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ABSTRACT The second-to-fourth digit ratio (2D:4D) more pronounced markers of PAE (lower 2D:4D) than
has been proposed as a biomarker reflecting prenatal pair-bonded species. Our results accord with those
androgen effects (PAE), such that individuals with found in humans: 2D:4D is lower in polygynous species
lower ratios have experienced higher PAE than those and higher (lower PAE) in pair-bonded species. Old
with higher ratios. 2D:4D has been correlated with a World monkeys have low, and relatively invariant
number of sex-linked traits in humans such as aggres- 2D:4D (high PAE), which is coupled with high levels of
sion, promiscuity, and competitiveness. In addition, intrasexual competition. This contrasts with higher and
polygynous societies reportedly have lower 2D:4D more variable ratios in both great apes and New World
(higher PAE) than more monogamous populations. This monkeys. In addition, both male and female ratios
evidence suggests that PAE may be implicated in the decrease with increasing levels of intrasexual competi-
development of sexually selected behaviors in humans. tion. Human ratios are intermediate between pair-
To place 2D:4D research into a broader context, we test bonded and more promiscuous hominoids. We propose
the relationship between digit ratios and behavior that PAE may be involved in promoting species charac-
across nonhuman anthropoids; polygynous species, with teristic social behavior in anthropoids. Am J Phys
higher levels of intrasexual competition, should have Anthropol 141:395–405, 2010. V 2009 Wiley-Liss, Inc.
C
A substantial body of research is built upon the 2006). Additionally, 2D:4D has been shown to be moder-
hypothesis that second-to-fourth digit length ratio (2D:4D) ately to highly heritable between generations (see Vora-
negatively correlates with prenatal androgen effects cek and Dressler, 2009). Although the physiological
(PAE), more specifically low 2D:4D is associated with high interplay between genetic and gestational effects (see
prenatal testosterone (Manning, 2002; 2008). 2D:4D has below) is not completely understood, it has been pro-
been shown to negatively correlate with indirect measures posed that 2D:4D can be used as a proxy for early andro-
of PAE across numerous studies (see Manning et al., 2007 gen exposure and can be informative about the develop-
for overviews). For example, low 2D:4D (high PAE) in ment of androgenic-programmed traits (Manning, 2002).
infants is associated with high levels of amniotic testoster- In light of this, a wide ranging literature has devel-
one (Lutchmaya et al., 2004). Females exposed to high oped that links 2D:4D to behavioral traits in humans
androgens in utero, such as those with congenital adrenal (Voracek and Loibl, 2009). Low 2D:4D, which potentially
hyperplasia and polycystic ovary syndrome have more indicates high levels of androgen exposure during devel-
masculinized (low) 2D:4D ratios, compared to healthy con- opment and masculinization, has been linked in both
trols (Brown et al., 2002; Ötken et al., 2002; but see Buck sexes to increased intrasexual competition (Hönekopp
et al., 2003; Cattrall et al., 2005). Females with a male co- et al., 2005a), mate seeking (Clark, 2004; Hönekopp
twin have lower 2D:4D ratios than females with a same- et al., 2005b), and higher levels of aggression (Bailey
sex co-twin that is suggestive of intrauterine hormonal and Hurd, 2004; Benderlioglu and Nelson, 2004). In
(androgen) transfer between siblings (van Anders et al., males, lower 2D:4D has been associated with higher
2006; but see Medland et al., 2008). dominance (Neave et al., 2003; Manning and Fink,
The mechanism proposed to underpin these associa-
tions is androgen sensitivity in the homeobox (HOX)
gene cluster (Manning et al., 1998). The posterior HOXa Grant sponsors: University of Liverpool Research Fund, British
Academy Centenary Research Project.
and HOXd genes organize the development of the termi-
nal limb-bud (digits) and parts of the reproductive sys-
*Correspondence to: Emma Nelson, School of Archaeology, Clas-
tem (including the gonads, penile bone and penis) sics and Egyptology, Hartley Building, Brownlow Street, University
(Kondo et al., 1997; Zákány et al., 1997; Montavon et al., of Liverpool, Liverpool L69 3GS, United Kingdom.
2008). The fourth digit (ring finger) appears to be partic- E-mail: enelson@liv.ac.uk
ularly sensitive to PAE such that individuals exposed to
high PAE have longer ring fingers relative to their index Received 29 January 2009; accepted 7 July 2009
fingers (McIntyre et al., 2005; 2006). Although there is
substantial overlap, 2D:4D tends to be lower in males DOI 10.1002/ajpa.21157
than females (McFadden and Shubel, 2002) with differ- Published online 27 October 2009 in Wiley InterScience
ences evident from 9 weeks of development (Malas et al., (www.interscience.wiley.com).
C 2009
V WILEY-LISS, INC.
396 E. NELSON AND S. SHULTZ
2008), status-seeking (Millet and Dewitte, 2008), physi- females, as is found in polygynous systems, could lead to
cal strength (Fink et al., 2006), and behaviors that selection for high PAE (Manning et al., 2004b; Manning,
attract mates (Roney and Maestripieri, 2004). PAE is 2008). High circulating androgens promote male compet-
negatively associated with reproductive success in males, itive behavior (Klein, 2000) and mechanisms facilitating
but positively associated with fitness in females (Man- dominance and aggression may be most adaptive in pop-
ning and Fink, 2008). Low male 2D:4D has been linked ulations where males experience strong competition for
to a higher number of sexual partners in males (Höne- access to females (Grey, 2003). In addition, in species
kopp et al., 2005b), although this was unsupported by an that experience high competition for resources (mates
earlier study (Rahman et al., 2005). Similarly, higher and food), exposure to high prenatal androgens may also
sperm quality and plasma testosterone has been linked be important in supporting female social hierarchies
with lower 2D:4D in some studies (Manning et al., (Ostner et al., 2003; Dloniak et al., 2006).
1998), but is not supported by others (e.g. Neave et al., On the basis of the associations between 2D:4D and
2003; Benderlioglu and Nelson, 2004; Bang et al., 2005). sex-linked traits, Fink et al. (2006) proposed that
In contrast to traits linked with low 2D:4D (high PAE), variation in human 2D:4D should be viewed within a
high ratios (low PAE) have been implicated in the devel- framework of sexual selection theory. Demonstrating
opment of prosocial behaviors and sensitivity in children relationships between 2D:4D and levels of sexual compe-
(Williams et al., 2003; Fink et al., 2007). Although intra- tition in other species would extend this conclusion.
population trends tend to be in the predicted direction HOX genes are strongly conserved within and between
(low 2D:4D 5 more masculine traits), correlations are taxonomic groups (Zákány et al., 1997), associations
generally weak and some studies have been difficult to between 2D:4D and traits organized by PAE should
replicate (Putz et al., 2004). However, these issues may, therefore be common in pentadactyl organisms (Man-
in-part, be associated with methodological inconsisten- ning, 2002). Although 2D:4D has been studied in a num-
cies (see Manning and Fink, 2008) and sampling differ- ber of diverse vertebrate species (see Lombardo and
ences (i.e. variation in genetic and maternal effects Thorpe, 2008 for an overview), there have been no com-
within and between samples). prehensive cross-species studies of the relationship
Prenatal androgens organize the brain and body tis- between 2D:4D and sexually selected behaviors. Most
sues at a cellular level according to sex-specific patterns nonhuman studies have concentrated on demonstrating
(Collaer and Hines, 1995; Cooke et al., 1998; Fitch and intraspecific sex differences in 2D:4D or bone derived
Bimonte, 2002). They are crucial to sexing the male phe- ratio (McFadden and Bracht, 2005) but these have not
notype, but also play a role in female development always been in the expected directions, that is, males do
(Herman et al., 2000). Studies observing individual dif- not always have lower 2D:4D ratios than females (see
ferences in social behavior after manipulation of prena- Roney et al., 2004; Rubolini et al., 2006).
tal androgens in female rhesus macaques suggest that A few studies have looked at sexually selected physical
high levels of PAE may be implicated in programming traits within species, but these have yielded conflicting
some masculinized behaviors such as foot-clasp mount- results. For example, hind-limb 2D:4D is negatively
ing and rough-and-tumble play, although these were related to tail length in barn swallows (Dreiss et al.,
dependent on dosage and timing of the treatment (Goy 2007), but positively related to visible badge size in male
et al., 1988; Wallen, 1996). Expression of sex-linked house sparrows (Navarro et al., 2007), although both are
social behaviors (whether manipulated by hormone sexually selected characters. In mice, aggression is sig-
treatments or not), however, were also influenced by nificantly related to 2D:4D but in the opposite direction
social learning and context (Wallen, 1996; 2005). In to humans (2D:4D was positively related to aggression
humans, studies correlating the development of social in the mice) (Bailey et al., 2005). However, a recent
behaviors with prenatal testosterone (PT), assayed from study in which rats were administered androgens during
amniotic fluid, also suggest that PAE may influence neu- pregnancy, showed that the 2D:4D ratios of their adult
ral pathways implicated in social development (Knick- offspring (males and females) were more masculinized
meyer and Baron-Cohen, 2006). Lower levels of amniotic (lower) than controls (Talaroviı̂cová et al., 2008). In addi-
fluid PT were associated with higher sociality scores in tion, sex-linked activity patterns became more masculi-
the sample of infants (i.e. higher frequency of eye con- nized in the females compared to controls. A cross-taxa
tact, higher scores in assessments of parent–child rela- study in two distantly related lizard species showed that
tionship quality), while higher levels of PT were linked sexual dimorphism in 2D:4D differed between the taxa
to lower sociality scores. Although females had higher (Rubolini et al., 2006). In primates lower 2D:4D ratios in
sociality scores than males, children of both sexes chimpanzees (Pan troglodytes) compared to bonobos (Pan
exposed to high PT had lower scores for social relation- paniscus) are hypothesized to be associated with the
ship quality and higher scores for restricted interests more competitive social behavior of chimpanzees com-
(Knickmeyer et al., 2005). It is proposed that sex-differ- pared to the more tolerant social-style observed in bono-
ences in bonding-style are a product of adaptations to bos (McIntyre et al., 2009).
differences in reproductive investment between males Comparisons between human 2D:4D studies and those
and females (Knickmeyer and Baron-Cohen, 2006). of distantly related species may be of little value other
Relationships between 2D:4D and sexual selection than to show discordance and the complexity of the
have been shown at the population-level (Manning et al., issue. Comparisons between closely related species, how-
2000; 2003a; 2004a) and demonstrate that within ethnic ever, should be more informative and allow for more
groups male and female ratios are highly correlated, but meaningful comparisons with the main body of 2D:4D
between populations the ratios of males and females in research. Anthropoid primates are the most obvious test
some groups appear more masculinized than the ratios case to look for systematic variation in 2D:4D across dif-
of other groups. Manning (2008) proposed that popula- ferent social systems because they are closely related to
tion differences may be linked to marriage systems and humans (within the same suborder) and will have more
levels of polygyny. High competition between males for similar biological profiles than distantly related taxa.
(see Fig. 1). Nonpair-bonded Ceboidea did not differ from high level of female competition also have high levels of
those of nonpair-bonded Hominoidea or Cercopithecoidea male competition. 2D:4D was significantly associated
(Ceboidea-Hominoidea, F1,5 5 0.045, P 5 0.84; Ceboidea- with intramale competition estimates using nonphyloge-
Cercopithecoidea, F1,16 5 0.34, P 5 0.57). 2D:4D ratios netic tests; lower 2D:4D ratios (higher PAE) were associ-
of the Cercopithecoidea (nonpair-bonded) were less vari- ated with higher levels of competition, while higher
able and were significantly lower than nonpair-bonded 2D:4D ratios (lower PAE) were associated with lower lev-
Hominoidea (F1,16 5 44.31, P \ 0.001) (see Fig. 1). els of competition (Table 4; Fig. 3). Because of high levels
Thus, 2D:4D was higher in pair-bonded than nonpair- of phylogenetic autocorrelation (lambda values presented
bonded anthropoids. The 2D:4D ratios of pair-bonded in Table 4), this association was not robust to phyloge-
and nonpair-bonded New World monkey and apes did netic analysis (PGLS analysis). However, if socially
not differ. Cercopithecines had lower 2D:4D than non- monogamous Saguinus sp. and Leontopithecus sp.
pair-bonded apes, but not significantly lower than non- (Goldizen, 2003) (level 2; high frequency-low intensity)
pair-bonded species within Ceboidea. are reclassified as level 1 (low frequency-low intensity),
Ape species (Hominoidae) had significantly different the category to which they were originally assigned
mean 2D:4D ratios (F1,7 5 53.19, P \ 0.001. In pairwise (Plavcan and van Schaik, 1997), the association is robust
comparisons, pair-bonded gibbon species (Hylobatidae) to phylogenetic control (species 2D:4D; F3,31 5 7.66,
had significantly higher 2D:4D ratios than the nonpair- P \ 0.001).
bonded great apes (Hominidae) (P \ 0.001). Within the 2D:4D and intra-female competition levels were
Hominidae, the ratios of Pongo pygmaeus were signifi- strongly associated, even after controlling for a strong
cantly lower than ratios of African ape species (Homi- phylogenetic signal (Table 4). Lower 2D:4D ratios
ninae) (P \ 0.05) (see Fig. 2). Ratios of the Homininae (higher PAE) were associated with higher levels of intra-
did not significantly differ from each other. We trans- female competition and female philopatry, and higher
posed human 2D:4D ratios (Manning et al., 2007) onto 2D:4D ratios (lower PAE) were significantly associated
2D:4D patterns within the Hominoidea. As predicted, with lower levels of competition and heterosexual or
human 2D:4D ratios fell between the ratios of paired female dispersal (Table 4; Fig. 3).
and nonpair-bonded taxa (Figs. 1 and 2) and were signif-
icantly different from both (humans versus nonpair-
bonded apes, t 5 6.75, P \ 0.001; humans versus pair-
bonded apes, t 5 6.69, P \ 0.001). 2D:4D and sex differences
2D:4D and intrasexual competition Male and female 2D:4D ratios were significantly corre-
lated across the whole sample (r2 5 0.90, P \ 0.001,
Male and female competitive regimes were highly df 5 36). Controlling for species differences we found a
associated (Likelihood ratio 5 61.83, P \0.001, n 5 37). near significant difference in sex across the dataset (spe-
Thus, pair-bonded species tended to have low levels of cies: F36,1047 5 53.76, P \ 0.001; sex: F1,1047 5 3.48, P 5
both male and female competition, whereas species with 0.06).
Males in nonpair-bonded species had significantly
lower 2D:4D ratios than females (males 0.845 6 0.003
s.e., females 0.852 6 0.003 s.e., species: F23,817 5 23.82,
P \ 0.001; sex: F1,817 5 5.13, P 5 0.02). There was no
sex difference, however, in pair-bonded species (males
0.971 6 0.008 s.e., females 0.973 6 0.008 s.e., species:
F13,174 5 21.84, P \ 0.001; sex: F1,174 5 0.04, P 5 0.85).
Within the Hominoids there were significant differences
in mean 2D:4D ratios between males and females (spe-
cies: F7,375 5 32.95, P \ 0.001; sex: F1,375 5 4.41, P 5
0.04); however, there were no significant sex differences
in other super families (Cercopithecoidea and Ceboidea).
Significant sex differences in 2D:4D ratios at the spe-
cies level were detectable only in competition Level 2 for
both males and females (high frequency-low intensity;
species: F3,316 5 24.49, P \ 0.001; sex: F3,316 5 6.62,
P 5 0.01; dispersed-egalitarian; species: F3,415 5 13.39,
P \ 0.001; sex: F3,415 5 3.74, P 5 0.05). Within this level
females had significantly lower 2D:4D ratios than males.
Fig. 2. Mean 2D:4D across hominoids. Star represents Sex differences in the other categories (in both male and
human values for comparison. Bars represent 95% confidence female competition classifications systems) were non-
intervals. significant.
Over all sampled species, there was a trend for males social behavior is, by definition, manifested through
to have lower ratios than females. However, these sex interactions between individuals and thus cannot occur
effects were not consistent over all species. Nonpair- in utero. Rather we suggest that 2D:4D may inform us
bonded species (i.e. those with higher levels of male– about how variation in PAE, including AR gene morphol-
male competition) had significantly lower male than ogy, differentially programs the brain and body tissues
female 2D:4D ratios, whereas there was no difference and how physiological foundations for social development
between sexes in pair bonded species. This is consistent vary between related taxa. Exploring the relationship
with our predictions and the assumption that male–male between sex steroid receptor sensitivity and behaviors
competition may be a key factor driving PAE. More chal- across vertebrates may uncover an ontogenetic basis for
lenging was that the pattern was not consistent over all affiliative and competitive social behavior and augment
taxonomic groups; male apes had lower ratios than our understanding of mechanisms underpinning social
females but in other groups the difference was nonsigni- bonding (Walum et al., 2008).
ficant. One potential explanation is that the genes re- Finally, our results are the first to show human 2D:4D
sponsible for androgen sensitivity are sexually antago- in evolutionary context. Human 2D:4D ratios are
nistic, such that strong selection on male reproductive couched within the Hominoidea positioned, as predicted,
characteristics can have knock on effects on females. between pair-bonded Hylobatidae (gibbons) and the pro-
These effects have been shown to occur in promiscuous miscuous Hominidae (great apes) (Figs. 1 and 2). This
species where reproductive skew between males and result fits with evidence from comparative analysis of
females is high (Rice, 2000; also see Manning et al., variation in relative testis size and sperm competition
2000). However, a more parsimonious explanation may within primate social systems (Harcourt et al., 1981;
be that the androgenic mechanisms associated with com- Anderson and Dixson, 2002) and supports links between
petitive regimes of both males and females are strongly PAE and 2D:4D. It is interesting to speculate if
associated, such that both males and females experience evolutionary shifts in PAE within the African apes, and
either high or low levels of intrasexual competition. The associated changes in the AR gene, have contributed to
only competition category where there was some discrep- the behavioral flexibility of apes, and ultimately of
ancy between male and female competition strength was humans.
in the level two, which is also where there were sex dif-
ferences.
Although it is clear that we do not fully understand ACKNOWLEDGMENTS
the mechanisms by which PAE is manifested (i.e. We thank all the zoos and primate facilities world-wide
whether the androgens are maternally or fetally derived, who contributed data to this study; Antwerp, Apenheul
how sensitive they are to environmental effects, and how Primate Park, Atlanta, Banham and Suffolk Wildlife
important underlying genetic variation is in determining Parks, Blackpool, Bristol, Busch Gardens, Chester, Chey-
sensitivity), the key issue is that there is substantial evi- enne Mountain, Cleveland Metro Parks, Colchester, Cots-
dence that links androgen and estrogens to sexual differ- wolds, Columbus, Cricket St.Thomas Wildlife Park,
entiation of the brain during gestation (Cooke et al., Dakota, Dallas, Drusillas Park, Dudley, Edinburgh, Fota
1998). Therefore, assuming that 2D:4D is at some level a Eire Wildlife Park, Fresno, Great Vancouver, Hagenbeck,
proxy for PAE then these results suggest that early Hogle, Johannesburg, Kansas City, Knoxville, Lincoln,
androgen exposure may be implicated in priming behav- Louisville, Marwell Wildlife Park, Melbourne, Milwaukee,
iors associated with sexual competition in adulthood. The Monkey Sanctuary, North Carolina, Oregon, Paing-
Additionally, circulating androgens (and other hormones) ton, Philadelphia, Phoenix, Regents Park, San Francisco,
clearly play a role throughout an individual’s life, not Taronga Western Plains, Toledo, Topeka, Toronto, Twy-
just prenatally. Thus although not conclusive, the consis- cross, Wellington, Welsh Mountain, Whipsnade Wildlife
tency and strength of the associations we have docu- Park, and Santa Fe Community College Teaching Zoo.
mented here are certainly provocative and consistent Also National Primate Research Centres; California, New
with the existing 2D:4D framework. England, Oregon, Southwest, Wisconsin, Elaine Videan
A caveat must also be made about variation in hand (Primate Foundation of Arizona). Josie Harder (University
morphology within and between taxonomic groups. It of Massachusetts), James Roney (University of California
could be argued that some differences in interspecific Santa Barbara), Adrienne Zihlman and Carol Underwood
2D:4D may be attributable to locomotor adaptations to (University of California Santa Cruz) and Joke Van Laere
substrate use or phylogenetic inertia (Jouffroy et al., and Phil Howard and Andrew Kitchener of the National
1993; Richmond, 2007). Additionally, some elements of Museums of Scotland. We also thank Martin Voracek,
primate hand anatomy may be associated with HOX- Kobe Millet and two anonymous reviewers for providing
gene pleiotropy between anatomical structures (Kondo suggestions that improved the manuscript.
et al., 1997; Zákány et al., 1997). Our analyses controlled
for phylogeny and substrate use (arboreality and terres-
triality) to try to remove functional and evolutionary
influences on hand morphology, yet relationships LITERATURE CITED
between 2D:4D and social behaviors were maintained.
We propose that if variation in digit ratios were primar- Anderson MJ, Dixson AF. 2002. Motility and the midpiece in
primates. Nature 416:496.
ily a consequence of functional variation in hand mor-
Anderson MJ, Hessel JK, Dixson AF. 2004. Primate mating sys-
phology, large-scale relationships would be obscured. tems and the evolution of immune response. J Reprod Immu-
Analysis of 2D:4D at large-scale and small-scale taxo- nol 61:31–38.
nomic groupings across anthropoid species has allowed Andrés AM, Soldevila M, Lao O, Volpini V, Saitou N, Jacobs HT,
us to speculate on how broad-scale trends in PAE may Hayasaka I, Calafell F, Bertranpetit J. 2004. Comparative
underpin aspects of anthropoid sociality. We are not pro- genetics of functional trinucleotide tandem repeats in humans
posing that PAE programs social behavior per se, as and apes. J Mol Evol 59:329–339.