Abstract
Many key questions in evolutionary ecology require the use of variance ratios such as heritability, repeatability, and individual resource specialization. These ratios allow researchers to understand how phenotypic variation is structured into genetic and non-genetic components, to identify how much organisms vary in the resources they use or how functional traits structure species communities. Understanding how evolutionary and ecological processes differ among populations and environments therefore often requires the comparison of these ratios across groups (i.e., populations, sexes, species). Inference based on comparisons of ratios can be limited, however. Variance ratios can remain the same across group despite very different values in the numerator and denominator variances. Moreover, evolutionary ecologists are most often interested in differences in specific variance components among groups rather than in differences in variance ratios per se. Recommendations for how to infer whether groups differ in variance are not clear in the literature. Using simulations, we show how questions regarding the estimation of variance components and their differences among groups can be answered with linear mixed models (LMMs). Frequentist and Bayesian frameworks have similar abilities to identify differences in variance components. However, variance differences at higher levels of organization can be difficult to detect with low sample sizes. We provide tools to conduct power analyses to determine the appropriate sample sizes necessary to detect differences in variance of a given magnitude. We conclude by supplying guidelines for how to report and draw inferences based on the comparisons of variance components and variance ratios
Significance statement
Many critical questions in ecology and evolution use variance ratios, such as repeatability, heritability, or individual resource specialization, to make inferences about ecological and evolutionary processes. In many cases, these inferences rely on the comparison of variance ratios among datasets (populations, sexes, or environments). In this article, we show that current approaches of drawing inferences about group differences from comparisons of ratios are inappropriate because ratios can differ due to differences in the numerator, denominator, or both. We investigated how questions regarding differences in variance ratios and constituent variance components can be evaluated using linear mixed model (LMM) approaches and provide guidance for appropriate sampling schemes under different scenarios and discuss common pitfalls associated with estimation of differences in variance component among datasets.
Similar content being viewed by others
Data availability
All the data for simulations is available on the Open Science Framework’s project for this article: https://osf.io/5aw42/.
Code availability
All codes for simulations are available on the Open Science Framework’s project for this article: https://osf.io/5aw42/.
References
Aguirre JD, Hine E, McGuigan K, Blows MW (2014) Comparing G: multivariate analysis of genetic variation in multiple populations. Heredity 112:21–29. https://doi.org/10.1038/hdy.2013.12
Arnold SJ, Phillips PC (1999) Hierarchical comparison of genetic variance-covariance matrices. II Coastal-inland divergence in the garter snake, Thamnophis elegans. Evolution 53:1516–1527. https://doi.org/10.1111/j.1558-5646.1999.tb05415.x
Austin PC, Hux JE (2002) A brief note on overlapping confidence intervals. J Vasc Surg 36:194–195. https://doi.org/10.1067/mva.2002.125015
Barr DR (1969) Using confidence intervals to test hypotheses. J Qual Technol 1:256–258
Bates D, Maechler M, Bolker B et al (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2002) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400
Bucklaew A, Dochtermann NA (2021) The effects of exposure to predators on personality and plasticity. Ethology 127:158–165. https://doi.org/10.1111/eth.13107
Bürkner P-C (2017) brms: an R package for Bayesian multilevel models using Stan. J Stat Softw 80:1–28
Carmona CP, de Bello F, Mason NW, Lepš J (2016) Traits without borders: integrating functional diversity across scales. Trends Ecol Evol 31:382–394
Chartois J, Claudel C (1945) Hunting the Dahut: a French folk custom. J Am Folk 58:21–24. https://doi.org/10.2307/535332
Coblentz KE, Rosenblatt AE, Novak M (2017) The application of Bayesian hierarchical models to quantify individual diet specialization. Ecology 98:1535–1547. https://doi.org/10.1002/ecy.1802
Dingemanse NJ, Dochtermann NA (2013) Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol 82:39–54
Dochtermann NA, Roff DA (2010) Applying a quantitative genetics framework to behavioural syndrome research. Philos Trans R Soc B Biol Sci 365:4013–4020. https://doi.org/10.1098/rstb.2010.0129
Dochtermann NA, Royauté R (2019) The mean matters: going beyond repeatability to interpret behavioural variation. Anim Behav 153:147–150. https://doi.org/10.1016/j.anbehav.2019.05.012
Fontana S, Thomas MK, Moldoveanu M, Spaak P, Pomati F (2018) Individual-level trait diversity predicts phytoplankton community properties better than species richness or evenness. ISME J 12:356
Gilmour AR, Gogel BJ, Cullis BR, Welham Sj, Thompson R (2015) ASReml user guide release 4.1 structural specification. VSN International Ltd, Hemel Hempstead
Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22
Hamilton JA, Royauté R, Wright JW, Hodgskiss P, Ledig FT (2017) Genetic conservation and management of the California endemic, Torrey pine (Pinus torreyana Parry): Implications of genetic rescue in a genetically depauperate species. Ecol Evol 7:7370–7381
Hansen TF, Pélabon C, Houle D (2011) Heritability Is Not Evolvability Evol Biol 38:258. https://doi.org/10.1007/s11692-011-9127-6
Hector A (2021) The new statistics with R: an introduction for biologists. University Press, Oxford
Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204
Jacquat MS (1995) Le dahu: monographie ethno-étho-biologique publiée à l’occasion de l’exposition inaugurée le 1er avril 1995. Editions de la Girafe, Musée d’histoire naturelle, La Chaux-de-Fonds
Jenkins SH (2011) Sex differences in repeatability of food-hoarding behaviour of kangaroo rats. Anim Behav 81:1155–1162
Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121
Lindgren F, Rue H (2015) Bayesian spatial modelling with R-INLA. J Stat Softw 63:1–25. https://doi.org/10.18637/jss.v063.i19
MacGregor-Fors I, Payton ME (2013) Contrasting diversity values: statistical inferences based on overlapping confidence intervals. PLoS ONE 8:e56794. https://doi.org/10.1371/journal.pone.0056794
Martin JG, Nussey DH, Wilson AJ, Réale D (2011) Measuring individual differences in reaction norms in field and experimental studies: a power analysis of random regression models. Methods Ecol Evol 2:362–374
Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197
Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956
Nakagawa S, Poulin R, Mengersen K, Reinhold K, Engqvist L, Lagisz M, Senior AM (2015) Meta-analysis of variation: ecological and evolutionary applications and beyond. Methods Ecol Evol 6:143–152. https://doi.org/10.1111/2041-210X.12309
Nakagawa S, Schielzeth H (2012) The mean strikes back: mean–variance relationships and heteroscedasticity. Trends Ecol Evol 27:474–475. https://doi.org/10.1016/j.tree.2012.04.003
Pinheiro J, Bates D (2006) Mixed-effects models in S and S-PLUS. Springer Science & Business Media, New York
R Core Team (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Roff D (2002) Comparing G matrices: a Manova approach. Evolution 56:1286–1291. https://doi.org/10.1111/j.0014-3820.2002.tb01439.x
Roff DA, Prokkola JM, Krams I, Rantala MJ (2012) There is more than one way to skin a G matrix. J Evol Biol 25:1113–1126. https://doi.org/10.1111/j.1420-9101.2012.02500.x
Rönnegård L, Shen X, Alam M (2010) hglm: A package for fitting hierarchical generalized linear models. R J 2:20–28
Royauté CR, Buddle CM, Vincent (2015) Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider. Funct Ecol 29:962–970
Royauté R, Dochtermann NA (2017) When the mean no longer matters: developmental diet affects behavioral variation but not population averages in the house cricket (Acheta domesticus). Behav Ecol 28:337–345
Royauté R, Garrison C, Dalos J, Berdal MA, Dochtermann NA (2019) Current energy state interacts with the developmental environment to influence behavioural plasticity. Anim Behav 148:39–51
Santostefano F, Wilson AJ, Araya-Ajoy YG, Dingemanse NJ (2016) Interacting with the enemy: indirect effects of personality on conspecific aggression in crickets. Behav Ecol 27:1235–1246
Schenker N, Gentleman JF (2001) On judging the significance of differences by examining the overlap between confidence intervals. Am Stat 55:182–186. https://doi.org/10.1198/000313001317097960
Shaw RG (1991) The comparison of quantitative genetic parameters between populations. Evolution 45:143–151. https://doi.org/10.1111/j.1558-5646.1991.tb05273.x
Tüzün RN, Müller S, Koch K, Stoks, (2017) Pesticide-induced changes in personality depend on the urbanization level. Anim Behav 134:45–55
van de Pol M (2012) Quantifying individual variation in reaction norms: how study design affects the accuracy, precision and power of random regression models. Methods Ecol Evol 3:268–280
Violle C, Enquist BJ, McGill BJ, Jiang LIN, Albert CH, Hulshof C, Jung V, Messier J (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252
White SJ, Pascall DJ, Wilson AJ (2020) Towards a comparative approach to the structure of animal personality variation. Behav Ecol 31:340–351. https://doi.org/10.1093/beheco/arz198
Wilson AJ (2018) How should we interpret estimates of individual repeatability? Evol Lett 2:4–8. https://doi.org/10.1002/evl3.40
Wilson AJ, Réale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26. https://doi.org/10.1111/j.1365-2656.2009.01639.x
Acknowledgements
We thank the participants of the Statistical Quantification of Individual Differences (SQuID) Symposium at the 2016 ISBE Congress for helpful discussions. We also thank Russel Bonduriansky, Ben Bolker, and six anonymous reviewers for helpful comments on previous versions of this manuscript.
Funding
This study was funded by NSF IOS-1557951 (to NAD) and the Department of Biological Sciences at North Dakota State University.
Author information
Authors and Affiliations
Contributions
Each author contributed equally to the design, analysis, and writing of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Communicated by J. Lindström.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Royauté, R., Dochtermann, N.A. Comparing ecological and evolutionary variability within datasets. Behav Ecol Sociobiol 75, 127 (2021). https://doi.org/10.1007/s00265-021-03068-3
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-021-03068-3