© 2004 by The Society for Integrative and Comparative Biology
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Sensitivity of Intraspecific Latitudinal Clines of Body Size for Tetrapods to Sampling, Latitude and Body Size1
1 Department of Biology, Kutztown University, Kutztown, Pennsylvania 19530
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Recent studies have shown that most tetrapod groups (mammals, birds, chelonians, amphibians) show general intraspecific tendencies for increasing body size with latitude, whereas squamates (lizards and snakes) show an intraspecific tendency towards decreasing body size with latitude. Here I evaluate whether these size trends are general by using independent contrasts analysis to investigate the dependence of intraspecific size-latitude relationships (r), and the magnitude alone of size-latitude relationships ([r]), for tetrapod vertebrates, on sample size, range of latitudes sampled, average latitude sampled, and body size. Range of latitudes sampled, average latitude sampled, and body size did not influence body size-latitude relationships (r) or the magnitude alone of body size-latitude relationship ([r]). Sample size did not influence size-latitude relationships (r), but did influence the magnitude alone of size-latitude relationships ([r]), possibly indicating increased precision of estimating size-latitude relationships with increased sampling. In short, intraspecific size-latitude relationships are similar for species of different sizes, occurring at different latitudes, sampled over different latitudinal ranges, and differing in number of populations sampled (though magnitude alone is influenced by sample size). These results suggest that intraspecific size-latitude trends are general, and biologically significant (i.e., are not artifacts of sampling), thus deserving explanation.
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INTRODUCTION |
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Geographic variation of organismal characteristics has long fascinated biologists. This fascination is due, at least in part, to the important role that geographic variation has played in evolutionary biology. Showing that populations differ in characteristics, and that the traits of interest are at least partly genetically based, demonstrates potentially adaptive variation among populations. Such adaptive variation, combined with other factors, may lead to speciation, a fundamental aspect of evolution. Researchers interested in geographic variation often search for repeated clines because repeated patterns provide evidence of adaptation (Endler, 1977
), and can be used to infer possible causes of geographic variation.
General intraspecific clines of body size variation relative to latitude have been documented. Among tetrapods, most species of mammals (Ashton et al., 2000; Meiri and Dayan, 2003), birds (Ashton, 2002a; Meiri and Dayan, 2003), amphibians (Ashton, 2002b), and chelonians (Ashton and Feldman, 2003) are larger at higher latitudes. In contrast, most species of squamates (lizards and snakes) are larger at lower latitudes (Ashton and Feldman, 2003). The existence of general intraspecific body size clines for tetrapods suggests that body size is responding in an adaptive way to variation in a general factor that varies with latitude, possibly temperature. However, such patterns may also be artifacts of sampling.
Here I evaluate the sensitivity of intraspecific size-latitude relationships for tetrapods to four general factors, two artifactual and two biological, to better understand the robustness and significance of the observed patterns of clinal variation in body size. Size-latitude relationships are represented by correlation coefficients, which have two properties, the magnitude and the direction (+ or –) of the relationship. I evaluate the sensitivity of both the correlation coefficient (r), which contains information on magnitude and direction, and the absolute value of the correlation coefficient ([r]), which contains information only about magnitude, because it is possible for a general factor to influence the magnitude alone. For each general factor I briefly explain how and why it may impact the correlation coefficient (r) or the magnitude of the correlation coefficient ([r]).
Factor 1: number of populations sampled (artifactual)
Determining intraspecific relationships between body size and latitude involves sampling a number of populations or individuals throughout the range of a species. As more populations are sampled, more of the variation within a species is involved in the calculation of the size-latitude relationship. If most species of tetrapods really do show positive size-latitude relationships (as has been observed), then increased sampling would be expected to result in a higher probability of detecting positive size trends. Thus, size-latitude relationships (r) are predicted to show a positive relationship to sample size.
Sample size may also influence the magnitude of size-latitude relationships ([r]). If more populations are sampled, and therefore more variation is included, the size-latitude relationship for a species might be predicted to increase in magnitude with sampling (studies that sample more populations will have stronger size-latitude trends). Thus, the magnitude of size-latitude relationships ([r]) is predicted to show a positive relationship with sample size.
Factor 2: range of latitudes sampled (artifactual)
Researchers sample populations over a range of latitudes to calculate a correlation coefficient between body size and latitude for a particular species. If most species of tetrapods really do show positive size-latitude relationships, then actual size-latitude relationships (r) might be expected to increase (become more positive and of higher magnitude) with increased range of latitudes sampled. This would be true if species sampled over smaller latitudinal ranges show more random variation in size-latitude relationships whereas sampling over greater latitudinal ranges leads to increased probability of detecting actual size-latitude relationships. It would also be true if species with larger ranges (in this case assuming that species sampled over wider latitudinal ranges tend to have larger geographic ranges) generally express positive size-latitude trends more so than species with smaller ranges.
Latitudinal range sampled may also influence only the magnitude of size-latitude relationships. Specifically, environmental temperature and other factors influencing body size correlate broadly with latitude, thus sampling over a broader range of latitudes should result in sampling a greater range of environmental conditions among populations. Body size variation is expected to be largest among populations that differ most in environmental conditions, thus sampling over a greater range of latitudes should result in size-latitude correlation coefficients that are of higher magnitude.
Factor 3: average latitude sampled (biological)
Broad environmental conditions, particularly average temperatures, differ less among populations in equatorial regions than at higher latitudes. If the expression of a positive size-latitude relationship is positively related to the range of environmental conditions experienced throughout a species' range, then species in more variable environments (at higher latitudes) should show more positive size-latitude relationships, resulting in a positive relationship between size-latitude relationships and average latitude sampled.
With greater variation in environmental conditions experienced between populations at higher latitudes, we might also predict that species at higher latitudes will show stronger size-latitude trends. Thus, the magnitude alone of size-latitude relationships may show a positive relationship with average latitude sampled.
Factor 4: body size (biological)
Larger-bodied species tend to have larger geographic ranges, experiencing a greater variety of environmental conditions, which should lead to a stronger tendency toward showing positive size-latitude relationships, if positive size-latitude associations are the general response of organisms to experiencing environmental variation among populations. Measurement error might also lead to a tendency toward more positive, and higher magnitude, size-latitude relationships in larger-bodied species, particularly if measurement error influences the ability to detect actual size-latitude relationships in smaller bodied species (Freckleton et al., 2003). Alternatively, biophysical modeling of thermal dynamics of mammals suggests that smaller-bodied species should show stronger and more positive size-latitude relationships (see Ashton et al., 2000), in which case size-latitude relationships should be negatively related to body size. Similar biophysical arguments might be made for birds (see Ashton, 2002a).
Body size may also influence the magnitude alone of size-latitude relationships. From a statistical standpoint, measurement error is likely greater for smaller-bodied species than larger-bodied species. If measurement error tends to underestimate actual size-latitude relationships, then magnitude of size trends would be expected to increase with body size. Another reason that smaller bodied species might show lower magnitude size-latitude relationships is biological. Specifically, larger-bodied species tend to have larger ranges, and thus experience a wider range of environmental conditions, which should lead to stronger size-latitude relationships.
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Correlation coefficients between body size and latitude (some data were for body size and elevation) were compiled from published literature (Appendix 1). Most studies used mean adult size as the measure of body size, though some used minimum or maximum adult size.
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I used regression analysis of the correlation coefficients (size-latitude relationships), as well as the absolute value of the correlation coefficients (magnitude only of size-latitude relationships), versus each of the four general factors to evaluate the influence of each general factor on size-latitude trends. I performed each regression analysis using nonphylogenetic and phylogenetic approaches. Phylogenetic analyses were performed using independent contrasts, implemented by PDTREE (Garland et al., 1993
, 1999), using composite phylogenies (presented in Ashton et al., 2000; Ashton, 2002a, b; Ashton and Feldman, 2003) and two arbitrary methods to calculate branch lengths. One arbitrary method, equal branch lengths, sets all branch lengths equal to one. The other method, developed by Pagel (1992), sets all internode branch lengths equal to one and constrains tips to be contemporary. Recently, a test of phylogenetic signal has been proposed as a means to evaluate whether phylogenetic analyses are necessary for a given dataset (Blomberg et al., 2003). Using this approach, at least one variable in each analysis contained significant phylogenetic signal (and the other, if insignificant, often approached significance; analyses not shown), thus the phylogenetic analyses are more appropriate. For brevity, I only present results using equal branch lengths (results using Pagel's branch lengths were very similar). All variables, except the size-latitude relationships (r), the absolute value of size-latitude relationships ([r]), and the average latitude, were log (X + 1) transformed prior to analysis (raw data reported in Appendix 1). |
RESULTS |
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Sensitivity of size-latitude trends to Factor 1 (number of populations sampled)
The number of populations sampled does not influence intraspecific size-latitude relationships (r) for tetrapods overall (Fig. 1a; Table 1). Further, number of populations sampled does not influence size-latitude relationships when data are analyzed separately for amphibians, chelonians, squamates, birds or mammals (Table 1).
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However, the magnitude of intraspecific size-latitude relationships ([r]) is significantly negatively related to the number of populations sampled for tetrapods overall (Fig. 1b; Table 1). The magnitude of size-latitude relationships is also significantly negatively related to sample size for amphibians, chelonians, and mammals, but not for squamates or birds (Table 1).
Sensitivity of size-latitude trends to Factor 2 (range of latitudes sampled)
Tetrapods fail to show any relationship between size-latitude relationships (r) and range of latitudes sampled (Fig. 2a; Table 1). Analyzed separately, amphibians, chelonians, squamates, birds and mammals fail to show significant relationships between size-latitude relationships and range of latitudes sampled (Table 1).
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Tetrapods also show no relationship between the magnitude of intraspecific size-latitude relationships ([r]) and range of latitudes sampled (Fig. 2b; Table 1). Likewise, amphibians, chelonians, squamates, birds and mammals fail to show any significant relationship between the magnitude of size-latitude relationships and range of latitudes sampled (Table 1).
Sensitivity of size-latitude trends to Factor 3 (average latitude sampled)
Tetrapods overall show no association between size-latitude relationships (r) and average latitude sampled (Fig. 3a; Table 1). Analyzed separately, amphibians, chelonians, squamates, birds and mammals all fail to show any relationship between size-latitude relationships and average latitude sampled (Table 1).
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Tetrapods also do not show any relationship between the magnitude of intraspecific size-latitude relationships ([r]) and mean latitude sampled (Fig. 3b; Table 1). Amphibians fail to show any relationship between the magnitude of size-latitude relationships and mean latitude, as do chelonians, squamates, birds and mammals (Table 1).
Sensitivity of size-latitude trends to Factor 4 (body size)
Size-latitude relationships (r) are not significantly related to body size for amphibians (Fig. 4a), chelonians (Fig. 4b), squamates (Fig. 4c), birds (Fig. 4d) or mammals (Fig. 4e; Table 1). Similarly, the magnitude of size-latitude relationships ([r]) is not significantly related to body size for any group of tetrapods (Fig. 5; Table 1).
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DISCUSSION |
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The results of this study have three major implications, one statistical and the other two biological. Ashton et al. (2000)
proposed three ways to perform vote count analyses (tests for general patterns involving counting the number of species showing positive, negative, or no trends) of intraspecific size-latitude relationships, though they preferred the "all species" approach. This approach includes data for all species, regardless of statistical significance, assuming that even data for poorly sampled (over a small area or few populations) species are useful as indicators of overall tendencies. Intraspecific relationships between body size and latitude are not influenced by sample size or range of latitudes sampled for tetrapods overall, or for most major groups of tetrapods, indicating that studies based on small sample size and/or small range of latitudes sampled should be included in any analysis for general size-latitude patterns because they are just as good indicators of direction of size-latitude relationships (+ or – relationship of size with latitude) as studies based on more extensive sampling. That said, the magnitude of size-latitude relationships is negatively related to sample size, which may be a result of increased precision and accuracy of estimating actual size-latitude relationships with more sampling. Given this result, any formal meta-analysis (calculating a grand mean effect size from values reported in individual studies) that uses actual values of correlation coefficients should only use correlation coefficients from studies of large sample size or should include a weighting scheme to minimize the effect of studies of small sample size on overall trends (the latter approach has been used by Ashton [2002a, b;] Ashton and Feldman, [2003]).
Some authors have suggested that size-latitude trends vary with latitude (e.g., McNab, 1971). However, size-latitude relationships (r), and the magnitude only of size-latitude relationships ([r]), do not vary with average latitude, indicating that species at higher latitudes do not tend to have stronger or more positive size-latitude trends. This result is surprising, given that species occurring at lower latitudes likely experience less environmental variation (particularly temperature) among populations. If most species at all latitudes show a positive intraspecific size-latitude relationship, then explanations that assume no variation in a causal factor across populations at lower latitudes are unable to account for all instances of such size trends.
Body size has been suggested to influence intraspecific size-latitude relationships (Ashton et al., 2000; Freckleton et al., 2003; Meiri and Dayan, 2003), yet in this study the two are not related for any major group of tetrapods, suggesting that size-latitude relationships are just as strong, and positive, for small-bodied species as for large-bodied species. Although lack of a significant association between size-latitude relationships and body size has also been reported elsewhere for birds (Meiri and Dayan, 2003) and mammals (Freckleton et al., 2003), Meiri and Dayan (2003), using a vote-count approach, reported that larger-bodied mammals were more likely to show positive size-latitude relationships. The differences in results for mammals may be due to different methodological approaches (vote-count vs. regression) or different datasets. Criteria for selection of studies to include in reviews may have also played a role. For this study, and that of Freckleton et al. (2003), only correlation coefficients between body size and latitude were included, whereas Meiri and Dayan (2003) did not separate correlation coefficients for body size and latitude from those of body size and other environmental variables (e.g., temperature, wet-bulb temperature, and actual evapotranspiration). Because broad environmental variables are not perfectly correlated with latitude (r-values are less than 1), it is possible for intraspecific size trends to show no relationship with latitude, but show a significant relationship with temperature or another broad environmental factor. In fact, Freckleton et al. (2003) found no significant relationship between body size and size-latitude relationships, but did find that larger-sized mammals show stronger and more negative size-temperature relationships. New analyses of the influence of body size on size-latitude and size-temperature trends, using vote-count and regression approaches, are needed to resolve the different results for mammals.
In sum, the tendency to show a positive intraspecific size-latitude relationship is not related to range of latitudes sampled, average latitude or body size. In other words, wide-ranging species (or, at least, species that have been sampled over wider ranges), species at higher latitudes, and larger-bodied species do not show stronger or more positive size-latitude relationships than other species. Overall, sampling does not influence size-latitude relationships, other than by increased precision and accuracy in estimating the magnitude of the size-latitude relationship with increased sample size. Therefore, based on available data, general intraspecific patterns of body size variation in tetrapods are biologically significant (i.e., not artifacts of sampling or analysis) and deserve explanation.
The existence of general clines suggests that the observed intraspecific size-latitude clines are adaptive and many possible adaptive explanations have been proposed (reviewed by Ashton et al., 2000; Ashton, 2002a, b; Ashton and Feldman, 2003). Here I suggest future directions for research aimed at understanding the mechanisms generating observed intraspecific body size trends. Although latitude is a useful proxy for a number of environmental variables, it alone is unlikely to influence body size (Hawkins and Diniz-Filho, 2004). Thus, evaluating causes of size-latitude trends will require examination of how body size responds to specific environmental variables. General factors that have been hypothesized to influence geographic variation in body size include seasonality, temperature, moisture, a combination of moisture and temperature, and productivity of the environment (Bergmann, 1847; Rosenzweig, 1968; James, 1970; Boyce, 1979). More studies comparing the influence of each of these factors on body size are needed. Of the few that have been performed (Boyce, 1978; Murphy, 1985; Wigginton and Dobson, 1999; Ashton, 2001), seasonality appears to be the strongest influence. If this turns out to be the general case, then some possible explanations for intraspecific body size trends (e.g., fasting endurance) are more likely. Biotic factors, such as competition and predation, may also influence body size trends (reviewed in Ashton et al., 2000). Development of models of intraspecific body size variation incorporating abiotic and biotic factors would be useful. Yet, to fully understand the causes of body size variation, a comprehensive life-history perspective, including body size as one of several traits (e.g., growth rate, age at maturity, reproductive output, longevity) that vary between populations, will be required because it is possible that selection is acting on a suite of life history traits. Though comparative studies can yield insight about possible mechanisms, detailed experimental studies (e.g., Sears and Angilletta, 2003) will be necessary to completely explain intraspecific size trends.
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ACKNOWLEDGMENTS |
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For comments and discussion I thank M. Angilletta, Jr., A. de Queiroz, P. Doughty, R. Huey and R. Freckleton.
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FOOTNOTES |
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1 From the Symposium Evolution of Thermal Reaction Norms for Growth Rate and Body Size in Ectotherms presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 5– 9 January 2004, at New Orleans, Louisiana.
2 E-mail: ashton{at}kutztown.edu
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References |
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