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Annu. Rev. Ecol. Syst. 1997. 28:65987 Copyright c 1997 by Annual Reviews Inc.

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ALLOMETRY FOR SEXUAL SIZE DIMORPHISM: Pattern and Process in the Coevolution of Body Size in Males and Females
D. J. Fairbairn
Department of Biology, Concordia University, 1455 de Maisonneuve Blvd., West, Montreal, Quebec, Canada H3G 1M8; e-mail: fairbrn@vax2.concordia.ca
KEY WORDS: sexual dimorphism, allometric constraint, sexual selection, correlational selection, genetic correlation

ABSTRACT
Sexual size dimorphism (SSD) is common in both plants and animals, and current evidence suggests that it reects the adaptation of males and females to their different reproductive roles. When species are compared within a clade, SSD is frequently found to vary with body size. This allometry is detected as =1, where is the slope of a model II regression of log(male size) on log(female size). Most frequently, exceeds 1, indicating that SSD increases with size where males are the larger sex, but decreases with size where females are larger, a trend formalized as Renschs rule. Exceptions are uncommon and associated with female-biased SSD. These trends are derived from a sample of 40 independent clades of terrestrial animals, primarily vertebrates. Their extension to plants and aquatic animals awaits quantitative assessments of allometry for SSD within these groups. Many functional hypotheses have been proposed to explain the evolution of allometry for SSD, most featuring sexual selection on males or reproductive selection on females. Of these, the hypothesis that allometry evolves because of correlational selection between the sexes appears most promising as a general model but remains untested.

INTRODUCTION
Sexual dimorphism, dened as morphological differentiation of sexually mature males and females, is a conspicuous feature of dioecious plants and gonochoristic 659 0066-4162/97/1120-0659$08.00

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animals (6, 29, 49, 50, 88, 100, 107, 140). Differentiation of reproductive roles leads directly to morphological differentiation of organs and structures associated with the production and release of gametes and, if fertilization is internal, with the formation and early development of the zygotes. Differences between the sexes in parental investment and in the relationship between mating frequency and reproductive success (sexual selection) also lead to dimorphism (68, 25, 88, 96, 100, 127, 150, 164, 165, 167), and such selection is frequently associated with hyperallometric growth of organs and structures associated with combat or display in males (22, 34, 53, 56, 77, 84, 87, 114, 115, 126, 134, 153, 165, 166). Although sexual selection and selection associated with differences in reproductive roles are often treated as independent explanations for the evolution of sexual dimorphism (29, 67, 120, 143), they can be viewed as components of a continuum determined by anisogamy, separation of the sexes, and the resulting specialization of reproductive roles (6, 24, 50, 88, 107, 124, 125, 127, 151, 164, 165). Hypotheses invoking selective processes along this continuum have the common property that the pattern (relative dimorphism of different traits), direction (which sex is larger), and magnitude of sexual dimorphism can be predicted from components of reproductive success (16, 24, 27, 31, 33, 36, 43, 47, 49, 50, 60, 66, 70, 71, 88, 92, 94, 98, 116118, 125, 134, 135, 139, 141, 152, 159, 160, 161, 164, 166). An alternative hypothesis, intersexual niche divergence or ecological sexual dimorphism, proposes that sexual dimorphism evolves to reduce intraspecic competition for food and is not associated directly with selection on reproductive traits (6, 67, 120, 134, 136, 143). Empirical tests of this hypothesis have produced both positive (89, 106, 134, 136, 141, 154) and negative conclusions (16, 27, 33, 46, 65, 75, 94, 103, 104, 118, 129, 137). Even where the results are positive, it is difcult to exclude the hypothesis that trophic dimorphism evolved as a consequence of pre-existing sexual dimorphism (6, 46, 120, 127, 136, 137). Further, although intersexual competition for food may lead to trophic dimorphism, it cannot explain the prevalence of dimorphism in reproductive and sexually-selected traits. Given the extensive evidence of the importance of reproductive and sexual selection, it seems unlikely that intersexual niche divergence plays more than a subsidiary role in the evolution and maintenance of common patterns of sexual dimorphism (6, 16, 46, 75, 88, 103, 118, 127, 136, 137, 164). In many species, the selective processes producing sexual dimorphism result in dimorphism for overall body size (sexual size dimorphism or SSD). Malebiased size dimorphisms (i.e. males larger than females) tend to predominate in polycarpic seed-bearing plants (Gymnospermae and Angiospermae), while females tend to be the larger sex in other dioecious plants (49, 50, 57, 86, 88, 100,

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101, 164, 165). In animals, female-biased SSD predominates among invertebrates (5, 14, 50, 66, 72, 129, 142, 149, 152, 158, 161) and poikilothermic vertebrates (50, 51, 57, 135, 138, 139, 145). In these taxa, extreme female-biased SSD is not uncommon, with females of some species weighing several hundred times as much as their mates (6, 50, 52, 57, 59, 152). Male-biased SSD predominates only among birds and mammals, reaching its greatest extreme in the mammalian orders Primates, Pinnipedia, Proboscidea, and Artiodactyla, where males of larger species may weigh two to eight times as much as females (4, 13, 18, 57, 58, 112, 121, 134, 155). Sexual size dimorphism varies within as well as among taxa, and it is not unusual for SSD to range from female-biased to male-biased among species within a single family (Table 1 and 112, 124, 125, 138) or even a single genus (Table 1 and 7, 35, 138). These patterns of variation provide the necessary data for hypothesis testing, and quantitative comparative analyses have been widely used to test hypotheses concerning the evolution and adaptive signicance of SSD. Such studies have provided much of the evidence for the importance of selection on reproductive traits, particularly traits associated with sexual selection in males (4, 5, 13, 27, 32, 33, 38, 44, 45, 69, 75, 107, 109, 112, 135, 138, 139, 141, 151, 155, 158), fecundity selection in females (16, 18, 45, 66, 142, 151, 161), and patterns of parental investment (68, 85, 104, 108, 138, 141). Comparative analyses of SSD also frequently reveal a strong statistical association between SSD and body size (Table 1 and 35, 107, 112, 120, 124, 125, 135, 146). In many studies, the effect of body size (allometry) is statistically removed before hypotheses for the adaptive divergence of SSD are tested (13, 21, 26, 35, 84, 109, 137), the allometry itself being considered a functional constraint (cf 19, 42, 53, 63, 73, 147, 148). Other authors seek to understand the evolutionary processes responsible for the underlying allometry. Although many hypotheses have been proposed (26, 27, 37, 48, 57, 82, 96, 135, 157), none has proven sufciently robust to emerge as a viable general hypothesis (6, 124, 125, 155). Thus, the functional and adaptive signicance of allometry for SSD remains obscure. In the following sections, I consolidate empirical and theoretical studies of allometry for SSD with the aim of discovering a general, functional hypothesis. The rst section formally denes allometry and considers the problems of measuring allometry for SSD. The second section reviews the available quantitative evidence of allometry for SSD and assesses its prevalence and pattern. The third section reviews and evaluates functional hypotheses for the evolution of allometry for SSD with reference to both the observed patterns of variation in allometry and knowledge of the adaptive signicance of SSD, and the nal section considers methods of testing these hypotheses.

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Table 1 Quantitative evidence of interspecic allometry for sexual size dimorphism SSDb Clade or taxon MAMMALIA Primates Platyrrhini Carnivora (excl. Mustelidae) Mustelidae Artiodactyla & Perisodactyla Sciuridae (Tamias) AVES Passeriformes Icterinae Pipridae Paradisaidae Pelicaniformes, Sphenisciformes Procellariformes, Pelicaniformes Galliformes Trocholoformes Falconiformes Strigiformes Anseriformes Charadriiformesg Haematopodidae Charadriidae Scolopacidae Tringini Numeniini Calidridini Gallinagonini REPTILIA Squamata Elapidae Division A Division B Division C Colubridae Natracinae Colubrinae, Lycodontinae, Xenodontinae Viperidae Lacertidae Na Mean Range RRc ++ ++ 0 0 0 0 ++ ++ ++ ++ ++ ++ ++ ++ 0 0 0 0 0 0 0 + 0 Allometry d 1.15f 1.05 1.01f 1.05f 1.02f 1.07 1.13 1.20 1.14 1.14 re 0.987f 0.992 0.991f 0.991f 0.992f 0.977 0.990 0.964 0.983 0.950 Reference

36 52 17 26 27 21 65 35 30 42 58

0.32 1.04 0.08 0.19 0.760.17 0.25 1.180.14 0.44 1.330.03 0.34 0.770.00 0.03 0.010.06 0.03 0.07 0.02 0.08 0.210.03 0.230.03 0.110.06 0.240.04 0.530.32 0.320.40 1.280.14 0.240.14 0.041.17 0.010.65 0.250.04 0.500.42 00.03 0.020.03 0.500.32 0.010.06 0.010.05 0.210.05 0.040.02

2 44 2 2 2 78 13 155 112 112 38 2 2 2 2 2 2 2 75 75 2 75 75 75 75

40 0.06 27 0.24 14 0.03 22 0.36 25 0.21 28 0.13 65 0.04 8 0.02 25 0.01 35 0.11 15 0.03 9 0.03 24 0.00 12 0.01

1.08f 0.985f 1.34f 1.16f 1.00f 0.91f 1.02f 1.00f 1.00 0.96 1.01f 1.02 0.96 1.10 0.95 0.961f 0.950f 0.951f 0.962f 0.985f 0.953f 0.978 0.998 0.913f 0.993 0.999 0.972 0.995

19 0.16 31 0.02 16 0.06 14 18 0.19 0.05

0.250.53 0.190.32 0.220.09 0.090.33 0.300.35 0.210.08 0.060.11

0 ++ 0 0 + ++ 0

0.91f 0.762f 1.21f 0.854f 1.05f 0.795f 0.93f 0.924f 1.19f 0.814f

2 2 2 2 2

16 0.09 8 0.00

1.17f 0.915f 1.03 0.972

2 16

(Continued )

ALLOMETRY FOR SEXUAL SIZE DIMORPHISM


Table 1 (Continued ) SSDb Clade or taxon Iguanidae Chelonia Kinosterninae AMPHIBIA Anura Bufo ARACHNIDA Araneae (excl. Araneidae) Araneidae INSECTA Gerridae Tephritidae Phasmatodea
aNumber bSSD

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Allometry RRc 0 ++ ++ 0 0 d 0.99f 1.18 re 0.902 0.935 Reference 2 51 74 124 124 1.02f 0.89 1.17f 1.12 0.84h 0.750f 0.919 0.952f 0.989 0.923 2 1 2 142 142

Na 90 77 24 51 18 44 19 33 27 152

Mean 0.12 0.05

Range 0.490.24 0.201.75 0.350.11

0.23 0.57 0.13 0.05 >0

0.030.68 0.131.70 0.000.32 0.170.19

0 0 ++ ++

of species compared. estimated using the index of Lovich and Gibbons (90): SDI = ([mean size of largest sex]/[mean size of smallest sex])1, arbitrarily dened as positive when females are larger and negative when males are larger. cRenschs rule: ++, statistically signicant allometry consistent with Renschs rule (P < 0.05); +, allometry consistent with Renschs rule with 0.05 P 0.20; no allometric trend (P > 0.20); , allometry inconsistent with Renschs rule with 0.05 P 0.20; , statistically signicant allometry inconsistent with Renschs rule (P < 0.05). dSlope of the major axis regression of log(male size) on log(female size), estimated from the data provided in the original source. ePearson product moment correlation coefcient between log(male size) and log(female size). fCorrected for phylogeny using independent contrasts analysis (2, 40, 110). gAlcidae, Charadriidae, Jacanidae, Laridae, Recurvirosridae, Rostratulidae, Rynchopidae, and Stercoraridae. hOLS slope from the original source.

ESTIMATING ALLOMETRY FOR SEXUAL SIZE DIMORPHISM


Allometry is formally dened as a departure from geometric similarity (53, 78, 133) or, more fully, as differences in proportions correlated with changes in the absolute magnitude of the total organism (53). By convention, allometric relationships are quantied using the power function, y = x , where x is body size, y is a measure of the trait of interest, and and are constants (19, 113, 125, 133, and see 53, 61, 73, 78 for justication of this model). If x and y are measured on the same scale, the ratio y/x will be a constant ( ) when = 1. This denes geometric similarity or isometry. By extension, allometry occurs when

>

> > >

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=1. If > 1, y increases faster than x, and y/x increases as x increases. This is termed positive allometry or hyperallometry (19, 53). Negative allometry or hypoallometry occurs when < 1, indicating that y increases more slowly than x, and y/x declines as x increases. Quantifying allometry requires estimating the allometric coefcient , and this is achieved by logarithmic transformation so that becomes the slope of the linear regression, log( y) = log( ) + log(x) (53, 61, 78, 125). Allometry for SSD has most frequently been estimated by regressing some measure of SSD against mean body size (27, 38, 51, 74, 139, 141), size of females (13, 44, 48, 84, 112, 155, 162), or size of males (16, 44). Unfortunately, the pattern of allometry revealed by these studies depends strongly on whether SSD is estimated as a difference or a ratio (48). For size ratio to remain constant as body size increases (i.e. isometry for size ratio), the difference in size between the sexes must increase with body size and thus must show positive allometry. Similarly, a constant size difference requires negative allometry for size ratio. In addition to this confusion, a regression of any index of SSD on body size violates the basic assumption of mathematical independence of the x and y variables (78, 131, 144). For example, in a regression of size ratio on mean size we expect x and y to covary because mean male size and mean female size are included in both variables. Because of the interdependence of y and x, the null hypothesis is not = 0, and normal techniques of hypothesis testing are not valid. Both of these problems are solved if allometry for SSD is estimated from a log/log plot of the size of one sex against the size of the other sex (2, 5, 27, 35, 37, 82, 94, 142, 155). As neither sex is, a priori, the independent variable, there is as yet no convention as to placement of the sexes on the x- and y-axes. Fairbairn & Preziosi (37) and Abouheif & Fairbairn (2) proposed assigning males to the x-axis. However, other authors have preferred to place females on this axis, both in regressions of SSD on size (13, 84, 112, 155, 162) and in regressions of the size of one sex against the size of the other sex (27, 48, 82, 94, 142, 155). To facilitate comparisons among studies, I adopt the convention of placing female size on the x-axis (Figure 1). Because body size, x, is not xed and is estimated with error, ordinary least squares regression (OLS, model I) will tend to underestimate both and the condence interval around . Some form of model II regression is therefore more appropriate for both parameter estimation and hypothesis testing (53, 78, 97, 144). Given that male and female sizes are measured in the same manner and using the same scale, both measurement and intrinsic error should be very similar in the two sexes, especially when transformed to a logarithmic scale. Under these conditions, major axis regression (MA) provides an accurate estimate of and allows statistical testing of the general null hypothesis,

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Figure 1 Regression model for estimating allometry for SSD. The diagonal solid line represents a size ratio of one (size of males = size of females). Male-biased size dimorphisms lie above the diagonal, female-biased dimorphisms below. The dotted line represents an allometric relationship in which female size varies more among species than male size and therefore the regression slope, , is less than 1. The dot-dashed line represents an allometric relationship in which male size varies more among species than female size and therefore > 1. Deviations of these lines from the 1:1 line illustrate the degree of SSD. When > 1, SSD declines as size increases for female-biased SSD, but increases with size for male-biased SSD, as predicted by Renschs rule (see text). If < 1, the pattern of allometry for SSD is reversed and is inconsistent with Renschs rule.

= 0, as well as the null hypothesis of isometry, = 1 (63, 78, 97, 144). Reduced major axis regression (RMA) would also provide an accurate estimate of , but methods of testing the null hypothesis, = 0, remain controversial for this technique (63, 78, 97, 144). Because of the high correlation generally found between male and female body sizes (Table 1), the two techniques should give almost identical estimates for . To illustrate this, I compared slopes calculated by OLS, MA, and RMA regressions of log(male size) on log(female size) for ten independent data sets with sample sizes ranging from 14 to 65 species. The MA slopes ranged from 0.89 to 1.26. The mean difference between the MA and RMA slopes was only 0.0003 (SD 0.0040), while OLS slopes averaged 0.018 (SD 0.021) lower. Thus, choosing model II rather than model I regression may signicantly inuence the results, but the model II technique used is of little consequence for parameter estimation. One problem remains for statistical assessments of allometry for SSD. As in any comparative analysis, the accuracy of both parameter estimation and

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hypothesis testing may be adversely inuenced by phylogenetic autocorrelation among the taxa being compared (40, 55, 64, 95, 110, 119). Although several methods have been developed to remove phylogenetic effects from comparative data (reviewed in 64), the most efcient method for parameter estimation from species means is the method of pairwise independent comparisons or independent contrasts (40, 54, 110, 119). Simulation analyses indicate that the independent contrasts method performs better than standard comparisons across the tips of the phylogeny (i.e. comparisons among species, uncorrected for phylogeny) for both parameter estimation and hypothesis testing, even in the absence of a fully resolved phylogeny and branch length information (54, 95, 119). Abouheif (1) used the regression methods outlined above to estimate allometry for SSD in 21 independent clades and to compare the results of the standard analyses using species means (tips analyses) with those from independent contrasts analyses. The independent contrasts analyses were less powerful than the tips analyses, with an average reduction in power of 10%, and ve slopes judged signicant (i.e. P < 0.05) according to the tips analysis were not signicant after independent contrasts. This reduction in power reects both the reduction in degrees of freedom associated with the independent contrasts analyses and the higher type I error rate of the tips analyses (1, 55, 95, 119). The allometric slopes estimated by the two methods were quite strongly correlated (r19 = 0.71, P < 0.0005) and did not differ systematically (paired t-test, t20 = 0.607, P > 0.50), indicating no relative bias. However, the coefcient of variation between the two estimates was only 51%, indicating considerable variance between methods. Thus, the slopes estimated from the standard tips regressions were unbiased but relatively inaccurate predictors of the slopes estimated from the independent contrasts (1). Because the latter are expected to be more accurate, with respect to both parameter values and statistical conclusions (40, 54, 64, 110, 119), independent contrasts analysis should be an integral part of assessments of allometric relationships (1, 2).

EMPIRICAL EVIDENCE OF ALLOMETRY FOR SSD


Numerous authors have stated that SSD generally increases with body size in taxa in which males are the larger sex (2, 27, 37, 112, 120, 124126, 135, 155, 162). An overall trend is less apparent where females are the larger sex, but the most common pattern appears to be one of decreasing SSD with increasing size (2, 35, 37, 126, 157). Rensch formalized these trends into a general rule (2, 124 126). When male size is regressed against female size, allometry consistent with Renschs rule yields a slope greater than one, regardless of which sex is larger (Figure 1). The major characteristic of this trend is that male size varies more among species than female size (i.e. y > x). In contrast, allometry

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inconsistent with Renschs rule ( < 1 in Figure 1) would indicate greater interspecic variance in female size than in male size. Previous reviews of the quantitative evidence for Renschs rule (2, 124, 125) indicate that it is indeed the most common allometric trend but that exceptions occur, particularly in taxa in which females are the larger sex. The available quantitative evidence of allometry for SSD is consolidated in Table 1. I have restricted the data to interspecic comparisons because allometric patterns are often strongly inuenced by taxonomic level (i.e. comparisons among species yield different slopes than comparisons among genera, families, etc; 2, 26, 63, 111). Allometry for SSD has also been recorded among populations within species, but these patterns may be poor indicators of evolutionary trends because of strong environmental effects (37, 146) and, if growth continues after sexual maturity, because of the confounding interaction between age and size distributions (146). Although all of the studies in Table 1 are based upon comparisons among species, the constituent species have been grouped at various taxonomic levels, from a single genus to combinations of two related orders. In most cases the level of grouping may simply reect the taxonomic scope of interest of the authors. However, Abouheif & Fairbairn (2) dened their 21 species groups objectively based on both phylogeny and homogeneity of allometric slopes, combining sister clades if the slopes were homogeneous, but analyzing them separately if the slopes were heterogeneous. Table 1 includes only studies that assess allometry for overall body size measured as weight (16 analyses), length (19 analyses), or length of a body component known to be strongly correlated with overall size (9 analyses). In all examples, allometry was originally estimated from a bivariate plot of either SSD against body size, or the size of one sex against the size of the other sex. Where possible, I have used the data provided in the original sources to estimate the mean and range of SSD, the allometric coefcient ( ), and the correlation coefcient (r) for log(body size) between the sexes. These standard statistics are then used in quantitative assessments of the overall pattern and prevalence of allometry. Unfortunately, very few authors have corrected for phylogeny when assessing allometry for SSD (1, 2), and only 21 of the 42 analyses in Table 1 are based on independent contrasts. However, given that slopes estimated from standard tips regressions are unbiased estimators of slopes estimated from independent contrasts (1), the inclusion of both types of estimates should not bias our assessment of overall qualitative trends. However, the probability of a type I error may be higher than 0.05 in the tips analyses (54, 95, 119), and, conversely, the power is lower for the independent contrasts analyses if the underlying phylogeny is poorly resolved. Thus, the probability of concluding that the allometric trend is

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statistically signicant is higher for tips analyses than for analyses based upon independent contrasts. Where this may inuence interpretation of the data, it has been noted in the text. In several cases, the same species have been included in more than one study, and thus the estimates of allometry cannot be considered independent. For example, signicant allometry consistent with Renschs rule has been demonstrated repeatedly for Primates, based on broadly overlapping data sets (2, 27, 44, 48, 8284). Only the estimates from Abouheif & Fairbairn (2) and Ford (44) appear in Table 1. The former was chosen because it is based on independent contrasts (40, 110) and is therefore independent of phylogenetic effects. The latter was chosen because it is based primarily on Neotropical species not included in the other studies. Although Fords analysis shares 10 species with that of Abouheif & Fairbairn (2), removal of these species did not affect the statistical conclusion and changed the major axis slope only from 1.052 to 1.058. Because of the large differences in both SSD and allometric slope between these two species sets (Table 1), I have included both as representative of patterns of allometry in different groups of Primates. Three overlapping species sets occur in the bird data: Eight species of Ictinerae analyzed by Webster (155) are also included in Bjorklunds analysis of Passeriformes (13); seven species of Pelicaniformes occur in the data sets of both Fairbairn and Shine (12) and Abouheif & Fairbairn (2); and the subfamilies of Scolopacidae analyzed by Jehl & Murray (75) overlap with the Scolopacidae analyzed by Abouheif & Fairbairn (2). I have considered these data independent if at least 75% of species are unique to a given data set. By that criterion, only the Numeniini (75) are not independent, and these are therefore excluded from the quantitative analyses. Among the reptiles, Abouheif & Fairbairns analyses of six separate snake clades (2) supersede earlier analyses (41, 139) that combined snakes from clades differing markedly in behavior, ecology, reproductive biology, body size, SSD, and allometric slope (2, 138, 139). Similarly, the separate analyses of the lizard families Lacertidae (16) and Iguanidae (2) supersede earlier analyses (41, 145), and the recent analyses of allometry in turtles (51, 74) replace an earlier analysis (12) based on a much smaller sample size (eight species). The two turtle data sets share only ve species and so are considered independent. A nal area of overlap occurs in between the two estimates of allometry in Amphibia. It is likely that some of the Bufo species used by Arak (unpublished data, cited in 124, 125) also occur in Crumps data set (28, cited in 124, 125). In the absence of evidence to the contrary, I do not consider them independent estimates. For two clades, the Mustelidae and Araneae, the allometric pattern reported in Table 1 conicts with patterns reported by previous authors. The mustelids

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have been used as an example of allometry inconsistent with Renschs rule because SSD appears to decrease with body size even though males are larger than females (102, 122, 124, 125). However, controlling for the inuence of phylogeny removes this apparent allometric trend (1, 2) resulting in 1 (Table 1). Allometry inconsistent with Renschs rule has also been reported for the Araneae (66, 152). Female spiders are the larger sex, but SSD appears to increase with body size. However, both SSD and the pattern of allometry vary greatly among families within the Araneae (2, 66, 152), and as in the Mustelidae, removal of phylogenetic effects removed the apparent allometry among species (2), resulting in 1 for Aranae excluding the Araneidae (Table 1). The Araneidae (orb weavers) are clear outliers, with a strongly female-biased SSD, and an allometric slope less than one (1, 2, 66, Table 1). The interspecic variance in size is clearly much greater for females than for males in this family, but the correlation between the sexes is not sufcient to generate statistically signicant allometry in our sample of 18 species (Table 1 and see 66). However, the slope for the Araneidae is lower than that reported for any other clade, and the hypothesis of signicant allometry inconsistent with Renschs rule in orb weaving spiders should not be rejected without further testing. After consideration of nonindependence among data sets, there remain 40 independent estimates of allometry for SSD and 37 independent, quantitative estimates of the allometric and correlation coefcients. The correlations between the sexes are all high and statistically signicant, indicating that strong covariation between the sexes is a conspicuous feature of interspecic variation in body size, regardless of the allometric pattern for SSD. Allometry for SSD is statistically signicant ( =1) in 18 independent data sets (10 of 19 tips analyses, and 8 of 13 independent contrasts analyses), across a wide range of clades. Sixteen of the estimates demonstrate statistically signicant allometry consistent with Renschs rule, and two estimates show the same trend with 0.20 > P > 0.05. This pattern occurs in mammals, birds, reptiles, and insects, and in taxa in which females are the larger sex, as well as in taxa in which males are larger (Table 1, Figure 2a). Two clades, Strigiformes (owls) and Phasmatodea (walking sticks), show statistically signicant allometry inconsistent with Renschs rule, and a similar trend may also occur in the Araneidae. In all of these clades, females are the larger sex. Overall, 28 of the MA slopes are greater than one (consistent with Renschs rule), and eight are less than one (Table 1, Figure 2). The allometric slopes are negatively correlated with the index of SSD (Figure 2a, r34 = 0.40, P < 0.02). Since this index is negative when males are the larger sex (Table 1, and see 90 for a discussion of the statistical properties of this index), the negative correlation indicates that the slopes tend to decrease as SSD becomes more female-biased. Thus allometry consistent with Renschs rule is more prevalent and more pronounced in clades with male-biased SSD.

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Figure 2 Scatter plots of allometric slopes against the (a) mean and (b) range in SSD, for 36 independent species groups (Table 1 and see text). The allometric slope is estimated as the slope of the major axis regression of log(male size) on log(female size). Sexual size dimorphism is estimated using the sexual dimorphism index of Lovich & Gibbons (90), which is negative when males are larger, zero for sexes of equal size, and positive when females are larger. The horizontal and vertical dotted lines indicate = 1 (isometry), and SSD = 0 (no sexual size dimorphism), respectively. Filled symbols indicate slopes that differ signicantly from 1.0. , mammals; , birds; **, reptiles; , invertebrates.

Conversely, allometry tends to be weaker or inconsistent with Renschs rule in clades with female-biased SSD. Abouheif & Fairbairn (2) reached similar conclusions based on a signicant correlation between the effect sizes from their meta-analysis and SSD for their 21 clades. The allometric slopes are not correlated with the within-clade range in SSD (Figure 2b, r34 = 0.12, P = 0.49). Thus, lack of signicant allometry does not signal lack of variance in SSD. Several taxa of Charadriiformes and the Tamias species cluster at the far left and show neither allometry nor variance in SSD. However, some clades, notably the Araneidae, Carnivora, Mustelidae, and Falconiformes, show no allometry in spite of a broad range of size dimorphism. In these taxa, SSD varies but is not sufciently correlated with overall size to generate a signicant allometric slope. The clades or taxa sampled have not been selected at random, and thus we cannot use these data to derive a quantitative estimate of the prevalence of allometry for SSD. In particular, plants are missing from our sample, invertebrates

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are severely underrepresented, and there are no aquatic organisms. However, the available evidence demonstrates that SSD is correlated with body size in many clades and is sufciently common to warrant further attention. Allometry consistent with Renschs rule is clearly the more common trend and tends to be both stronger and more prevalent in clades in which males are the larger sex. In contrast, allometry inconsistent with Renschs rule is uncommon, at least among the available samples, and appears to be restricted to clades in which females are the larger sex. A nal generalization from the empirical evidence is that even the most extreme allometry for SSD occurs in the presence of very strong covariation for body size between males and females. This implies that the pattern of evolutionary divergence leading to allometry among contemporary species consists primarily of correlated changes in size in males and females, allometry being produced because one sex (usually males) shows a greater magnitude of change than the other.

FUNCTIONAL HYPOTHESES FOR THE EVOLUTION OF ALLOMETRY FOR SSD 1. Allometry as a Functional Constraint
Allometry for SSD is merely a statistical description of the relationship between male and female body size and hence of the pattern of interspecic variation in SSD. The discovery of signicant allometry for SSD neither establishes a causal relationship between body size and SSD nor suggests the evolutionary mechanism that might produce such a relationship. Nevertheless, body size is often treated as one of a suite of variables potentially affecting SSD, the other variables typically being indices of natural or sexual selection such as mating system, diet, or habitat. In some cases each variable is considered independently (35, 38, 51), but more often adaptive hypotheses are tested using residual variation after body size effects are statistically removed (13, 21, 35, 44, 83, 84, 166) or body size is entered as one variable in a simultaneous analysis including other variables representing adaptive hypotheses (48, 141, 155). All of these approaches assume that body size explains some subset of the variation in SSD not explained by the postulated mechanisms of natural or sexual selection. The concept of considering allometry as distinct from adaptive patterns of divergence derives from the principle of functional similarity or size-required allometry (53, 113, 133). This principle refers to changes in the shape of structures or organs that must accompany changes in size to preserve the original function. For example, animals become increasingly stockier (i.e. bones become disproportionally thicker) as size increases. The allometric increase in bone cross-sectional area preserves the elastic strength of the bones so that the

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bones of larger animals are able to support the increased load without buckling (99). Such size-required allometry is clearly adaptive, but it describes changes in form required to maintain a given function. In this sense, it represents the functional constraints on shape imposed by changes in size. This is the meaning of the term allometric constraint. Changes in the function of organs and body components are, by extension, revealed as deviations from this size-required allometry. Hence, adaptive divergence in function is often assessed by analyses of residuals from allometric relationships (10, 19, 53). In the case of SSD, we have no a priori expectation of size-required allometry. What function is being preserved, and how does this translate into changes in SSD with size? Until these questions can be answered, it is premature to consider empirically derived allometric relationships for SSD as lines of functional equivalence, and hence, as representing allometric constraints (53). The observed divergence of SSD among species within a clade includes both the variance described by the allometric regression (i.e. the line of allometry) and the residual variance around this line; both components of variance require adaptive or functional explanation (35, 36, 53). Researchers who remove body size effects before testing functional hypotheses or include body size as one of a suite of functional variables predicting SSD may therefore be removing much of the variance that should be explained by their adaptive hypotheses.

2. Allometric Growth of Secondary Sexual Characters


Rensch (126) attributed allometry consistent with Renschs rule to allometric growth of secondary sexual characters in males. This hypothesis is frequently cited (6, 27, 124, 125, 155), but to my knowledge has never been explained. The extent to which allometry for secondary sexual characters is associated with allometry for SSD has not been determined, but even if it proves to be general, the juxtaposition of two statistical relationships does not constitute a functional hypothesis. Recent studies indicate that the allometric growth patterns of secondary sexual traits respond to selection (34, 163), and patterns of interspecic allometry for such traits are expected to evolve in response to selection on the traits concerned (168). It therefore seems unlikely that the allometry of secondary sexual characters represents a functional constraint on the evolution of SSD. More probably, this allometry is simply one aspect of the adaptive divergence of SSD. A functional hypothesis attributing allometry for SSD to the allometric growth of secondary sexual characters in males would have to include both an adaptive explanation for the pattern of allometric growth and a mechanism that could produce the required correlation between this growth pattern in males and the body size of females. In the absence of these components, Renschs hypothesis is only a description of allometric patterns, not a functional explanation for them.

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3. Correlated Response of Females to Sexual Selection on Males


One of the earliest and most pervasive hypotheses for the evolution of allometry consistent with Renschs rule is that female size evolves as a correlated response to sexual selection acting on male size (6, 37, 96, 112, 123, 155, 158). This expectation can be derived from basic quantitative genetic theory as follows. The direct response (R) of a trait to selection is given by h2i , where h2 is the heritability of the trait (additive genetic variance/total phenotypic variance), i is the selection intensity in standard deviation units, and is the phenotypic standard deviation of the trait (39). If a trait is expressed in both sexes, the response of each sex is due to the direct response to selection in that sex plus the correlated response to selection on the other sex: Rm = 0.5 h 2 m i m m + r h m h f i f m R f = 0.5 h 2f i f f + r h f h m i m f , 1. 2.

where r is the additive genetic correlation for that trait between the sexes and the subscripts m and f refer to male and female, respectively (39, 84, 123). If body size is measured on a log scale, as in the standard allometric model, allometry occurs whenever Rm = Rf (i.e. the ratio of body sizes before and after selection is not the same). Since the correlated response model only species sexual selection acting on males and a positive genetic correlation between the 2 sexes, we can simplify by setting h2 m = h f , m = f , and if = 0. The ratio Rm / R f then reduces to 1/r, indicating allometry that is inversely proportional to the genetic correlation between the sexes. (See 79 for a similar analysis of expected allometry for two traits correlated within individuals, and 21 and 84 for a similar analysis based on SSD measured as the difference between the sexes, with allometry assessed as SSD/female size.) In this scenario, female size changes only as a correlated response to selection on males. However, body size is unlikely to be a neutral trait (i.e. it is unlikely that if = 0), and most authors assume that female body size is at or near its natural selection optimum (80). As male size changes in response to sexual selection, natural selection on females is expected to slow and then reverse the correlated response of females, and females eventually return to their natural selection optimum while males stabilize at a size that balances the opposing forces of natural and sexual selection (80, Figure 3). Allometry consistent with Renschs rule is expected only during the very early stages of evolutionary divergence (Figure 3). At equilibrium this model predicts no correlation between male and female body size and no allometry for SSD (33, 80, 168).

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Figure 3 Typical theoretical trajectory for the evolution of male and female body size in response to sexual selection for increased size in males, based on Landes quantitative genetic model (80, 123; J Reeve, unpublished data). With the exception of sexual selection, all parameters are the same for males and females. Natural (stabilizing) selection favors a body size of 10.0, the heritability of body size is 0.5, and the genetic correlation between the sexes is 0.9. Altering the model parameters alters the rate, duration, and maximum response to selection but does not change the basic shape of the trajectories.

Genetic correlations between the sexes are therefore unlikely to account for the widespread occurrence of allometry for SSD.

4. Variance Dimorphism
Cheverud et al (21) and Leutenegger & Cheverud (83, 84) used the same quantitative genetic model to derive the hypothesis that allometry for SSD can evolve solely as a consequence of differences between the sexes in the phenotypic variance for body size. Since the heritability of body size is set as equal in the males and females in the model, it is important to note that dimorphism in phenotypic variance implies dimorphism in additive genetic variance, a point that is insufciently stressed in the original papers. To illustrate the effect of 2 variance dimorphism, set im = if , and h2 m = h f in Equations 1 and 2, and dene allometry as before as Rm/Rf =1. The response ratio reduces to m/ f , indicating that allometry now depends only upon the standard deviations of body size in each sex. Leutenegger & Cheverud (83, 84) used a difference rather than ratio measure of SSD and concluded that allometry is enhanced by both variance dimorphism and high genetic correlations between the sexes. However, the inuence of the genetic correlation is not evident for allometry based on size ratios. The key aw in this model as a general explanation for allometry is that it predicts only transitory allometry as one sex responds faster than the other to the same direction and intensity of selection. No allometry is predicted at equilibrium. Further, while the sexes initially diverge in size, SSD will decline as the

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slower responding sex approaches equilibrium, producing a reversal of the allometric pattern along any given trajectory. Although Leutenegger and Cheverud (21, 83, 84) argue that variance dimorphism may be responsible for the strong allometric trend seen in primates, empirical evaluations of this hypothesis in other clades have produced negative results (35, 123, 155). Thus, it seems unlikely that variance dimorphism accounts for the evolution of allometry for SSD.

5. Large Size Facilitates the Evolution of SSD


Hypotheses in this category assume that natural selection acts similarly on males and females to produce both the interspecic divergence in mean body size and the covariance in body size between males and females. Allometry for SSD then evolves because large size itself facilitates the evolution of SSD by (a) promoting polygyny and thus increasing the intensity of sexual selection (82, 162); (b) facilitating response to sexual selection (27, 48); or (c) increasing the probability that sexual selection will act on body size rather than some other trait such as plumage, color, or vocalization (22, 44, 48, 135). The mechanism by which an increase in mean size promotes polygyny is not specied, and the rst hypothesis therefore lacks theoretical justication. The second hypothesis derives from the assumption that energetic or competitive constraints on increasing size are relaxed in larger species (27, 48), an assumption that has not been supported analytically or empirically (124, 125). However, several arguments support the third hypothesis. Gaulin & Sailer (48) argue that the effectiveness of weapons and of contests of strength increases with body size because the energy that can be delivered by a blow increases faster with size than the ability to absorb the energy from that blow. Clutton-Brock (22) argues that, as size increases, strength increases but agility declines, leading larger species to rely more on tests of strength, and smaller species to rely more on agility and display. Finally, Shine (135) argues that large size reduces the risk of predation and thus increases the probability of sexual selection through male-male combat (the assumption being that combatants suffer increased predation risk). Therefore, it may be that as size increases within a clade, sexual selection is more likely to target size rather than some other male trait, resulting in allometry for SSD consistent with Renschs rule.

6. Resource Distribution Inuences Both Body Size and SSD


The central assumption of hypotheses in this category is that body size and SSD covary because both are inuenced by the distribution of resources (4, 27, 155). For example, Clutton-Brock et al (27) suggested that dispersed, unpredictable food resources might favor both large size and intersexual niche divergence in primates. However, this hypothesis has been criticized on the grounds that it

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predicts greatest SSD in monogamous species and so is not consistent with the general relationship between SSD and polygygny (48, 124, 125). Alternatively, the key resource may be females rather than food. Mating systems associated with a clumped distribution of breeding females favor monopolization of many females by individual males, thus facilitating sexual selection for large males (4, 155). Webster (155) proposed that breeding aggregations may also favor large size in females, because larger females are more successful in intrasexual competition. This hypothesis predicts allometry for SSD only if female dispersion has a proportionally greater effect on male size than on female size, and it excludes many taxa in which allometry occurs in the absence of breeding aggregations (i.e. 2, 5, 13, 51, 74, 112, 139). It is therefore unlikely to provide a general explanation of allometry for SSD.

7. Stabilizing Selection on Females


Several authors have suggested that reproductive selection on females opposes further increases or decreases in female size at the extremes of size within a clade (6, 27, 58, 121, 155). Thus, in large species with very large males, selection should favor females that are small relative to their mates. At the other extreme, if males are very small, selection should favor females that are large relative to their mates. Because sexual selection on males is not expected to alter the equilibrium body size of females (80, 143), this hypothesis actually predicts covariation of male and female body sizes only if the diversifying selection is natural selection acting on both sexes. If the diversifying selection is sexual selection on males, no allometry is predicted. This contrasts with the predictions of most of the previous hypotheses and with the empirical evidence of a strong association between allometry and sexual selection (e.g. 2, 13, 27, 37, 44, 48, 112, 139, 155), and thus it seems unlikely that stabilizing selection alone accounts for the observed patterns of allometry for SSD.

8. Correlational Selection
All of the preceding hypotheses assume that, at equilibrium, the selective forces affecting body size in each sex are independent of the size of the other sex. This concept is implicit in the verbal hypotheses and explicit in the quantitative genetic models (21, 80, 83, 84, 123, 143). However, in many clades such independence seems unlikely (18). If one sex carries the other during courtship or mating, or if mating pairs remain physically joined for prolonged periods, as in many invertebrates, the mating success of males may depend signicantly on their size relative to their mates (3, 11, 15, 30, 35, 93, 105). Similarly, if males must physically overcome female reluctance to mate, the mating success of males, the energetic cost of the struggle, and the risk of injury to both sexes are likely to be inuenced by the relative sizes of the struggling pair (9, 132, 156).

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The size ratio of mating pairs may also inuence the proportion of eggs fertilized in a given clutch and so directly impact female tness (11, 15). Even in the absence of correlational selection due to mating interactions, sexual selection favoring large males may be accompanied by selection favoring large females because larger females tend to produce larger sons (25, 155). The general correlation between mothers size and the size of eggs, neonates, and juveniles (6, 18, 113, 120, 130) suggests that any selection favoring larger males will ultimately favor larger size in mothers. If, as suggested by these examples, the optimal body size in one sex is inuenced by the mean size of the other sex, changes in the size of one sex will be accompanied by selection favoring correlated changes in the size of the other sex. This model is analogous to Zengs quantitative genetic model for the evolution of allometry among traits within individuals, which predicts that, although patterns of genetic correlation among traits inuence the evolutionary trajectories, the allometric pattern at equilibrium is determined only by the patterns of correlational selection (168). Although Zeng did not specically consider the evolution of SSD, his model would predict allometry consistent with Renschs rule whenever interspecic divergence in size was due to directional selection on males, with weaker, correlational selection on females. If the diversifying directional selection acts primarily on females (e.g. fecundity selection in spiders or butteries; 66, 161), allometry inconsistent with Renschs rule is expected, as males show the lower response to correlational selection. The correlational selection hypothesis has the advantages of being consistent with quantitative genetic theory and at the same time predicting covariance in size between the sexes, greater interspecic variance in one sex than the other, and allometry for SSD at equilibrium. It is also one of the few hypotheses capable of predicting allometry inconsistent with Renschs rule. It shows promise as a general, unifying hypothesis for the evolution of allometry for SSD but may be difcult to distinguish empirically from hypotheses in categories 5 and 7, which assume that the covariation between the sexes is caused by similar patterns of natural selection on males and females, rather than by correlational selection between sexes.

TESTING HYPOTHESES FOR THE EVOLUTION OF ALLOMETRY FOR SSD


Most of the functional hypotheses for the evolution of allometry for SSD suffer from a lack of both theoretical rigor and empirical validation, and they remain essentially post-hoc explanations for allometry within a given clade. Further, many of these hypotheses incorporate the same variables and differ mainly in the order of cause and effect. For example, hypotheses in category 5 assume

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that large size facilitates the evolution of SSD in response to sexual selection (i.e. sexual selection causes increased SSD only in species whose average size is initially large), while the correlated response hypothesis (category 3) assumes that sexual selection on males causes a correlated increase in both mean size and SSD. Is large average size a cause or a consequence of sexual selection? Similarly, does a clumped distribution of females promote polygyny and thus sexual selection for large size in males (category 6), or does large size of males promote polygyny (category 5[a]) Because these competing hypotheses were derived to explain similar patterns of correlation among mating systems, body size, and SSD, they cannot be distinguished by a purely correlative approach. Directional comparative analyses that seek to determine the order of appearance of traits within a phylogeny (17, 64, 91, 128) hold more promise of distinguishing among the various hypotheses. H oglund (69) and Oakes (109) used this approach to test the hypothesis that lekking promotes the evolution of SSD in birds through increased sexual selection for large males (69, 112, 162). If this hypothesis is correct, cladistic analysis should reveal that the evolution of lekking is followed by the evolution of increased male size and SSD. Unfortunately, H oglund concluded that lekking did not precede dimorphism more often than the reverse, while Oakes concluded that SSD is more likely to evolve when birds lek (109), and so the controversy is not yet resolved. However, Oakes provides an excellent comparison of the two studies, as well as explanations of the statistical problems associated with directional phylogenetic analyses. His study provides a good starting point for similar tests of hypotheses for the evolution of allometry for SSD within other clades. A second promising approach to hypothesis testing in this area is construction of quantitative models to determine the plausibility of the proposed evolutionary mechanisms. For example, Reiss (124, 125) used simple analytical models to show that the degree to which the evolution of SSD is constrained by interspecic competition or by energetic requirements is expected to be independent of species size, contrary to the assumptions made by Clutton-Brock et al (27; category 5[b]). Similarly, the quantitative genetic models derived by Lande (80) and Cheverud et al (21) demonstrate that neither the correlated response hypothesis (category 3) nor the variance dimorphism hypothesis (category 4) are sufcient to generate persistant interspecic allometry for SSD. In these examples, quantitative modeling suggested that the prior verbal models were not plausible. In contrast, Zengs quantitative genetic model for the evolution of allometry of correlated traits within individuals (168) provides the theoretical justication for the hypothesis that allometry for SSD is a function of correlational selection (category 8). Quantitative models can also greatly facilitate hypothesis testing by providing estimates of constituent parameters, evolutionary trajectories, and equilibrium

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distributions that can then be compared to data collected from nature or from manipulative experiments. For example, although neither the correlated response hypothesis nor the variance dimorphism hypothesis predict allometry for SSD at equilibrium, they do predict allometry during the initial period of divergence of species from a common ancestor. Reeve & Fairbairn (123) used these models to predict the short-term evolution of mean size and SSD in Drosophila melanogaster in response to articial selection on thorax width. Although body size responded well to selection, the response in SSD was consistently less than predicted by either model, and selection did not produce the predicted allometry for SSD among selected lines. Thus, these models are insufcient to account for even the short-term evolution of allometry. Ultimately, our ability to test functional hypotheses for the evolution of allometry, whether through comparative analyses or the application of quantitative models, depends upon the accuracy with which the relevant parameters are estimated within species. Lack of accurate, quantitive estimates of the pattern and intensity of selection is a serious limitation throughout most of this literature. For example, sexual selection is typically reduced to a simple categorical classication of mating systems as monogamous (presumably low intensity of sexual selection) or polygynous (presumably high intensity of sexual selection) (5, 13, 21, 69, 75, 82, 83, 109, 112, 141). Other surrogate measures such as level of competition between males for access to mates (44), presence or absence of male combat (138, 139), number of matings per male (155), and socionomic sex ratio (27) have also been used. All but the latter two indices provide very little power because the presumed driving variable, sexual selection, is reduced to an ordinal variable with few classes. Further, using any of these indices as estimates of sexual selection on body size presupposes that sexual selection uniformly targets body size rather than other traits such as song, color, or vigor, an assumption that is unlikely to be correct (22, 44, 48, 135). The ability of such analyses to detect underlying functional relationships between sexual selection on body size and SSD is questionable, at best. Fairbairn & Preziosi (37) provide an example of a more rigorous approach. To test the hypothesis that allometry for SSD among populations of the water strider, Aquarius remigis, is caused by sexual selection on males, they estimated sexual selection gradients (81) for male total length in 12 wild populations and found the predicted positive correlation between the magnitude of sexual selection for large size and mean male size across populations. This study illustrates the potential for more accurate comparative analyses of the relationships among selection intensity, body size, and SSD. At present, we suffer from a surfeit of functional hypotheses for the evolution of allometry for SSD, and a clear deciency of rigorous, quantitative tests of these hypotheses. While strictly correlational studies may still be valuable,

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particularly within less-studied clades, they will not be sufcient to sort out the morass of overlapping hypotheses. Signicant progress in this direction is likely to be achieved only through a combination of more accurate parameter estimation, quantitative modeling, and directional comparative techniques that estimate the order of appearance of traits within a phylogeny.

SUMMARY AND CONCLUSIONS


Sexual size dimorphism varies greatly in direction and degree, both among and within clades. Given the importance of body size in the ecology, life history, and reproductive tness of most organisms, patterns of interspecic variation in body size are expected to reect patterns of adaptive divergence. This is true not only for the mean size of species, but also for the sizes of males and females, respectively. Quantitative genetic theory leads us to expect independent adaptation of males and females to the net selection acting on each sex. At equilibrium, therefore, each sex should be at its optimal size, and SSD should, in this sense, be adaptive. By extension, the patterns of variation in SSD among species should reect differences in the patterns of adaptive divergence of males and females. In many clades, interspecic variation in SSD is correlated with body size. When this variation is presented using the statistical methods of standard allometric analysis, it translates into slopes that deviate signicantly from one when the size of one sex is plotted against the size of the other sex on a logarithmic scale. Such analyses reveal a predominant allometric pattern characterized by a strong correlation for body size between males and females and greater interspecic variance in male size than in female size. This pattern occurs in taxa as disparate as water striders and primates, increases in body size being associated with increasing SSD where males are the larger sex, and with decreasing SSD where females are the larger sex. Rensch (126) was the rst to describe this general pattern, and it has been summarized as Renschs rule. Although found in some clades in which females are larger than males, allometry consistent with Renschs rule is more common where males are the larger sex, and exceptions (i.e. allometry in which females vary more among species than do males) have been found exclusively in taxa with female-biased SSD. We have no a priori reason to expect that allometry for SSD reects patterns of functional constraint or nonadaptive divergence. In the absence of evidence to the contrary, we must assume that the observed allometric patterns reect evolutionary divergence in response to the same selection that produces SSD within individual species. Therefore, selection associated with the different reproductive roles of the two sexes is likely to play a key role. Not surprisingly, almost all of the functional hypotheses for the evolution of allometry for SSD

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have invoked either sexual selection on males or reproductive selection on females, and it seems likely that the former is an important component of the evolutionary mechanism responsible for allometry consistent with Renschs rule. Many functional hypotheses have been proposed to explain the evolution of allometry for SSD, but few have been adequately tested. Many of these hypotheses incorporate the same variables (e.g. sexual selection, mating system) and differ mainly in the postulated order of cause and effect. They therefore cannot be distinguished by simple analyses of correlations among variables. Directional comparative analyses that estimate the order of appearance of traits within a clade hold more promise. Quantitative modeling of the proposed evolutionary mechanisms also holds promise as a tool for both assessment of the plausibility of the verbal hypotheses and generation of testable, quantitative predictions. However, in addition to the difculty of rigorously testing and distinguishing among these hypotheses, many of them are specic to a given clade and lack sufcient generality to account for the observed prevalence and pattern of allometry for SSD. A satisfactory general hypothesis must be applicable to a wide range of taxa, regardless of mean body size or direction of SSD, and must explain both the covariance of male and female size and the greater interspecic variance in one sex than the other. Hypotheses based on quantitative genetic models for the evolution of SSD (the correlated response and variance dimorphism hypotheses) hold the promise of generality, but they predict neither allometry at equilibrium nor a consistent pattern of allometry along the evolutionary trajectory. The correlational selection hypothesis derived from a quantitative genetic model for the evolution of interspecic allometry is more promising. According to this hypothesis, interspecic allometry for SSD evolves as a consequence of directional selection acting primarily on one sex (e.g. sexual selection on males or fecundity selection on females) combined with correlational selection on the other sex. This hypothesis appears to satisfy the requirements of a general model but has yet to be tested empirically. Allometry for SSD is clearly a conspicuous component of patterns of variation in SSD among species. While factors inuencing the evolution of SSD have intrinsic interest for many ecologists and evolutionary biologists, studies of allometry for SSD have an even broader appeal. As indicated by the plethora of hypotheses summarized above, attempts to understand the evolution of allometry for SSD force us to address many of the central issues of evolutionary biology such as adaptation versus constraint, equilibrium versus non-equilibrium models, and evolutionary mechanisms governing the correlated evolution of suites of traits. It is my hope that, by drawing together analytical techniques, empirical evidence, and current hypotheses, this review

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will encourage a transition from hypothesis generation to hypothesis testing, and so set the stage for greater understanding not only of the evolution of allometry for SSD, but also of these issues of broader signicance to evolutionary biology. ACKNOWLEDGMENTS I thank J Reeve and A Abouheif for many lively and insightful discussions, for constructive comments on an earlier draft of the manuscript, and for allowing me access to unpublished data and analyses. The work was supported by the Natural Sciences and Engineering Research Council and Canada (individual research grant number OGP0000347).
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