Przegld Antropologiczny Anthropological Review Vol.

67, 33-55 (2004)

Methods to estimate sexual dimorphism from unsexed samples: A test with computer-generated samples
Krzysztof Kociski, Sergiusz Pietraszewski
Institute of Anthropology, Adam Mickiewicz University, Umultowska 89, 61-614 Pozna, Poland; E-mail: dser@go2.pl

ABSTRACT Sexual dimorphism can provide information on behavioral and ecological characteristics of extinct species. However, estimation of sexual dimorphism becomes very difficult, as identification of sex in skeletal specimens is often impossible. Several methods have been developed to estimate dimorphism from unsexed data: mean method, median method, finite mixture analysis (FMA), method of moments (MoM), binomial dimorphism index (BDI), coefficient of variation (CV) method, and assigned resampling method (ARM). We tested the methods using computer-generated samples of given size and having descended from virtual populations of strictly defined parameters. The analysis showed that precision of estimating sexual dimorphism was affected by small sample size, unbalanced sex ratio, and increased intrasexual CV (but not by skewness). Mean and CV methods turned out to be the best ones in most circumstances. CV is the best method when within-sex CV value is assumed accurately. In conditions of low within-sex CV (about 5%) and large sample size (about 50 or more) MoM proved to be the best method. However, in most situations, the error of estimation resulted mainly from sampling error, not from the error of method, so we believe that rather than seeking new methods or improving existing ones, one should accept the impossibility of precise estimation of sexual dimorphism from unsexed fossil samples. KEY WORDS sexual dimorphism, primates, hominids, fossils, estimation, drawing
Prz. Antropol.Anthropol. Rev. (2004), vol. 67, pp. 33-55, Figs. 2, Tables 13. ISBN 8389529-05-X, ISSN 0033-2003

Introduction
Sexual dimorphism among living vertebrates, especially primates, is closely related to ecological characteristics such as mating system (and associated be-

havior), social organization, operational sex ratio and competition level [CLUTTON-BROCK et al. 1977, PLAVCAN 2000, LEE 2001]. Therefore, sexual dimorphism can also be used for predicting the characteristics of extinct primate

34

K. Kociski, S. Pietraszewski

species [MARTIN 1977, LEUTENNEGER and KELLY 1977, FLEAGLE et al. 1980, GINGERICH 1981, KAY 1982a, RUFF et al. 1989, KRISHTALKA et al. 1990, SIMONS et al. 1999], especially hominids [LOVEJOY 1981, MCHENRY 1992, KRAMER 1993, MCHENRY 1994, RICHMOND and JUNGERS 1995, LOCKWOOD 1996, PLAVCAN and VAN SCHAIK 1997a, LOCKWOOD 1999, LARSEN 2003, RENO et al. 2003], but the prediction methods need updating and are far from perfect [PLAVCAN 2000, 2001]. For example, different traits may display different degrees of dimorphism [OXNARD 1982]. In some species of primates, for example, canine tooth dimorphism is strong, but other craniodental traits show little or no sexual dimorphism [FLEAGLE et al. 1980, KRISHTALKA et al. 1990]. On the other hand, another hominid species of moderate or high body size dimorphism can represent slight canine dimorphism [LEUTENEGGER and SHELL 1987, MCHENRY 1991, RICHMOND and JUNGERS 1995]. This renders inferring ecological characteristics of a species from sexual dimorphism ambiguous. Dimorphism in canine tooth size and body weight is associated with intrasexual competition and variation in mating system [CLUTTON-BROCK et al. 1977; HARVEY et al. 1978; FOLEY and LEE 1989; MCHENRY 1992; PLAVCAN and VAN SCHAIK 1992, 1997b; PLAVCAN et al. 1995; PLAVCAN 2000]. Usually, the most dimorphic species tend to practice polygyny and have a social organization that depends on male dominance, while the less dimorphic species are organized in family groups and are monogamous. Comparison of patterns of dimorphism in many primate species, which are dimorphic in morphological characters,

can also be useful for interpreting the taxonomic variation in extinct species or fossil record [PLAVCAN 2002] which can be helpful in accurate assignment of fossil specimen to species [COPE and LACY 1994a, KELLEY and PLAVCAN 1998]. Assessment of sexual dimorphism of a species can be done only on the basis of a sample(s) of the species. A common problem is that fossil samples are usually small, which makes them unrepresentative of the population. Fossil records from one site are often a mixture of species, sexes and specimens, which presents another problem. Determination of sexual dimorphism in a sample requires knowledge of sex of its specimens. Unfortunately, it is often the case that no qualitative sex markers exist or are preserved and quantitative traits are not precise sex indicators. In conditions of impossibility of sex assignment one cannot determine sexual dimorphism using traditional methods that just assume knowledge of the sex of individuals. Hence, several methods that do not rely on the assumption but make use of unsexed data have been developed: mean method, median method, finite mixture analysis, method of moments, binomial dimorphism index, coefficient of variation method, and assigned resampling method [FLEAGLE et al. 1980; KAY 1982a,b; GODFREY et al. 1993; PLAVCAN 1994; JOSEPHSON et al. 1996; KRAMER and KONIGSBERG 1999; REHG and LEIGH 1999; LEE 2001]. All these methods are aimed to estimate sexual dimorphism on the basis of one quantitative trait of specimens with unidentified sex. However, contrary to some opinions in the literature [PLAVCAN 1994, LEE 2001], the estima-

Methods to estimate sexual dimorphism from unsexed samples

35

tion is not trivial even when combinedsex distribution of a quantitative trait is bimodal. This is because the peaks of the distribution are not equal to sex means, so computing ratio for peak values yields a biased dimorphism estimation (Fig. 1).

Description of methods tested

We tested seven methods aimed to estimate sexual dimorphism from unsexed samples: mean method (MeanM), median method (MeM), finite mixture analysis (FMA), method of moments (MoM), binomial dimorphism index (BDI), coefficient of variation method (CVM), and assigned resampling method (ARM). Below we briefly outline each of them, putting emphasis on their algorithm and assumptions. Mean method (MeanM) This, along with median method, is the simplest way to estimate sexual dimorphism in a sample [GODFREY et al. 1993, PLAVCAN 1994, JOSEPHSON et al. 1996, REHG and LEIGH 1999]. The sample with ordered data is divided into two subsamples at the sample mean. The subsamples are assumed to be males (above mean) and females (below mean) separated from each other. Thus, the means of the subsamples are regarded as means for each sex and sexual dimorphism is calculated as their quotient. The method makes no assumptions on the distribution of the analyzed variable. However, the assumption that the sample mean ideally separates male data from female ones is met only in cases when distributions of sexes overlap minimally or not at all. Therefore, one can suppose that MeanM performs better under conditions of substantial sexual dimorphism and small sex-specific variation. On the other hand, in case of lack of dimorphism, MeanM artificially creates male and female means that differ from each other, and thereby states the presence of dimorphism.

Fig. 1. Female and male distributions of a trait (black lines) produce a distribution observed in combined-sex samples (gray line). Notice that peaks of the combined bimodal distribution are not equal to the sex means.

In this paper we review and test the methods using computer-generated samples of a given size and which have descended from virtual populations of strictly defined parameters, such as sex ratio, coefficient of skewness and coefficient of variation. To determine goodness of the methods, sexual dimorphism in a sample is estimated with each method, and the estimates obtained are set against the true value of dimorphism. The closer to the actual sexual dimorphism a method's estimate is, the better the method is. Precision of estimation of dimorphism in a population by a method depends on two factors: accuracy of the method in determining dimorphism in a sample and similarity of the samples dimorphism to that of the population. Therefore, we examined also the relation between dimorphism in a population and in a sample drawn from it.

36

K. Kociski, S. Pietraszewski

Median method (MeM) This method is very similar to MeanM but it divides the sample at the median and not at the mean. It assumes that each male measurement is larger than any female one (as does MeanM) and also that the numbers of males and females in the sample are equal. Similar to MeanM, MeM fixes male mean greater than female mean, even if they are equal in the sample. Finite mixture analysis method (FMA) This method was proposed by GODal. [1993] and, unlike the others, it was designed to assess not exact but maximum dimorphism that could be present within a unimodal distribution. Therefore, it is reasonable not to use this method for bimodal distributions. The essence of the method is to determine mean number of sample standard deviations (SDs) in sample range for different sizes (k values in Table 1) and to find dependencies among (1) sample SD, (2) a sex SD, and (3) amount of difference between sex means. The considerations assume (1) normality of distribution, (2) equal numbers of both sexes, (3) equal SDs of both sexes, and (4) unimodal distribution of combined-sex sample. The procedure of estimating sexual dimorphism is the following: (1) From Table 1 get k value appropriate to sample size n. (2) Calculate sample range R = maximum minimum. (3) Calculate distance between sample mean and a sex mean = R / k 2 . (4) Maximum sexual dimorphism (assuming unimodal distribution) is then ( x + ) /( x ) .
FREY et

Table 1. Mean number of sample SDs in sample range for different sample sizes n (from GODFREY et al. 1993). The values are used by FMA method. n 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 35 40 45 50 55 60 k 3.08 3.17 3.26 3.34 3.41 3.47 3.53 3.59 3.64 3.69 3.73 3.78 3.82 3.86 3.90 3.93 3.96 4.00 4.03 4.06 4.09 4.21 4.32 4.42 4.50 4.57 4.64

Method of moments (MoM) MoM was proposed by JOSEPHSON et al. [1996]. The method assumes normality of distribution, equality of SDs of sexes, and equality of numbers of the sexes. MoM makes use of the fact that the greater the difference between means of sexes is, the less the 4th moment about the origin calculated for a pooled-sex sample (this moment is given by the formula m4 = xi4 / n ). The sexual dimorphism is estimated in the following way:

Methods to estimate sexual dimorphism from unsexed samples

37

(1) Ln-transform sample data, yi = Ln(xi). (2) Standardize Y variable, u i = ( y y ) / SDY . (3) Calculate m4 for U variable. (4) Calculate D = 3/2 m4/2. If D < 0 then D = 0. (5) Sexual dimorphism is equal to Exp(2 SDY D1/4). Binomial dimorphism index method (BDI) This method was proposed by LOVEJOY et al. [1989] as Technique Dimorphism, and subsequently referred to as Binomial Dimorphism Index [RENO et al. 2003]. Here it is assumed that (1) each male in a sample is bigger than any female in the sample, (2) both sexes are present in the sample, and (3) probability of being female is 0.5. So, for a sample of size n there could be 1 or 2 or ... or n-1 females, i.e., n-1 possibilities. For each possibility we can compute sexual dimorphism:

Coefficient of variation method (CVM) This method relies on the fact that variation in the pooled-sex sample increases with sexual dimorphism. Some studies [FLEAGLE et al. 1980; KAY 1982a,b; LEUTENEGGER and SHELL 1987] showed very high correlation between sexual dimorphism and coefficient of variation (CV = SD / x 100%) of combined-sex sample in extant species. This makes it possible to estimate sexual dimorphism in extinct species, because we can always calculate CV in unsexed samples. However, the relation between a sample CV and sexual dimorphism depends on the within-sex CV. Since most fossil remains are teeth, PLAVCAN [1994] determined average primates postcanine teeth within-sex CV to be 5.5% and calculated the equation for predicting sexual dimorphism with pooled-sex CV (expressed as percentage): SexDim = Exp(0.0214 CV 0.047) The equation is as good as the value of 5.5% corresponds to the value of the within-sex CV in the population. In particular, one should assess the parameter for the studied extinct species by analogy to its living relative and, if necessary, change parameters in the equation above. CVM is the only method that needs extant species as analogs to estimate sexual dimorphism in extinct ones. On the other hand, the method does not make such assumptions as normality of distribution, equal numbers of sexes in sample etc. Assigned resampling method (ARM) ARM was proposed by LEE [2001] and consists in repeated drawing (with

SexDimk =

i = k +1

x x
i i =1

where k is the number of females and data are sorted in ascending order. Then we calculate a weight (Wk) for each SexDimk, which is the probability of the presence of k females in n-specimen sample. From binomial distribution we get:
W k = n! [ k!( n k )!] 0.5 k 0.5 n k

The final estimate of sexual dimorphism is the weighted mean of SexDims:

SexDim = ( SexDim k Wk ) / Wk

38

K. Kociski, S. Pietraszewski

replacement) pairs of elements from a sample and taking their ratios. The average ratio is to be an estimate of sexual dimorphism. The algorithm of ARM is as follows: (1) Draw two specimens from sample, it gives xa and xb values. (2) If both xa and xb are less than (x 0.5 SD) or both xa and xb are greater than (x + 0.5 SD), then the pair is considered invalid (go back to step 1). (3) Divide greater from xa and xb values by smaller of them, this gives ratio r. (4) Repeat steps 1-3 1000 times and calculate mean r which is an estimate of sexual ratio in the sample. ARM is the only method that makes no assumptions, either on type of distribution or sample sex ratio or within-sex variation of a studied trait.

Materials and methods

In order to assess the goodness of methods for estimating sexual dimorphism from unsexed samples we decided to use virtual samples generated with a computer program rather than actual ones. Inferring from natural samples is risky when one method is better than the other for one sample, but worse for another. The number of real samples we have is very limited; besides, having a natural sample, we test the methods in conditions set by parameters of the sample. On the other hand, virtual samples may descend from population with whatever values of parameters we want. In the study, samples were generated with a computer program written by one of the authors (KK) in Visual Basic

programming language. One program simulation runs the following steps: (1) User sets female and male popu lation means, xf and xm, or sexual dimor phism and one of the means. Sexual dimorphism is a function of means of two sexes. From among many formulae for sexual dimorphism [BORGOGNINI and REPETTO 1986] we used the simplest one, SexDim = xm/ xf, similar to many other papers on estimating sexual dimorphism from unsexed samples. After each users change of one of these parameters the program alters another one so as to ensure the formula is met. (2) User sets some other parameters of population: female and male standard deviation (SD) or coefficient of variation (CV), skewness, and sex ratio. In the paper, sex ratio means percentage of males, but not quotient males to females. (3) Now all necessary parameters of virtual population are set. In order to draw virtual samples from it, the user should specify number of samples to draw (k) and size of the samples (n, number of elements in each sample). (4) There are two approaches to set the sex of generated elements. Firstly, each element becomes male with a given probability (e.g., 0.5), thus producing sample with random value of sex ratio. Secondly, the fraction of males in the sample is fixed, so sex ratio must be equal to a specific number. Drawing of the sex reflects phenomena occurring in reality, but fixed sample sex ratio makes definite the conditions for testing of the methods. In the study, samples were generated in both of these ways. We did not take into consideration taphonomic processes that may skew sex ratio by preferentially preserving the more ro-

Methods to estimate sexual dimorphism from unsexed samples

39

bust, dense (and likely male) specimens from initial assemblage [JOSEPHSON et al. 1996]. Resolving this could be done by using traits that are less sensitive to taphonomic skewing, e.g., teeth [LYMAN 1985]. (5) According to set parameters, the program generates k samples of size n. Elements values are drawn assuming normal distribution of a trait with mean and SD appropriate for given sex. For each sample, sexual dimorphism (SexDim) is calculated as well as estimated by the seven above-described methods which do not know sex of any specimen in the samples. For both sample SexDim and estimated SexDims some statistics are calculated: mean SexDim, standard deviation of SexDim and standard error of SexDim with regard to population SexDim:
SE j =
th

(SexDim
i =1

i, j

SexDimpop ) 2 / k ,

for j method. The goal of a researcher using a method is to assess sexual dimorphism of the species under study. Thus, the closer a methods mean SexDim to population SexDim is (less bias of the method), the better the method is. In addition, the smaller a methods SD of SexDim is, the better the method is. The two criteria of goodness of a method may be divergent (one method could have less bias, the other less SD), so we introduced SE as the third criterion which depends both on bias and SD of a method, which thus can be decisive in vague situations. Therefore, bias together with SE sufficiently characterizes goodness of a method, yet we computed SDs as well for the purposes of compari-

son with SDs obtained by PLAVCAN [1994]. We tested all methods in many situations that were combinations of values of population parameters. The values were as follows: sample size: 10, 20, 50; sex ratio: 0.2, 0.5, 0.8; coefficient of skewness: -0.5, 0, 0.5; coefficient of variation: 5%, 10%, 15%. This yielded 81 combinations; for each of them seven methods of estimating sexual dimorphism from unsexed samples were compared in respect of mean of assessed SexDim and its SE. For each combination a comparison of methods was carried out for the following levels of sexual dimorphism: 1.0, 1.1, 1.2, 1.3, 1.5, 1.8. Choice of which method to employ should not depend on SexDim in a population because this is not known to a researcher who wants to assess its level. That is why our choice of best method relied on its averaged performance in various levels of SexDim, for given sample size, sex ratio, skewness and within-sex CV. For high precision of inferring we generated k = 1000 samples for each simulation (see Fig. 2). Even an ideal method cannot precisely determine sexual dimorphism in population when its sample value differs substantially from that of the population. We analyzed differences between sample and population values of sexual dimorphism as related to sex ratio, trait skewness, its CV, and sample size. For various combinations of the parameters values we generated 1000 random samples and calculated SE of sample SexDim with respect to population SexDim. Some samples may, by chance, consist of individuals of one sex only. Then, sexual dimorphism does not exist and any attempt to estimate it makes no sense.

Values of parameters: - sample size: 10, 20, 50 - sex ratio: 0.2, 0.5, 0.8 - skewness: , 0, + - within-sex CV: 5, 10, 15 % give 3 3 3 3 = 81 combinations 1 . . . . . . . . . 2 81

For each combination 6 levels of sex. dim. are considered 1.0 1.1 1.2 1.3 1.5 1.8

3 . . . . . . . . . Sex dim. in sample: assessed with method 1 2 ... 7 . . . . . . . . . . . . . . . . . .

In each level of sex. dim. 1000 samples are generated 1 2 1000

bias

SD

SE

For each sample compute sex. dim. and assess it with each method. Compute biases, SDs and SEs for sample and for each method.

Biases, SDs and SEs for all levels of sex. dim. make average performance of each method in given combination of parameters. Comparison of methods in a combination is based on the averaged performances.

1.0

1.1

1.2

1.3

1.5

1.8

Fig. 2. Conceptual scheme of evaluation of methods.

Methods to estimate sexual dimorphism from unsexed samples

41

We computed the probability of obtaining such a unisex sample, given by formula pn + (1 p)n, where p is percentage of males in a population and n is the sample size.

Results
Initial conditions We begin the presentation of results from a situation of large samples (n = 50) drawn from a population of balanced sex ratio (0.5). The analyzed trait has intra-sex CV = 5% and is characterized by normal distribution (without skewness). This seems to be the optimal conditions for good estimation of sexual dimorphism and almost all methods precisely determine the population sexual dimorphism for the whole analyzed range of its values (1.0 to 1.8, see Table 2).

The estimation is worst for lack of sexual dimorphism (SexDim) when all methods overestimate by 0.05-0.08. All methods, except MeanM, underestimate for SexDim 1.3. Generally, bias of methods decreases as sexual dimorphism increases, being positive for SexDim equal 1.0 or 1.1 and zero or negative for greater values of sexual dimorphism. The best method proves to be MoM. It is characterized by far the smallest overestimation for lack of sexual dimorphism and it is the only method with no bias for SexDim = 1.1. For substantial values of sexual dimorphism (SexDim 1.5) it underestimates slightly. The second best method is CVM. It has somewhat bigger positive bias for small SexDim and slightly bigger negative bias for a large one. Slightly less accurate than CVM is MeanM. It is the

Table 2. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 50, sex ratio = 0.5, no skewness, within-sex CV = 5%. Sex. dim. Sample 1.0 0.001 1.1 -0.001 1.2 0.002 1.3 0.001 1.5 0.000 1.8 0.000 1.0 0.012 1.1 0.014 1.2 0.015 1.3 0.018 1.5 0.017 1.8 0.020 1.0 0.012 1.1 0.014 1.2 0.015 1.3 0.018 1.5 0.017 1.8 0.020 MeanM 0.083 0.018 0.004 0.000 0.000 0.000 0.009 0.010 0.013 0.018 0.017 0.020 0.084 0.021 0.014 0.018 0.017 0.020 MeM 0.082 0.017 0.000 -0.011 -0.032 -0.069 0.008 0.011 0.014 0.019 0.029 0.059 0.083 0.020 0.014 0.022 0.043 0.091 FMA 0.072 -0.006 -0.074 -0.147 -0.295 -0.526 0.008 0.012 0.012 0.014 0.013 0.015 0.073 0.013 0.075 0.147 0.295 0.526 Method MoM 0.048 -0.002 0.000 -0.003 -0.007 -0.014 0.034 0.027 0.014 0.018 0.019 0.026 0.059 0.027 0.014 0.018 0.020 0.030 ARM 0.067 -0.004 -0.030 -0.037 -0.026 -0.016 0.007 0.009 0.014 0.021 0.030 0.038 0.067 0.010 0.033 0.042 0.040 0.041 CVM 0.061 0.004 -0.006 -0.012 -0.014 -0.020 0.011 0.014 0.014 0.019 0.021 0.042 0.062 0.014 0.016 0.022 0.025 0.046 BDI 0.083 0.018 -0.001 -0.016 -0.044 -0.093 0.009 0.011 0.013 0.017 0.020 0.035 0.083 0.021 0.013 0.023 0.049 0.099

Bias

SD

SE

42

K. Kociski, S. Pietraszewski

best for SexDim 1.3, for which it has no bias. However, for small sexual dimorphism (SexDim = 1.0 or 1.1), it has the biggest bias among all methods. The 4th-most precise method for such population parameters is ARM, having medium biases for both small and large values of sexual dimorphism. The other methods are characterized by substantial underestimation for SexDim 1.5. FMA in particular strongly underestimates for SexDim 1.2. Analysis of SEs of estimates of sexual dimorphism leads to the same conclusions as analysis of biases. Medium and small samples The above analysis was based on rather large samples of size 50. Such number is often unattainable in paleontological research and thus an analysis for smaller sample sizes has to be carried out. Simulations for two other sam-

ple sizes, n = 10 and n = 20, were completed (Tabs 3-4). Predictably, the smaller sample size, the bigger is SE of estimation. Besides, decreasing sample size enlarges underestimation for SexDim > 1.3 for each method except MeanM and CVM (they are almost equally precise as for large sample), as well as FMA (which is equally imprecise). For small or no sexual dimorphism, the magnitude of overestimation did not change and neither did the relation between biases of methods, except for a smaller bias for CVM than for MoM when n = 10. For n = 20 the best method is CVM. MoM is slightly more accurate than CVM for small sexual dimorphism, but apparently less accurate for larger ones, whereas MeanM is almost perfectly precise for substantial dimorphism but strongly biased for small or no dimorphism. Standard error of MoM is much

Table 3. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 20, sex ratio = 0.5, no skewness, within-sex CV = 5%. Sex. dim. Sample -0.001 1.0 1.1 0.002 1.2 0.002 1.3 -0.002 1.5 -0.002 1.8 -0.002 0.024 1.0 1.1 0.028 1.2 0.029 1.3 0.032 1.5 0.035 1.8 0.044 0.024 1.0 1.1 0.029 1.2 0.029 1.3 0.032 1.5 0.035 1.8 0.044 MeanM 0.082 0.020 0.001 -0.005 -0.003 -0.002 0.013 0.023 0.029 0.033 0.036 0.045 0.083 0.031 0.029 0.034 0.036 0.045 MeM 0.079 0.015 -0.012 -0.032 -0.076 -0.161 0.013 0.022 0.028 0.035 0.064 0.115 0.080 0.027 0.031 0.048 0.099 0.198 FMA 0.073 -0.001 -0.063 -0.128 -0.268 -0.482 0.013 0.016 0.017 0.018 0.022 0.029 0.074 0.016 0.065 0.129 0.269 0.483 Method MoM 0.052 -0.004 -0.014 -0.022 -0.035 -0.069 0.034 0.044 0.040 0.040 0.053 0.094 0.062 0.044 0.042 0.046 0.064 0.116 ARM 0.066 -0.003 -0.035 -0.049 -0.058 -0.073 0.011 0.019 0.028 0.038 0.069 0.116 0.067 0.020 0.045 0.062 0.090 0.136 CVM 0.059 0.006 -0.008 -0.015 -0.020 -0.028 0.017 0.026 0.030 0.034 0.048 0.090 0.061 0.027 0.031 0.037 0.052 0.094 BDI 0.081 0.017 -0.012 -0.037 -0.085 -0.170 0.013 0.022 0.026 0.030 0.045 0.078 0.082 0.028 0.029 0.048 0.096 0.187

Bias

SD

SE

Methods to estimate sexual dimorphism from unsexed samples

43

Table 4. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.5, no skewness, within-sex CV = 5%. Sex. dim. Sample 0.005 1.0 1.1 -0.003 1.2 0.002 1.3 0.003 1.5 -0.001 1.8 0.003 0.036 1.0 1.1 0.042 1.2 0.043 1.3 0.048 1.5 0.080 1.8 0.070 0.036 1.0 1.1 0.042 1.2 0.043 1.3 0.048 1.5 0.080 1.8 0.070 MeanM 0.082 0.015 -0.005 -0.011 -0.010 -0.003 0.016 0.032 0.043 0.059 0.082 0.087 0.084 0.035 0.043 0.060 0.083 0.087 MeM 0.078 0.008 -0.022 -0.056 -0.120 -0.224 0.015 0.031 0.038 0.059 0.101 0.160 0.079 0.032 0.044 0.081 0.157 0.275 FMA 0.073 0.000 -0.054 -0.112 -0.233 -0.427 0.016 0.026 0.025 0.028 0.038 0.050 0.075 0.026 0.060 0.116 0.236 0.430 Method MoM 0.065 -0.008 -0.028 -0.057 -0.111 -0.181 0.030 0.049 0.062 0.095 0.170 0.266 0.072 0.050 0.068 0.111 0.203 0.321 ARM 0.067 -0.006 -0.040 -0.068 -0.100 -0.127 0.014 0.028 0.037 0.061 0.110 0.174 0.068 0.028 0.055 0.091 0.148 0.216 CVM 0.059 0.000 -0.011 -0.018 -0.023 -0.032 0.020 0.038 0.043 0.059 0.091 0.135 0.062 0.038 0.045 0.061 0.094 0.139 BDI 0.081 0.011 -0.022 -0.057 -0.122 -0.222 0.016 0.031 0.035 0.048 0.080 0.109 0.082 0.033 0.041 0.075 0.146 0.247

Bias

SD

SE

higher than that of MeanM or CVM. Surprisingly, MoM shows evidently the most SE for SexDim = 1.1, for which it has almost no bias. This indicates that MoM is here a poorer method even though its bias is not large. For n = 10 only MeanM and CVM may be regarded as precise. These generally have the smallest biases and, for SexDim 1.2, the smallest SE of estimation. CVM appears to be a better method than MeanM because of much smaller bias for no dimorphism. Unbalanced sex ratio If we depart from initial parameter values and set the percentage of males in population to values 0.2 (Table 5) or 0.8 (Table 6), then sex ratio has no influence for SexDim = 1.0 (overestimation about 0.06-0.08, the smallest for MoM and CVM, the biggest for MeanM) and

for SexDim = 1.1 (very small bias for all methods). However, it exerts a strong effect on accuracy of sexual dimorphism estimation in the case of substantial dimorphism. The greater the dimorphism is the more the underestimation is for each method. When SexDim = 1.8, the amount of bias exceeds 0.4 and even 0.5. Only MeanM and CVM, for sex ratio equal 0.2, show a relatively small bias of about 0.1. For a sex ratio of 0.8 these methods are still characterized by large biases, though considerably smaller than for other methods. Sample size has minimal influence on the results. Its increase causes slight improvement only of MeanM and CVM. Sex ratio in primates populations is about 0.5 so the above analyses may seem superfluous. However, they show how tested methods cope with samples of unbalanced sex ratio drawn from

44

K. Kociski, S. Pietraszewski

Table 5. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.2, no skewness, within-sex CV = 5%. Sex. dim. Sample 0.002 1.0 1.1 -0.006 1.2 -0.019 1.3 -0.030 1.5 -0.063 1.8 -0.087 0.038 1.0 1.1 0.059 1.2 0.083 1.3 0.107 1.5 0.174 1.8 0.270 0.038 1.0 1.1 0.059 1.2 0.085 1.3 0.111 1.5 0.185 1.8 0.283 MeanM 0.084 0.005 -0.042 -0.077 -0.114 -0.123 0.019 0.029 0.056 0.088 0.165 0.266 0.086 0.029 0.070 0.117 0.200 0.293 MeM 0.079 -0.001 -0.063 -0.125 -0.253 -0.420 0.018 0.027 0.045 0.067 0.116 0.198 0.081 0.027 0.077 0.142 0.278 0.464 FMA 0.073 -0.006 -0.065 -0.122 -0.237 -0.401 0.019 0.026 0.037 0.048 0.077 0.130 0.076 0.026 0.075 0.131 0.249 0.421 Method MoM 0.068 -0.027 -0.108 -0.195 -0.356 -0.565 0.029 0.050 0.081 0.118 0.192 0.321 0.074 0.057 0.134 0.228 0.405 0.650 ARM 0.068 -0.015 -0.079 -0.141 -0.259 -0.405 0.015 0.024 0.043 0.067 0.132 0.240 0.070 0.028 0.090 0.156 0.291 0.471 CVM 0.060 -0.010 -0.047 -0.073 -0.116 -0.126 0.023 0.035 0.060 0.086 0.151 0.265 0.064 0.037 0.076 0.113 0.190 0.294 BDI 0.082 0.000 -0.065 -0.131 -0.266 -0.447 0.018 0.026 0.042 0.058 0.102 0.173 0.083 0.026 0.077 0.143 0.285 0.479

Bias

SD

SE

Table 6. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.8, no skewness, within-sex CV = 5%. Sex. dim. Sample 0.002 1.0 1.1 -0.006 1.2 -0.021 1.3 -0.033 1.5 -0.045 1.8 -0.118 0.041 1.0 1.1 0.062 1.2 0.074 1.3 0.114 1.5 0.158 1.8 0.303 0.041 1.0 1.1 0.062 1.2 0.077 1.3 0.118 1.5 0.164 1.8 0.325 MeanM 0.084 0.007 -0.048 -0.101 -0.143 -0.248 0.016 0.028 0.052 0.086 0.171 0.300 0.085 0.029 0.071 0.132 0.223 0.389 MeM 0.079 0.000 -0.064 -0.135 -0.273 -0.495 0.016 0.027 0.043 0.065 0.108 0.191 0.080 0.027 0.077 0.150 0.294 0.530 FMA 0.074 -0.005 -0.075 -0.143 -0.283 -0.522 0.018 0.024 0.030 0.040 0.054 0.096 0.076 0.025 0.081 0.149 0.288 0.531 Method MoM 0.064 -0.022 -0.100 -0.194 -0.356 -0.564 0.032 0.048 0.080 0.117 0.194 0.319 0.071 0.053 0.128 0.227 0.405 0.648 ARM 0.068 -0.013 -0.077 -0.143 -0.258 -0.428 0.014 0.023 0.041 0.066 0.119 0.229 0.069 0.026 0.088 0.158 0.284 0.486 CVM 0.061 -0.009 -0.058 -0.106 -0.188 -0.351 0.021 0.034 0.052 0.079 0.127 0.229 0.065 0.035 0.078 0.132 0.227 0.419 BDI 0.082 0.005 -0.051 -0.113 -0.225 -0.419 0.017 0.027 0.044 0.068 0.111 0.199 0.084 0.028 0.068 0.132 0.251 0.463

Bias

SD

SE

Methods to estimate sexual dimorphism from unsexed samples

45

a population of a balanced one. When samples are generated with a sex ratio fixed to 0.2 or 0.8, the results are quite similar to above ones. Skewness Neither negative nor positive skewness causes any visible effect (Tabs 7-8). Both the amount of biases and SEs are almost identical as in a symmetrical distribution. Large within-sex coefficient of variation Thus far, we have analyzed results for within-sex coefficient of variation of a studied trait equal to 5%. This is the typical value for many traits, but greater variability is also frequently found. Enlargement of CV in simulations exerts a dramatic effect on precision of methods (Tabs 9-10). Generally, for CV = 10% or 15%, all tested methods seem poor. They largely overestimate for small to medium sexual dimorphism (for SexDim = 1.0, by about 0.15 for CV = 10% and by more than 0.2 for CV = 15%) and underestimate for strong dimorphism. An exception is CVM, which overestimates across the whole range of sexual dimorphism values. For sample size n = 10 MeanM could be regarded as the best one, or least bad for CV = 10%. However, for CV = 15% all methods seem to be equally poor. For bigger sample sizes (n = 20 and particularly n = 50) MoM is marked by clearly the smallest biases which, again, is associated with a rather large SE of the method. So far, we have used CVM assuming the equation of PLAVCAN [1994]: SexDim = Exp(0.0214 CV 0.047),

where CV is pooled-sex coefficient of variation. The equation was established for within-sex CV = 5.5%. Yet, the samples we generated were for within-sex CV = 5, 10 or 15%. This is the reason we set the equations appropriate to these values. For this purpose, we generated balanced sex ratio samples of size 20,000 for SexDims ranging from 1.0 to 2.0 in increments of 0.1. For each SexDim level, pooled-sex CV was computed, and then we fitted regression to the 11 pairs of numbers obtained. Thus, we arrived at the following equations: SexDim = Exp(0.0229 CV 0.073) for CV = 5%, SexDim = Exp(0.0259 CV 0.193) for CV = 10%, SexDim = Exp(0.0291 CV 0.352) for CV = 15%. Table 11 shows the mean biases of CVM for various CV in the population and for CV assumed by the method (for samples size 10, sex ratio 0.5 and without skewness). Estimation of dimorphism performed with CVM is the best method when assumed within-sex CV is in accord with the population one. In such cases CVM is by far better than any other method. Sampling error Standard errors of sexual dimorphism in a sample are given in Tabs. 2-10 together with results for tested methods. Table 12 summarizes these errors for various sample sizes, sex ratios and CVs (skewness was omitted because it had little effect on the performance of the methods). Standard error increases along with sexual dimorphism, CV and amount of sex ratio unbalance, and decreases

46

K. Kociski, S. Pietraszewski

Table 7. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.5, negative skewness, within-sex CV = 5%. Sex. dim. Sample 0.006 1.0 1.1 0.000 1.2 -0.004 1.3 -0.001 1.5 -0.007 1.8 0.001 0.035 1.0 1.1 0.040 1.2 0.042 1.3 0.051 1.5 0.070 1.8 0.079 0.036 1.0 1.1 0.040 1.2 0.043 1.3 0.051 1.5 0.070 1.8 0.079 MeanM 0.085 0.017 -0.010 -0.012 -0.017 -0.010 0.019 0.031 0.042 0.055 0.079 0.105 0.087 0.036 0.044 0.057 0.080 0.106 MeM 0.080 0.008 -0.027 -0.051 -0.119 -0.210 0.017 0.028 0.036 0.060 0.098 0.169 0.081 0.029 0.045 0.079 0.154 0.269 FMA 0.072 0.000 -0.058 -0.113 -0.237 -0.424 0.017 0.023 0.026 0.029 0.036 0.056 0.074 0.023 0.064 0.117 0.240 0.428 Method MoM 0.067 -0.008 -0.033 -0.050 -0.107 -0.176 0.033 0.046 0.059 0.087 0.159 0.274 0.075 0.047 0.068 0.101 0.191 0.326 ARM 0.070 -0.006 -0.045 -0.063 -0.104 -0.115 0.015 0.025 0.036 0.061 0.102 0.179 0.071 0.026 0.057 0.088 0.146 0.212 CVM 0.061 0.001 -0.017 -0.018 -0.028 -0.020 0.023 0.034 0.043 0.058 0.085 0.146 0.065 0.034 0.046 0.061 0.089 0.147 BDI 0.084 0.012 -0.025 -0.054 -0.124 -0.220 0.018 0.028 0.036 0.049 0.077 0.117 0.086 0.031 0.044 0.073 0.146 0.249

Bias

SD

SE

Table 8. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.5, positive skewness, within-sex CV = 5%. Sex. dim. Sample -0.004 1.0 1.1 -0.005 1.2 -0.004 1.3 -0.002 1.5 -0.001 1.8 -0.010 0.034 1.0 1.1 0.041 1.2 0.046 1.3 0.048 1.5 0.059 1.8 0.081 0.034 1.0 1.1 0.041 1.2 0.046 1.3 0.048 1.5 0.059 1.8 0.081 MeanM 0.084 0.016 -0.010 -0.010 -0.006 -0.017 0.017 0.030 0.043 0.053 0.066 0.098 0.085 0.034 0.045 0.054 0.067 0.100 MeM 0.079 0.007 -0.028 -0.054 -0.113 -0.212 0.016 0.027 0.039 0.052 0.095 0.170 0.080 0.028 0.048 0.075 0.147 0.271 FMA 0.073 -0.002 -0.058 -0.114 -0.234 -0.427 0.017 0.023 0.023 0.027 0.032 0.048 0.075 0.023 0.062 0.117 0.236 0.430 Method MoM 0.066 -0.007 -0.032 -0.043 -0.095 -0.167 0.030 0.047 0.057 0.070 0.150 0.252 0.073 0.048 0.065 0.083 0.177 0.302 ARM 0.068 -0.007 -0.044 -0.066 -0.095 -0.128 0.014 0.025 0.039 0.056 0.104 0.178 0.069 0.026 0.059 0.086 0.141 0.219 CVM 0.060 0.000 -0.017 -0.019 -0.019 -0.033 0.022 0.034 0.044 0.053 0.079 0.135 0.064 0.034 0.047 0.056 0.081 0.139 BDI 0.079 0.010 -0.027 -0.054 -0.119 -0.224 0.016 0.028 0.035 0.044 0.072 0.117 0.081 0.030 0.045 0.070 0.139 0.253

Bias

SD

SE

Methods to estimate sexual dimorphism from unsexed samples

47

Table 9. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.5, no skewness, within-sex CV = 10%. Sex. dim. Sample -0.003 1.0 1.1 -0.008 1.2 0.004 1.3 0.004 1.5 -0.002 1.8 -0.011 0.070 1.0 1.1 0.079 1.2 0.086 1.3 0.087 1.5 0.114 1.8 0.126 0.070 1.0 1.1 0.080 1.2 0.086 1.3 0.087 1.5 0.114 1.8 0.127 MeanM 0.169 0.088 0.042 0.012 -0.021 -0.061 0.038 0.046 0.066 0.075 0.109 0.159 0.174 0.099 0.078 0.075 0.111 0.170 MeM 0.158 0.077 0.025 -0.011 -0.072 -0.177 0.037 0.043 0.060 0.068 0.102 0.164 0.163 0.088 0.065 0.069 0.125 0.241 FMA 0.144 0.066 0.007 -0.042 -0.161 -0.354 0.033 0.040 0.054 0.052 0.061 0.080 0.147 0.077 0.054 0.067 0.172 0.363 Method MoM 0.137 0.046 -0.005 -0.052 -0.083 -0.164 0.065 0.077 0.098 0.129 0.161 0.246 0.152 0.090 0.098 0.139 0.181 0.296 ARM 0.138 0.055 -0.002 -0.042 -0.103 -0.183 0.032 0.039 0.055 0.066 0.102 0.170 0.142 0.067 0.055 0.079 0.145 0.250 CVM 0.168 0.098 0.065 0.054 0.034 0.009 0.047 0.057 0.081 0.081 0.119 0.169 0.175 0.113 0.104 0.097 0.123 0.170 BDI 0.165 0.084 0.035 -0.004 -0.067 -0.176 0.038 0.043 0.063 0.066 0.088 0.134 0.170 0.094 0.072 0.066 0.110 0.221

Bias

SD

SE

Table 10. Mean biases, standard deviations (SD) and standard errors (SE) of estimation of sexual dimorphism by various methods, for sexual dimorphism in population. n = 10, sex ratio = 0.5, no skewness, within-sex CV = 15%. Sex. dim. Sample 0.011 1.0 1.1 0.003 1.2 0.009 1.3 -0.009 1.5 0.008 1.8 -0.008 0.117 1.0 1.1 0.109 1.2 0.129 1.3 0.139 1.5 0.153 1.8 0.202 0.118 1.0 1.1 0.109 1.2 0.129 1.3 0.139 1.5 0.153 1.8 0.202 MeanM 0.274 0.182 0.133 0.071 0.012 -0.043 0.055 0.074 0.083 0.098 0.130 0.193 0.279 0.196 0.157 0.121 0.130 0.198 MeM 0.258 0.165 0.110 0.042 -0.025 -0.118 0.052 0.070 0.078 0.093 0.118 0.187 0.264 0.179 0.135 0.102 0.120 0.221 FMA 0.237 0.147 0.092 0.019 -0.090 -0.258 0.055 0.067 0.079 0.086 0.085 0.112 0.244 0.161 0.121 0.088 0.124 0.281 Method MoM 0.209 0.119 0.051 -0.028 -0.070 -0.138 0.106 0.120 0.140 0.164 0.195 0.265 0.234 0.169 0.148 0.166 0.207 0.299 ARM 0.229 0.138 0.077 0.007 -0.067 -0.161 0.048 0.068 0.072 0.087 0.117 0.193 0.234 0.154 0.105 0.087 0.135 0.251 CVM 0.310 0.222 0.193 0.140 0.117 0.102 0.071 0.095 0.110 0.125 0.148 0.215 0.318 0.242 0.222 0.187 0.189 0.238 BDI 0.273 0.180 0.126 0.061 -0.008 -0.103 0.058 0.075 0.083 0.101 0.112 0.171 0.279 0.195 0.151 0.118 0.112 0.200

Bias

SD

SE

48

K. Kociski, S. Pietraszewski

Table 11. Mean biases of CVM for various within-sex CV in population and within-sex CV assumed by the method (n = 10, sex ratio = 0.5, no skewness). within-sex CV (%) in population assumed by CVM 5 10 5 15 5 10 10 15 5 10 15 15 1.0 0.041 -0.066 -0.190 0.167 0.066 -0.064 0.310 0.211 0.084 1.1 -0.018 -0.115 -0.244 0.091 -0.006 -0.132 0.221 0.127 0.005 Sexual dimorphism 1.2 1.3 -0.033 -0.027 -0.128 -0.122 -0.254 -0.248 0.066 0.048 -0.034 -0.046 -0.159 -0.160 0.179 0.155 0.105 0.090 -0.036 -0.052 1.5 -0.012 -0.098 -0.227 0.045 -0.037 -0.151 0.143 0.075 -0.047 1.8 0.004 -0.052 -0.157 0.056 0.003 -0.109 0.186 0.095 0.018

Table 12. Standard error of sample sexual dimorphism compared to that of population. n SR* 0.2 CV** (%) 5 10 15 5 10 15 5 10 15 5 10 15 5 10 15 5 10 15 5 10 15 5 10 15 5 10 15 1.0 0.038 0.076 0.126 0.036 0.070 0.118 0.041 0.082 0.113 0.029 0.057 0.093 0.024 0.055 0.068 0.029 0.065 0.092 0.016 0.031 0.047 0.012 0.024 0.035 0.015 0.030 0.050 1.1 0.059 0.089 0.145 0.042 0.080 0.109 0.062 0.094 0.135 0.034 0.065 0.102 0.029 0.060 0.075 0.034 0.066 0.104 0.018 0.034 0.048 0.014 0.025 0.040 0.015 0.035 0.047 Sexual dimorphism 1.2 1.3 0.085 0.111 0.120 0.158 0.152 0.190 0.043 0.048 0.086 0.087 0.129 0.139 0.077 0.118 0.119 0.145 0.145 0.191 0.050 0.047 0.074 0.082 0.107 0.129 0.029 0.032 0.065 0.067 0.088 0.093 0.043 0.051 0.079 0.080 0.099 0.111 0.018 0.020 0.035 0.039 0.055 0.058 0.015 0.018 0.029 0.030 0.042 0.052 0.018 0.018 0.038 0.038 0.052 0.058 1.5 0.185 0.205 0.250 0.080 0.114 0.153 0.164 0.233 0.263 0.072 0.096 0.125 0.035 0.074 0.115 0.043 0.107 0.146 0.026 0.048 0.072 0.017 0.038 0.051 0.022 0.042 0.070 1.8 0.283 0.273 0.328 0.070 0.127 0.202 0.325 0.308 0.332 0.089 0.122 0.176 0.044 0.082 0.126 0.143 0.134 0.163 0.029 0.059 0.085 0.020 0.041 0.067 0.026 0.050 0.079

10

0.5

0.8

0.2

20

0.5

0.8

0.2

50

0.5

0.8

* sex ratio (percentage of males in population) ** within-sex CV

Methods to estimate sexual dimorphism from unsexed samples

49

with sample size. The lowest errors are for n = 50, CV = 5% and balanced sex ratio, and take values 0.01-0.02. For such a sample size error never exceeds 0.1, regardless of sex ratio and CV. For n = 10 such small errors are only for balanced sex ratio together with CV = 5%. If any of the conditions is not met, error increases dramatically, especially for substantial sexual dimorphism. For SexDim = 1.0 or 1.1, only for CV = 15% error exceeds 0.1, but for marked dimorphism, it is in the order of 0.2-0.3. For n = 20 errors are intermediate and usually below 0.1, except for marked dimorphism in the presence of substantial CV. Unisex samples, composed of only males or females, are particularly risky for estimating sexual dimorphism. Dimorphism determined for such a sample is a pure artifact and has nothing to do with the dimorphism in the population. Of course, the smaller sample size is and the more unbalanced sex ratio is, the greater the risk of obtaining a unisex sample is (Table 13). Assuming the stan-

dard value of statistical risk = 0.05 we can see that for balanced sex ratio it is sufficient to select a six-specimen sample to be quite sure that it contains both sexes. For sex ratio equal 0.4 or 0.6 the number of elements is 7, and for 0.3 or 0.7 it is 9. The number increases rapidly the more sex is unbalanced, e.g., for sex ratio 0.2 or 0.8 we need at least 15, and for sex ratio 0.1 or 0.9 at least 30 specimens to minimize the risk of obtaining a unisex sample to the acceptable level.

Discussion
The analysis shows that precision of estimation of sexual dimorphism from unsexed samples depends on particular parameters and is distorted by small sample size, unbalanced sex ratio and increased intrasexual variation. Skewness exerts no effect on the estimation. Before discussing which method is best it should be noted that in some conditions estimation should not be carried out at all (compare with the algorithm in

Table 13. Probability of obtaining a unisex sample for different sample sizes and population sex ratios. n 1 2 3 4 5 6 7 8 9 10 15 20 30 0.1 or 0.9 1.000 0.820 0.730 0.656 0.591 0.531 0.478 0.430 0.387 0.349 0.206 0.122 0.042 0.2 or 0.8 1.000 0.680 0.520 0.411 0.328 0.262 0.210 0.168 0.134 0.107 0.035 0.012 0.001 Sex ratio 0.3 or 0.7 1.000 0.580 0.370 0.248 0.171 0.118 0.083 0.058 0.040 0.028 0.005 0.001 0.000 0.4 or 0.6 1.000 0.520 0.280 0.155 0.088 0.051 0.030 0.017 0.010 0.006 0.000 0.000 0.000 0.5 1.000 0.500 0.250 0.125 0.063 0.031 0.016 0.008 0.004 0.002 0.000 0.000 0.000

50

K. Kociski, S. Pietraszewski

Appendix 1). When the sample size is too low the risk of obtaining unisex sample is considerable. Minimum acceptable size depends on sex ratio in the population and is about 7 to 10 (Table 13). If sample size is about 10 and if: (1) sex ratio is low (low percentage of males), or (2) within-sex CV is substantial (at least 10%), then sampling error is high (sample sexual dimorphism often differs markedly from that of the population). Besides, in two specific cases none of the methods is appropriate for estimation: (1) high sex ratio, (2) not known, but probably large ( 10%) within-sex CV. If none of the above conditions is met, one may seek the most precise method to use. For most circumstances the best methods are MeanM and CVM. MeanM is robust and estimates reasonably well for broad range of parameter values. A common fault of this method is the relatively large overestimation for lack of sexual dimorphism. CVM might then be even better than MeanM, provided that an accurate assumption for within-sex CV is made. Otherwise, the method could be very poor. Within-sex CV in studied extinct species could be assessed by analogy to its extant relative. If one believes it can reliably determine the parameter in this way, use of CVM seems a good choice. Otherwise it is more safe to use the more robust MeanM. MoM is best in one specific situation where within-sex CV is low (about 5%), sex ratio is balanced (about 0.5) and sample size is large (about 50 or more). This method, however, shows a small overestimation for lack of sexual dimorphism. The fault of the method is high SE of estimation even when bias is small; it indicates a large variation (SD) of estimates obtained by MoM in given

experimental condition. (Refer also to the algorithm in Appendix 1 on how to choose the most appropriate method of estimation). We do not recommend using the other methods tested as their biases and standard errors are usually unduly large. FMA is used to assess not exact but maximum dimorphism that could be present within a unimodal distribution. Thus one might suspect that it tends to overestimate for small sexual dimorphism and gives estimates greater than those for other methods. However, our analysis shows this is not the case the method overestimates, but no more than for other methods. Thus estimation of maximum dimorphism gives similar results as estimation of its exact value. On the other hand, as expected, FMA underestimates dramatically when its assumption of unimodality is not met, i.e., in cases of substantial population dimorphism. Other researchers have, however, not always obtained similar results to ours. Generally, authors praise the method they propose. Yet, both GODFREY et al. [1993] with FMA, and LEE [2001] with ARM used natural samples for methods testing rather than computer-generated ones. The number of natural samples is limited and their parameters are not controlled which renders results somewhat random. JOSEPHSON et al. [1996] tested MoM against MeanM and CVM using simulated data, but the samples were of size 50 or 100. Our study confirms that MoM works well for large samples, but natural ones are often much smaller, for which MoM performs rather poorly. PLAVCAN [1994] in the paper testing MeanM, MeM, CVM and FMA with computer-generated samples, states

Methods to estimate sexual dimorphism from unsexed samples

51

that the best method is MeanM. He points out sensitivity of CVM to increased within-sex CV, but he uses the method only in the way assuming 5.5% within-sex CV. However, our analysis shows that proper assessment of the parameter dramatically improves the methods precision. REHG and LEIGH [1999] examined MeanM, MeM and MoM methods using samples of 1,737 females and 1,134 males representing 42 anthropoid species and confirmed the superiority of the MeanM method. As regards parameters influencing precision of estimation, we are generally in agreement with other authors findings that it is distorted by unbalanced sex ratio, large within-sex CV and small sample size [GODFREY et al. 1993, PLAVCAN 1994, JOSEPHSON et al. 1996, REHG and LEIGH 1999, LEE 2001]. Contrary to REHG and LEIGH [1999], who found that skewness (negative or positive) worsen estimation of dimorphism, we did not observe such an effect. We suppose it might have been be a specific effect of the natural samples they studied. In a specific research situation one wishes to know how much true dimorphism may differ from an assessed one. If one assumes that a 95% confidence interval is very roughly equal to estimated dimorphism 2 SE, standard error of used estimator depends on some parameters usually unknown to the researcher (sex ratio and within-sex CV). Its typical values are 0.03-0.2, which gives a magnitude of uncertainty of one or a few tenths. This proves that inferring sexual dimorphism in studied extinct species cannot be exact and the statement should rather read that sexual dimorphism is low (or medium, or

high). Discerning small dimorphism from no dimorphism at all seems to be impossible. The methods for estimating sexual dimorphism assess the dimorphism in sample, but researchers aim is to recognize dimorphism in a population (species). Precision of determination of dimorphism in a population by a method depends on two factors: accuracy of the method in estimating dimorphism in a sample (goodness of the method) and similarity of the samples dimorphism to that of the population (sampling error). Tabs. 2-10 contain SEs for a sample (measure of sampling error) and for each method (precision of estimation). The difference between them indicates the amount of a methods imprecision. SEs for a sample are usually almost as large as SEs for the best methods, i.e., MeanM and CVM. This means that imprecision of the methods themselves is relatively very small; error of estimation is caused mainly by sampling error. Thus, only very limited improvement of methods of estimating sexual dimorphism from unsexed samples is possible. The only situation for which such improvement seems to be important is that when intrasexual CV is supposed to be substantial and it cannot be reliably assessed by comparison with CV in living relatives; to date no method has been shown to be satisfactory in such a situation. Thus, estimating sexual dimorphism of extinct species from unsexed samples is a difficult task and no precise answer can usually be determined. The common obstacle is small sample size, which increases: (1) SE of sex means and consequently SE of sexual dimorphism in the sample, (2) risk of having a unisex

52

K. Kociski, S. Pietraszewski

sample, which renders any estimation misleading. Other problems are: (1) unbalanced sample sex ratio reflecting population unbalance or being random effect of a small sample, (2) large within-sex CV. Even in very favorable circumstances, the 95% interval of confidence of estimation is rarely narrower than 0.1. Usually, its width is 0.2 or more. Therefore, one is rarely able to give more precise answer than sexual dimorphism is low (or medium, or high). In most situations error of estimation results mainly from sampling error, not the error of method, and we believe that formulating new methods of

estimating sexual dimorphism or improving existing ones is of limited value. Rather, there is a need to accept the fact that exact, and sometimes even approximate, estimation of sexual dimorphism from unsexed samples of fossil species is unfeasible.

Acknowledgements
We are grateful to Professor J.M. Plavcan for the forwarding of relevant articles and for his comments on the methods discussed here and the final draft of the paper. We also thank the anonymous reviewer for helpful suggestions.

Appendix 1: Algorithm for choosing a method to estimate sexual dimorphism

Step 1 2 3 4 5 5.1 5.2 5.3 5.3.1 5.3.2 5.3.2.1 5.3.2.2 Condition Probably high sex ratio ( 0.8) n < 7-10 n 10 and low sex ratio ( 0.2) n 10 and CV 10% What is CV? CV not known but probably 10% CV known and 10% Probably small CV ( 5%) Low sex ratio ( 0.2) Balanced sex ratio ( 0.5) n 10-20 n 50 Action Exit. No precise method Exit. Risk of unisex sample Exit. High sampling error Exit. High sampling error Go through steps 5.1-5.3 Exit. No precise method Best method: CVM Go through steps 5.3.1-5.3.2 Best methods: CVM and MeanM Go through steps 5.3.2.1-5.3.2.2 Best methods: (1) CVM, (2) MeanM Best methods: (1) MoM, (2) CVM, (3) MeanM

Begin from step 1 and continue. At each step check whether condition is met. If yes, perform the action. If action is exit then no method should be chosen because of imprecision of estimation. The algorithm can be simplified to the sentence: if, in given circumstances, estimation is not unrecommended, use CVM unless within-sex CV is low, sex ratio is balanced and sample size is large in those cases use MoM.

Methods to estimate sexual dimorphism from unsexed samples

53

References
BORGOGNINI TARLI S.M., E. REPETTO, 1986, Methodological considerations on the study of sexual dimorphism in past human populations, J. Hum. Evol., 1, 51-66 CLUTTON-BROCK T.H., P.H. HARVEY, B. RUDDER, 1977, Sexual dimorphism, socionomic sex ratio and body weight in primates, Nature, 269, 797-800 COPE D.A., M.G. LACY, 1994a, Testing single species hypothesis using the combined referent CV: applications to fossil hominoid dental samples, Am. J. Phys. Anthropol., 16 (Suppl.), 71 FLEAGLE J.G., R.F. KAY, E.L. SIMONS, 1980, Sexual dimorphism in early anthropoids, Nature, 287, 328-330 FOLEY R.A., P.C. LEE, 1989, Finite social space, evolutionary pathways, and reconstructing hominid behavior, Science, 243, 901-905 GINGERICH P.D., 1981, Cranial morphology and adaptations in Eocene Adapidae. I. Sexual dimorphism in Adapis magnus and Adapis parisiensis, Am. J. Phys. Anthropol., 56, 217-234 GODFREY L.R, S.K. LYON, M.R. SUTHERLAND, 1993, Sexual dimorphism in large-bodied primates: The case of the subfossil lemurs, Am. J. Phys. Anthropol., 90, 315-334 HARVEY P.H., M. KAVANAGH, T.H. CLUTTONBROCK, 1978, Sexual dimorphism in primate teeth, J. Zool. Lond., 186, 475-485 JOSEPHSON S.C., K.E. JUELL, A.R. ROGERS, 1996, Estimating sexual dimorphism by Method-ofMoments, Am. J. Phys. Anthropol., 100, 191206 KAY R.F., 1982a, Sivapithecus simonsi, a new species of Miocene hominoid, with comments on the phylogenetic status of Ramapithecinae, Int. J. Primatol., 3, 113-173 KAY R.F., 1982b, Sexual dimorphism in the Ramapithecinae, Proc. Natl. Acad. Sci. USA, 79, 209-212 KELLEY J., J.M. PLAVCAN, 1998, A simulation test of hominoid species number at Lufeng, China: implications for the use of the coefficient of variation in paleotaxonomy, J. Hum. Evol., 35, 577-596 KRAMER A., 1993, Human taxonomic diversity in the Pleistocene: Does Homo erectus represent multiple hominid species? Am. J. Phys. Anthropol., 91, 161-171

KRAMER A., L.W. KONIGSBERG, 1999, Recognizing species diversity among large-bodied hominoids: a simulation test using missing data finite mixture analysis, J. Hum. Evol., 36, 409-421 KRISHTALKA L., R.K. STUCKY, K.C. BEARD, 1990, The earliest fossil evidence for sexual dimorphism in primates, Proc. Natl. Acad. Sci. USA, 87, 5223-5226 LARSEN C.S., 2003, Equality for the sexes in human evolution? Early hominid sexual dimorphism and implicatons for mating systems and social behavior, Proc. Natl. Acad. Sci. USA, 100, 9103-9104 LEE S.-H., 2001, Assigned Resampling Method: A new method to estimate size sexual dimorphism in samples of unknown sex, Przegld Antropol.- Anthropol. Rev., 64, 21-39 LEUTENEGGER W., B. SHELL, 1987, Variability and sexual dimorphism in canine size of Australopithecus and extant hominoids, J. Hum. Evol., 16, 359-367 LEUTENNEGER W., J.T. KELLY, 1977, Relationship of sexual dimorphism in canine size and body size to social, behavioral and ecological correlates in anthropoid primates, Primates, 8, 117-136 LOCKWOOD C.A., 1999, Sexual dimorphism in the face of Australopithecus afarensis, Am. J. Phys. Anthropol., 108, 97-127 LOCKWOOD C.A., B.G. RICHMOND, W.L. JUNGERS, W.H. KIMBEL, 1996, Randomization procedures and sexual dimorphism in Australopithecus afarensis, J. Hum. Evol., 31, 537548 LOVEJOY C.O., 1981, The origin of man, Science, 211, 341-350 LOVEJOY C.O., K.F. KERN, S.W. SIMPSON, R.S. MEINDL, 1989, A new method for estimation of skeletal dimorphism in fossil samples with an application to Australopithecus afarensis, [in:] Proceedings of the 2nd International Congress of Human Paleoanthropology, Editoriale Jaca Books, Milan, 103-108 LYMAN R.L., 1985, Bone frequencies: Differential destruction, in situ destruction, and bone transport and their archeological implications, J. Archeol. Sci., 12, 221-236 MARTIN R.D., 1977, Sexual dimorphism and the evolution of higher primates, Nature, 287, 273275

54

K. Kociski, S. Pietraszewski

MCHENRY H.M., 1991, Sexual dimorphism in Australopithecus afarensis, J. Hum. Evol., 20, 21-32 MCHENRY H.M., 1992, Body size proportions in early hominids, Am. J. Phys. Anthropol., 87, 407-431 MCHENRY H.M., 1994, Behavioral ecological implications of early hominid body size, J. Hum. Evol., 27, 77-87 OXNARD C.E., 1982, Commentary on two misconceptions of phylogeny and classification, Am. J. Phys. Anthropol., 59, 305-306 PLAVCAN J.M, 1994, Comparison of four simple methods for estimating sexual dimorphism in fossils, Am. J. Phys. Anthropol., 94, 465-476 PLAVCAN J.M., 2000, Inferring social behavior from sexual dimorphism in the fossil record, J. Hum. Evol., 39, 327-344 PLAVCAN, J.M., 2001, Sexual dimorphism in primate evolution, Yrbk. Phys. Anthropol., 44, 22-53 PLAVCAN J.M., 2002, Taxonomic variation in the patterns of craniofacial dimorphism in primates, J. Hum. Evol., 42, 579-608 PLAVCAN J.M., C.P. VAN SCHAIK, 1992, Intrasexual competition and canine dimorphism in anthropoid primates, Am. J. Phys. Anthropol., 87, 461-477 PLAVCAN J.M., C.P. VAN SCHAIK, 1997a, Interpreting hominid behavior on the basis of sexual dimorphism, J. Hum. Evol., 32, 345-374

PLAVCAN J.M., C.P. VAN SCHAIK, 1997b, Intrasexual competition and body weight dimorphism in anthropoid primates, Am. J. Phys. Anthropol., 103, 37-68 PLAVCAN J.M., C.P. VAN SCHAIK, P.M. KAPPELER, 1995, Competition, coalitions and canine size in primates, J. Hum. Evol., 28, 245-276 REHG J.A, S.R. LEIGH, 1999, Estimating sexual dimorphism and size differences in the fossil record: A test of methods, Am. J. Phys. Anthropol., 110, 95-104 RENO P.L., R.S. MEINDL, M.A. MCCOLLUM, C.O. LOVEJOY, 2003, Sexual dimorphism in Australopithecus afarensis was similar to that of modern human, Proc. Natl. Acad. Sci. USA, 100, 9404-9409 RICHMOND B.G., W.L. JUNGERS, 1995, Size variation and sexual dimorphism in Australopithecus afarensis and living hominoids, J. Hum. Evol., 29, 229-245 RUFF C.B., A. WALKER, M.F. TEAFORD, 1989, Body mass, sexual dimorphism and femoral proportions of Proconsul from Rusinga and Mfangano Islands, Kenya, J. Hum. Evol., 18, 515-536 SIMONS E.L., J.M. PLAVCAN, J.G. FLEAGLE, 1999, Canine sexual dimorphism in Egyptian anthropoid primates: Catopithecus and Proteopithecus, Proc. Natl. Acad. Sci. USA, 96, 25592562

Streszczenie
Dymorfizm pciowy wrd yjcych gatunkw krgowcw, zwaszcza naczelnych, powizany jest z charakterystykami ekologicznymi, takimi jak system kojarze (i zwizane z nim zachowanie), struktura spoeczna, efektywna proporcja pci czy poziom konkurencji. Dymorfizm pciowy moe by take pomocny w okrelaniu ekologii wymarych gatunkw naczelnych, a zwaszcza hominidw. Jego znajomo umoliwia rwnie interpretacj zmiennoci taksonomicznej wrd wymarych form, moe wic by pomocna przy oznaczaniu przynalenoci gatunkowej znalezisk. Poniewa identyfikacja pci okazu kopalnego nie zawsze jest moliwa czy pewna, oszacowanie dymorfizmu pciowego metodami tradycyjnymi (zakadajcymi wczeniejsz wiedz na temat pci) staje si niemoliwe. W zwizku z tym przydatne staj si metody okrelajce dymorfizm pciowy bez znajomoci pci osobnikw w prbie: metoda redniej (MeanM), mediany (MeM), wspczynnika zmiennoci (CVM), momentw (MoM), metoda Finite mixture analysis (FMA), Binomial dimorphism index (BDI) oraz Assigned resampling method (ARM). W pracy sprawdzilimy precyzj tych metod, wykorzystujc wygenerowane komputerowo prby o okrelonej wielkoci, pochodzce z teoretycznej populacji o cile okrelonych parametrach, takich jak proporcja pci, skono oraz wewntrzpciowy wspczynnik zmiennoci (WPCV). Dokadno oznaczania dymorfizmu w populacji dan metod

Methods to estimate sexual dimorphism from unsexed samples

55

zaley nie tylko od dokadnoci, z jak ta metoda wyznacza dymorfizm w prbie, ale rwnie od podobiestwa dymorfizmu w badanej prbie do dymorfizmu w populacji. W zwizku z tym dokonalimy rwnie analizy bdu zwizanego z losowaniem prby. Nasze badania wykazay, e dokadno wyznaczania dymorfizmu pciowego zmniejszaj takie czynniki jak maa liczebno prby, dysproporcja pci oraz dua zmienno wewntrzpciowa; adnego wpywu nie wywiera natomiast skono. W wikszoci przypadkw najlepszymi metodami okazay si CVM i MeanM. CVM daje szczeglnie dobre wyniki, gdy zaoona warto WPCV jest trafna. Z kolei, gdy dysponujemy prb o duej liczebnoci (ok. 50 lub wicej), a WPCV jest niewielki (ok. 5%), najlepsz metod okazuje si MoM. Okrelanie dymorfizmu pciowego na materiaach kopalnych o nieokrelonej pci jest zadaniem trudnym i nie daje dokadnych wynikw. Podstawow przeszkod jest niewielka zazwyczaj liczebno prby, przez co zwiksza si 1) bd standardowy rednich dla pci, a w konsekwencji bd standardowy dymorfizmu pciowego w prbie, 2) ryzyko posiadania prby zoonej z osobnikw tylko jednej pci, przez co estymacja dymorfizmu moe da cakowicie bdne wyniki. Kolejnymi utrudnieniami s 1) dysproporcja pci w prbie, odzwierciedlajca dysproporcj w populacji lub bdca losowym efektem niewielkiej liczebnoci prby, oraz 2) dua wewntrzpciowa zmienno. Nawet w bardzo sprzyjajcych okolicznociach 95% przedzia ufnoci dla szacownego dymorfizmu pciowego rzadko jest wszy od 0,1. Zwykle jego szeroko wynosi 0,2 lub wicej. W zwizku z tym podawanie odpowiedzi bardziej precyzyjnej ni dymorfizm pciowy jest niski (lub redni lub wysoki) jest raczej zbyt ryzykowne.