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. Author manuscript; available in PMC: 2024 Mar 29.
Published in final edited form as: Glob Ecol Biogeogr. 2021 Sep 28;30(12):2431–2441. doi: 10.1111/geb.13396

Diet influences latitudinal gradients in life-history traits, but not reproductive output, in ectotherms

Udita Bansal 1,✉, Maria Thaker 1
PMCID: PMC7615780  EMSID: EMS194939  PMID: 38560415

Abstract

Aim

Latitudinal gradients in life-history traits are apparent in many taxa and are expected to be strong for ectotherms that have temperature-driven constraints on performance and fitness. The strength of these gradients, however, should also be affected by diet. Because diet type (carnivory, omnivory, herbivory) influences accessibility to nutrition and assimilation efficiency, we aim to study how diet affects latitudinal gradients in lifetime reproductive output and the underlying life-history traits in ectotherms.

Location

Global.

Time period

Recent.

Major taxa studied

Lizards (Reptilia, Squamata, Sauria).

Methods

We used empirical (352 species) and phylogenetically imputed data (563 species) to analyse the interactive effects of latitude and diet on life-history traits (longevity, age at maturity, reproductive life span, hatchling mass, clutch/brood size, clutch/brood frequency, female mass) and lifetime reproductive output of lizards.

Results

Lifetime reproductive output does not significantly differ in lizards across diet types, and only carnivores exhibit a small increase at higher latitudes. Diet type, however, influences latitudinal patterns of individual life-history traits. Carnivores exhibit a shift towards ‘slower-paced’ life histories at higher latitudes for most traits (increased longevity, age at maturity, reproductive life span, and decreased clutch frequency). By contrast, herbivores either display ‘faster-paced’ life histories (reduction in reproductive life span, hatchling mass, female mass) or no change (clutch frequency, clutch size, age at maturity) at higher latitudes. Omnivores exhibit intermediate and muted latitudinal patterns.

Main conclusions

We suggest that the nutritional challenges of herbivory, compounded by thermal constraints at higher latitudes, may explain differences in life-history characteristics of herbivorous ectotherms. Intermediate patterns exhibited by omnivores highlight how flexibility in diet can buffer environmental challenges at higher latitudes. Our results indicate that lizards with different diet types display various trends in their life histories across latitudes, which eventually balance out to result in similar reproductive outputs throughout their lifetime, with little benefits to carnivory.

Keywords: carnivore, herbivore, latitude, lifetime reproductive output, lizards, omnivore

1. Introduction

Latitudinal gradients of many abiotic and biotic components of the environment have been well characterized for centuries. Unlike conditions along Earth’s longitudes, which are relatively uniform, environmental conditions along latitudes vary dramatically (Stevens, 1989). Climatic variables, especially temperature and seasonality, follow regular patterns along the latitudes (Chown & Gaston, 2000; Stevens, 1989), and these patterns directly influence multiple biotic components, such as species richness and abundance of plants and animals (Behrens & Lafferty, 2007; Hillebrand, 2004; Lim et al., 2015; Rosenzweig, 1995; Zimmerman & Tracy, 1989). Latitudinal gradients are also apparent in functional traits, such as metabolic rate (Tieleman et al., 2006), body size (Bergmann, 1847), and longevity of animals (Scharf et al., 2015; Wikelski et al., 2003); and gradients in such traits result in consistent patterns of life-history strategies across latitude (Cabezas-Cartes et al., 2018; Scharf et al., 2015; Tinkle, 1969; Wikelski et al., 2003).

Interestingly, however, latitudinal patterns of life-history strategies are often different in ectothermic vertebrates compared to endotherms. Unlike in birds, reptiles at higher latitudes mature at an older age and have higher longevity (Cabezas-Cartes et al., 2018; Scharf et al., 2015; Tinkle, 1969); these life-history characteristics are often correlated with higher hatchling mass, but lower annual brood frequency and clutch size (Scharf et al., 2015). Because environmental temperature strongly correlates with performance (Huey, 1982), productivity (Meiri et al., 2012) and life-history traits (Meiri et al., 2013) of reptiles, latitudinal gradients in temperature (De Frenne et al., 2013) and seasonality (Meiri et al., 2020) are expected to influence the expression of life-history traits across latitudes (Meiri et al., 2020; Stark et al., 2018). Direction and strength of these latitudinal trends in ectotherms, however, should also be influenced by diet, an integral animal trait often not accounted for.

Lizards are a geographically widespread group of ectothermic vertebrates, which include species that vary in diet type (herbivory, omnivory, carnivory). In lizards, diet and temperature affect various digestive processes. Compared to protein rich animal-based diets of carnivores, plant material is less nutritious and more difficult to digest (McConnachie & Alexander, 2004; Pietczak & Vieira, 2017; Pough, 1973; Zimmerman & Tracy, 1989). And thus, herbivorous lizards typically have longer gut passage times and lower assimilation efficiency compared to carnivorous lizards (McConnachie & Alexander, 2004; Pough, 1973; Zimmerman & Tracy, 1989). Total energetic requirements are also, in general higher for an ectothermic herbivore compared to an ectothermic carnivore because of their larger body mass (Burness et al., 2001; Clauss et al., 2013; cf. Espinoza et al., 2004; Pough, 1973). As a consequence, herbivores need to feed more frequently than carnivores to obtain their energetic requirements (Arrington et al., 2002; Behrens & Lafferty, 2007; Meiri et al., 2012; Szarski, 1962). Body temperature is also known to affect several digestive processes, influencing gut passage time, apparent digestive efficiencies, digestion rate, and food consumption, as well as foraging behaviour in all lizards (Adolph & Porter, 1993; Pafilis et al., 2007; Van Damme et al., 1991). Cold temperatures particularly affect these processes in herbivorous lizards (Harlow et al., 1976; Zimmerman & Tracy, 1989), resulting in herbivores needing to maintain higher body temperatures or remain active longer (Tracy et al., 2005; Vitt et al., 2005) to allow for faster fermentation of plant materials (Espinoza et al., 2004; Zimmerman & Tracy, 1989) and reduce gut passage time (van Marken Lichtenbelt, 1992). This requirement to maintain higher body temperatures can be particularly challenging at higher latitudes. Lower environmental temperatures and higher seasonality at higher latitudes limit thermally-suitable activity periods and feeding opportunities for ectothermic vertebrates (Christian & Weavers, 1994; Meiri et al., 2020; Vidan et al., 2017), as well as increase gut passage times for all lizards (Du et al., 2000; Harlow et al., 1976; Waldschmidt et al., 1986). Environmental productivity also peaks seasonally at high latitudes (Huston & Wolverton, 2011), further constraining the time available for feeding over the year. Therefore, unlike carnivorous lizards, who can obtain and assimilate protein-rich food sources, herbivorous lizards at higher latitudes are expected to be challenged with obtaining sufficient feeding time to compensate for the lower nutritional content of their protein-poor food, lower digestive efficiency, lower assimilation rate and longer gut passage times. This challenge for herbivorous ectotherms to fully compensate nutritionally at higher latitudes is likely to have consequences for life-history processes, performance, and reproductive output (Behrens & Lafferty, 2007).

Here, we examine the influence of diet type (herbivory, omnivory, carnivory) on the latitudinal pattern of lifetime reproductive output. Measures of reproductive investment vary across studies and include different temporal scales of an animal’s life (reviewed in Pincheira-Donoso & Hunt, 2017). We posit that the total bio-mass produced by an average individual of a particular species over its entire life accounts for trade-offs between current and future reproductive investments across its life span (Williams, 1966). And thus, we define lifetime reproductive output as the product of clutch size, hatchling mass, clutch frequency and reproductive life span divided against female mass. ‘Lifetime reproductive output’ provides a better metric of total energetic allocation to a key fitness component than annual measures of reproductive output or fecundity (Charnov et al., 2007). Dividing by female mass makes this measure of lifetime biomass output a dimensionless value that is comparable across species (similar to lifetime reproductive effort by Charnov et al. (2007)). Given that lifetime reproductive output is a ratio of lifetime biomass produced per unit female mass and a product of multiple, possibly independent, life-history traits, we also examine how diet type influences latitudinal patterns of these traits separately.

Latitudinal gradients in life-history traits have been characterized in lizards previously, with consistent patterns of higher longevity and age at maturity at higher latitudes (Cabezas-Cartes et al., 2018; Scharf et al., 2015; Tinkle, 1969). Thus, changes in re-productive life span (the period between age of sexual maturity and death) with latitude depend on the degree of change in longevity and age at maturity. Latitudinal gradients in clutch size seem less consistent across studies (Meiri et al., 2020; Scharf et al., 2015), but since lower clutch frequency and smaller clutch sizes are often correlated with higher longevity (Scharf et al., 2015), we expect these clutch-based trait components to decrease with latitude. Unlike clutch size and frequency, hatchling mass is positively correlated with longevity in lizards (Scharf et al., 2015), and hence we expect an increase in hatchling mass at higher latitudes. Similarly, adult body mass of lizards is also correlated positively with longevity as part of the shift towards ‘slower’ life histories (Scharf et al., 2015) leading to an expectation of increase in female body mass at higher latitudes. We predict that the net outcome of these opposing patterns on lifetime reproductive output will be influenced by diet. The additional constraints imposed by herbivory, especially at higher latitudes, are expected to result in different latitudinal gradients for herbivores, compared to omnivores and carnivores. We aim to determine whether and in what ways the nutritional constraints of herbivory affect latitudinal gradients in survival-related and reproduction-related life-history traits. Overall, our analysis provides a more mechanistic view of latitudinal gradients in lifetime reproductive output in ectotherms, by explicitly considering the influence of diet and the relative importance of trade-offs among the underlying life-history traits.

2. Methods

2.1. Data

Data for lizard traits and latitudinal centroids were first obtained from papers deposited in the Global Assessment of Reptile Distributions (GARD), 2020 (http://www.gardinitiative.org/data.html) or the Dryad repository (see Supporting Information S1 for a list of data sources). These traits included maximum longevity (years) and average values for the following: age at maturity (age at first reproduction in months), hatchling mass (grams), clutch/brood size (number of eggs/young per clutch), clutch frequency (clutches/broods per year), female body mass (grams). We also included diet type, insularity (island endemic/mainland species) and latitudinal centroids for species’ geographical ranges (degree decimals). Data for female mass were calculated from mean snout–vent length (SVL) of lizards using allometric equations derived for specific clades (from Feldman et al., 2016; Meiri, 2010). For all life-history traits, we used data from the most updated reference, or if unavailable, used the next most recent dataset (see Supporting Information S1 for full data description). For longevity, we additionally replaced values from un-verified websites with values from museums or published resources, and corrected some month-to-year conversion errors from the original datasets. Our final dataset of included species follows the taxonomic nomenclature from the May 2021 Reptile Database (Uetz et al., 2021). While collating different datasets, information from two or more synonymized species were merged when identical, or averaged when values for the same trait differed.

Diet types for all species were classified into one of three categories. Species with less than 10% plant material in their diets as adults were classified as carnivores, those with 10%–50% were classified as omnivores and those with greater than 50% were classified as herbivores (Cooper & Vitt, 2002; Meiri, 2018; Meiri et al., 2012, 2013; Scharf et al., 2015; Stark et al., 2018). Only one species, Sitana ponticeriana, was recorded as having different diet categories before species synonymization, and we categorized it as a carnivore based on the categories of its close relatives in the same genera. All species in the dataset belong to the global region lying within 60° N and 60° S latitudes (Figure 1).

Figure 1.

Figure 1

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Geographical distribution of study species. Latitudinal centroids from the geographical distribution of carnivorous (n = 240, orange circles), omnivorous (n = 82, purple squares) and herbivorous (n = 30, green triangles) lizard species in this study. Sphere-Mollweide projection

The complete dataset with values for all life-history traits of interest included 352 lizard species, although data for individual traits included more species. To phylogenetically interpolate life-history trait data to additional species, we first pruned the phylogenetic tree from Tonini et al. (2016) to include only lizards, and used the command phyEstimate (R package ‘Picante’; Kembel et al., 2010) to impute trait values where missing, based on species with known values. We imputed trait values for longevity, age at maturity, hatchling mass, clutch size, clutch frequency and female mass. Since the accuracy of imputation is based on the phylogenetic signal in the trait and the sample size for which the values are already known (Goberna & Verdú, 2016), the predicted values were filtered to retain only conservative estimates. Thus, we only retained life-history trait data for species in which the standard errors were less than the estimated trait value. We also removed any species with interpolated values for more than three life-history traits. Merging these datasets for all life-history traits with imputed and original values resulted in a dataset of 563 lizard species of which 389 were classified as carnivores, 122 as omnivores and 52 as herbivores (see Table S2.1 in Supporting Information S2 for a family level categorization). For this larger dataset, values of diet, latitudinal centroids and insularity were obtained from references cited in Supporting Information S1. Despite the seemingly low sample size given the number of lizard species globally, our resulting dataset accurately captures the proportion of diet types currently known (c. 15% omnivores, >80% carnivores, c. 5% herbivores; Meiri, 2018).

The life-history data collected were used to calculate lifetime reproductive output, as [(average clutch/brood size) × (average clutches/broods per year) × (average hatchling mass) × (reproductive life span)]/(female mass). Reproductive life span, which is the duration for which a species is reproductively active (years), was calculated by subtracting the age at maturity (converted to years) from longevity of each species, assuming that all species can reproduce until death once they reach maturity (Hoekstra et al., 2020). Mass-specific annual productivity, calculated as (hatchling mass × clutch size × number of clutches per year)/(female mass) has been used by other studies to understand patterns in lizard reproductive output (Meiri et al., 2012). We add the reproductive life span term to account for the reproductive output across their entire life spans. Our calculation can be considered similar to ‘lifetime reproductive effort’ with slight differences in the calculation of individual variables (Charnov et al., 2007).

2.2. Analyses

To test the hypothesis that diet type influences latitudinal trends in lifetime reproductive output, and the expression of individual life-history traits in lizards, we built separate linear models with lifetime reproductive output, clutch/brood size, clutch/brood frequency, longevity, age at maturity, reproductive life span, hatchling mass and female mass as response variables. Lifetime reproductive output and life-history traits were natural log-transformed to conform with the assumptions of normality and homogeneity of variances of simple linear and mixed models. For ease of interpretation, we report and interpret the relative magnitude of effects in the logged form, as opposed to the inverse transformed form (Changyong et al., 2014). For all models, diet and latitude were predictors along with an interaction between diet and latitude. Since insular species are known to include more plant matter in their diets (Van Damme, 1999), we initially included an interaction term between diet and insularity in the model with lifetime reproductive output as the response variable. This interaction term was not significant (Supporting Information Table S2.2), and after step-wise deletion, we found no significant effect of insularity on lifetime reproductive output in our dataset (t = −1.534, p = .126, Supporting Information Table S2.3). Henceforth, we only retained the main predictors of interest, diet and latitude, in sub-sequent analyses (also see Supplementary Methods in Supporting Information S2). To quantify the magnitude of the diet effect on latitudinal trends of individual traits, we proceeded to construct separate models per trait for each diet type with latitude as the only fixed predictor.

We used both ordinary least squares regressions as a linear mixed model (LMM) and phylogenetic generalized least squares (PGLS) regressions to model these relationships since many traits are phylogenetically conserved (Clobert et al., 1998; Dunham & Miles, 1985), and phylogeny is known to affect correlations between latitude and life-history traits (Cardillo, 2002). In the LMM, we added the taxonomic rank of family as a random effect on the intercept to account for the nested structure of the data (R package ‘lmerTest’— Kuznetsova et al., 2017). For the PGLS, we directly accounted for phylogenetic relatedness using a pruned phylogenetic tree of lizards (Tonini et al., 2016) that included only the species in our dataset (R packages ‘geiger’—Harmon et al., 2008; ‘ape’—Paradis & Schliep, 2019). We ran the PGLS, assuming a Brownian motion (BM) model for trait evolution with the scaling parameter value λ (Felsenstein, 1985; Pagel, 1999; R package ‘phylolm’— Tung Ho & Ané, 2014). All statistical analyses were performed in R 3.5.2 (R Core Team, 2018). The LMM and PGLS models showed qualitatively similar results for all traits, and hence we report results from PGLS in the main text and LMM in Supporting Information S2 (Tables S2.4–S2.21) and S3 (Figure S3.1).

We ran one set of analyses with the original dataset of only species with empirically measured trait values (n = 352). We then repeated the analyses using the expanded dataset with phylogeneti-cally interpolated trait values (n = 563). Results from the interpolated dataset are qualitatively similar to the results from the empirically-derived dataset and are reported in Supporting Information S2 (Tables S2.4–S2.21) and S3 (Figures S3.2–S3.4).

3. Results

Here we report results from the PGLS regression analyses from the empirically measured data (full model outputs in Supporting Information S2).

At the equator, we find that lifetime reproductive output of herbivorous (t = 1.749, p = .081) and omnivorous (t = 1.528, p = .127) lizards is not significantly different from that of carnivorous lizards (Table 1, Figure 2). As latitude increases, however, lifetime reproductive output of carnivores increases (t = 2.068, p = .040), while that of herbivores (t = −1.454, p = .157) and omnivores (t = −0.718, p = .475) remain at similar levels (Table 1, Figure 2).

Table 1.

Parameter estimates from the phylogenetic generalized least squares (PGLS) regression, showing the effect of latitude on lifetime reproductive output and life-history traits of lizards with different diet types. All response variables were natural log-transformed. Values reported were obtained from separate models for each diet category and trait. Significant values (at p < .05) are denoted in bold (n = 352 species)

Lifetime reproductive output Clutch/brood size Clutch/brood frequency Longevity Age at maturity Reproductive life span Hatchling mass Female mass
Intercept (at the equator)
Carnivores 0.535 1.270 1.033 1.582 2.239 1.265 −0.063 2.954
Herbivores 1.703 1.717 0.008 3.496 3.897 3.356 3.454 6.881
Omnivores 1.435 1.679 1.212 1.994 2.279 1.858 −0.023 3.478
Slope (along latitude)
Carnivores 0.014 0.001 −0.018 0.017 0.022 0.019 −0.012 −0.024
Herbivores −0.020 0.002 0.002 −0.019 −0.005 −0.022 −0.055 −0.053
Omnivores −0.007 −0.006 −0.023 0.014 0.023 0.011 −0.001 −0.016
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Note: Lifetime reproductive output = (reproductive life span × clutch size × annual brood frequency × hatchling mass)/(female mass). Reproductive life span = longevity – age at maturity.

Figure 2.

Figure 2

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Latitudinal trends in lifetime reproductive output of lizards. Latitudinal trends in lifetime reproductive output for lizard species that are carnivorous (n = 240, orange circles), omnivorous (n = 82, purple squares) and herbivorous (n = 30, green triangles). The trend lines are derived from phylogenetic generalized least squares regressions accounting for phylogeny

Diet also affected the equatorial and latitudinal trends in most life-history traits except clutch size (Table 1, Figure 3, Supporting Information S2). At the equator, herbivorous lizards have highest longevity (t = 4.671, p < .001; Table 1, Figure 3b), highest age at maturity (t = 3.864, p < .001; Table 1, Figure 3d), longest reproductive life spans (t = 4.527, p < .001; Table 1, Figure 3f), highest hatchling mass (t = 6.928, p < .001; Table 1, Figure 3e), and highest female mass (t = 5.113, p < .001; Table 1, Figure 3g), followed by omnivorous lizards and then carnivorous lizards (Table 1, Figure 3). But higher number of clutches/broods per year are laid by carnivorous (t = 3.517, p < .001; Table 1, Figure 3a) and omnivorous (t = 1.027, p = .305; Table 1, Figure 3a) lizards at the equator.

Figure 3.

Figure 3

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Latitudinal trends in life-history traits of lizards (a–g). Latitudinal trends for carnivorous (orange circles, n = 240), omnivorous (purple squares, n = 82) and herbivorous (green triangles, n = 30) lizards are derived from phylogenetic generalized least squares regressions accounting for phylogeny. Life-history traits for the different diet types include (a) annual clutch/brood frequency (ln), (b) maximum longevity (years, ln), (c) average clutch/brood size (ln), (d) age at maturity/age at first reproduction (months, ln), (e) average hatchling mass (g, ln), and (f) maximum reproductive life span (years, ln), (g) average female mass (g, ln)

For some of these life-history traits, latitudinal changes depended on diet type (Table 1, Figure 3). As latitude increases, carnivorous lizards have higher longevity (t = 3.606, p < .001; Table 1, Figure 3b), gain maturity at an older age (t = 5.379, p < .001; Table 1, Figure 3d) and have longer reproductive life spans (t = 3.238, p = .001; Table 1, Figure 3f). However, the annual clutch/brood frequency for carnivores decreases significantly at higher latitudes (t = −4.892, p < .001; Table 1, Figure 3a) along with hatchling mass (t = −2.029, p = .044; Table 1, Figure 3e) and female mass (t = −3.023, p = .003; Table 1, Figure 3g).

For herbivorous lizards, longevity decreases significantly at higher latitudes (t = −2.066, p = .048; Table 1, Figure 3b) along with reproductive life span (t = −2.224, p = .034; Table 1, Figure 3f), hatchling mass (t = −3.864, p = .001; Table 1, Figure 3e) and female mass (t = −2.835, p = .008; Table 1, Figure 3g). Clutch frequency (t = 0.246, p = .807; Table 1, Figure 3a) and age at maturity (t = −0.490, p = .628; Table 1, Figure 3d) of herbivorous lizards remains unchanged across latitudes.

For omnivorous lizards, clutch/brood frequency decreases significantly at higher latitudes (t = −3.250, p = .002; Table 1, Figure 3a), while longevity increases (t = 2.065, p = .042; Table 1, Figure 3b) along with age at maturity (t = 3.479, p = .001; Table 1, Figure 3d). Other traits of omnivorous lizards do not exhibit significant changes across latitude (Table 1, Figure 3).

As expected, all traits also showed high phylogenetic signatures (Pagel’s λ: .43–.97; Supporting Information Table S2.21).

4. Discussion

Environmental temperatures strongly influence performance (Huey, 1982), productivity (Meiri et al., 2012) and life-history traits of lizards (Meiri et al., 2013). Since latitude is strongly correlated with temperature (De Frenne et al., 2013) and seasonality (Meiri et al., 2020), both of which directly affect the period of climatic suitability for lizards (Meiri et al., 2020), latitudinal trends in the expression of life-history traits are fully expected (Meiri et al., 2020; Stark et al., 2018). Here, we show that the direction and strength of these latitudinal trends are also influenced by diet. Individual life-history traits show strong diet-specific latitudinal gradients, but notably, trade-offs between these traits result in relatively consistent lifetime reproductive outputs across different diet types and latitude. Temperature-driven challenges on nutritional acquisition and assimilation were expected to reduce lifetime reproductive output from the equator towards the poles for herbivorous lizards but not carnivorous lizards. Omnivorous lizards were expected to show an intermediate pattern between that of herbivores and carnivores. Contrary to our expectations, we found that carnivorous lizards exhibit only a very slight increase in lifetime reproductive output at higher latitudes while this fitness metric does not change significantly for omnivorous and herbivorous lizards. Moreover, these latitudinal trends in lifetime reproductive output of carnivores, omnivores and herbivores were not significantly different from each other. Our results are not only consistent with the findings from Charnov et al. (2007), which report similar values of lifetime reproductive effort across lizard species, but provide new insight on how latitudinal trends in the underlying life-history traits can exhibit trade-offs to influence life-time reproductive output of lizards with different diet types.

Survival-related traits, such as longevity, age at maturity and reproductive life span were highest at the equator for herbivorous lizards; a result consistent with findings from Scharf et al. (2015), who suggest that poorer food for herbivores overall could lead to delayed maturity and consequently longer life spans. Moreover, the higher metabolic rates for carnivores compared to herbivores (Anderson & Jetz, 2005; Meiri et al., 2012), may explain the lower longevity, age at maturity and reproductive life span for carnivorous lizards in the equatorial region. However, as latitude increases, values of these traits increase for carnivores but not herbivores. Rather, herbivores display a decreasing trend in longevity as well as reproductive life span towards higher latitudes. Since reproductive life span is the difference between longevity and age at maturity, a decrease in longevity with no significant change in age at maturity at higher latitudes leads to an overall reduction in reproductive life span of herbivores. Latitudinal trends in longevity, age at maturity and reproductive life span for carnivores are consistent with findings from other studies, and seem best explained by a shift to slower life-history traits potentially induced by lower temperatures and greater seasonality (Meiri et al., 2013; Scharf et al., 2015; Tinkle, 1969). The significant decrease in these survival-related traits in herbivorous lizards, however, is interesting and likely reflects the nutritional constraints of herbivory at high latitudes.

Apart from the survival-related life-history traits, reproductive-based fitness metrics also show latitudinal trends that differ depending on diet. Near the tropics, we find that hatchling mass was significantly higher for herbivorous lizards compared to carnivorous and omnivorous lizards, which may be a consequence of the long thermally-suitable activity periods in the tropics that allow maximum extraction of nutrients from plant material for herbivores (Zimmerman & Tracy, 1989). This added advantage to acquire and assimilate nutrition that herbivores gain at the tropics compared to temperate regions could be allocated to offspring mass. Since herbivores are generally larger-bodied than carnivores (Burness et al., 2001; Clauss et al., 2013; Pough, 1973; Zimmerman & Tracy, 1989), they also have comparatively lower daily energy expenditures per unit body mass (Wilson & Lee, 2016). Given the positive correlation between hatchling size and adult body size (Meiri et al., 2015), the above-mentioned factors could further explain the higher hatchling mass and slower life histories of herbivores at the equator. As latitude increases, hatchling mass decreases dramatically for herbivores, as well as carnivores. Decline in hatchling mass for these lizards is most likely a consequence of the latitudinal decline in female mass (Meiri et al., 2015). Unlike other life-history traits, clutch/brood frequency was lowest for herbivorous lizards near the equator and remains unchanged with latitude. Thus, at the equator, herbivores invest in fewer but heavier offspring per year. By contrast, clutch/brood frequency for carnivores and omnivores decrease with latitude (Scharf et al., 2015). Overall, these patterns suggest an alternative strategy for herbivores, involving the production of many offspring in the short activity periods at high latitudes instead of slowing down their pace of life, which we find in carnivores and omnivores.

Diet does not seem to influence latitudinal gradients in clutch or brood size of lizards. Previous studies of latitudinal trends in lizard clutch sizes have found mixed results (Fitch, 1985; Meiri et al., 2013, 2020; Scharf et al., 2015; Tinkle et al., 1970). A recent study on more than 4,000 species of lizards reported a positive latitudinal pattern of clutch size, but suggested it may be driven by greater seasonality instead of lower temperature (Meiri et al., 2020). Although clutch sizes in lizards generally align with the latitudinal trend seen in birds (Ricklefs, 1980; Vaugoyeau et al., 2016), there have been similarly mixed results in a few bird species as well (Donázar, 1990; Murray, 1976). Our study reinforces this variable response and suggests that there may be other factors governing clutch size of lizards (see also Meiri et al., 2020), apart from latitude and diet.

Overall, considering the life-history traits in the numerator term of our calculation of lifetime reproductive output, carnivorous lizards seem to be able to adapt at higher latitudes by having slower life-history traits, such as increased age at maturity and longevity, increased period of their lives during which they are reproductively active, along with reduced clutch frequency. The only unexpected trend for carnivores is the smaller hatchling mass at higher latitudes. At the other extreme, herbivorous lizards do not seem to be able to nutritionally compensate at higher latitudes and exhibit the opposite trends than have been previously found for lizards as a group (Scharf et al., 2015; Tinkle, 1969), with reduced longevity, reproductive life span and hatchling mass, and no change in clutch frequency. Despite these latitudinal patterns of life-history traits in herbivores, we do not find an overall reduction in the lifetime reproductive output, likely because female mass is an integral variable in this fitness metric.

The mass of a female strongly influences her reproductive fitness (Brown & Sibly, 2006; Meiri et al., 2012; Sibly et al., 2012) and hence, our calculation of lifetime reproductive output corrects for the variation in female mass between species by including this term in the denominator. Regardless of latitude, herbivorous species are larger than non-herbivorous species (Figure 3g), a pattern of evolution widely repeated across terrestrial vertebrates (Burness et al., 2001; Clauss et al., 2013; Pough, 1973; Zimmerman & Tracy, 1989). Higher latitudes, however, coincide with lowering of female mass for herbivorous and carnivorous lizards. For carnivorous lizards, larger body sizes may not be supported at higher latitudes because of the challenges associated with balancing the energetic costs of foraging for sparsely distributed prey along with increased total energetic requirements in colder and more seasonal areas (Carbone et al., 2007; Pough, 1973). Herbivores may be further limited by the lower nutritional content of plant food at higher latitudes, and their lower digestive efficiency, lower assimilation rate and longer gut passage times in those colder and more seasonal environments (Harlow et al., 1976; McConnachie & Alexander, 2004; Pietczak & Vieira, 2017; Pough, 1973; Zimmerman & Tracy, 1989).

All these constraints can compound to reduce availability of nutrition for growth. Herbivores at higher latitudes also need to maintain higher body temperatures for extended periods of time to allow for reduced gut passage times and faster fermentation (Espinoza et al., 2004; Tracy et al., 2005; van Marken Lichtenbelt, 1992; Vitt et al., 2005; Zimmerman & Tracy, 1989). At higher latitudes, smaller body sizes irrespective of diet would enable faster thermoregulation (Ashton & Feldman, 2003; Cowles, 1945; Espinoza et al., 2004; Stevenson, 1985), thereby facilitating higher body temperatures and allowing longer activity periods in cold and seasonal environments (Ashton & Feldman, 2003; Espinoza et al., 2004). Hence, smaller bodies at higher latitudes could be beneficial for both carnivores and herbivores to overcome mobility and nutritional allocation constraints, respectively. Overall, differences in females mass particularly help to elucidate the mechanism of maintenance of lifetime reproductive output for lizards across latitudes and different diet categories.

Some of the best evidence that supports the environmental and physiological constraints imposed by carnivory and herbivory across latitude is the fact that we find intermediate trends in omnivorous lizards. Omnivorous lizards are similar to carnivores in that they exhibit a reduction in clutch frequency and an increase in age at maturity and longevity at higher latitudes. But their reproductive life span does not change significantly across latitude, unlike that of carnivores. Furthermore, omnivores also tend to have the shallowest latitudinal gradients for most traits, including lifetime reproductive output, longevity, reproductive life span, hatchling mass and female mass. These intermediate and weak latitudinal patterns suggest that omnivores are able to buffer the latitudinal effects of changing environmental conditions, by adjusting the amount of plant versus animal material in their diet. Omnivores may be incorporating more plant material near the equator and more animal material at higher latitudes, thereby avoiding the unexpected latitudinal trends in life-history traits that both carnivores and herbivores experience. Such a latitudinal pattern in dietary change from plant to animal materials has been observed in omnivorous mammals (Vulla et al., 2009), and similarly in omnivorous fishes along a temperature gradient (Behrens & Lafferty, 2007). Whether omnivory in lizards shows diet composition shifts across latitudinal ranges remains to be empirically determined.

In summary, the net outcome of these various patterns of life-history traits is a relatively consistent lifetime reproductive output across latitude for lizards of all diet categories. The deviations in life-history traits of different diet categories from typical expectations for lizards are insightful and show the importance of taking diet into account when studying life-history strategies along the latitudinal gradient. For example, lizards have been previously found to follow Bergmann’s rule in some studies (Olalla-Tárraga et al., 2006) and the reverse of Bergmann’s rule in others (Ashton & Feldman, 2003). But here we show that body size gradients across latitudes vary with diet type of the lizards. We also highlight the importance of considering trade-offs in life-history traits across the entire life span of a species when understanding reproductive output. Our results refute a long-standing hypothesis about lower allocation of resources to re-production by herbivores as compared to carnivores (Szarski, 1962). We show that when studied in terms of resource allocation per unit body mass of the female, this expected cost of herbivory disappears. Additional factors such as elevation, which may have similar underlying abiotic patterns as latitude, could provide further insights into the specific environmental drivers of these patterns. As life-history data continue to accumulate, especially for data depauperate regions of the globe where species richness is high, a combined examination of both latitudinal and altitudinal gradients for lizards of different diet types would be highly informative.

Supplementary Material

Supplementary Material

Acknowledgments

We thank Shai Meiri and the Global Assessment of Reptile Distribution group, along with Joāo Filipe Riva Tonini, for making their databases available online for public use. We thank Kartik Shanker for insightful comments on an earlier version of this manuscript, and Vivek Philip Cyriac and Aparna Lajmi for discussions on phylogenetic modelling concepts. We also thank Vivek Philip Cyriac for providing code to fix non-ultrametric phylogenetic trees. UB also thanks the Masters course in Ecology, Evolution and Conservation at Imperial College London for giving her an opportunity to think about these ideas. We acknowledge Parkjisun from the Noun Project for the lizard images used in the figures.

Funding information

Funding support for this project was provided by Department of Science and Technology-Science and Engineering Research Board (DST-SERB) grant (EMR/2017/002228) and in part by the Department of Biotechnology (DBT)/Wellcome Trust India Alliance Fellowship/Grant (IA/I/19/2/504639) to MT.

Biographies

Biosketches

Udita Bansal is interested in whole organism morphology and physiology, trait evolution and global patterns in animals.

Maria Thaker studies behavioural and physiological ecology of animals, especially in response to predation risk and sexual selection. Link to her website: https://mariathaker.weebly.com

Footnotes

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Author Contributions

UB conceived the idea, performed all analyses and wrote the manuscript. MT provided guidance and co-wrote the manuscript.

Data Availability Statement

Data used in the analyses are available on the Dryad repository https://doi.org/10.5061/dryad.5mkkwh76n.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Material
EMS194939-supplement-Supplementary_Material.zip (2.5MB, zip)

Data Availability Statement

Data used in the analyses are available on the Dryad repository https://doi.org/10.5061/dryad.5mkkwh76n.

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