A naked ape would have fewer parasites

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A naked ape would have

fewer parasites

Mark Pagel1* and Walter Bodmer2

1School of Animal and Microbial Sciences, University of Reading,

Reading RG6 6AJ, UK

2Cancer and Immunogenetics Laboratory, Cancer Research UK,

Weatherall Institute of Molecular Medicine, John Radcliffe Hospital,

Headington, Oxford OX3 9DS, UK

* Author for correspondence (m.pagel@reading.ac.uk).

Recd 03.03.03; Accptd 02.05.03; Online 09.06.03

Unusually among the mammals, humans lack an

outer layer of protective fur or hair. We propose the

hypothesis that humans evolved hairlessness to

reduce parasite loads, especially ectoparasites that

may carry disease. We suggest that hairlessness is

maintained by these naturally selected benefits and

by sexual selection operating on both sexes. Hair-

lessness is made possible in humans owing to their

unique abilities to regulate their environment via

fire, shelter and clothing. Clothes and shelters allow

a more flexible response to the external environment

than a permanent layer of fur and can be changed

or cleaned if infested with parasites. Naked mole-

rats, another hairless and non-aquatic mammal

species, also inhabit environments in which ecto-

parasite transmission is expected to be high, but in

which temperatures are closely regulated. Our

hypothesis explains features of human hairlessness—

such as the marked sex difference in body hair, and

its retention in the pubic regions—that are not

explained by other theories.

Keywords: human hairlessness; parasites;

sexual selection; naked apes

1. INTRODUCTION

Humans are unique among the monkeys and apes in lack-

ing a dense layer of hair covering their bodies. More gen-

erally, hairlessness is rare in the mammals. Of the ca. 5000

extant mammals, the only other effectively hairless species

are elephants, rhinoceroses, hippopotamuses, walruses,

pigs, whales and naked mole-rats, and at least four of these

species are aquatic or semi-aquatic.

Hairlessness, then, demands some sort of explanation

in evolutionary terms, and especially so as, in humans at

least, hairlessness is not without its costs. Humans are

more exposed to the sun, may suffer greater heat loss

when the ambient temperature is low (Newman 1970;

Amaral 1996) and, with the exception of the naked mole-

rats, differ from the other hairless mammals in not having

a thick or toughened hide for protection.

What, then, accounts for our relatively naked state?

Before proceeding we must clarify our use of the term

‘hairless’ as applied to humans. Humans are not literally

hairless, having about the density of hair follicles expected

of an ape of our body size (Schwartz & Rosenblum 1981).

Proc. R. Soc. Lond. B (Suppl.) 270, S117–S119 (2003)

S117

© 2003 The Royal Society

DOI 10.1098/rsbl.2003.0041

What distinguishes human body hair is that it is very fine

and short, making it, effectively, invisible. We use ‘hair-

less’ with respect to humans, then, to mean that they lack

a dense layer of thick fur.

2. THE BODY-COOLING HYPOTHESIS

The best-known hypothesis to explain human hairless-

ness is that it evolved to promote cooling of the body. In

a series of papers beginning in 1984, Wheeler argued that

the loss of body hair occurred when bipedal hominids

moved to open savannah environments. According to

Wheeler (1984), animals living on the hot savannah would

suffer from excess exposure to the sun. Bipedality may

have evolved in part to reduce exposure, meaning that

upright hominids could forage for longer in the open sun

than comparably sized quadrupeds (Wheeler 1991). Later,

Wheeler (1992) suggested that the combination of an

upright posture and lack of hair made it easier to radiate

heat back into the environment or to lose heat by convec-

tive cooling from the wind. But these thermoregulatory

advantages of nakedness are limited. Wheeler (1992)

acknowledges that naked skin increases the rates of both

energy gain and loss during periods of too much or too

little heat, respectively. This might mean that naked skin

is actually a worse solution when the entire day is taken

into account: more heat must be dissipated from daytime

exposure and, at night time, more heat is lost (Amaral

1996).

3. THE AQUATIC-APE HYPOTHESIS

Another idea is that between 6 and 8Myr ago, the

ancestors to the hominids had a 1 or 2 million year phase

of aquatic or semi-aquatic existence (Morgan 1997). Mor-

gan’s view (1997) is that hairlessness and high levels of

body fat evolved in these ancestors for the same reasons as

in other aquatic mammals, viz., that fur is not an effective

thermal layer under water. This theory then supposes that

the aquatic adaptations were retained as ancestral charac-

ters throughout at least 5million years of subsequent

hominid evolution in predominantly terrestrial habitats.

Although human fossil remains are often found near

bodies of water (Foley 1987), evidence for an aquatic

phase of proto-hominid existence as yet eludes palaeontol-

ogists. Morgan’s theory (1997) also fails to explain why

features supposedly adaptive to an aquatic lifestyle should

have been retained despite several millions of years of sub-

sequent evolutionary change in other features of hominids.

In a similar vein, the body-cooling hypothesis does not

directly explain why hairlessness has been retained despite

human populations having occupied colder regions of the

Earth for perhaps 100 000 years, and possibly for up to

800 000 years for their Homo erectus and later Homo for-

bearers (Arsuaga 2002). The amount of body hair can

change rapidly in evolutionary time as seen from compar-

ing mammoths with extant savannah-dwelling and rela-

tively hairless elephants, or domestic pigs and some dog

breeds with their closely related and hairy wild cousins.

Among modern humans there is variation in the degree of

body hair, suggesting substantial genetic variance for this

trait. Finally, neither the aquatic ape nor the body-cooling

hypotheses has a ready explanation for the marked differ-

ence in body hair between males and females.

S118 M. Pagel and W. Bodmer Naked apes fewer parasites

4. HAIRLESSNESS AS AN ADAPTATION TO

REDUCE PARASITE LOADS

It is desirable to seek explanations for human hairless-

ness that link its origin and continued maintenance to

advantages that arose and operated throughout hominid

evolution, and differentially so between the sexes. We pro-

pose here the view that hominid cultural adaptations made

it possible for hairlessness to evolve in humans as an adap-

tation to reduce parasite loads, especially ectoparasite

loads. We suggest that hairlessness is maintained by its

naturally selected advantages in reducing disease, and by

sexually selected effects arising from mate choice for hair-

less partners. This mechanism could have worked either

alone or in concert with other factors that might have

favoured hairlessness.

Elements of our hypothesis have existed at least since

the time of Darwin, although he was convinced that no

naturally selected advantage could be adduced for the lack

of body hair in humans. Instead, noting that ‘in all parts

of the world women are less hairy than men’, Darwin

argued ‘we may reasonably suspect that this character has

been gained through sexual selection’ (Darwin 1888,

p. 600). Darwin considered the idea—attributed to a Mr

Belt (Naturalist in Nicaragua 1874, p. 209, cited in Darwin

1888)—that within the tropics human hairlessness pro-

vides a naturally selected advantage for freeing oneself of

‘the multitude of ticks (acari) and other parasites’ (Darwin

1888, p. 57). He even noted that ‘as some confirmation

of Mr Belt’s view, I may quote the following passage from

Sir W. Denison (Varieties of vice-regal life, vol. i, 1870,

p. 440): “it is said to be a practice with the Australians,

when the vermin get troublesome, to singe themselves”’

(Darwin leaves unspecified to which Australians Sir Wil-

liam refers). But he dismissed Belt’s idea as unlikely

because ‘none of the many quadrupeds inhabiting the

tropics have … acquired any specialised means of relief’.

We suggest, based upon information and ideas not

available to Darwin, that the ectoparasite hypothesis is, in

concert with sexual selection, the most plausible expla-

nation for hairlessness in humans. There would not have

been any real understanding in the late nineteenth century

of the important role that pathogens play in natural selec-

tion. Ectoparasites exact a large toll on the fitness of furry

or feathered animals (Lehmann 1993). Fleas and ticks

affect animals directly by biting and causing local irri-

tation, and indirectly by carrying a variety of infectious—

including viral—diseases. Animals have specialized

muscles for twitching their skin, long tails to swat at flies

and many other anti-parasite morphological and behav-

ioural adaptations (Hart 1997). The colourful feathers and

displays of many bird species may be metabolically costly

advertisements to prospective mates of their lack of para-

sites (Hamilton & Zuk 1982; Read 1987). Features of

beak size and shape in some birds may be adaptations to

removing parasites from feathers (Clayton 1991). Pri-

mates devote substantial amounts of time to grooming,

increasingly so as group size increases, most of which is

to remove ectoparasites (Dunbar 1991). When humans

suffer ectoparasite infection it is largely confined to the

head and pubic hair. This may be because it is easier to

remove ectoparasites from hairless regions, or that ecto-

parasites are less attracted to hairless skin, or both.

Proc. R. Soc. Lond. B (Suppl.)

What features of early hominid evolution make hairless-

ness a plausible response to the toll exacted by parasites?

Humans most likely evolved in Africa (Ingman et al. 2000)

where biting flies and other ectoparasites are found in

abundance. Early humans probably lived in close quarters

in hunter–gatherer social groups in which rates of ectopar-

asite transmission were high. Precisely when humans or

their hominid ancestors evolved hairlessness must remain

a matter of speculation. What we can say is that having

fire and the intelligence to produce clothes and shelter,

early humans (and possibly even earlier hominids—

H. erectus may have had fire) were well equipped to evolve

hairlessness as a means of reducing ectoparasite loads,

while avoiding the costs of exposure to sun, cold and rain.

Ectoparasites can and do infest clothing, but clothes,

unlike fur, can be changed and cleaned. Infections that do

occur on hairless skin can be more easily cleaned than

when fur is present. We suggest, then, that a set of cultural

adaptations unique to humans made hairlessness a flexible

and advantageous naturally selected adaptation.

By contrast, we do not suggest that the ectoparasite

hypothesis explains other mammalian hairlessness, with

the possible exception of the naked mole-rat. Naked mole-

rats inhabit arid regions of Kenya, Ethiopia and Somalia,

where they live underground in large social colonies, rarely

coming above ground (Sherman 2002). Ectoparasite

transmission is expected to be high in these colonies, but

their climate tends to be regulated within narrow bounds,

making hairlessness feasible for a species that does not

produce clothes or fire. Like humans, they are effectively

hairless—having been described as resembling ‘over-

cooked sausages with buck teeth’ (Sherman 2002,

p. 793)—and like humans they lack a thick and protec-

tive hide.

Sir Ronald Fisher, one of the founders of modern gen-

etically based Darwinian thinking, emphasized that sexual

selection typically relies upon a trait having a naturally

selected advantage to begin the process of its exaggeration

(Fisher 1930). The ectoparasite hypothesis provides this

advantage: initial naturally selected evolution towards

reduced amounts of body hair may then have been

reinforced by Fisherian or other forms of sexual selection

as hairlessness—by virtue of advertising reduced ecto-

parasite loads—became a desirable trait in a mate.

Unusually among sexually selected traits, reduced body

hair would be desirable in both sexes. Greater loss of body

hair in females plausibly follows from the conventionally

stronger sexual selection from male versus female mate

choice in humans. Common use of depilatory agents

testifies to the continuing attractions of hairlessness,

especially in human females.

The retention of hair on the face, head, and pubic

regions may also be linked to sexual selection. Head hair

may have naturally selected advantages—such as reducing

exposure to the sun—that permitted further elaboration

by sexual selection. Darwin noted—and contemporary

practises attest to—the important role of facial and head

hair in attraction and mate choice. The retention of pubic

hair poses a challenge for the ectoparasite hypothesis, as

it provides a warm and humid environment favourable to

ectoparasites—and indeed many specialize on these

regions. An interesting possibility is that pubic areas may,

owing to their warmth and humidity, be especially conducive

Naked apes fewer parasites M. Pagel and W. Bodmer S119

to pheromonal signalling between the sexes. In support of

this idea, the density of sweat glands in pubic regions is

high (Stoddart 1990).

Our hypothesis can be tested. We might expect less

body hair among human groups whose evolutionary his-

tory has been in regions of the Earth with higher ectopar-

asite concentrations. Ectoparasite loads should, in general,

be greater on the hairy parts of our bodies, as anecdotal

evidence would already seem to suggest. We should find

that apes suffer from higher ectoparasite loads despite hav-

ing the ability to remove them with their hands. We might

also expect that attacks by biting flies are not particularly

well defended against by fur—the biting fly simply evolv-

ing adaptations to circumvent it.

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