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ArticlesPhylogeny, phylogeography, phylobetadiversity and the molecular analysis of biological communities
Published:27 August 2011https://doi.org/10.1098/rstb.2011.0057
Abstract
There has been much recent interest and progress in the characterization of community structure and community assembly processes through the application of phylogenetic methods. To date most focus has been on groups of taxa for which some relevant detail of their ecology is known, for which community composition is reasonably easily quantified and where the temporal scale is such that speciation is not likely to feature. Here, we explore how we might apply a molecular genetic approach to investigate community structure and assembly at broad taxonomic and geographical scales, where we have little knowledge of species ecology, where community composition is not easily quantified, and where speciation is likely to be of some importance. We explore these ideas using the class Collembola as a focal group. Gathering molecular evidence for cryptic diversity suggests that the ubiquity of many species of Collembola across the landscape may belie greater community complexity than would otherwise be assumed. However, this morphologically cryptic species-level diversity poses a challenge for attempts to characterize diversity both within and among local species assemblages. Recent developments in high throughput parallel sequencing technology, combined with mtDNA barcoding, provide an advance that can bring together the fields of phylogenetic and phylogeographic analysis to bear on this problem. Such an approach could be standardized for analyses at any geographical scale for a range of taxonomic groups to quantify the formation and composition of species assemblages.
Footnotes
References
- 1
Webb C. O. . 2000Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. Am. Nat. 156, 145–155.doi:10.1086/303378 (doi:10.1086/303378). Crossref, PubMed, ISI, Google Scholar - 2
Cavender-Bares J., Kozak K. H., Fine P. V. A.& Kembel S. W. . 2009The merging of community ecology and phylogenetic biology. Ecol. Lett. 12, 693–715.doi:10.1111/j.1461-0248.2009.01314.x (doi:10.1111/j.1461-0248.2009.01314.x). Crossref, PubMed, ISI, Google Scholar - 3
Emerson B. C.& Gillespie R. G. . 2008Phylogenetic analysis of community assembly and structure over space and time. Trends Ecol. Evol. 23, 619–630.doi:10.1016/j.tree.2008.07.005 (doi:10.1016/j.tree.2008.07.005). Crossref, PubMed, ISI, Google Scholar - 4
Johnson M. T. J.& Stinchcombe J. R. . 2007An emerging synthensis between community ecology and evolutionary biology. Trends Ecol. Evol. 22, 250–257.doi:10.1016/j.tree.2007.01.014 (doi:10.1016/j.tree.2007.01.014). Crossref, PubMed, ISI, Google Scholar - 5
Vamosi S. M., Heard S. B., Vamosi J. C.& Webb C. O. . 2009Emerging patterns in the comparative analysis of phylogenetic community structure. Mol. Ecol. 18, 572–592.doi:10.1111/j.1365-294X.2008.04001.x (doi:10.1111/j.1365-294X.2008.04001.x). Crossref, PubMed, ISI, Google Scholar - 6
Hubbell S. P. . 2001The unified neutral theory of biodiversity and biogeography.Princeton, NJ: Princeton University Press. Google Scholar - 7
MacArthur R. H.& Wilson E. O. . 1967The theory of island biogeography. Princeton, NJ: Princeton University Press. Google Scholar - 8
Weiher E., Freund D., Bunton T., Stefanski A., Lee T.& Bentivenga S. . 2011Advances, challenges, and a developing synthesis of ecological community assembly theory. Phil. Trans. R. Soc. B. 366, 2403–2413.doi:10.1098/rstb.2011.0056 (doi:10.1098/rstb.2011.0056). Link, ISI, Google Scholar - 9
Ricklefs R. E. . 1987Community diversity: relative roles of local and regional processes. Science 235, 167–171.doi:10.1126/science.235.4785.167 (doi:10.1126/science.235.4785.167). Crossref, PubMed, ISI, Google Scholar - 10
Emerson B. C.& Kolm N. . 2005Species diversity can drive speciation. Nature 434, 1015–1017.doi:10.1038/nature03450 (doi:10.1038/nature03450). Crossref, PubMed, ISI, Google Scholar - 11
Ricklefs R. E. . 2006Evolutionary diversification and the origin of the diversity–environment relationship. Ecology 87, S3–S13.doi:10.1890/0012-9658(2006)87[3:EDATOO]2.0.CO;2 (doi:10.1890/0012-9658(2006)87[3:EDATOO]2.0.CO;2). Crossref, PubMed, ISI, Google Scholar - 12
Hickerson M. J., Carstens B. C., Cavender-Bares J., Crandall K. A., Graham C. H., Johnson J. B., Rissler L., Victoriano P. F.& Yoder A. D. . 2010Phylogeography's past, present, and future: 10 years after Avise, 2000. Mol. Phylogenet. Evol. 54, 291–301.doi:10.1016/j.ympev.2009.09.016 (doi:10.1016/j.ympev.2009.09.016). Crossref, PubMed, ISI, Google Scholar - 13
Avise J. C. . 2000Phylogeography: the history and formation of species.Cambridge, MA: Harvard University Press. Crossref, Google Scholar - 14
Carstens B. C.& Knowles L. L. . 2007Shifting distributions and speciation: species divergence during rapid climate change. Mol. Ecol. 16, 619–627.doi:10.1111/j.1365-294X.2006.03167.x (doi:10.1111/j.1365-294X.2006.03167.x). Crossref, PubMed, ISI, Google Scholar - 15
Knowles L. L.& Carstens B. C. . 2006Estimating a geographically explicit model of population divergence. Evolution 61, 477–493.doi:10.1111/j.1558-5646.2007.00043.x (doi:10.1111/j.1558-5646.2007.00043.x). Crossref, ISI, Google Scholar - 16
Knowles L. L.& Maddison W. P. . 2002Statistical phylogeography. Mol. Phylogeogr. 11, 2623–2635. Google Scholar - 17
Knowles L. L. . 2009Statistical phylogeography. Annu. Rev. Ecol. Evol. Syst. 40, 593–612.doi:10.1146/annurev.ecolsys.38.091206.095702 (doi:10.1146/annurev.ecolsys.38.091206.095702). Crossref, ISI, Google Scholar - 18
Galbreath K. E., Hafner D. J., Zamudio K. R.& Agnew K. . 2010Isolation and introgression in the intermountain west: contrasting gene genalogies reveal the complex biogeographic history of the American pike (Ochotona princeps). J. Biogeogr. 37, 344–362.doi:10.1111/j.1365-2699.2009.02201.x (doi:10.1111/j.1365-2699.2009.02201.x). Crossref, ISI, Google Scholar - 19
Peters J. L., Zhuravlev Y. N., Fefelov I., Humphries E. M.& Omland K. E. . 2008Multilocus phylogeography of a holarctic duck: colonization of North America from Eurasia by Gadwall (Anas strepera). Evolution 62, 1469–1483.doi:10.1111/j.1558-5646.2008.00372.x (doi:10.1111/j.1558-5646.2008.00372.x). Crossref, PubMed, ISI, Google Scholar - 20
Carnaval A. C., Hickerson M. J., Haddad C. F. B., Rodrigues M. T.& Moritz C. . 2009Stability predicts genetic diversity in a Brazilian Atlantic forest hotspot. Science 323, 785–789.doi:10.1126/science.1166955 (doi:10.1126/science.1166955). Crossref, PubMed, ISI, Google Scholar - 21
Garrick R. C., Rowell D. M., Simmons C. S., Hillis D. M.& Sunnucks P. . 2008Fine-scale phylogeographic congruence despite demographic incongruence in two low-mobility saproxylic springtails. Evolution 62, 1103–1118.doi:10.1111/j.1558-5646.2008.00349.x (doi:10.1111/j.1558-5646.2008.00349.x). Crossref, PubMed, ISI, Google Scholar - 22
Ilves K. L., Huang W., Wares J. P.& Hickerson M. J. . 2010Colonization and/or mitochondrial selective sweeps across the North Atlantic intertidal assemblage revealed by multi-taxa Bayesian computation. Mol. Ecol. 19, 4505–4519.doi:10.1111/j.1365-294X.2010.04790.x (doi:10.1111/j.1365-294X.2010.04790.x). Crossref, PubMed, ISI, Google Scholar - 23
McCulloch G. A., Wallis G. P.& Waters J. M. . 2010Onset of glaciation drove simultaneous vicariant isolation of alpine insects in New Zealand. Evolution 64, 2033–2043.doi:10.1111/j.1558-5646.2010.00980.x (doi:10.1111/j.1558-5646.2010.00980.x). Crossref, PubMed, ISI, Google Scholar - 24
Emerson B. C.& Hewitt G. M. . 2005Phylogeography. Curr. Biol. 15, R367–R371.doi:10.1016/j.cub.2005.05.016 (doi:10.1016/j.cub.2005.05.016). Crossref, PubMed, ISI, Google Scholar - 25
Pons J., Barraclough T. G., Gomez-Zurita J., Cardoso A., Duran D. P., Hazell S., Kamoun S., Sumlin W.& Vogler A. . 2006Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 55, 595–609.doi:10.1080/10635150600852011 (doi:10.1080/10635150600852011). Crossref, PubMed, ISI, Google Scholar - 26
Beaumont M. A., Zhang W.& Balding D. J. . 2002Approximate Bayesian computation in population genetics. Genetics 162, 2025–2035. Crossref, PubMed, ISI, Google Scholar - 27
Hickerson M. J.& Meyer C. P. . 2008Testing comparative phylogeographic models of marine vicariance and dispersal using a hirearchical Bayesian approach. BMC Evol. Biol. 8, 322.doi:10.1186/1471-2148-8-322 (doi:10.1186/1471-2148-8-322). Crossref, PubMed, ISI, Google Scholar - 28
Lemey P., Rambaut A., Drummond A.& Suchard M. A. . 2009Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520.doi:10.1371/journal.pcbi.1000520 (doi:10.1371/journal.pcbi.1000520). Crossref, PubMed, ISI, Google Scholar - 29
Navascués M., Depaulis F.& Emerson B. C. . 2010Combining contemporary and ancient DNA in population genetic and phylogeographical studies. Mol. Ecol. Resour. 10, 760–772.doi:10.1111/j.1755-0998.2010.02895.x (doi:10.1111/j.1755-0998.2010.02895.x). Crossref, PubMed, ISI, Google Scholar - 30
Navascués M.& Emerson B. C. . 2009Elevated substitution rate estimates from ancient DNA: model violation and bias of Bayesian methods. Mol. Ecol. 18, 4390–4397.doi:10.1111/j.1365-294X.2009.04333.x (doi:10.1111/j.1365-294X.2009.04333.x). Crossref, PubMed, ISI, Google Scholar - 31
Crandall K. A.& Templeton A. R. . 1993Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny construction. Genetics 134, 959–969. Crossref, PubMed, ISI, Google Scholar - 32
Posada D.& Crandall K. A. . 2001Intraspecific gene genealogies: trees grafting into networks. Trends Ecol. Evol. 16, 37–45.doi:10.1016/S0169-5347(00)02026-7 (doi:10.1016/S0169-5347(00)02026-7). Crossref, PubMed, ISI, Google Scholar - 33
Emerson B. C., Forgie S., Goodacre S. L.& Oromi P. . 2006Testing phylogeographic predictions on an active volcanic island: Brachyderes rugatus (Coleoptera: Curculionidae) on La Palma (Canary Islands). Mol. Ecol. 15, 449–458.doi:10.1111/j.1365-294X.2005.02786.x (doi:10.1111/j.1365-294X.2005.02786.x). Crossref, PubMed, ISI, Google Scholar - 34
Miraldo A., Hewitt G. M., Paulo O. S.& Emerson B. C. Submitted. Phylogeography and demographic history of Lacerta lepida in the Iberian Peninsula: multiple refugia, range expansions and secondary contact zones. BMC Evol. Biol.. ISI, Google Scholar - 35
Zarza E., Reynoso V. H.& Emerson B. C. . 2008Diversification in the northern neotropics: mitochondrial and nuclear DNA phylogeography of the iguana Ctenosaura pectinata and related species. Mol. Ecol. 17, 3259–3275.doi:10.1111/j.1365-294X.2008.03826.x (doi:10.1111/j.1365-294X.2008.03826.x). Crossref, PubMed, ISI, Google Scholar - 36
Graham C. H.& Fine P. V. A. . 2008Phylogenetic beta diversity: linking ecological and evolutionary processes over space and time. Ecol. Lett. 11, 1265–1277.doi:10.1111/j.1461-0248.2008.01256.x (doi:10.1111/j.1461-0248.2008.01256.x). Crossref, PubMed, ISI, Google Scholar - 37
Chu H. Y., Fierer N., Lauber C. L., Caporaso J. G., Knight R.& Grogan P. . 2010Soil bacterial diversity in the Arctic is not fundamentally different from that found in other biomes. Environ. Microbiol. 12, 2998–3006.doi:10.1111/j.1462-2920.2010.02277.x (doi:10.1111/j.1462-2920.2010.02277.x). Crossref, PubMed, ISI, Google Scholar - 38
Fulthorpe R. R., Roesch L. F. W., Riva A.& Triplett E. W. . 2008Distantly sampled soils carry few species in common. ISME J. 2, 901–910.doi:10.1038/ismej.2008.55 (doi:10.1038/ismej.2008.55). Crossref, PubMed, ISI, Google Scholar - 39
Kaspari M., Stevenson B. S., Shik J.& Kerekes J. F. . 2010Scaling community structure: how bacteria, fungi, and ant taxocenes differentiate along a tropical forest floor. Ecology 91, 2221–2226.doi:10.1890/09-2089.1 (doi:10.1890/09-2089.1). Crossref, PubMed, ISI, Google Scholar - 40
Lauber C. L., Hamady M., Knight R.& Fierer N. . 2009Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111–5120.doi:10.1128/AEM.00335-09 (doi:10.1128/AEM.00335-09). Crossref, PubMed, ISI, Google Scholar - 41
Rousk J., Baath E., Brookes P. C., Lauber C. L., Lozupone C., Caporaso J. G., Knight R.& Fierer N. . 2010Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J. 4, 1340–1351.doi:10.1038/ismej.2010.58 (doi:10.1038/ismej.2010.58). Crossref, PubMed, ISI, Google Scholar - 42
Creer S., 2010Ultra-deep sequencing of the meiofaunal biosphere: practice, pitfalls and promises. Mol. Ecol. 19, 4–20.doi:10.1111/j.1365-294X.2009.04473.x (doi:10.1111/j.1365-294X.2009.04473.x). Crossref, PubMed, ISI, Google Scholar - 43
Fonseca V. G., 2010Second-generation environmental sequencing unmasks marine metazoan biodiversity. Nat. Commun. 1, 98.doi:10.1038/ncomms1095 (doi:10.1038/ncomms1095). Crossref, PubMed, ISI, Google Scholar - 44
Decaëns T. . 2010Macroecological patterns in soil communities. Global Ecol. Biogeogr. 19, 287–302.doi:10.1111/j.1466-8238.2009.00517.x (doi:10.1111/j.1466-8238.2009.00517.x). Crossref, Google Scholar - 45
Usher M. B., Davis P., Harris J.& Longstaff B. . 1979A profusion of species? Approaches towards understanding the dynamics of the populations of microarthropods in decomposer communities. Population dynamics (eds, Anderson A. M., Turner B. D.& Taylor L. R. ), pp. 359–384. Oxford, UK: Blackwell Scientific. Google Scholar - 46
Giller P. S. . 1996The diversity of soil communities, the ‘poor man's tropical rainforest.’. Biodivers. Conserv. 5, 135–168.doi:10.1007/BF00055827 (doi:10.1007/BF00055827). Crossref, ISI, Google Scholar - 47
Hopkin S. P. . 1997Biology of the springtails (Insecta: Collembola).Oxford, UK: Oxford University Press. Google Scholar - 48
Regier J. C., Schultz J. W., Zwick A., Hussey A., Ball B., Wetzer R., Martin J. W.& Cunningham C. W. . 2010Athropod relationships revealed by phylogenomic analysis of nuclear protein coding sequences. Nature 463, 1079–1083.doi:10.1038/nature08742 (doi:10.1038/nature08742). Crossref, PubMed, ISI, Google Scholar - 49
Rapoport E. H. . 1971The geographical distribution of Neotropical and Antarctic Collembola. Pacific Insects Monogr. 25, 99–118. Google Scholar - 50
Christiansen K. . 1971Notes on Miocene amber Collembola from Chiapas. Univ. California Publ. Entomol. 63, 45–48. Google Scholar - 51
Mari Mutt J. A. . 1983Collembola in amber from the Dominican Republic. Proc. Entomol. Soc. Wash. 85, 575–587. ISI, Google Scholar - 52
Cicconardi F., Nardi F., Emerson B. C., Frati F.& Fanciulli P. P. . 2010Deep phylogeographic divisions and long-term persistence of forest invertebrates in the North-Western Mediterranean basin. Mol. Ecol. 19, 386–400.doi:10.1111/j.1365-294X.2009.04457.x (doi:10.1111/j.1365-294X.2009.04457.x). Crossref, PubMed, ISI, Google Scholar - 53
Mayr E. . 1942Systematics and the origin of species from the viewpoint of a zoologist.Cambridge, MA: Harvard University Press. Google Scholar - 54
Timmermans M. J. T. N., Ellers J., Marien J., Verhoeff S. C.& Ferwerda E. B. & Van Straalen, N. M. 2005 Genetic structure in Orchesella cincta (Collembola): strong subdivision of European populations inferred from mtDNA and AFLP markers. Mol. Ecol. 14, 2017–2024.doi:10.1111/j.1365-294X.2005.02548.x (doi:10.1111/j.1365-294X.2005.02548.x). Crossref, PubMed, ISI, Google Scholar - 55
Stevens M. I., Greenslade P., Hogg I. D.& Sunnucks P. . 2006Southern hemisphere springtails: could any have survived glaciation of Antarctica?Mol. Biol. Evol. 23, 874–882.doi:10.1093/molbev/msj073 (doi:10.1093/molbev/msj073). Crossref, PubMed, ISI, Google Scholar - 56
Torricelli G., Carapelli A., Convey P., Nardi F., Boore J. L.& Frati F. . 2009High divergence across the whole mitochondrial genome in the ‘pan-Antarctic’ springtail Friesea grisea: evidence for cryptic species?Gene 449, 30–40.doi:10.1016/j.gene.2009.09.006 (doi:10.1016/j.gene.2009.09.006). Crossref, PubMed, ISI, Google Scholar - 57
Garrick R. C., Sands C. J., Rowell D. M., Hillis D. M.& Sunnucks P. . 2007Catchments catch all: long-term population history of a giant springtail from the southeast Australian highlands—a multigene approach. Mol. Ecol. 16, 1865–1882.doi:10.1111/j.1365-294X.2006.03165.x (doi:10.1111/j.1365-294X.2006.03165.x). Crossref, PubMed, ISI, Google Scholar - 58
Folmer O., Black M., Hoeh W., Lutz R.& Vrijenhoek R. . 1994DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299. PubMed, Google Scholar - 59
Ratnasingham S.& Hebert P. D. N. . 2007BOLD: the barcode of life data system. Mol. Ecol. Notes 7, 355–364.doi:10.1111/j.1471-8286.2007.01678.x (doi:10.1111/j.1471-8286.2007.01678.x). Crossref, PubMed, Google Scholar - 60
Blaxter M. L. . 2004The promise of a DNA taxonomy. Phil. Trans. R. Soc. B 359, 669–679.doi:10.1098/rstb.2003.1447 (doi:10.1098/rstb.2003.1447). Link, ISI, Google Scholar - 61
Blaxter M. L., Elsworth B.& Daub J. . 2004DNA taxonomy of a neglected anumal phylum: an unexpected diversity of tardigrades. Biol. Lett. 271, S189–S192.doi:10.1098/rsbl.2003.0130 (doi:10.1098/rsbl.2003.0130). Link, ISI, Google Scholar - 62
Heethoff M., Domes K., Laumann M., Maraun M., Norton R. A.& Scheu S. . 2007High genetic divergences indicate ancient separation of parthenogenetic lineages of the oribatid mite Platynothrus peltifer (Acari, Oribatida). J. Evol. Biol. 20, 392–402.doi:10.1111/j.1420-9101.2006.01183.x (doi:10.1111/j.1420-9101.2006.01183.x). Crossref, PubMed, ISI, Google Scholar - 63
Mortimer E., van Vuuren B. J., Lee J. E., Marshall D. J., Convey P.& Chwon S. L. . 2010Mite dispersal among the Southern Ocean Islands and Antarctica before the last glacial maximum. Proc. R. Soc. Lond. B 278, 1247–1255.doi:10.1098/rspb.2010.1779 (doi:10.1098/rspb.2010.1779). Link, ISI, Google Scholar - 64
Schäffer S., Pfingstl T., Koblmüller S., Winkler K. A., Sturmbauer C.& Krisper G. . 2010Phylogenetic analysis of European Scutovertex mites (Acari, Oribatida, Scutoverticidae) reveals paraphyly and cryptic diversity: a molecular genetic and morphological approach. Mol. Phylogenet. Evol. 55, 677–688.doi:10.1016/j.ympev.2009.11.025 (doi:10.1016/j.ympev.2009.11.025). Crossref, PubMed, ISI, Google Scholar - 65
Stevens M. I.& Hogg I. D. . 2006Contrasting levels of mitochondrial DNA variability between mites (Penthalodidae) and springtails (Hypogastruridae) from Trans-Antarctic Mountains suggest long-term effects of glaciation and life history on substitution rates, and speciation process. Soil Biol. Biochem. 38, 3171–3180.doi:10.1016/j.soilbio.2006.01.009 (doi:10.1016/j.soilbio.2006.01.009). Crossref, ISI, Google Scholar - 66
Powers T. O., Neher D. A., Mullin P., Esquivel A., Giblin-Davis R. M., Kanzaki N., Stock S. P., Mora M. M.& Uribe-Lorio L. . 2009Tropical nematode diversity: vertical stratification of nematode communities in a Costa Rican humid lowland rainforest. Mol. Ecol. 18, 985–996.doi:10.1111/j.1365-294X.2008.04075.x (doi:10.1111/j.1365-294X.2008.04075.x). Crossref, PubMed, ISI, Google Scholar - 67
Huber J. A., Mark Welch D., Morrison H. G., Huse S. M., Neal P. R., Butterfield D. A.& Sogin M. L. . 2007Microbial population structures in the deep marine biosphere. Science 318, 97–100.doi:10.1126/science.1146689 (doi:10.1126/science.1146689). Crossref, PubMed, ISI, Google Scholar - 68
Roesch L. F., Fulthorpe R. R., Riva A., Casella G., Hadwin A. K. M., Kent A. D., 2007Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1, 283–290.doi:10.1038/ismej.2007.53 (doi:10.1038/ismej.2007.53). Crossref, PubMed, ISI, Google Scholar - 69
Sogin M. L., Morrison H. G., Huber J. A., Mark Welch D., Huse S. M., Neal P. R., Arrieta J. M.& Herndl G. J. . 2006Microbial diversity in the deep sea and the underexplored ‘rare biosphere.’. Proc. Natl Acad. Sci. USA 103, 12 115–12 120.doi:10.1073/pnas.0605127103 (doi:10.1073/pnas.0605127103). Crossref, ISI, Google Scholar - 70
Medinger R., Nolte V., Pandey R. V., Jost S., Ottenwalder B., Schlotterer C.& Boenigk J. . 2010Diversity in a hidden world: potential and limitation of next-generation sequencing for surveys of molecular diversity of eukaryotic microorganisms. Mol. Ecol. 19, 32–40.doi:10.1111/j.1365-294X.2009.04478.x (doi:10.1111/j.1365-294X.2009.04478.x). Crossref, PubMed, ISI, Google Scholar - 71
Nolte V., Pandey R. V., Jost S., Medinger R., Ottenwalder B., Boenigk J.& Schlötterer C. . 2010Contrasting seasonal niche separation between rare and abundant taxa conceals the extent of protist diversity. Mol. Ecol. 19, 2908–2915.doi:10.1111/j.1365-294X.2010.04669.x (doi:10.1111/j.1365-294X.2010.04669.x). Crossref, PubMed, ISI, Google Scholar - 72
Hamilton H. C., Strickland M. S., Wickings K., Bradford M. A.& Fierer N. . 2009Surveying soil faunal communities using a direct molecular approach. Soil Biol. Biochem. 41, 1311–1314.doi:10.1016/j.soilbio.2009.03.021 (doi:10.1016/j.soilbio.2009.03.021). Crossref, ISI, Google Scholar - 73
Quince C., Lanzén A., Curtis T. P., Davenport R. J., Hall N., Head I. M., Read L. F.& Sloan W. T. . 2009Accurate determination of microbial diversity from 454 pyrosequencing data. Nat. Meth. 6, 639–641.doi:10.1038/nmeth.1361 (doi:10.1038/nmeth.1361). Crossref, PubMed, ISI, Google Scholar - 74
Reeder J.& Knight R. . 2009The ‘rare biosphere’: a reality check. Nat. Meth. 6, 636–637.doi:10.1038/nmeth0909-636 (doi:10.1038/nmeth0909-636). Crossref, PubMed, ISI, Google Scholar - 75
Boyce R., Chilana P.& Rose T. P. . 2009iCODEHOP: a new interactive program for designing COnsensus-DEgenerate Hybrid Oligonucleotide Primers from multiply aligned protein sequences. Nucleic Acids Res. 37, w222–w228.doi:10.1093/nar/gkp379 (doi:10.1093/nar/gkp379). Crossref, PubMed, ISI, Google Scholar - 76
Rose T. M., Henikoff J. G.& Henikoff S. . 2003CODEHOP (COnsensus-DEgenerate Hybrid Oligonucleotide Primer) PCR primer design. Nucleic Acids Res. 31, 3763–3766.doi:10.1093/nar/gkg524 (doi:10.1093/nar/gkg524). Crossref, PubMed, ISI, Google Scholar - 77
Bensasson D., Zhang D.-X., Hartl D. L.& Hewitt G. M. . 2001Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends Ecol. Evol. 16, 314–321.doi:10.1016/S0169-5347(01)02151-6 (doi:10.1016/S0169-5347(01)02151-6). Crossref, PubMed, ISI, Google Scholar
