Home LiteratureArticle Details
PMID: 21444315 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S. Review

Controlling for non-independence in comparative analysis of patterns across populations within species.

Stone GN, Nee S, Felsenstein J

Abstract

How do we quantify patterns (such as responses to local selection) sampled across multiple populations within a single species? Key to this question is the extent to which populations within species represent statistically independent data points in our analysis. Comparative analyses across species and higher taxa have long recognized the need to control for the non-independence of species data that arises through patterns of shared common ancestry among them (phylogenetic non-independence), as have quantitative genetic studies of individuals linked by a pedigree. Analyses across populations lacking pedigree information fall in the middle, and not only have to deal with shared common ancestry, but also the impact of exchange of migrants between populations (gene flow). As a result, phenotypes measured in one population are influenced by processes acting on others, and may not be a good guide to either the strength or direction of local selection. Although many studies examine patterns across populations within species, few consider such non-independence. Here, we discuss the sources of non-independence in comparative analysis, and show why the phylogeny-based approaches widely used in cross-species analyses are unlikely to be useful in analyses across populations within species. We outline the approaches (intraspecific contrasts, generalized least squares, generalized linear mixed models and autoregression) that have been used in this context, and explain their specific assumptions. We highlight the power of 'mixed models' in many contexts where problems of non-independence arise, and show that these allow incorporation of both shared common ancestry and gene flow. We suggest what can be done when ideal solutions are inaccessible, highlight the need for incorporation of a wider range of population models in intraspecific comparative methods and call for simulation studies of the error rates associated with alternative approaches.

MeSH Terms
Animals Biological Evolution Gene Flow Genetics, Population Models, Genetic Phenotype
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Stone Graham N
Institute of Evolutionary Biology, The King's Buildings, West Mains Road, Edinburgh EH9 3JT, UK. [email protected]
Nee Sean
Felsenstein Joseph
References (86)
86 references, click to expand
  1. Likelihood and Bayes estimation of ancestral population sizes in hominoids using data from multiple loci.
    Genetics. 2002 Dec;162(4):1811-23 PMID: 12524351
  2. An intraspecific comparative analysis of character divergence between sympatric species.
    Evolution. 2005 Mar;59(3):554-64 PMID: 15856698
  3. Wild pedigrees: the way forward.
    Proc Biol Sci. 2008 Mar 22;275(1635):613-21 PMID: 18211868
  4. Adaptation and the comparative method.
    Trends Ecol Evol. 2000 Jul;15(7):296-299 PMID: 10856957
  5. Testing for phylogenetic signal in comparative data: behavioral traits are more labile.
    Evolution. 2003 Apr;57(4):717-45 PMID: 12778543
  6. Natural selection drives the fine-scale divergence of a coevolutionary arms race involving a long-mouthed weevil and its obligate host plant.
    BMC Evol Biol. 2009 Nov 27;9:273 PMID: 19941669
  7. Gene genealogies in a metapopulation.
    Genetics. 2001 Oct;159(2):893-905 PMID: 11606561
  8. Metapopulation models for historical inference.
    Mol Ecol. 2004 Apr;13(4):865-75 PMID: 15012761
  9. Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computation.
    Bioinformatics. 2008 Dec 1;24(23):2713-9 PMID: 18842597
  10. Genetic evidence for complex speciation of humans and chimpanzees.
    Nature. 2006 Jun 29;441(7097):1103-8 PMID: 16710306
  11. Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis.
    Genetics. 2004 Jun;167(2):747-60 PMID: 15238526
  12. Detecting non-Brownian trait evolution in adaptive radiations.
    PLoS Biol. 2006 Nov;4(11):e373 PMID: 17090217
  13. Phylogenetic analysis and comparative data: a test and review of evidence.
    Am Nat. 2002 Dec;160(6):712-26 PMID: 18707460
  14. Is a new and general theory of molecular systematics emerging?
    Evolution. 2009 Jan;63(1):1-19 PMID: 19146594
  15. Concordant phylogeography and cryptic speciation in two Western Palaearctic oak gall parasitoid species complexes.
    Mol Ecol. 2010 Feb;19(3):592-609 PMID: 20070516
  16. Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers.
    Syst Biol. 2007 Jun;56(3):400-11 PMID: 17520504
  17. Understanding patterns of genetic diversity in the oak gallwasp Biorhiza pallida: demographic history or a Wolbachia selective sweep?
    Heredity (Edinb). 2001 Sep;87(Pt 3):294-304 PMID: 11737276
  18. The effect of intraspecific sample size on type I and type II error rates in comparative studies.
    Evolution. 2005 Dec;59(12):2705-10 PMID: 16526516
  19. Estimating a geographically explicit model of population divergence.
    Evolution. 2007 Mar;61(3):477-93 PMID: 17348914
  20. Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum-Mediterranean oak gallwasp Andricus quercustozae.
    Mol Ecol. 2003 Aug;12(8):2153-74 PMID: 12859636
  21. A framework for community and ecosystem genetics: from genes to ecosystems.
    Nat Rev Genet. 2006 Jul;7(7):510-23 PMID: 16778835
  22. Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics.
    Proc Natl Acad Sci U S A. 2007 Feb 20;104(8):2785-90 PMID: 17301231
  23. Estimating genetic parameters in natural populations using the "animal model".
    Philos Trans R Soc Lond B Biol Sci. 2004 Jun 29;359(1446):873-90 PMID: 15306404
  24. PHYLOGENIES, SPATIAL AUTOREGRESSION, AND THE COMPARATIVE METHOD: A COMPUTER SIMULATION TEST.
    Evolution. 1996 Oct;50(5):1750-1765 PMID: 28565598
  25. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters.
    J Evol Biol. 2010 Mar;23(3):494-508 PMID: 20070460
  26. Adaptive constraints and the phylogenetic comparative method: a computer simulation test.
    Evolution. 2002 Jan;56(1):1-13 PMID: 11913655
  27. Extending genomics to natural communities and ecosystems.
    Science. 2008 Apr 25;320(5875):492-5 PMID: 18436780
  28. STEM: species tree estimation using maximum likelihood for gene trees under coalescence.
    Bioinformatics. 2009 Apr 1;25(7):971-3 PMID: 19211573
  29. Plant genetic determinants of arthropod community structure and diversity.
    Evolution. 2005 Jan;59(1):61-9 PMID: 15792227
  30. Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach.
    Genetics. 1999 Jun;152(2):763-73 PMID: 10353916
  31. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach.
    Proc Natl Acad Sci U S A. 2001 Apr 10;98(8):4563-8 PMID: 11287657
  32. Gene tree discordance, phylogenetic inference and the multispecies coalescent.
    Trends Ecol Evol. 2009 Jun;24(6):332-40 PMID: 19307040
  33. Inferring the historical patterns of biological evolution.
    Nature. 1999 Oct 28;401(6756):877-84 PMID: 10553904
  34. Phylogenetic signal, evolutionary process, and rate.
    Syst Biol. 2008 Aug;57(4):591-601 PMID: 18709597
  35. Unified framework to evaluate panmixia and migration direction among multiple sampling locations.
    Genetics. 2010 May;185(1):313-26 PMID: 20176979
  36. Quantifying the pleistocene history of the oak gall parasitoid Cecidostiba fungosa using twenty intron loci.
    Evolution. 2010 Sep;64(9):2664-81 PMID: 20455927
  37. Plant genetics predicts intra-annual variation in phytochemistry and arthropod community structure.
    Mol Ecol. 2007 Dec;16(23):5057-69 PMID: 17927708
  38. Effect of hybridization of the Quercus crassifolia x Quercus crassipes complex on the community structure of endophagous insects.
    Oecologia. 2006 Apr;147(4):702-13 PMID: 16463057
  39. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data.
    Comput Appl Biosci. 1995 Jun;11(3):247-51 PMID: 7583692
  40. Host niches and defensive extended phenotypes structure parasitoid wasp communities.
    PLoS Biol. 2009 Aug;7(8):e1000179 PMID: 19707266
  41. Warm-up rates during arousal from torpor in heterothermic mammals: physiological correlates and a comparison with heterothermic insects.
    J Comp Physiol B. 1992;162(3):284-95 PMID: 1613167
  42. Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa.
    Ann Bot. 2010 May;105(5):707-17 PMID: 20228089
  43. The phylogenetic mixed model.
    Am Nat. 2004 Jan;163(1):84-96 PMID: 14767838
  44. Importance of species interactions to community heritability: a genetic basis to trophic-level interactions.
    Ecol Lett. 2006 Jan;9(1):78-85 PMID: 16958871
  45. Accommodating phylogenetic uncertainty in evolutionary studies.
    Science. 2000 Jun 30;288(5475):2349-50 PMID: 10875916
  46. A new approach to estimate parameters of speciation models with application to apes.
    Genome Res. 2007 Oct;17(10):1505-19 PMID: 17712021
  47. Comparative methods with sampling error and within-species variation: contrasts revisited and revised.
    Am Nat. 2008 Jun;171(6):713-25 PMID: 18419518
  48. Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts.
    Proc Biol Sci. 2005 Aug 7;272(1572):1525-34 PMID: 16048766
  49. Inferring the population structure and demography of Drosophila ananassae from multilocus data.
    Genetics. 2004 Dec;168(4):1975-85 PMID: 15611168
  50. STABILIZING SELECTION AND THE COMPARATIVE ANALYSIS OF ADAPTATION.
    Evolution. 1997 Oct;51(5):1341-1351 PMID: 28568616
  51. Geographic Patterns in the Evolution of Resistance and Virulence in Drosophila and Its Parasitoids.
    Am Nat. 1999 May;153(S5):S61-S74 PMID: 29578778
  52. Does gene flow destroy phylogenetic signal? The performance of three methods for estimating species phylogenies in the presence of gene flow.
    Mol Phylogenet Evol. 2008 Dec;49(3):832-42 PMID: 18845264
  53. Ecological impacts of genotypic diversity in the clonal seagrass Zostera marina.
    Ecology. 2009 May;90(5):1412-9 PMID: 19537560
  54. PHYLOGENETIC ANALYSES OF THE CORRELATED EVOLUTION OF CONTINUOUS CHARACTERS: A SIMULATION STUDY.
    Evolution. 1991 May;45(3):534-557 PMID: 28568838
  55. Genetic structure of a foundation species: scaling community phenotypes from the individual to the region.
    Heredity (Edinb). 2008 Feb;100(2):121-31 PMID: 17047690
  56. Comparative Analysis of Character Displacement and Spatial Adaptations as Illustrated by the Evolution of Dalechampia Blossoms.
    Am Nat. 2000 Oct;156(S4):S17-S34 PMID: 29592584
  57. COMPARATIVE METHODS AT THE SPECIES LEVEL: GEOGRAPHIC VARIATION IN MORPHOLOGY AND GROUP SIZE IN GREY-CROWNED BABBLERS (POMATOSTOMUS TEMPORALIS).
    Evolution. 1995 Dec;49(6):1134-1146 PMID: 28568526
  58. The seven deadly sins of comparative analysis.
    J Evol Biol. 2009 Jul;22(7):1367-75 PMID: 19508410
  59. Tree hybridization and genotypic variation drive cryptic speciation of a specialist mite herbivore.
    Evolution. 2008 Dec;62(12):3027-40 PMID: 18752612
  60. Differences in spawning date between populations of common frog reveal local adaptation.
    Proc Natl Acad Sci U S A. 2010 May 4;107(18):8292-7 PMID: 20404185
  61. The phylogeographical clade trade: tracing the impact of human-mediated dispersal on the colonization of northern Europe by the oak gallwasp Andricus kollari.
    Mol Ecol. 2007 Jul;16(13):2768-81 PMID: 17594446
  62. Using the quantitative genetic threshold model for inferences between and within species.
    Philos Trans R Soc Lond B Biol Sci. 2005 Jul 29;360(1459):1427-34 PMID: 16048785
  63. Comparative methods for examining adaptation depend on evolutionary models.
    Folia Primatol (Basel). 1989;53(1-4):203-20 PMID: 2691365
  64. From genes to geography: a genetic similarity rule for arthropod community structure at multiple geographic scales.
    Mol Ecol. 2006 Nov;15(13):4215-28 PMID: 17054514
  65. The phylogenetic regression.
    Philos Trans R Soc Lond B Biol Sci. 1989 Dec 21;326(1233):119-57 PMID: 2575770
  66. Comparing phylogenetic signal in intraspecific and interspecific body size datasets.
    J Evol Biol. 2004 Sep;17(5):1157-61 PMID: 15312088
  67. Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci.
    Genetics. 2003 Aug;164(4):1645-56 PMID: 12930768
  68. Expected coalescence times and segregating sites in a model of glacial cycles.
    Genet Mol Res. 2006 Jul 31;5(3):466-74 PMID: 17117361
  69. A comparative method for studying adaptation to a randomly evolving environment.
    Evolution. 2008 Aug;62(8):1965-77 PMID: 18452574
  70. METHODS FOR THE ANALYSIS OF COMPARATIVE DATA IN EVOLUTIONARY BIOLOGY.
    Evolution. 1991 Aug;45(5):1065-1080 PMID: 28564168
  71. THE QUANTITATIVE ASSESSMENT OF PHYLOGENETIC CONSTRAINTS IN COMPARATIVE ANALYSES: SEXUAL DIMORPHISM IN BODY WEIGHT AMONG PRIMATES.
    Evolution. 1985 Nov;39(6):1335-1351 PMID: 28564267
  72. Statistics for correlated data: phylogenies, space, and time.
    Ecol Appl. 2006 Feb;16(1):20-32 PMID: 16705958
  73. Speciational history of Australian grass finches (Poephila) inferred from thirty gene trees.
    Evolution. 2005 Sep;59(9):2033-47 PMID: 16261740
  74. A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences.
    Ecology. 2009 Jul;90(7):1762-72 PMID: 19694126
  75. Space versus phylogeny: disentangling phylogenetic and spatial signals in comparative data.
    Proc Biol Sci. 2009 Jan 7;276(1654):21-30 PMID: 18796398
  76. How to separate genetic and environmental causes of similarity between relatives.
    J Evol Biol. 2007 Sep;20(5):1890-903 PMID: 17714306
  77. Within-species variation and measurement error in phylogenetic comparative methods.
    Syst Biol. 2007 Apr;56(2):252-70 PMID: 17464881
  78. Overrun by the neighbors: landscape context affects strength and sign of local adaptation.
    Ecology. 2010 Aug;91(8):2253-60 PMID: 20836447
  79. The probability of topological concordance of gene trees and species trees.
    Theor Popul Biol. 2002 Mar;61(2):225-47 PMID: 11969392
  80. Plant genotypic diversity predicts community structure and governs an ecosystem process.
    Science. 2006 Aug 18;313(5789):966-8 PMID: 16917062
  81. Inferring phylogeny despite incomplete lineage sorting.
    Syst Biol. 2006 Feb;55(1):21-30 PMID: 16507521
  82. Quantitative genetic models for describing simultaneous and recursive relationships between phenotypes.
    Genetics. 2004 Jul;167(3):1407-24 PMID: 15280252
  83. The distribution of the coalescence time and the number of pairwise nucleotide differences in the "isolation with migration" model.
    Theor Popul Biol. 2008 Mar;73(2):277-88 PMID: 18215405
  84. Local adaptation in Trinidadian guppies alters ecosystem processes.
    Proc Natl Acad Sci U S A. 2010 Feb 23;107(8):3616-21 PMID: 20133670
  85. Discordance of species trees with their most likely gene trees.
    PLoS Genet. 2006 May;2(5):e68 PMID: 16733550
  86. Isolation with migration models for more than two populations.
    Mol Biol Evol. 2010 Apr;27(4):905-20 PMID: 19955477
Article Info
Journal
Philosophical transactions of the Royal Society of London. Series B, Biological sciences
Abbr.
Philos Trans R Soc Lond B Biol Sci
ISSN
1471-2970
Published
2011-05-12
Pages
1410-24
Language
English
Region
England
NLM ID
7503623
PMCID
PMC3081573
Subset
IM
Grants
NIGMS NIH HHS · R01 GM071639 · United States
NIGMS NIH HHS · GM071639 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]