How Animals And Humans Have Similar Bodies
PLoS One. 2009; 4(9): e6876.
How Humans Differ from Other Animals in Their Levels of Morphological Variation
Ann East. McKellar
one Department of Biological science, Queen'south Academy, Kingston, Canada
Andrew P. Hendry
ii Redpath Museum and Department of Biology, McGill Academy, Montreal, Canada
Rebecca Sear, Editor
Received 2009 Mar xi; 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 fauna populations.
(0.25 MB Medico)
GUID: 064AD077-C7C7-45C4-BE73-FA559125F7EC
Table S2: List of all studies used to obtain CVs for male person and/or female person height and/or mass for man populations. Also included is the state of origin, name of specific population or survey title, year of sampling (if provided), indigenous/ancient status (every bit defined in each report), and development status (http://world wide web.united nations.org/special-rep/ohrlls/ldc/list.htm).
(0.11 MB DOC)
GUID: CF7CBAC0-EC0F-42A1-8AC9-BB912056C247
Table S3: Percentiles for hateful within- and amongst-population male and female human summit and mass in relation to species-mean amphibian, invertebrate, mammal, and reptile length and mass distributions. Percentiles are not shown for taxa distributions with n<5 animal species.
(0.03 MB DOC)
GUID: 10F768E8-24CF-48F0-B123-5CE52D8BEC5C
Effigy S1: Distributions of coefficients of variation (CV) for within-population torso mass. Shown are species means for animals (blackness) and population means for humans (grey) for males (A) and females (B). Arrows point the locations of CVs for hateful human mass.
(i.80 MB TIF)
GUID: 0DC9C367-A944-43A9-BD69-1F6DBF031B66
Figure S2: Distributions of CVs for among-population body length or height. Shown are data for males (A) and females (B). Arrows indicate the locations of CVs for hateful human height.
(1.72 MB TIF)
GUID: 658843AF-A106-48BC-AA59-68CC0F8CA476
Figure S3: Bergmann'due south rule in humans. Mean male height (A, Rtwo = 0.126, P<0.001), female height (B, R2 = 0.097, P = 0.002), male mass (C, R2 = 0.183, P<0.001), and female person mass (D, R2 = 0.155, P<0.001) all increase 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 World Factbook (https://www.cia.gov/library/publications/the-world-factbook/fields/2011.html).
(1.06 MB TIF)
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Effigy S4: Species-mean CVs for amid- 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 DOC)
GUID: 813EDECB-A50A-4E5E-BE6F-62FA8CE9091C
Abstract
Fauna species come up in many shapes and sizes, every bit exercise the individuals and populations that make up each species. To the states, humans might seem to prove particularly loftier levels of morphological variation, but perhaps this perception is simply based on enhanced recognition of individual conspecifics relative to individual heterospecifics. We hither more than considerately ask how humans compare to other animals in terms of body size variation. We quantitatively compare levels of variation in body length (height) and mass within and among 99 human being populations and 848 animal populations (210 species). We find that humans show low levels of within-population body height variation in comparison to trunk length variation in other animals. Humans do not, still, prove distinctive levels of within-population body mass variation, nor of amid-population body height or mass variation. These results are consistent with the thought that natural and sexual selection have reduced human top variation inside populations, while maintaining it among populations. Nosotros therefore hypothesize that humans have evolved on a rugged adaptive landscape with strong pick for body peak optima that differ among locations.
Introduction
Variation is the raw material for development, and it is ubiquitous both within and among populations [1]. Withal, the balance between forces enhancing variation and forces eroding it likely differs among populations and species. Accordingly, the magnitude of morphological variation tin can differ markedly amidst species [one]. As humans, how do 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 beast group, such as a flock of birds or a shoal of fish. But perhaps this apparent contrast betwixt humans and other animals is but a matter of our perception – that is, evolution has probably shaped animals to be more than discriminating amongst individual conspecifics than among individual heterospecifics [2], [3]. Alternatively, gimmicky homo populations might indeed show greater morphological variation than other species. Possible reasons might include relaxed natural choice on some human traits [4] (although mayhap non on others [v]), the great multifariousness of conditions we can (and do) inhabit, and recurrent migration and gene flow [half dozen] among populations. Or possibly humans instead show lower levels of variation – a point we will render to later.
Our goal is to quantitatively determine how levels of morphological variation inside humans compare to those in other animal species. Nosotros use body size as our focal morphological variable because this trait tin exist logically compared among species, and considering body size data are readily available for a broad diversity of fauna populations, both human and non-human (see Tables S1 and S2). In an effort to obtain unbiased information, nosotros searched the literature for ways and variances in body height or body length (these 2 terms are here used interchangeably, depending on context) and body mass both inside and among populations of humans and other animals. From these information, we calculated the coefficient of variation (CV; standard deviation divided by the mean) as a standardized measure of variance among individuals inside populations and among population ways. In total, our dataset included trunk 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
Ane interesting result was that humans, in comparison to other animals, show a loftier level of within-population variation in mass because their inside-population variation in height (Figure 1). Specifically, when considering 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 information for males (A, Rtwo = 0.81, P<0.001) and females (B, Rtwo = 0.58, P<0.001).
Why, in comparison to other animals, do humans show high variation in mass relative to summit? Ane contributing factor might exist that human height is developmentally determinate, and is therefore relatively stable once an individual reaches maturity. Mass, in contrast, tin can fluctuate dramatically subsequently maturity based on historic period, diet, and activeness level. In line with this greater ecology (equally opposed to genetic) contribution to mass than to length, heritabilities are commonly lower for mass than for peak in humans [7]–[nine]. One important environmental factor contributing particularly to variation in mass might exist socioeconomic status. For example, status influences mass differences in both adult and developing countries [x], also every bit mass change over fourth dimension in developed countries [11]. Although socioeconomic status also influences human acme, this effect might exist more the result of social assortment than variation in diet or activity [12], [13]. It is, of grade, truthful that other animals are also influenced by status and nutrition [fourteen]–[16], but perchance humans accept a greater and more consequent availability of the cheap, loftier free energy, processed foods that promote mass proceeds [17] or greater exposure to societal pressures that contribute to mass loss [18]. Testing these hypotheses for differences betwixt humans and other animals in relative levels of superlative versus mass variation will crave further report.
Some other interesting result was that humans show low within-population variation in trunk height in comparison to body length in not-human being animals (Figure 2), but the same was non true for homo mass relative to animal mass (Figure S1). These differences tin be quantified through several different comparisons. First, the mean within-population CVs for male and female human height correspond to the 8th and ivth percentiles, respectively, of the mean within-population CVs for animate being length. In contrast, the hateful inside-population CVs for male and female man mass correspond to the 56th and 60th percentiles, respectively, of the inside-population CVs for animal mass. Second, we compared each homo population hateful individually to the distribution of animal species means – to come across whether our results were robust to which particular human population was considered. Here nosotros found that all simply 8 of 101 man male person samples, and all merely 5 of 96 human being female samples, had within-population CVs for height that fell beneath the 25thursday percentile of the mean inside-population CVs for animal length. In contrast, 82 of 98 human male samples and 62 of 90 homo female samples vicious between the 25th and 65th percentiles of the mean within-population CVs for animal mass. All of the above results are robust to correction for associations between CVs and mean trait sizes (encounter Methods and Materials).
Distributions of coefficients of variation (CV) for inside-population torso length or top.
Shown are species means for animals (black) and population means for humans (grey) for males (A) and females (B). Arrows indicate the locations of CVs for hateful human height.
Why, in comparing to other animals, exercise humans show depression within-population variation in superlative? The first critical point is that this divergence in CVs might reflect differences between humans and other animal species in any of the components of quantitative variation, including additive genetic variance (VA), dominance genetic variance (VD), epistatic genetic variance (VI), maternal effects variance (VOne thousand), and ecology variance (5East) – with the final of these including potential phenotypic plasticity [19]. 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 animal species and humans. While acknowledging these possible alternative sources of differences in variation, we here consider the specially interesting set of hypotheses related to possible differences in VA, the currency of adaptation. Thus, differences betwixt species might reflect differences in factors that increase VA (mutation, recombination, gene flow) or decrease VA (stabilizing or directional selection, genetic drift). In view of the wealth of show for selection on body size across the creature kingdom [20], we here focus on developing hypotheses related to selection, before after considering some alternatives.
Several possibilities exist for how selection might strongly reduce additive genetic variation for human height. First, some studies have suggested stabilizing natural pick on human height by manner of increased wellness problems in very curt and very alpine individuals [21], [22]. Second, some studies have suggested directional sexual choice on male person human top; taller men often take more sexual partners [21]–[23] and more children [24]. Given that both stabilizing and directional option should erode genetic variation [25], natural and sexual option might act together to decrease homo height variation. (Note that low genetic variation for meridian is non incompatible with a significant heritability - if environmental furnishings are likewise depression.) Perhaps these selective factors are stronger in humans than in other animals – merely this has not been studied.
Our analyses of among-population variation assist to refine the above hypothesis that selection might reduce height variation in humans relative to other animals. In particular, humans evidence levels of among-population variation in height that are similar to that seen in other animals (Figure S2). Specifically, the mean amongst-population CVs for male and female human meridian correspond to the 47th and 51st percentiles, respectively, of mean among-population CVs for animal length. Illustrated another style, humans bear witness relatively depression levels of within-population variation in peak given their amongst-population variation in meridian (Figure three). Specifically, when considering residuals from a regression of within-population CVs for length on among-population CVs for length, homo males and females fall into the 20th and 9thursday percentiles, respectively.
Species-mean CVs for among-population versus within-population body length or peak.
Shown are regression lines (solid), ten = y lines (dashed), and data for males (A, R2 = 0.29, P = 0.001) and females (B, Rii = 0.23, P<0.001).
Nosotros hypothesize that this blueprint of unremarkable among-population variation in human meridian, coupled with relatively depression within-population variation in human being height, is consistent with evolution in response to strong selection for optima that differ among geographic locations. In the lexicon of evolutionary biological science [26], the hypothesis is that humans have evolved on a rugged adaptive landscape characterized by sharp 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 latitude [27] (equally was besides the case in our data set, Figure S3), and with decreasing mean annual temperature [28]. Humans thus follow Bergmann'southward rule, perhaps because larger bodies are more resistant to heat loss in cold climates – or for other reasons [29]. As some other example, the short stature of human pygmies is thought to have evolved via strong option for small-scale body sizes [30] or life-history trade-offs [31] that characterize their particular tropical forest environments. Our study complements these previous adaptive interpretations by revealing that top variation is low within populations. In short, we hereby add the "rugged" attribute to the existing idea of adaptive peaks that differ amidst locations.
Several potential complications and alternatives to the role of selection demand to be discussed. Kickoff, for local accommodation to exist substantial, factor catamenia has to be somewhat express among populations [32]. This does seem to exist the case for humans, at to the lowest degree historically, given the evidence for broad-scale regional clustering of neutral genetic variation [33]–[35]. If populations tin diverge appreciably in these neutral genetic markers, then they should be able to diverge easily in response to unlike selection pressures. Moreover, gene flow might be reduced for genes specifically influencing summit considering humans often show height-assortative mating [36], [37]. Second, genetic drift is an unlikely caption for variation in human height amongst populations because correlations with likely selective factors (e.g., temperature) then would not be so strong and repeatable. Tertiary, plasticity due to geographical differences in childhood nutrition or other environmental factors could business relationship for high variation amongst, relative to within, populations. Fourth, within-population CVs for human height might be depression due to reduced VE rather than reduced VA, for instance due to niche construction leading to reduced environmental variance [38]. However, arguing against these latter 2 possibilities, human being mass, which is even more plastic than human height (see higher up) and is probable influenced by similar ecology factors every bit is homo height, does not show reduced inside-population variation relative to among-population variation in comparison to other animals (Effigy S4).
In conclusion, we accelerate the hypothesis that humans have evolved on a rugged adaptive landscape, at to the lowest degree for body height. It would be interesting to see if this hypothesis is supported by analyses of variation in other traits that are shared betwixt humans and other animals. In add-on, comparison humans specifically to closely related beast species (i.eastward., other primates) might give some clue every bit to whether these forces are specific to humans within the primate society. In whatsoever case, nosotros suggest that the adaptive landscape metaphor might provide a useful framework for advancing our agreement of diversification in humans.
Materials and Methods
We searched the literature for studies reporting means and variation in trunk size for at least one population of a species. Primal 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 further consider only those that examined wild populations (for not-human being animals) and developed individuals (equally divers in each written report, or 18+ years for humans). If more than than one written report examined the same population, only the near 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 variety of animal taxa (x amphibian, 15 bird, 3 fish, 54 invertebrate, 95 mammal, and 33 reptile) and different types of homo populations (e.g., 29 ethnic/aboriginal, 40 To the lowest degree Adult (http://www.un.org/special-rep/ohrlls/ldc/list.htm)). Raw data is available from the authors upon asking. Due to the large size of our creature dataset, and the nifty variety of species and populations from across the whole beast phylogeny, we did not use phylogenetic-based analyses (for a simpler culling analysis see below).
For each sample, nosotros calculated the within-population coefficient of variation (CV) for body length (height) or mass then averaged these inside-population CVs across the sampled populations. This procedure yielded mean within-population CVs for each species. We calculated among-population CVs by using the hateful torso size measures for each population. Nosotros then evaluated in what percentile human means lie inside the overall distribution of animal means. This was done both for distributions of mean values (i.e., Figures 2, S1 and S2) besides as for residuals of regression plots (i.e., Figures one, 3, and S4). When comparing the relative association between torso length and mass CVs among species (i.e., Figure 1), CVs for mass were divided by iii so every bit to be directly comparable in dimensionality to CVs for length [39].
We institute no association between CVs and sample sizes either inside or amidst populations for length or mass (results not shown), suggesting that variation in sample size did not influence our results. In contrast, we did find a negative clan betwixt trait size (e.g., mean body length) and trait CV (run into Houle [twoscore]) inside 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 mass (r = −0.24, P<0.01), and amidst populations for female length (r = −0.063, P = 0.031) but not male length (r = 0.0052, P = 0.56). Even so, restricting our analysis to creature species with body sizes within the range of human torso size did not influence our conclusions that (1) humans have low levels of within-population variation in height (vithursday percentile for males and 0th percentile for females), simply (2) not within-population variation in mass (65thursday percentile for males and 42nd percentile for females) or (3) among-population variation in height (45thursday percentile for males and 71st percentile for females).
To assess the generality of our results, we performed the above analyses with various subsets of the data. Our main conclusions, as described to a higher place, did not change in whatever case. Nosotros therefore only here list these boosted analyses without providing the details. Offset, the authors of a given study typically divers each "population" as such, or these designations were implicitly obvious. In a few studies, yet, the specific populations were less articulate (e.g., museum collections over broad regions) – only our conclusions were the same when excluding these more than ambiguous cases. 2d, conclusions were the same when including or excluding animal species in which tail length was included in torso length measurements. 3rd, conclusions were the same when considering (1) only human studies published before or later 1974 (the median report appointment, run into Table S2), (2) human studies of only indigenous/aboriginal populations (as defined in each report) or only non-indigenous/aboriginal populations, and (three) human studies from only Least Developed Countries (http://www.un.org/special-rep/ohrlls/ldc/listing.htm) or merely non-Least Developed Countries. Fourth, conclusions were the same when humans were compared specifically to different taxomonic groups (Table S3), although the distinctiveness of inside-population CVs for male person (but non female) acme was less strong (18thursday percentile) when humans were compared only to other mammals. Overall, then, our conclusions are robust to the inclusion or exclusion of particular human being populations or creature species.
Supporting Information
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 person length and/or mass for creature populations.
(0.25 MB Medico)
Tabular array S2
List of all studies used to obtain CVs for male person and/or female superlative and/or mass for human populations. Also included is the land of origin, name of specific population or survey championship, year of sampling (if provided), indigenous/aboriginal status (as defined in each study), and development status (http://world wide web.un.org/special-rep/ohrlls/ldc/list.htm).
(0.xi MB Doc)
Table S3
Percentiles for mean within- and among-population male and female human being height and mass in relation to species-hateful amphibian, invertebrate, mammal, and reptile length and mass distributions. Percentiles are not shown for taxa distributions with north<five animal species.
(0.03 MB DOC)
Figure S1
Distributions of coefficients of variation (CV) for within-population body mass. Shown are species means for animals (black) and population ways for humans (grey) for males (A) and females (B). Arrows signal the locations of CVs for mean human mass.
(1.lxxx MB TIF)
Effigy S2
Distributions of CVs for among-population torso length or height. Shown are data for males (A) and females (B). Arrows betoken the locations of CVs for mean human pinnacle.
(1.72 MB TIF)
Figure S3
Bergmann's dominion in humans. Hateful male height (A, Rtwo = 0.126, P<0.001), female height (B, R2 = 0.097, P = 0.002), male mass (C, Rtwo = 0.183, P<0.001), and female mass (D, Rtwo = 0.155, P<0.001) all increase significantly with absolute latitude. Breadth of each population was approximated using the geographic eye of the country from which the population was sampled. Coordinates were obtained from the CIA World Factbook (https://www.cia.gov/library/publications/the-globe-factbook/fields/2011.html).
(one.06 MB TIF)
Figure S4
Species-hateful CVs for among- versus within-population body mass. Shown are regression lines (solid), x = y lines (dashed), and information for males (A, R2 = 0.26, P<0.001) and females (B, R2 = 0.37, P<0.001).
(ane.72 MB Doctor)
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 accept declared that no competing interests be.
Funding: AEM and APH are funded by the Natural Sciences and Engineering Enquiry Council of Canada (www.nserc-crsng.gc.ca). The funders had no role in study design, data collection and analysis, determination to publish, or preparation of the manuscript.
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