacial colonization and population genetic structure of whitebark pine (Pinus albicaulis). Mol Ecol 11:215–227

    Article  CAS  PubMed  Google Scholar 

  • Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584

    Article  PubMed  PubMed Central  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Res 4:137–138

    Google Scholar 

  • Rosentreter R, Bowker M, Belnap J (2007) A field guide to biological soil crusts of western US drylands: common lichens and bryophytes. US Government Printing Office, Denver. p. 104

    Google Scholar 

  • Sexton JP, Hangartner SB, Hoffmann AA (2014) Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution Int J org Evolution 68:1–15

    Article  CAS  Google Scholar 

  • Shaw AJ (2000) Molecular phylogeography and cryptic speciation in the mosses. Mielichhoferia elongata and M. mielichhoferiana (Bryaceae). Mol Ecol 9:595–608

    Article  CAS  PubMed  Google Scholar 

  • Shryock DF, Havrilla CA, DeFalco LA, Esque TC, Custer NA, Wood TE (2015) Landscape genomics of Sphaeralcea ambigua in the Mojave Desert: a multivariate, spatially-explicit approach to guide ecological restoration. Conserv Genet 16:1303–1317

    Article  Google Scholar 

  • Smith AT (1974) The distribution and dispersal of pikas: influences of behavior and climate. Ecology 55:1368–1376

    Article  Google Scholar 

  • Stark LR, Brinda JC, Nicholas McLetchie D, Oliver MJ (2012) Extended periods of hydration do not elicit dehardening to desiccation tolerance in regeneration trials of the moss Syntrichia caninervis. Int J Plant Sci 173:333–343

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Takahashi T, Nagata N, Sota T (2014) Application of RAD-based phylogenetics to complex relationships among variously related taxa in a species flock. Mol Phylogenet Evol 80:137–144

    Article  PubMed  Google Scholar 

  • Vanderpoorten A, Devos N, Goffinet B, Hardy OJ, Shaw AJ (2008) The barriers to oceanic island radiation in bryophytes: insights from the phylogeography of the moss Grimmia montana. J Biogeogr 35:654–663

    Article  Google Scholar 

  • Wang C, Zöllner S, Rosenberg NA (2012) A quantitative comparison of the similarity between genes and geography in worldwide human populations. PLOS Genet 8:e1002886

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weber WA, Wittman RC (2007). Bryophytes of Colorado. Pilgrims Process

  • Weber B, Büdel B, Belnap J (2014) Biological soil crusts: an organizing principle in drylands. Springer International Publishing, Cham

    Google Scholar 

Download references

Acknowledgements

The authors are grateful for the support and helpful advice of their colleagues, including E. Milano for assistance with next-generation sequencing, M. Bowker for moss expertise, and J. Belnap and two anonymous reviewers for comments that improved the quality of this manuscript. This work was funded by the Bureau of Land Management’s Colorado Plateau Native Plant Program. Any use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rob Massatti.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 2595 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Massatti, R., Doherty, K.D. & Wood, T.E. Resolving neutral and deterministic contributions to genomic structure in Syntrichia ruralis (Bryophyta, Pottiaceae) informs propagule sourcing for dryland restoration. Conserv Genet 19, 85–97 (2018). https://doi.org/10.1007/s10592-017-1026-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-017-1026-7

Keywords

Navigation