How Sexual Are Humans Compare To Other Animals
PLoS 1. 2009; 4(9): e6876.
How Humans Differ from Other Animals in Their Levels of Morphological Variation
Ann Eastward. McKellar
1 Department of Biology, Queen's University, Kingston, Canada
Andrew P. Hendry
2 Redpath Museum and Department of Biology, McGill University, Montreal, Canada
Rebecca Sear, Editor
Received 2009 Mar 11; Accepted 2009 Aug 10.
- Supplementary Materials
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Table S1: List of all studies, species, and taxa (amphibian, bird, fish, invertebrate, mammal, or reptile) used to obtain coefficients of variation (CV) for male and/or female length and/or mass for animal populations.
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Table S2: List of all studies used to obtain CVs for male and/or female height and/or mass for man populations. Likewise included is the country of origin, name of specific population or survey title, year of sampling (if provided), indigenous/aboriginal status (as defined in each study), and development condition (http://www.united nations.org/special-rep/ohrlls/ldc/list.htm).
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Table S3: Percentiles for mean within- and among-population male and female person human being height and mass in relation to species-hateful amphibian, invertebrate, mammal, and reptile length and mass distributions. Percentiles are non shown for taxa distributions with n<5 animal species.
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Figure S1: Distributions of coefficients of variation (CV) for within-population body mass. Shown are species means for animals (black) and population means for humans (greyness) for males (A) and females (B). Arrows betoken the locations of CVs for hateful human mass.
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Effigy S2: Distributions of CVs for amongst-population body length or pinnacle. Shown are information for males (A) and females (B). Arrows point the locations of CVs for mean human tiptop.
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Effigy S3: Bergmann'due south rule in humans. Mean male top (A, R2 = 0.126, P<0.001), female meridian (B, R2 = 0.097, P = 0.002), male mass (C, R2 = 0.183, P<0.001), and female person mass (D, Rtwo = 0.155, P<0.001) all increment significantly with absolute latitude. Latitude of each population was approximated using the geographic middle of the country from which the population was sampled. Coordinates were obtained from the CIA Globe Factbook (https://www.cia.gov/library/publications/the-world-factbook/fields/2011.html).
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Figure S4: Species-hateful CVs for among- versus within-population body mass. Shown are regression lines (solid), x = y lines (dashed), and data for males (A, R2 = 0.26, P<0.001) and females (B, R2 = 0.37, P<0.001).
(1.72 MB Medico)
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Abstract
Fauna species come in many shapes and sizes, every bit exercise the individuals and populations that brand upward each species. To us, humans might seem to bear witness particularly high levels of morphological variation, but perhaps this perception is simply based on enhanced recognition of individual conspecifics relative to individual heterospecifics. Nosotros here more objectively enquire how humans compare to other animals in terms of trunk size variation. We quantitatively compare levels of variation in torso length (height) and mass within and among 99 human being populations and 848 brute populations (210 species). We detect that humans prove low levels of inside-population body height variation in comparison to torso length variation in other animals. Humans do not, nevertheless, show distinctive levels of within-population body mass variation, nor of among-population torso acme or mass variation. These results are consistent with the thought that natural and sexual selection have reduced human height variation within populations, while maintaining it amongst populations. We therefore hypothesize that humans have evolved on a rugged adaptive mural with strong pick for torso pinnacle optima that differ among locations.
Introduction
Variation is the raw material for evolution, and it is ubiquitous both inside and among populations [1]. However, the balance between forces enhancing variation and forces eroding it probable differs among populations and species. Accordingly, the magnitude of morphological variation can differ markedly amid species [i]. Every bit humans, how practice we compare to other animals in terms of this variation? Taking a subjective look, morphological variation in a crowd of people might seem large compared to the apparent uniformity of an animal group, such as a flock of birds or a shoal of fish. Only perhaps this apparent contrast between humans and other animals is simply a matter of our perception – that is, evolution has probably shaped animals to exist more discriminating amid individual conspecifics than among private heterospecifics [two], [3]. Alternatively, contemporary man populations might indeed bear witness greater morphological variation than other species. Possible reasons might include relaxed natural selection on some human traits [4] (although perhaps not on others [5]), the keen diversity of conditions nosotros tin (and do) inhabit, and recurrent migration and gene period [vi] amongst populations. Or perchance humans instead show lower levels of variation – a point nosotros will return to afterward.
Our goal is to quantitatively determine how levels of morphological variation within humans compare to those in other animate being species. Nosotros apply body size as our focal morphological variable because this trait tin be logically compared among species, and considering trunk size data are readily bachelor for a broad variety of fauna populations, both man and non-homo (meet Tables S1 and S2). In an endeavor to obtain unbiased data, we searched the literature for means and variances in body height or trunk length (these two terms are here used interchangeably, depending on context) and body mass both within and among populations of humans and other animals. From these data, we calculated the coefficient of variation (CV; standard deviation divided past the mean) as a standardized measure of variance among individuals within populations and amongst population means. In total, our dataset included body size variation from 55 studies (99 populations) of humans and 107 studies (210 species and 848 populations) of other animals (Tables S1 and S2).
Results and Discussion
One interesting effect was that humans, in comparison to other animals, show a high level of within-population variation in mass considering their within-population variation in height (Effigy one). Specifically, when because residuals from a regression of within-population CVs for mass on inside-population CVs for length, human males and females fell into the 71st and 91st percentiles, respectively, for the entire distribution of animal species.
Species-hateful CVs for within-population mass (divided by three; see Materials and Methods) versus length.
Shown are regression lines (solid), x = y lines (dashed), and data for males (A, R2 = 0.81, P<0.001) and females (B, R2 = 0.58, P<0.001).
Why, in comparison to other animals, do humans show high variation in mass relative to height? One contributing factor might be that human height is developmentally determinate, and is therefore relatively stable in one case an individual reaches maturity. Mass, in contrast, can fluctuate dramatically after maturity based on historic period, diet, and activity level. In line with this greater environmental (as opposed to genetic) contribution to mass than to length, heritabilities are normally lower for mass than for top in humans [vii]–[nine]. One important ecology factor contributing particularly to variation in mass might be socioeconomic condition. For example, condition influences mass differences in both developed and developing countries [10], equally well equally mass modify over fourth dimension in adult countries [eleven]. Although socioeconomic status besides influences homo elevation, this effect might exist more than the consequence of social assortment than variation in diet or activeness [12], [xiii]. It is, of course, true that other animals are also influenced by status and nutrition [xiv]–[16], but perhaps humans have a greater and more consistent availability of the cheap, high energy, processed foods that promote mass gain [17] or greater exposure to societal pressures that contribute to mass loss [18]. Testing these hypotheses for differences between humans and other animals in relative levels of acme versus mass variation volition require further study.
Another interesting consequence was that humans testify low within-population variation in trunk height in comparing to torso length in not-homo animals (Figure two), only the same was not true for human mass relative to animal mass (Effigy S1). These differences can be quantified through several different comparisons. First, the hateful inside-population CVs for male and female person man height correspond to the 8th and 4th percentiles, respectively, of the hateful inside-population CVs for fauna length. In dissimilarity, the mean within-population CVs for male and female person human mass represent to the 56th and 60th percentiles, respectively, of the within-population CVs for animate being mass. Second, we compared each human population mean individually to the distribution of brute species ways – to meet whether our results were robust to which detail human being population was considered. Here nosotros constitute that all but 8 of 101 human being male samples, and all just 5 of 96 human female samples, had within-population CVs for height that brutal beneath the 25thursday percentile of the mean within-population CVs for creature length. In dissimilarity, 82 of 98 human male samples and 62 of xc human female person samples fell between the 25th and 65th percentiles of the mean within-population CVs for fauna mass. All of the in a higher place results are robust to correction for associations between CVs and mean trait sizes (run across Methods and Materials).
Distributions of coefficients of variation (CV) for within-population body length or pinnacle.
Shown are species means for animals (black) and population ways for humans (gray) for males (A) and females (B). Arrows indicate the locations of CVs for mean homo elevation.
Why, in comparing to other animals, practice humans show depression within-population variation in peak? The first critical point is that this difference in CVs might reflect differences betwixt humans and other creature species in whatsoever of the components of quantitative variation, including condiment genetic variance (VA), say-so genetic variance (VD), epistatic genetic variance (VI), maternal effects variance (VM), and environmental variance (FiveDue east) – with the concluding of these including potential phenotypic plasticity [nineteen]. We are not enlightened of whatever studies that directly discriminate among each of these alternatives in a quantitative comparison based on comparable methods applied across many creature species and humans. While acknowledging these possible alternative sources of differences in variation, we here consider the particularly interesting set up of hypotheses related to possible differences in VA, the currency of adaptation. Thus, differences between species might reverberate differences in factors that increment VA (mutation, recombination, gene period) or decrease VA (stabilizing or directional option, genetic drift). In view of the wealth of evidence for selection on body size across the creature kingdom [20], we here focus on developing hypotheses related to selection, before later considering some alternatives.
Several possibilities exist for how choice might strongly reduce additive genetic variation for homo height. First, some studies take suggested stabilizing natural selection on human height by way of increased wellness problems in very brusque and very alpine individuals [21], [22]. Second, some studies take suggested directional sexual choice on male homo height; taller men often have more sexual partners [21]–[23] and more children [24]. Given that both stabilizing and directional selection should erode genetic variation [25], natural and sexual pick might act together to decrease human meridian variation. (Note that depression genetic variation for meridian is not incompatible with a pregnant heritability - if ecology effects are likewise low.) Mayhap these selective factors are stronger in humans than in other animals – but this has not been studied.
Our analyses of amongst-population variation assist to refine the above hypothesis that selection might reduce height variation in humans relative to other animals. In detail, humans show levels of amid-population variation in height that are similar to that seen in other animals (Figure S2). Specifically, the mean among-population CVs for male and female human meridian correspond to the 47th and 51st percentiles, respectively, of hateful among-population CVs for animal length. Illustrated another way, humans show relatively low levels of within-population variation in acme given their among-population variation in height (Figure 3). Specifically, when considering residuals from a regression of inside-population CVs for length on among-population CVs for length, human males and females fall into the twentyth and ixth percentiles, respectively.
Species-mean CVs for among-population versus within-population body length or height.
Shown are regression lines (solid), x = y lines (dashed), and data for males (A, R2 = 0.29, P = 0.001) and females (B, R2 = 0.23, P<0.001).
Nosotros hypothesize that this pattern of unremarkable amidst-population variation in human height, coupled with relatively low inside-population variation in homo peak, is consistent with evolution in response to potent selection for optima that differ amidst geographic locations. In the dictionary of evolutionary biological science [26], the hypothesis is that humans have evolved on a rugged adaptive landscape characterized by abrupt fettle peaks that correspond to locally-optimal body sizes that differ among locations. This idea is consistent with several previous arguments for local adaptation in human height. For example, human height increases with increasing breadth [27] (equally was too the case in our data set, Figure S3), and with decreasing mean annual temperature [28]. Humans thus follow Bergmann's rule, perhaps considering larger bodies are more resistant to heat loss in cold climates – or for other reasons [29]. As another case, the short stature of human being pygmies is thought to take evolved via strong selection for small body sizes [30] or life-history trade-offs [31] that characterize their particular tropical forest environments. Our study complements these previous adaptive interpretations past revealing that height variation is low within populations. In short, we hereby add the "rugged" aspect to the existing idea of adaptive peaks that differ among locations.
Several potential complications and alternatives to the part of selection need to be discussed. First, for local adaptation to exist substantial, gene period has to be somewhat express amidst populations [32]. This does seem to be the case for humans, at least historically, given the evidence for broad-calibration regional clustering of neutral genetic variation [33]–[35]. If populations can diverge appreciably in these neutral genetic markers, and so they should be able to diverge easily in response to different selection pressures. Moreover, factor menstruum might exist reduced for genes specifically influencing height because humans often show pinnacle-assortative mating [36], [37]. Second, genetic drift is an unlikely explanation for variation in human height among populations because correlations with likely selective factors (due east.1000., temperature) then would not be and so strong and repeatable. Third, plasticity due to geographical differences in babyhood nutrition or other environmental factors could account for high variation among, relative to within, populations. Fourth, within-population CVs for human being elevation might be depression due to reduced FiveDue east rather than reduced FiveA, for instance due to niche construction leading to reduced environmental variance [38]. However, arguing confronting these latter two possibilities, human mass, which is even more than plastic than man height (meet higher up) and is probable influenced by like environmental factors equally is man height, does not testify reduced within-population variation relative to amid-population variation in comparing to other animals (Figure S4).
In decision, nosotros accelerate the hypothesis that humans have evolved on a rugged adaptive mural, at least for body elevation. Information technology would be interesting to encounter if this hypothesis is supported by analyses of variation in other traits that are shared between humans and other animals. In addition, comparing humans specifically to closely related creature species (i.east., other primates) might requite some clue equally to whether these forces are specific to humans within the primate order. In any example, we suggest that the adaptive mural metaphor might provide a useful framework for advancing our understanding of diversification in humans.
Materials and Methods
We searched the literature for studies reporting means and variation in body size for at to the lowest degree one population of a species. Cardinal words for searches included "body size" and "variation." Citations from the resulting sources were also examined; for humans, many additional sources were taken from Katzmarzyk and Leonard [28]. Of these studies, we farther consider simply those that examined wild populations (for non-human animals) and adult individuals (as divers in each study, or 18+ years for humans). If more than ane study examined the same population, simply the about recent study was used. In total, our dataset (Tables S1 and S2) comprised of 55 studies (99 populations) of humans and 107 studies and 210 species (848 populations) of other animals. This included studies from a diversity of fauna taxa (10 amphibian, xv bird, three fish, 54 invertebrate, 95 mammal, and 33 reptile) and dissimilar types of human populations (e.g., 29 indigenous/ancient, 40 Least Developed (http://www.un.org/special-rep/ohrlls/ldc/list.htm)). Raw data is bachelor from the authors upon asking. Due to the big size of our animate being dataset, and the great diversity of species and populations from across the whole beast phylogeny, nosotros did not apply phylogenetic-based analyses (for a simpler culling analysis run across below).
For each sample, we calculated the within-population coefficient of variation (CV) for body length (peak) or mass so averaged these within-population CVs across the sampled populations. This procedure yielded mean within-population CVs for each species. We calculated among-population CVs by using the mean body size measures for each population. We and so evaluated in what percentile homo means lie within the overall distribution of animal means. This was done both for distributions of mean values (i.e., Figures two, S1 and S2) as well equally for residuals of regression plots (i.e., Figures ane, 3, and S4). When comparing the relative association betwixt body length and mass CVs amid species (i.due east., Figure 1), CVs for mass were divided by three so as to exist straight comparable in dimensionality to CVs for length [39].
We plant no association between CVs and sample sizes either within or among populations for length or mass (results not shown), suggesting that variation in sample size did not influence our results. In dissimilarity, we did find a negative association between trait size (eastward.g., hateful trunk length) and trait CV (see Houle [40]) within populations for male length (r = −0.35, P<0.01), female person length (r = −0.26, P<0.01), male person mass (r = −0.27, P<0.01), and female person mass (r = −0.24, P<0.01), and amongst populations for female length (r = −0.063, P = 0.031) simply not male person length (r = 0.0052, P = 0.56). However, restricting our analysis to animal species with trunk sizes within the range of human torso size did not influence our conclusions that (1) humans have depression levels of within-population variation in height (6th percentile for males and 0th percentile for females), but (two) not within-population variation in mass (65th percentile for males and 42nd percentile for females) or (3) among-population variation in height (45th percentile for males and 71st percentile for females).
To assess the generality of our results, nosotros performed the in a higher place analyses with various subsets of the data. Our chief conclusions, every bit described in a higher place, did not change in any case. We therefore merely here list these additional analyses without providing the details. First, the authors of a given written report typically defined each "population" as such, or these designations were implicitly obvious. In a few studies, however, the specific populations were less clear (due east.chiliad., museum collections over broad regions) – but our conclusions were the same when excluding these more ambiguous cases. Second, conclusions were the same when including or excluding animal species in which tail length was included in body length measurements. Third, conclusions were the same when considering (1) only human studies published before or after 1974 (the median study date, see Table S2), (two) human being studies of only indigenous/aboriginal populations (as divers in each study) or only non-indigenous/aboriginal populations, and (3) human studies from only Least Developed Countries (http://www.un.org/special-rep/ohrlls/ldc/list.htm) or merely non-To the lowest degree Developed Countries. 4th, conclusions were the same when humans were compared specifically to different taxomonic groups (Tabular array S3), although the distinctiveness of within-population CVs for male (merely non female) tiptop was less stiff (eighteenth percentile) when humans were compared only to other mammals. Overall, then, our conclusions are robust to the inclusion or exclusion of detail human populations or animal species.
Supporting Data
Table S1
List of all studies, species, and taxa (amphibian, bird, fish, invertebrate, mammal, or reptile) used to obtain coefficients of variation (CV) for male person and/or female length and/or mass for brute populations.
(0.25 MB DOC)
Table S2
List of all studies used to obtain CVs for male and/or female person acme and/or mass for human populations. Also included is the country of origin, name of specific population or survey title, year of sampling (if provided), indigenous/ancient condition (equally defined in each study), and development status (http://world wide web.un.org/special-rep/ohrlls/ldc/list.htm).
(0.eleven MB Doctor)
Table S3
Percentiles for mean within- and among-population male and female human tiptop and mass in relation to species-hateful amphibian, invertebrate, mammal, and reptile length and mass distributions. Percentiles are not shown for taxa distributions with n<5 brute species.
(0.03 MB DOC)
Figure S1
Distributions of coefficients of variation (CV) for within-population trunk mass. Shown are species ways for animals (black) and population means for humans (grey) for males (A) and females (B). Arrows bespeak the locations of CVs for mean human mass.
(one.80 MB TIF)
Figure S2
Distributions of CVs for amidst-population torso length or height. Shown are data for males (A) and females (B). Arrows indicate the locations of CVs for mean human being elevation.
(ane.72 MB TIF)
Effigy S3
Bergmann'southward dominion in humans. Mean male person height (A, R2 = 0.126, P<0.001), female superlative (B, R2 = 0.097, P = 0.002), male mass (C, Rtwo = 0.183, P<0.001), and female mass (D, R2 = 0.155, P<0.001) all increase significantly with accented latitude. Latitude of each population was approximated using the geographic centre of the country from which the population was sampled. Coordinates were obtained from the CIA World Factbook (https://www.cia.gov/library/publications/the-world-factbook/fields/2011.html).
(1.06 MB TIF)
Figure S4
Species-hateful CVs for among- versus within-population torso mass. Shown are regression lines (solid), x = y lines (dashed), and data for males (A, Rii = 0.26, P<0.001) and females (B, Rtwo = 0.37, P<0.001).
(1.72 MB Physician)
Acknowledgments
We thank Lonnie Aarssen, Alexandre Courtiol, Erika Crispo, Raymond Huey, David Lahti, Paul Martin, Laurene Ratcliffe, Michel Raymond, and Robert Walker for providing comments on the manuscript.
Footnotes
Competing Interests: The authors take alleged that no competing interests exist.
Funding: AEM and APH are funded by the Natural Sciences and Engineering Enquiry Council of Canada (world wide web.nserc-crsng.gc.ca). The funders had no part in study design, data collection and analysis, decision to publish, or grooming of the manuscript.
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