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The island rule explains consistent patterns of body size evolution in terrestrial vertebrates

Abstract

Island faunas can be characterized by gigantism in small animals and dwarfism in large animals, but the extent to which this so-called ‘island rule’ provides a general explanation for evolutionary trajectories on islands remains contentious. Here we use a phylogenetic meta-analysis to assess patterns and drivers of body size evolution across a global sample of paired island–mainland populations of terrestrial vertebrates. We show that ‘island rule’ effects are widespread in mammals, birds and reptiles, but less evident in amphibians, which mostly tend towards gigantism. We also found that the magnitude of insular dwarfism and gigantism is mediated by climate as well as island size and isolation, with more pronounced effects in smaller, more remote islands for mammals and reptiles. We conclude that the island rule is pervasive across vertebrates, but that the implications for body size evolution are nuanced and depend on an array of context-dependent ecological pressures and environmental conditions.

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Fig. 1: Conceptual figure showing body size evolution in island populations.
Fig. 2: Location of island populations included in our analyses for mammals, birds, reptiles and amphibians.
Fig. 3: ‘Island rule’ effects in terrestrial vertebrates.
Fig. 4: The effect of island area and spatial isolation on insular size shifts in terrestrial vertebrates.

Data availability

All data are available at https://github.com/anabenlop/Island_Rule and https://figshare.com/projects/Body_size_evolution_in_insular_vertebrates/89102.

Code availability

The code to conduct the analyses is available at https://github.com/anabenlop/Island_Rule.

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Acknowledgements

We are grateful to K. B. Aubry, J. E. Keehn, S. Michaelides and D. Strickland for sharing their data with us, and to P. Peres-Neto and S. Nakagawa for useful discussion on the analytical framework. A.B.-L. was supported by a Juan de la Cierva-Incorporación grant (IJCI-2017-31419) from the Spanish Ministry of Science, Innovation and Universities. L.S. and M.A.J.H. were supported by the ERC project (62002139 ERC—CoG SIZE 647224). We thank numerous biological collections, in particular the Natural History Museum, Tring, for providing access to specimens. Bird trait data collection was supported by Natural Environment Research Council grant nos. NE/I028068/1 and NE/P004512/1 (to J.A.T.).

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A.B.-L. conceived and coordinated the research, led the analyses and wrote the first draft; A.B.-L., L.S., J.G.-Z., M.A.J.H. and J.A.T. helped to develop the conceptual framework; L.S. compiled the environmental rasters; J.A.T., P.W. and B.M. provided morphometric data. All authors contributed to the data collection from the literature and to the writing of the final manuscript.

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Correspondence to Ana Benítez-López.

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Peer review information Nature Ecology & Evolution thanks Shai Meiri, Alfredo Sánchez-Tójar and Luis Valente for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 Conceptual models depicting the different hypotheses tested to explain insular size shifts in vertebrates.

Expected insular size shifts are depicted as a result of (a) Island rule effects; (b) island area; (c) spatial isolation (distance to mainland); (d) a combination of island area and distance to mainland; (e) primary productivity, (f) seasonality in resources; (g) mean temperature affecting mostly small species in cool islands; (h) mean temperature affecting mostly small species in warm islands; (i) mean temperature affecting all species; (j) seasonality in temperature; (k) precipitation; (l) species dietary preferences (carnivores vs non carnivores). Detailed information on the different hypotheses can be found in Supplementary Table 1.

Extended Data Fig. 2 Phylogenetic meta-regression models of island body size versus mainland body size.

Mean body size (ln-transformed mass, in g) on islands versus mainland is shown for (a) mammals, (b) birds, (c) reptiles and (d) amphibians. The dashed line has a slope of 1 and an intercept of 0. The solid lines represent the phylogenetic meta-regression slope estimate. The intercept a and slope b are presented in each plot along with CI. The island rule holds if the intercept is > 0 and the slope < 1.

Extended Data Fig. 3 Variation accounted for by random factors (Source, Species and Phylogeny) and residual variation.

The amount of variance accounted for by phylogeny was the largest for reptiles and mammals, and low for birds. The extent of variance explained by data sources was larger for mammals and reptiles, and low for amphibians and birds. The residual variance was highest for birds, followed by mammals, amphibians and reptiles, indicating that other factors besides mainland body size may help to explain insular size shifts (see Extended Data Fig. 58).

Extended Data Fig. 4 Phylogenetic random effects across taxonomic orders.

Boxplots of the variation in phylogenetic random effects across orders are shown for (a) mammals and (b) birds; and across families for (c) reptiles and (d) amphibians. Positive values indicate a tendency towards gigantism, whereas negative values indicate dwarfism.

Extended Data Fig. 5 Ecological factors explaining insular size shifts in mammals.

Only 1-2 variables are displayed per plot, while keeping the other predictors at median values. Continuous variables are represented at the 10% and 90% quantile for each extreme (close vs remote or small vs large, and low vs high). lnRR > 0 indicates gigantism, lnRR < 0 indicates dwarfism, and lnRR = 0 indicates no shift in body size in islands compared to mainland populations. Shaded areas represent 95% CI. QM indicates the explained heterogeneity (variance) by the interaction between each explanatory factor and body mass (for example mass:area in panel a), or the explanatory factor only in case of intercept-only models (for example temperature in this case). See Supplementary Table 7 for details.

Extended Data Fig. 6 Ecological factors explaining insular size shifts in birds.

Only 1-2 variables are displayed per plot, while keeping the other predictors at median values. Continuous variables are represented at the 10% and 90% quantile for each extreme (close vs remote or small vs large, and low vs high). lnRR > 0 indicates gigantism, lnRR < 0 indicates dwarfism, and lnRR = 0 indicates no shift in body size in islands compared to mainland populations. Shaded areas represent 95% CI. QM indicates the explained heterogeneity (variance) by the interaction between each explanatory factor and body mass (for example mass:area in panel a), or the explanatory factor only in case of intercept-only models (for example temperature in this case). See Supplementary Table 7 for details.

Extended Data Fig. 7 Ecological factors explaining insular size shifts in reptiles.

Only 1-2 variables are displayed per plot, while keeping the other predictors at median values. Continuous variables are represented at the 10% and 90% quantile for each extreme (close vs remote or small vs large, and low vs high). lnRR > 0 indicates gigantism, lnRR < 0 indicates dwarfism, and lnRR = 0 indicates no shift in body size in islands compared to mainland populations. Shaded areas represent 95% CI. QM indicates the explained heterogeneity (variance) by the interaction between each explanatory factor and body mass (for example mass:area in panel a), or the explanatory factor only in case of intercept-only models (for example temperature in this case). See Supplementary Table 7 for details.

Extended Data Fig. 8 Ecological factors explaining insular size shifts in amphibians.

Only 1-2 variables are displayed per plot, while keeping the other predictors at median values. Continuous variables are represented at the 10% and 90% quantile for each extreme (close vs remote or small vs large, and low vs high). lnRR > 0 indicates gigantism, lnRR < 0 indicates dwarfism, and lnRR = 0 indicates no shift in body size in islands compared to mainland populations. Shaded areas represent 95% CI. QM indicates the explained heterogeneity (variance) by the interaction between each explanatory factor and body mass (for example mass:area in panel a), or the explanatory factor only in case of intercept-only models (for example seasonality in resources – sdNDVI in this case). See Supplementary Table 7 for details.

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Supplementary Tables 1–8, Figs. 1 and 2, references and Appendices 1–3.

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Benítez-López, A., Santini, L., Gallego-Zamorano, J. et al. The island rule explains consistent patterns of body size evolution in terrestrial vertebrates. Nat Ecol Evol 5, 768–786 (2021). https://doi.org/10.1038/s41559-021-01426-y

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