The Island Syndrome in Lizards PAPER Maria Novosolov1*, Pasquale Raia2 and Shai Meiri1

Home , Cnemidophorus murinus, Island syndrome, Skyros wall lizard

Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2013) 22, 184–191

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RESEARCH The island syndrome in lizards PAPER Maria Novosolov1*, Pasquale Raia2 and Shai Meiri1

1Department of Zoology, Tel Aviv University, ABSTRACT Tel Aviv, Israel, 2Dipartimento di Scienzedella Aim Islands are thought to promote correlated ecological and life-history shifts in Terra, Università Federico II, Naples, Italy species, including increased population density, and an infrequent production of few, large, offspring. These patterns are collectively termed ‘the island syndrome’. We present here the first, phylogenetically informed, global test of the ‘island syndrome’ hypothesis, using lizards as our model organisms. Location World-wide. Methods We assembled a database containing 641 lizard species, their phylogenetic relationships, geographic ranges and the following life-history traits: female mass, clutch size, brood frequency, hatchling body mass and population density. We tested for life-history differences between insular and mainland forms in light of the island syndrome, controlling for mass and latitude, and for phylogenetic non- independence. We also examined the effects of population density and, in insular endemics, of island area, on lizard reproductive traits. Results We found that insular endemic lizards lay smaller clutches of larger hatchlings than closely related mainland lizards of similar size, as was expected by the island syndrome. In general, however, insular endemics lay more frequently than mainland ones. Species endemic to small islands lay as frequently as mainland species. Continental and insular lizards have similar productivity rates overall. Island area had little effect on lizard reproductive traits. No trait showed association with population density. Main conclusions Island endemic lizards mainly follow the island syndrome. We hypothesize that large offspring are favoured on islands because of increased intra- specific aggression and cannibalism by adults. Stable populations on islands lacking predators may likewise lead to increased intra-specific competition, and hence select for larger hatchlings that will quickly grow to adult size. This view is supported by the fact that lizard populations are denser on islands – although population density per se was uncorrelated with any of the traits we examined. *Correspondence: Shai Meiri, Department of Keywords Zoology, Tel Aviv University, 69978, Tel Aviv, Israel. Clutch size, island biogeography, island syndrome, life history, lizards, E-mail: [email protected] population density, reproduction, reversed island syndrome.

sometimes dwarf on islands (Van Valen, 1973; Lomolino, 2005). INTRODUCTION This pattern, known as the island rule, was considered universal. Animal populations conﬁned on islands frequently show several Recent data and analyses, however, have challenged this view substantial morphological and behavioural differences from (Meiri et al., 2008, 2012). Insular species likewise often evolve related mainland forms (Adler & Levins, 1994; Blondel, 2000; substantial differences from the mainland phenotype in their Raia et al., 2010). Small insular vertebrates often grow larger locomotor and feeding apparatuses (Grant, 1965; Sondaar, than their mainland counterparts do, whereas larger species 1977), behaviour and coloration, among others. For example, on

DOI: 10.1111/j.1466-8238.2012.00791.x 184 © 2012 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/geb Life history evolution in island lizards islands many birds (especially rails) became flightless (Roff, We hypothesize that insular lizards differ from continental 1994), dull-coloured (Omland, 1997) large-billed (Grant, 1999; species in their population densities and in their clutch size, Clegg & Owens, 2002) and relatively tame (Blondel, 2000). hatchling mass, brood frequency and productivity (progeny Insular rodents are often larger, less aggressive, and less fecund biomass produced per unit time). Specifically, we predict the than their mainland relatives are, and live in denser (and more following: stable) populations, a phenomenon termed ‘the island syn- 1. Because of lower predation and competition on islands, drome’ (Adler & Levins, 1994). The island syndrome thus pre- insular populations will be denser than mainland populations dicts changes in population dynamics, body size (Sondaar, 1977; (Case, 1975; Bennett & Gorman, 1979; Rodda & Dean-Bradley, Raia & Meiri, 2006), anti-predatory behaviour (Schoener et al., 2002; Buckley & Jetz, 2007). 2005) and life history (Raia et al., 2003, 2010). Aspects of this 2. Insular lizards shift towards K strategy in response to low syndrome have been erratically assigned to such different types predation, high population density and increased intra-specific of organisms as vertebrates, arthropods, molluscs and plants competition. Thus, we predict that insular lizards lay smaller (Whittaker & Fernandez-Palacios, 2007). MacArthur & Wilson clutches of larger hatchlings, and lay infrequently and thus their (1967, pp. 149–153) predicted that, in general, established overallproductivityrateislow. insular populations would shift towards K selection as the popu- 3. Island–mainland differences in life-history traits will be lation density of insular populations increases. Therefore, clutch strongest on small islands, while on large islands trait values will sizes would be lower on islands, especially in temperate regions. be similar to those observed on the mainland. Many models and data describe single aspects of life-history 4. Alternatively, a shift to K strategy on medium-sized islands, evolution on islands. Consistent, taxon-wide evidence for the predicted by the island syndrome, may be followed by a shift full range of phenomena predicted under the island syndrome, towards r strategy on very small islands, as predicted under the however, is currently limited to rodents (Adler & Levins, 1994) reversed island syndrome. and passerine birds (Blondel, 2000), and was never formally tested even in these groups. METHODS In reptiles, trait shifts consistent with the island syndrome are common. Many insular lizards are melanistic (Fulgione et al., We gathered data on mean female and hatchling body length, 2008; Runemark et al., 2010), have modified limb lengths and clutch size, brood frequency and productivity data for 641 head shapes (Herrel et al., 2008; Raia et al., 2010), altered body species of lizards. We collected data from the primary literature, sizes (Case, 1978; Meiri, 2007; Pafilis et al., 2011), small clutch field guides, our own observations and museum records. A com- sizes (Huang, 2007, cf. Case, 1975), and low growth rates plete list of the 1794 sources for the different trait values is (Andrews, 1976). Shifts to herbivorous diet (Van Damme, 1999; provided in Appendix S1 in Supporting Information. Of the Meiri, 2008) and either reduced or increased aggressiveness 641 species, 100 are insular endemics. Population density (Stamps & Buechner, 1985; Pafilis et al., 2009; Raia et al., 2010) estimates were available for 220 species (Appendix S1). We are also common on islands. Insular faunas often have few preda- determined whether lizard species were insular endemics or tors and competitors. This can lead to increased population mainland inhabitants using the reptile database (http://reptile- densities (‘density compensation’ and ‘density overcompensa- database.reptarium.cz), field guides and the primary literature. tion’).Such increased population density prompts the emergence Island endemic species are those inhabiting only islands, of the island syndrome according to Adler and Levins’ model whereas we treated all species that are found on the mainland as (Adler & Levins, 1994; see also Raia et al., 2010; Pafilis et al., mainland species regardless of whether they also occur on 2011). Increased population densities are thought to select for islands. We made sure, however, that the trait data we use for few, large-sized, offspring (MacArthur & Wilson, 1967; Andrews, these species originated from mainland populations. We 1979; Adler & Levins, 1994; Pafilis et al., 2011), which grow into recorded the area (in km2) of the largest island inhabited by large adults (Stamps & Buechner, 1985; Sinervo et al., 2000). Raia insular endemics for testing the correlation between island area et al. (2010) predicted that insular populations facing extreme and reproductive traits. Island areas were obtained from the UN environmental unpredictability would display an opposite array island directory (http://islands.unep.ch/Iindex.htm). Data that of trait shifts (a ‘reversed island syndrome’). They predicted that were unavailable in the directory were obtained from the such highly uncertain conditions,which may be common on very National Imagery and Mapping Agency (NIMA, 1997). small islands, will keep population density low and drive the We estimated female and hatchling masses from snout–vent production of frequent, large clutches of small hatchlings. lengths (SVLs) using family-specific equations for legged species, Theory predicts that evolutionary divergence should intensify and different equations for legless and leg-reduced lizards from as islands become more ‘insular’ – smaller and more isolated Meiri (2010) except for the following: for Liolaemus and Phyma- (Whittaker & Fernandez-Palacios, 2007). The larger and closer turus we used equations from Pincheira-Donoso et al.(2011); for to the mainland an island is the more it is assumed to resemble different gecko clades and for Anolis we used specific equations the mainland in important ecological attributes (e.g. in species using data gathered by S.M. (unpublished). Appendix S2 con- richness), and hence in the traits of organisms inhabiting it tains the allometric equations for converting SVLs to mass in (Heaney, 1978; Melton, 1982; Lomolino, 2005; cf. Meiri et al., these clades.For 22 species,we had no data for female SVL and we 2005). therefore used species-specific SVLs, or actual female mass (for

Phrynosoma blainvillii). For seven species, we had no data on as an additional covariate. We test two predictions with regard to hatchling SVL, and we used hatchling masses instead. We used island area: (1) a shift towards K strategy as islands grow smaller mean clutch/litter sizes and frequencies where possible. Where – as predicted by the island syndrome; (2) a shift towards K more than one mean was reported for a species we used the strategy on medium-sized islands; but a shift towards r strategy midpoint of the range of means. Where means were unavailable, on very small islands (the reversed island syndrome). We there- we used the midpoint of the reported trait range. fore also use the quadratic term of area in these models. Addi- Meiri et al. (2012) have recently shown that productivity is tionally, we used population density as a predictor for species for best quantified as a rate – biomass produced per unit time. We which we had these data. thus define productivity as the product of brood frequency, All four sets of analyses were duplicated to account for phy- clutch size and hatchling mass, in units of g per year. Mean logenetic non-independence by using phylogenetic generalized population densities (mean number of adult lizards per hectare) least square (PGLS) regression. PGLS fits the regression of a were recorded from the literature (Appendix S1). Where means given predictor variable on a given response variable via a GLS were unavailable, we used the mean of log-transformed procedure, by using a phylogenetically informed hypothesis for maximum and minimum population density values. the distribution of residuals around the response. The analysis is To correct for possible phylogenetic effects in the data, we based on the shared evolutionary history of different species assembled a composite species-level phylogeny from the litera- drawn from the phylogenetic tree. PGLS assumes that trait evo- ture, following the broad-scale squamate phylogenetic relation- lution proceeds according to a Brownian motion model (Freck- ship reported by Wiens et al. (2010). We used the taxonomy of leton et al., 2002). We adjusted the strength of phylogenetic the reptile database (http://reptile-database.reptarium.cz). In non-independence using the maximum likelihood value of the assembling the tree we gave priority to recently published phy- scaling parameter l (Freckleton et al., 2002) implemented in the logenies that are based on nuclear DNA, then on mitochondrial R package caper (Orme et al., in press). Pagel’s l is a multiplier DNA sequences. For species where no molecular phylogeny was of the off-diagonal elements of the variance–covariance matrix, available, we relied on phylogenies based on morphological which provides the best fit of the Brownian motion model to the data. Where phylogenetic data were unresolved, we sunk species tip data. into a polytomy within their genus. The phylogenetic relation- To further examine whether our results stem from compari- ships between the species and the sources of phylogenetic data sons of lizards belonging to very different clades, we compared for each are depicted in Appendix S3. hatchling size, clutch size, brood frequency and productivity in a We did not account for branch lengths. Instead, we scaled paired design across the 17 genera for which we have both island branches to make the tree ultrametric using the cladogram and mainland representatives. The results of these analyses transform in FigTree (Rambaut, 2010). Arbitrary branch lengths (Appendix S4) were similar to those of the phylogenetic analysis computed this way give a necessarily imprecise measure of the and are therefore not explored further. In all the analyses, we expected phenotypic covariation between species, yet they are selected models with a backwards elimination procedure based still much better than neglecting phylogenetic effect altogether. on P-values. To account for possible effects of climate we mapped the geographic ranges of the different species in ArcGIS using pub- RESULTS lished data on lizard distribution (Appendix S1). A full analysis of the climatic drivers of lizard life history is beyond the scope of All the results presented below are for models that include the current study. We thus used only a simplistic measure of female body mass as a covariate (mass was significantly corre- climate: the absolute value of latitudinal centroid for each lated with the response variable in all models). The effects of species. This variable was used to correct for, for example, the mass and latitude on the various response variables are pre- tendency of tropical species to produce more clutches than tem- sented in Appendix S5. perate species (Meiri et al., 2012). Island endemic lizards populations are, on average, nearly four times as dense as mainland ones (138.0 Ϯ 0.16 for islands and 36.3 Ϯ 0.08 lizards per hectare, for mainland, t = 3.11, Linear models and phylogenetic generalized P < 0.001). A difference remains after correcting for body mass least square (intercept: islands = 3.08 Ϯ 0.15; mainland = 2.22 Ϯ 0.11,

All the data except latitude were log10-transformed in all analy- t = 5.86, P < 0.001). Signiﬁcant, albeit smaller, differences ses. For each species we used the clutch size, number of yearly remain after phylogeny and mass are both accounted broods, hatchling mass and productivity (= clutch size ¥ for (l=0.62, intercept: islands = 2.61 Ϯ 0.16, mainland = number of yearly broods ¥ hatchling mass) as response variables 2.11 Ϯ 0.28, t = 3.20, P = 0.001). and regressed them against female mass (g) and latitude, using insularity as a main effect in ANCOVA. After analysing the entire Population density and island area dataset we repeated all analyses with only insular endemics inhabiting islands smaller than 1000 km2. To examine the rela- Population density shows no association with any of the tionship between island area and reproductive traits we ran response variables. Clutch size, brood frequency and hatchling similar analyses with all insular endemics, and used island area mass are likewise unassociated with island area. Productivity,

186 Global Ecology and Biogeography, 22, 184–191, © 2012 Blackwell Publishing Ltd Life history evolution in island lizards however, is negatively correlated with island area only in the when examining all insular endemic species (non-phylogenetic non-phylogenetic model (slope =-0.08 Ϯ 0.02, P = 0.001). The island intercept: 0.04 Ϯ 0.03; mainland: 0.22 Ϯ 0.03, slope = 0.27 results of all regressions of the various response variables on Ϯ 0.01, t =-6.72, P < 0.001; phylogenetic island intercept: 0.12 population density and island area are shown in Appendix S6. Ϯ 0.02; mainland: 0.24 Ϯ 0.08, slope = 0.23 Ϯ 0.02, t =-5.23, No quadratic terms of island area were signiﬁcant in any analysis P < 0.001, l=0.84). These results are in agreement with the (Appendix S7). predictions of the island syndrome.

Clutch size Brood frequency

Clutch sizes of lizards endemic to small (< 1000 km2) islands Brood frequency of small-island endemics is similar to that of are smaller than those of mainland species (female mass and mainland species (corrected for female mass and latitude) in latitude-corrected) (Fig. 1a), in both the non-phylogenetic both the non-phylogenetic (intercept islands: 0.64 Ϯ 0.06; (island intercept: 0.08 Ϯ 0.06; mainland: 0.21 Ϯ 0.04, slope = mainland: 0.58 Ϯ 0.03, slope =-0.14 Ϯ 0.02, t = 1.07, P = 0.29) 0.28 Ϯ 0.02, t =-2.21, P = 0.03) and phylogenetic models (island and phylogenetic models (island intercept: 0.41 Ϯ 0.05; main- intercept: 0.15 Ϯ 0.04; mainland: 0.23 Ϯ 0.08, slope = 0.25 Ϯ land: 0.45 Ϯ 0.08, slope: -0.07 Ϯ 0.02, t =-0.99, P = 0.32, 0.02, t =-2.29, P = 0.02, l=0.87). Similar results are obtained l=0.75) (Fig. 1b). However, across all insular endemic species

Clutch size on islands vs. mainland Brood frequency on islands vs. mainland

a)1.5 b) )

1.5 r a e /y

s 1.0 od ro b 1.0 ( 0.5 ency u req Log Clutch Size 0.5 F od 0.0 Bro og L 0.0 -0.5 01234 01234 Log Female Mass (g) Log Female Mass (g)

Hatchling mass on islands vs. mainland Productivity on islands vs. mainland

2.0 c) d) 1.5 ) g 1.0 ear) y (g/

0.5 y vit i uct

0.0 d

-0.5 Log Hatchling Mass ( Log Pro

-1.0

-1.5 -1 0 1 2 3 01234 01234 Log Female Mass (g) Log Female Mass (g)

Figure 1 Relationship of (a) (log-transformed) clutch size and (b) (log-transformed) brood frequency (broods per year) with (log-transformed) female mass (in g) on islands (white, solid line) and the mainland (black, dashed line). Relationship of (c) (log-transformed) hatchling mass (g) and (d) (log-transformed) productivity (g per year) (log transformed) with female body mass (g) on islands (white) and the mainland (black). For (c) and (d) the lines show the best ﬁt model regression. Only one regression line is shown where the difference between island and mainland was not signiﬁcant.

Global Ecology and Biogeography, 22, 184–191, © 2012 Blackwell Publishing Ltd 187 M. Novosolov et al. brood frequency is higher on islands than on the mainland The results of the phylogenetic and non-phylogenetic analy- (corrected for latitude and female mass; island intercept: 0.69 Ϯ ses are mostly congruent. However, the non-phylogenetic analy- 0.03; mainland: 0.62 Ϯ 0.03, slope =-0.15 Ϯ 0.01, t = 2.7, P = sis of all islands revealed higher brood frequencies, similar-sized 0.007). Phylogenetic models show no significant correlation hatchlings and low productivity on islands. In both the non- between insularity and brood frequency (island intercept: 0.44 phylogenetic analyses and in the phylogenetic analysis of small Ϯ 0.02; mainland: 0.45 Ϯ 0.08, slope =-0.07 Ϯ 0.02, t =-0.24, islands we found similar brood frequency and productivity on P = 0.8, l=0.84). islands and on the mainland – and larger hatchlings on islands. Higher brood frequency on islands was found only in the non- phylogenetic analysis that included large islands but not in the Hatchling mass phylogenetic analyses, and in analyses of only small islands. We Small-island endemic species have larger hatchlings than those therefore suggest that lizards belonging to lineages that lay fre- of mainland species of comparable size (non-phylogenetic quently (e.g. anoles and geckos), while having similar laying model; island intercept: -0.87 Ϯ 0.05; mainland: -0.98 Ϯ 0.03, rates on islands and continents, are relatively more common on slope = 0.69 Ϯ 0.01, t = 2.04, P = 0.04; phylogenetic model; islands than on the mainland. We suspect that members of these island intercept: -0.73 Ϯ 0.05; mainland: -0.86 Ϯ 0.07, slope = lineages are good colonizers of islands (i.e. have good dispersal 0.65 Ϯ 0.02, t = 2.91, P = 0.004, l=0.7) (Fig. 1c). Across all ability and/or low extinction probability on islands). A non- insular endemics we obtain similar results in a phylogenetic mutually exclusive alternative is that lizards belonging to such model (island intercept: -0.78 Ϯ 0.03; mainland: -0.86 Ϯ 0.07, lineages frequently radiate on large islands. The first hypothesis slope = 0.64 Ϯ 0.02, t = 3.05, P = 0.002, l=0.72), but not in the is supported by data on the geographic distribution of insular non-phylogenetic model (island intercept: -0.96 Ϯ 0.03; main- lizards (M.N., unpublished), and the second is supported by land: -0.99 Ϯ 0.03, slope = 0.71 Ϯ 0.01, t = 1.25, P = 0.21). There findings of lizard radiations on large islands (Losos & Schluter, is an interaction between insularity and female mass in the 2000). non-phylogenetic model (insular slope 0.11 Ϯ 0.05 higher than Overall, we detected no differences in productivity rates mainland slope, P = 0.04). These results are, in general, consist- between islands and continental areas. To us this suggests that ent with the island syndrome. insularity is neither a panacea of unlimited opportunity in the absence of predators and competitors on the one hand, nor is it the epitome of harsh environments, subjected to chronic food Productivity shortages that is often advanced as the cause of insular dwarfing (e.g. Köhler & Moyà-Solà, 2010, cf. Meiri & Raia, 2010). There are no significant differences in productivity rates It appears that insular lizards invest in fewer, larger offspring, between insular and continental species. Mass-corrected inter- as predicted by the island syndrome. At least on large islands cepts of small-island endemics and continental species are not lizards brood more frequently than on the mainland. Overall significantly different (non-phylogenetic model, islands: -0.21 there is no association between productivity rates and insularity. Ϯ Ϯ Ϯ 0.07; mainland: -0.25 0.02, slope = 0.85 0.02, t = 0.53, The rodent model of Adler & Levins (1994) predicts smaller Ϯ P = 0.6; phylogenetic model, islands: -0.21 0.07; mainland: broods of large offspring and high population density on Ϯ Ϯ -0.20 0.09, slope = 0.82 0.03, t =-0.06, P = 0.95, l=0.56, islands. This model applies to lizards as well. In fact, ours are the results corrected for latitude) (Fig. 1d). Similar results are first quantitative comparative and phylogenetic analyses to obtained with a phylogenetic model across all insular endemic present the island syndrome in any clade. Ϯ species (mass- and latitude-corrected; islands intercept: -0.23 Raia et al. (2010) experimentally studied a population of the Ϯ Ϯ 0.04; mainland: -0.18 0.09, slope = 0.80 0.02, t =-1.44, Italian wall lizard, Podarcis sicula, from the tiny islet of Licosa, off P = 0.15, l=0.59). Only the non-phylogenetic model across all the western coast of southern Italy. They pointed out that under species show a significant difference: productivity rates are lower the very unpredictable environmental conditions of Licosa, the on islands (corrected for female mass and latitude; islands inter- uncertain mortality schedule favours a great investment in the Ϯ Ϯ Ϯ cept: -0.21 0.04; mainland: -0.15 0.04, slope = 0.83 0.02, reproduction of numerous, small offspring. Such perturbations t =-2.14, P = 0.03). also make population density highly variable, and usually low. Raia et al. (2010) also showed that the Licosa P. sicula is very aggressive toward conspecifics. We found a single result DISCUSSION supporting the reversed island syndrome (Raia et al., 2010): a As expected under the island syndrome (Adler & Levins, 1994; negative relationship between island area and productivity. We Blondel, 2000), insular lizards lay smaller clutches of larger suspect that if such a pattern generalizes it is more likely to hatchlings than do mainland lizards of comparable size. Brood- manifest itself at intra-specific levels, on smaller islands than ing rates and productivity rates of mainland and insular lizards most of the ones we examined here. Island biogeography theory are similar. Thus in general we see a shift towards K selection in usually predicts more pronounced evolutionary shifts on small island taxa, in accordance with island biogeography theory islands, because their faunas are more different from those of the (MacArthur & Wilson, 1967) and the island syndrome (Adler & mainland and larger islands (e.g. Thomas et al., 2009). Perhaps Levins, 1994). the lack of relationship between island area and reproductive

188 Global Ecology and Biogeography, 22, 184–191, © 2012 Blackwell Publishing Ltd Life history evolution in island lizards traits implies that both the island syndrome and its reverse occur reported). Alternatively, increased population density need not on (different) small islands and together they therefore cancel always result in increased intra-specific competition. It is possi- each other out. ble, for example, that population density is controlled by the Surprisingly, although we found some relationship between amount of available food, and thus if dense areas also hold more insularity and reproductive traits (e.g. smaller clutches) neither resources the intensity of competition need not increase. This population density nor island area (or its quadratic) were cor- may partially depend on the frequent shift to herbivory which related with them. Because predator and competitor richness many insular lizards show (Van Damme, 1999; Meiri, 2008), and increase with island area, population density is predicted to certainly was the case, for instance, with the hugely dense popu- decrease with island area (Case, 1975; Rodda & Dean-Bradley, lation of Bonaire whiptail Cnemidophorus murinus (Dearing, 2002; Lomolino et al., 2010). However, across the 56 insular 1993). Although we think this hypothesis merits some quanti- endemic species from which we have both population density tative treatment, it is beyond the scope of this work. and area data, density and area are uncorrelated (correcting for Overall, lizards follow most of the predictions of the island mass, slope =-0.15 Ϯ 0.08, t =-1.71, P = 0.09; uncorrected slope syndrome: they lay fewer eggs, and occur at greater population =-0.06 Ϯ 0.12, t =-0.57, P = 0.57). This is surprising given that densities on islands than on the mainland. They also produce the islands with endemic lizards in our sample range in area larger offspring than closely related mainland forms. We found from 0.13 km2 (Columbretes Islands, Podarcis liolepis)tothec. no relationship between population density and life history, and 786,000 km2 island of New Guinea. On small islands, such as the island area is likewise unrelated to either population density or Columbretes, lizards are sometimes the only terrestrial verte- to the life-history traits we examined. Productivity rates are brates, yet the larger islands are inhabited by a panoply of similar across islands and the mainland suggesting a common lizards, snakes, birds and mammals (as well as much greater constraint on the amount of energy available for reproduction. diversity of arthropods) similar to the conditions on continental Predator-induced mortality is probably lower on many islands areas. (Adler & Levins, 1994). This is likely to result in increased intra- Population density was uncorrelated with any of the traits we specific competition, selecting for larger hatchlings. Intra- have examined. This is intriguing, as population density is often specific predation on juveniles may also impose a selection advocated as a major determinant of the intensity of intra- pressure for large hatchling size (Pafilis et al., 2009). Together specific competition, and thus the evolution of life history with the often high abundance of food on some islands these towards larger offspring that are assumed to be better competi- factors may explain most of the variation in population density tors. The large size of insular offspring, in turn, is hypothesized and life-history characteristics that is unaccounted for by body to result in longer embryonic development, and thus in smaller size and latitude. The increase in hatchling size will result in and less frequent clutches (Melton, 1982; Adler & Levins, 1994). smaller broods, thus explaining the island syndrome. Population density data are extremely noisy. For many of the species in our database for which we have more than one popu- ACKNOWLEDGEMENTS lation density estimate the variation spans at least one, and sometime even two or three orders of magnitude. Within We thank Lital Dabool for valuable discussion. Erez Maza has species, densities may often vary between habitats, between been instrumental in obtaining data on lizard distributions. We years, across climatic gradients etc. (e.g. Schoener & Schoener, thank Panayiotis Pafilis and two anonymous referees for con- 1980). To a large extent variation in reported values of popula- structive comments on an earlier version of this work. Shai tion density is greatly influenced by the spatial extent of the area Meiri is supported by an Alon Fellowship. over which population density was quantified (Blackburn & Gaston, 1996). Because population density estimates are always REFERENCES for areas in which lizards are found (i.e. areas with zero population density are excluded) smaller areas usually only encom- Adler, G.H. & Levins, R. (1994) The island syndrome in rodent pass the best habitat for a lizard, but larger areas do often populations. Quarterly Review of Biology, 69, 473–490. contain habitats where no individuals dwell. In our data the area Andrews, R.M. (1976) Growth rate in island and mainland over which population density was measured was strongly and anoline lizards. Copeia, 1976, 477–482. negatively correlated with population density – in fact, this Andrews, R.M. 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Roff, D.A. (1994) The evolution of flightlessness: is history SUPPORTING INFORMATION important? Evolutionary Ecology, 8, 639–657. Runemark, A., Hansson, B., Pafilis, P., Valakos, E.D. & Svensson, Additional Supporting Information may be found in the online E.I. (2010) Island biology and morphological divergence of version of this article: the Skyros wall lizard Podarcis gaigeae: a combined role for Appendix S1 The dataset and metadata (literature source). local selection and genetic drift on color morph frequency Appendix S2 Equations used to estimate mass from snout–vent divergence? BMC Evolutionary Biology, 10, 269. doi: 10.1186/ lengths in clades not reported in Meiri (2010) and the data used 1471-2148-10-269. to generate them. Schoener, T.W. & Schoener, A. (1980) Densities, sex ratios, and Appendix S3 Phylogenetic relationships between the lizard population structure in four species of Bahamian Anolis species in our dataset and the literature sources used to recon- lizards. Journal of Animal Ecology, 49, 19–53. struct them. Schoener, T.W., Losos, J.B. & Spiller, D.A. (2005) Island bioge- Appendix S4 Results of comparisons between life-history traits ography of populations: an introduced species transforms of congeneric insular and mainland species. survival patterns. Science, 310, 1807–1809. Appendix S5 The relationship between female mass and latitude Sinervo, B., Svensson, E. & Comendant, T. (2000) Density cycles in the best models for different life-history traits. and an offspring quantity and quality game driven by natural Appendix S6 Results of regressions of the four response vari- selection. Nature, 406, 985–988. ables on population density and island area. Sondaar, P.Y. (1977) Insularity and its effects on mammal evo- Appendix S7 Results of the quadratic regressions. lution. Major patterns of vertebrate evolution (ed. by M.K. Hecht, P.C. Goody and B.M. Hecht), pp. 671–707. Plenum As a service to our authors and readers, this journal provides Press, New York. supporting information supplied by the authors. Such materials Stamps, J.A. & Buechner, M. (1985) The territorial defense are peer-reviewed and may be re-organized for online delivery, hypothesis and the ecology of insular vertebrates. Quarterly but are not copy-edited or typeset. Technical support issues Review of Biology, 60, 155–181. arising from supporting information (other than missing files) Thomas, G.H., Meiri, S. & Phillimore, A.B. (2009) Body size should be addressed to the authors. diversification in Anolis: novel environment and island effects. Evolution, 63, 2017–2030. BIOSKETCHES Van Damme, R. (1999) Evolution of herbivory in lacertid lizards: effects of insularity and body size. Journal of Herpetol- Maria Novosolov is an MSc student studying the ogy, 33, 663–674. evolution of life-history traits in island endemic reptiles. Van Valen, L.M. (1973) A new evolutionary law. Evolutionary Pasquale Raia studies palaeobiology of insular Theory, 1, 1–30. vertebrates, evolutionary responses to insularity, and the Whittaker, R.J. & Fernandez-Palacios, J.M. (2007) Island bioge- evolutionary biology of Cenozoic mammals. ography. Ecology, evolution, and conservation, 2nd edn. Oxford University Press, Oxford. Shai Meiri studies the biogeography of animal traits in Wiens, J.J., Kuczynski, C.A., Townsend, T., Reeder, T.W., different vertebrate clades, evolutionary responses to Mulcahy, D.G. & Sites, J.W. (2010) Combining phylogenomics insularity, and the patterns, drivers and consequences of and fossils in higher-level squamate reptile phylogeny: the global distribution of reptiles molecular data change the placement of fossil taxa. Systematic Biology, 59, 674–688. Editor: Miguel Olalla-Tárraga