Joan Roughgarden - Recherche en IA spécialisée au MIT

Joan Roughgarden

Challenging Darwin’s theory
of sexual selection

May a biologist in these polarized

times dare suggest that Darwin is a bit
wrong about anything? Even worse,
does a biologist risk insult, ridicule, un-
ger, and intimidation to suggest that
Darwin is incorrect on a big issue? Nous
have a test case before us. Darwin ap-
pears completely mistaken in his theory
of sex roles, a subject called the ‘theory
of sexual selection.’1

In his 1871 book The Descent of Man,
et sélection en fonction du sexe, Darwin
wrote: “Males of almost all animals have
stronger passions than females," et
“the female . . . with the rarest of excep-
tions is less eager than the male . . . elle
is coy.”2 Notice that the exceptions are
dismissed as empirically insigni½cant

Joan Roughgarden, a Fellow of the American
Academy since 1993, is professor of biological
sciences and geophysics at Stanford University.
Her publications include “Theory of Population
Genetics and Evolutionary Ecology” (1979),
“Anolis Lizards of the Caribbean” (1995), “Evo-
lution’s Rainbow” (2004), which won a Stone-
wall Prize for non½ction from the American Li-
brary Association, et, most recently, “Evolution
and Christian Faith: Reflections of an Evolution-
ary Biologist” (2006).

(“almost all,” “rarest of exceptions”), donc
que, for all practical purposes, males are
universally “passionate” and females
collectively “coy.”

To explain this claim, Darwin consid-
ered the joint mechanisms of male-male
competition and female choice. He en-
visioned that males compete for access
to females, while females choose superi-
or males on the basis of success in male-
male competition and/or perceived
beauty. En effet, through their choice
of mates, females breed their offspring
to have their mates’ desirable traits,
“just as man can improve the breed of
his game-cocks by the selection of those
birds which are victorious in the cock-
pit.” Another example: “Many female
progenitors of the peacock must [have],
by the continued preference of the most
beautiful males, rendered the peacock
the most splendid of living birds.” From
a masculinist perspective, acquisition
of females is a just reward for victory in
male-male combat. From a maternalist
perspective, the duty of females is to bed

1 J.. Roughgarden, Evolution’s Rainbow: Diversity,
Gender and Sexuality in Nature and People (Berke-
ley: Presse de l'Université de Californie, 2004).

2 C. Darwin, The Descent of Man, and Selection
in Relation to Sex, facsimile edition (Princeton,
N.J.: Princeton University Press, 1871).

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Joan
Rough-
garden
sur
sex

the victors, thus endowing their off-
spring with valuable traits.

The Darwinian narrative of sex roles
is not some quaint anachronism. Restat-
ed in today’s biological jargon, the narra-
tive is considered proven scienti½c fact.
The geneticist Jerry Coyne, at the Uni-
versity of Chicago, declared: “Males,
who can produce many offspring with
only minimal investment, spread their
genes most effectively by mating pro-
miscuously. . . . Female reproductive out-
put is far more constrained by the met-
abolic costs of producing eggs or off-
printemps, and thus a female’s interests are
served more by mate quality than by
mate quantity.”3 So the passionate male
has become the promiscuous male, et
the coy female the constrained female.
Yet the spirit of this present-day narra-
tive is identical to Darwin’s of nearly 130
years ago, and the sexual conflict that
flows from attributing different objec-
tives to males and females remains the
starting point for sexual-selection theory
today just as it did in Darwin’s time.

I have been foolhardy enough to sug-

gest that this thoroughly entrenched
theory of male-female relationships is
biologically mistaken. The response to
my proposal offers a revealing commen-
tary on the willingness of evolutionary
biologists to face up to contrary evidence
and logic. Let us turn to the proposal and
then to the responses.4

3 J.. Coyne, “Charm Schools,” Times Literary
Supplement, Juillet 30, 2004.

4 The following exposition of the proposal is
condensed from a recent review, which should
be consulted for further detail and references
to primary literature: J.. Roughgarden, “Social
Selection vs. Sexual Selection: Comparison of
Hypotheses,” in Daniel Kleinman and Jo Han-
delsman, éd., Controversies in Science and Tech-
nology, vol. 2, Genetics of Race and Gender (Madi-
fils: University of Wisconsin Press, 2007).

I refer to sexual selection today as a sys-

thème, meaning a set of logically intercon-
nected theoretical propositions with a
truth status independent of the facts
they were originally intended to explain.
As contrary data appear, the theoretical
propositions are updated. Thus the sys-
tem cannot be challenged and becomes,
in effect, tautological.

By using the word system, I also echo
the phrase “sex-gender system,” coined
dans 1974 by the anthropologist and gen-
der theorist Gayle Rubin.5 Rubin empha-
sized how expectations flowing from
how a culture de½nes gender wind up
“the part of social life which is the locus
of the oppression of women, of sexual
minorities.” Although gender categories
may not be constructed for the purpose
of oppressing others, they end up autho-
rizing such oppression by de½ning what
counts as a norm and what counts as an
exception, thereby privileging one over
the other.

In place of sexual selection, I propose

social selection. It is equally extensive
but differs point by point from sexual
selection. Social selection is selection
pour, and in the context of, le social dans-
frastructure of a species within which
offspring are produced and reared. Le
social strategies in the infrastructure
generally include cooperation as much
as–or more than–they do competition;
and they revolve more around negotia-
tion than ‘winning.’ Social selection, dans
my formulation, does not extend sexual
selection but replaces it.

Finalement, the evolutionary system of

sex, genre, and sexuality that prevails
determines our worldview of nature it-
soi. Sexual selection’s view of nature
emphasizes conflict, deceit, and dirty

5 Gayle Rubin, “A Contribution to the Critique
of the Political Economy of Sex and Gender,»
Dissemination 1 (1) (1974): 6–13; 1 (2) (1974):
23–32.

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Challenging
Darwin’s
theory of
sexual selec-
tion

gene pools. If this Darwinian picture of
nature is true, so be it. But is it true?

To begin with, sexual selection and so-

cial selection differ in their accounts of
the very origin of sexual reproduction
and the sexes.

Origin of sexual reproduction. Accord-
ing to sexual selection, sexual reproduc-
tion evolved from asexual reproduction
as a mechanism to cleanse the gene pool
of deleterious mutations. According to
social selection, sexual reproduction
evolved from asexual reproduction to
maintain a diverse gene pool needed
for long-term population survival in an
ever-fluctuating environment.

Origin of gametic male/female binary.
The difference in size between the sperm
and the egg is the basis for de½ning male
and female in a sexually reproducing
species. Sexual selection imagines the
protosperm and protoegg playing a game
against each other. Initially, both the
protosperm and protoegg are the same
size. But then the protosperm ‘cheats,'
becoming a little smaller so that more
sperm can be produced with the leftover
energy. This numerical advantage allows
the smaller sperm to outcompete the less
numerous sperm of the original size. Le
protoegg responds by increasing its size,
restoring zygote viability to its original
level. This compensating move is better
than shrinking to try to match the small-
er sperm; otherwise, the zygote would
suffer a very deleterious double loss of
investissement. These responses of egg and
sperm to each other culminate in one
gamete–the protoegg–growing nearly
as large as the zygote, and the other–the
protosperm–becoming as tiny as possi-
ble.

In sexual selection, the distinction be-

tween male and female gametes arises
from a battle: the sexes are created as
combatants. But according to social se-

lection, a parent divides the material it
places into eggs and sperm to maximize
the number of gametic contacts that pro-
duce viable zygotes. The number of ga-
metic contacts increases as gametes be-
come more numerous and form a large,
dense cloud. The greatest number of
viable zygotes is thus created when one
of the gametes is close to the desired zy-
gote size while the other is as small as
possible.

Origin of whole-organism male/female bi-

nary. If a sexually reproducing species
produces more than one type of gamete,
each individual of that species (at least
among multicellular organisms) com-
monly makes both male and female
gametes at the same time, or at different
times, during its life–a condition known
as hermaphrodism. Species in which an in-
dividual generates only one size of gam-
ete are dioecious. In these species, one can
classify whole individuals as either male
or female, depending on the size of the
gametes an individual produces. Sexual
selection takes a whole-organism binary
as the starting point and views hermaph-
rodism as a special case arising in pecu-
liar circumstances. Social selection, sur
the other hand, takes hermaphrodism
as the starting point and sees dioecy as a
specialization for the ‘home delivery’ of
sperm.

The theories of sexual selection and so-

cial selection each tells its own central
narrative of male/female social dynam-
ics.

Universal sex roles. According to sexual
selection, males and females conform
to near-universal templates: Darwin’s
“passionate” male and “coy” female (ou
in today’s jargon, the “promiscuous”
male and the “constrained” female).
Though there are no general surveys of
reproductive habits across all dioecious
animal species, it is evident that these

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Joan
Rough-
garden
sur
sex

templates are, at best, unsubstantiated
et, as generalizations, apparently false.
In insect species, Par exemple, males
are often as choosy as females. And in
½sh, surveys show that, of those species
in which one or more parents care for
the eggs, the male is more likely than
the female to be the care provider. Birds
often provide biparental care, alors que
among mammals the female usually sup-
plies the care.

It is hard, moreover, to distinguish
‘care’ from ‘control.’ Often, the parent
who is caring for the eggs or young
might actually be more concerned with
the control of the young than in the pro-
vision of care for them.

No general pattern has actually been
demonstrated about male/female sex
roles throughout the animal kingdom,
although the stereotypes that Darwin
enunciated are widely accepted. Social
selection believes that no necessary and
universal sex roles exist; what each sex
does is subject to negotiation in local cir-
circonstances. Any statistical regularity
in sex roles may reflect a statistical fre-
quency of circumstance, together with
what constitutes a best bargain in such
circonstances. Également, if local ecology
shows statistical regularities, so will the
sex roles that emerge in those ecologies.
Purpose of reproductive social behavior.
The sexual-selection narrative explains
what happens within a reproductive so-
cial system primarily in terms of ‘mat-
ing.’ Within a mating-based system, nat-
ural selection arises from differences in
‘mating success,’ and particular behav-
iors are understood by how they con-
tribute to attaining plentiful mating op-
portunities. Females are regarded as a
‘limiting resource’ for males, and males
compete for access to, and control of,
mating opportunities with females.

En fait, evolution does not depend on
mating as such but on the number of off-

spring successfully reared. Sexual selec-
tion elevates one component of repro-
duction, namely mating, into an end in
lui-même. Entre-temps, social selection views
reproductive social behavior as compris-
ing an ‘offspring-rearing system.’ With-
in this system, natural selection arises
from differences in the number of off-
spring successfully reared, and particular
behaviors are understood by how they
contribute to building, or maintaining,
the social infrastructure within which
offspring are reared. The principal male-
female social dynamic is to determine
bargains and to exchange side-payments
that establish control over offspring and
manage the offspring-rearing social in-
frastructure.

Objective of female mate choice. Accord-

ing to sexual selection, females select
mates with the goal of endowing their
own sons with the traits they ½nd attrac-
tive in their mates. Females thus ensure
that their own sons are destined to suc-
ceed in the mating game–a rationale
called the ‘sexy son hypothesis.’ In fact,
data are scanty that female choice is
motivated more by indirect future ge-
netic bene½ts than by direct present-day
ecological bene½ts. En réalité, females
choose males who provide food and/or
protection, rendering the importance of
genes moot.

Under social selection, a female choos-
es mates based on maximizing the num-
ber of young she can successfully pro-
duce and rear–with help from her mates
and from the social infrastructure. Le
criterion for female choice is an expecta-
tion of direct bene½ts from a male dis-
counted by the probability that the male
will renege on, or somehow be prevent-
ed from, delivering those bene½ts. Ainsi,
a premium will be placed on the compat-
ibility and health of the prospective part-
ner. Health is important not as an indica-
tor of ‘good genes’ but as a sign of com-

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petency to deliver promised direct bene-
½ts.

Male genetic quality. According to sex-
ual selection, males can be ranked in a
hierarchy of genetic quality. En outre
to the good genes that females are sup-
posedly seeking in their mates, they aim
to avoid bad genes. But if, generation
after generation, female choice weeds
out males with bad genes, then eventu-
ally no bad genes should remain, lequel
presents an internal contradiction in the
logic of sexual selection. Donc, sex-
ual selection is logically compelled to
concoct genetic schemes, typically in-
volving high mutation rates spanning
polygenic loci, to replenish the supply
of bad genes that are being continually
eliminated by female choice. These ad-
ditional schemes have never been tested
much less veri½ed.

Social selection, in contrast, states
no hierarchy of genetic quality among
males exists. If genes matter at all to fe-
male choice, females are choosing for
genetic compatibility, and not overall
genetic quality. All males are equivalent
in genetic quality, excepting a rare frac-
tion that obviously contain deleterious
mutations and are present in a muta-
tion-selection balance (1 in 10^6).

Bateman’s principle. Dans 1948, the English
geneticist Angus Bateman published lab-
oratory experiments with Drosophila that
were presented as con½rming Darwin’s
theory of sexual selection.6 Bateman re-
ported that a male’s “fertility is seldom
likely to be limited by sperm production
but rather by the number of insemina-
tions or the number of females available
to him.” Similarly, he claimed to have
found in his flies an “undiscriminating
eagerness in males and discriminating
passivity in females” in accord with the

6 UN. J.. Bateman, “Intrasexual Selection in Dro-
sophila,” Heredity 2 (1948): 349–368.

sexual-selection narrative. Par conséquent,
in sexual selection, male ½tness has
come to be de½ned primarily in terms
of the number of matings, or ‘mating
success,’ and female ½tness in terms of
egg production, or ‘fecundity.’ In this
chemin, males and females are convention-
ally assumed to be governed by differ-
ent de½nitions of evolutionary ½tness.
The Bateman experiments are a cor-
nerstone of sexual selection and have
been widely cited in papers and text-
livres. Over the last ½ve years, cependant,
many critiques have revisited the 1948
Bateman paper and found that Bateman
overstated his results. Sexual-selection
advocates have quoted selectively from
what Bateman did report and have
sometimes even attributed to Bateman
quotations that they made up out of thin
air. In social selection, Bateman’s princi-
ple is nonexistent. Plutôt, both males
and females share the same de½nition of
½tness, namely, number of offspring suc-
cessfully reared.

Social selection departs from sexual

selection in the way it models behavior
in reproductive systems. Sexual selec-
tion relies on competitive evolutionary
game theory, considering particular be-
haviors as strategies. The prisoner’s di-
lemma game is an oft-cited example in
which the strategies of play are either to
cooperate or to defect. The ‘payoff ma-
trix’ tabulates the payoff to each player
for all combinations of these strategies.
The solution to the game is an evolution-
ary stable strategy (ess): a combination
of strategies for both players such that a
mutant allele for some other combina-
tion cannot increase when rare.

This is a single-tier approach in the
sense that particular behaviors are them-
selves viewed directly as evolutionary
strategies. The problem is that it re-
quires thinking of particular behaviors

Challenging
Darwin’s
theory of
sexual selec-
tion

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Dædalus Spring 2007

Joan
Rough-
garden
sur
sex

as having a genetic basis, par exemple., the gene
‘for’ cooperating, for defecting, for shy-
ness, for aggressiveness, etc.. Behaviors
rarely have much direct genetic basis.
But the single-tier approach forces nar-
ratives of genetic determinism.

Social selection approaches the model-
ing of social behavior as a two-tier prob-
lem: development on one tier, evolution
on another. Particular behaviors develop
as animals interact with one another,
similar to how morphological structures
develop through cell-cell contact during
embryogenesis. A social system is a ‘be-
havioral tissue’: a system of phenotypes
produced through interactive develop-
ment.

In social selection, the developmental
dynamics employ both cooperative and
competitive game theory. Cooperative
solutions mostly occur when parties play
with coordinated tactics and with the
perception of shared goals made possi-
ble through animal friendships. Même
though a seemingly cooperative out-
come may also result from competitive
behavior, as in a standoff between weary
combatants, the emphasis in social se-
lection is on attaining cooperative out-
comes through behavior that is explicit-
ly cooperative, involving coordinated ac-
tivities in pursuit of a shared goal. Social
selection also envisions an evolutionary
tier in which the payoff matrices and
rules of play evolve based on traditional
competitive evolutionary game theory.
Particular social behaviors evolve indi-
rectly as emergent properties from what-
ever payoff matrices and rules of play
have themselves evolved. Ainsi, evolution
produces the payoff matrix and rules of
play, which then allow development to
produce particular behaviors within the
social infrastructure.

Social selection thus accounts for cer-

tain characteristics of sexual reproduc-

tion very differently from the way sexual
selection views them.

Parental investment. According to sexu-
al selection, the female has a higher pa-
rental investment than the male because
the egg is bigger than the sperm. Le
sperm are considered ‘cheap’ and the
egg expensive. This initial difference is
then extrapolated to explain an entire
suite of female and male behaviors, tel
as male promiscuity and female coyness.
Social selection, on the other hand,
sees male and female parental invest-
ments as more or less the same initial-
ly. An ejaculate might typically contain
10^6 sperm while an egg is typically 10^6
times as large as a sperm. So the size of
the ejaculate and egg are often about
the same order of magnitude. Ainsi,
male and female sex roles emerge not
as a matter of logical necessity from
gamete size, but from the local context.
Sexual conflict. The sexual-selection
narrative regards a male and female as
always fundamentally in conflict and
male-female cooperation as a possible
(and unlikely) secondary development.
According to social selection, cependant,
male and female mates begin with a co-
operative relationship because they have
committed themselves to a common
‘bank account’ of evolutionary success.
Their offspring represent indivisible
earnings. Hurting the other hurts one-
soi, and helping the other helps oneself,
in terms of number of offspring success-
fully reared. En tant que tel, conflict develops
only secondarily if a division of labor
cannot be successfully negotiated.

Male promiscuity. According to sexual
selection, males are naturally and uni-
versally promiscuous, reflecting the low
parental investment of a sperm com-
pared to an egg. In social selection, male
promiscuity is a strategy of last resort
that occurs when males are excluded
from control of offspring rearing.

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Monogamy. In sexual-selection theo-
ry, monogamy is a violation of the basic
dictate that males should be promiscu-
ous. Donc, sexual selection explains
away the instances of monogamous-pair
bonds, including those of most birds and
some mammals, as entrapment of males
by females or as a default when no other
mates are available.

Social selection distinguishes two dis-

tinct forms of monogamy: économique
monogamy, an agreement to carry out
the work of rearing offspring in teams
of one male and one female, and genet-
ic monogamy, an agreement not to mate
outside the pair bond. Most monogamy
is economic monogamy, and nothing
requires economic monogamy and ge-
netic monogamy to coincide. In social
selection, economic monogamy emerges
in ecological situations where the work
of rearing offspring is most ef½ciently
done in male-female teams rather than
by solitary individuals or in teams of
more than two individuals.

Extrapair parentage. Extrapair paterni-
ty (epp) occurs when a male sires young
in a nest other than the one he is work-
ing on with a female; extrapair mater-
nité (epm) occurs when a female depos-
its eggs in a nest other than the one she
is working on with a male. Both epps
and epms result in extrapair parentage.
Sexual selection’s primary literature de-
scribes extrapair parentage as ‘cheating’
on the pair bond: the male is said to be
‘cuckolded’; offspring of extrapair par-
entage are said to be ‘illegitimate’; et
females who do not participate in extra-
pair copulations are said to be ‘faithful.’
This judgmental terminology reflects
the failure to distinguish economic from
genetic monogamy, and amounts to ap-
plying a contemporary de½nition of
Western marriage to animals. Plus loin-
plus, epps are assumed to reflect the
inevitable outcome of basic male pro-

miscuity, whereas epms are described as
‘sexual parasitism.’ Indeed, sexual selec-
tion refers to the females who deposit
eggs in a neighbor’s nest as ‘brood para-
sites.’

For social selection, extrapair parent-
age is a system of genetic side-payments
that stabilizes the social arrangement
of economic monogamy when individ-
uals differ asymmetrically in their capac-
ities to contribute to rearing offspring.
Distributed parentage also spreads the
risk of nest mortality across a network
of nests, acting as a social-insurance pol-
icy.

Secondary sexual characteristics. Accord-
ing to sexual selection, females choose
mates on the basis of secondary sexual
characteristics like the peacock’s tail and
the stag’s antlers so that their own sons
will be similarly attractive and success-
ful at mating. The ‘beauty’ of a male’s
ornaments is how she apprehends his
good genes; ils sont, in effect, ‘condi-
tion indicators’ of genetic quality.

Social selection sees ornaments, les deux

male and female, differently: ils sont
‘admission tickets’ to power-holding
cliques that control the resources for
successful rearing of offspring, y compris
the opportunity for mating, safety of the
young from predation risk, and access
of the young to food. Accordingly, a pea-
cock’s tail, a rooster’s comb, etc., facili-
tate male-male interactions, and females
are indifferent to them.

Admission tickets are expensive be-
cause the advantages to membership in
a clique reside in the power of monop-
oly, which is diluted when membership
is expanded. By requiring a high price of
admission, the monopolistic coalition is
kept exclusive, maximizing the bene½ts
to those within. Ornamental admission
tickets belong to a class of traits called
‘social-inclusionary traits’ that are need-
ed to participate in the social infrastruc-

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ture within which offspring are reared.
Other traits include those needed for
communication and cognition within
the social infrastructure. Not possessing
such traits, or not participating in social-
inclusionary behaviors, is reproductively
lethal.

The strong natural selection imposed

by the requirement of membership in
power-holding cliques can produce the
very fast evolution, including possibly
runaway evolution, that has long been
the signature of sexual selection. Admis-
sion tickets are not the only way to enter
power-holding cliques, cependant. Con-
ceivably, individuals might be recruited
to join, and the admission ticket waived,
if they supply capabilities or assets val-
ued by the other members. But if the
sole bene½t from membership is monop-
olistic, then membership should require
an expensive ticket.

Two phenomena in particular present

challenges to sexual selection.

Sexual monomorphism. Species in which

males and females are identical in ap-
pearance pose a direct contraction to
Darwinian templates, which say males
should be showy and females drab. Dar-
win dismissed these species as having
females that lack an aesthetic sense. Dans
social-selection theory, sexual mono-
morphism reflects the absence of same-
sex power-holding cliques whose mem-
bership requires admission tickets. Ce
should occur in ecological situations
where the most economically ef½cient
coalition is the coalition of the whole.
Sex-role reversal. Species in which the

male is drab and the female showy,
the reverse of the peacock/peahen com-
parison, also contradict the Darwinian
‘norm.’ In sex-role-reversed species, le
male provides more parental investment
than the female does by carrying and/
or tending the eggs–so the males are

in short supply for mating relative to fe-
males. In this situation, sexual selection
claims that females compete with one
another for access to males and become
the showy sex, whereas the male re-
mains drab, thus reversing the putative
peacock story. This account, even if it
were true, cannot be an explanation of
sex-role reversal–it is merely a redescrip-
tion of the phenomenon. Sexual selec-
tion does not say why the male in these
species should happen to be the sex pro-
viding the higher parental investment.
De plus, the mere existence of sex-
role-reversed species challenges a basic
tenet of sexual selection–that sex roles
can be traced to gamete size–because
sex-role-reversed males, like all other
males, produce tiny sperm. Ainsi, gam-
ete size does not entail sex role.

Reversed sex roles are not especially
problematic for social selection, because
sex roles are always negotiated in local
ecological situations anyway. It is in a
male’s interest to secure some control
of the eggs, thereby retaining some con-
trol of his evolutionary destiny. In some
ecological circumstances, doing so may
mean the male winds up with more pa-
rental responsibility than the female
does.

Social selection provides peripheral

narratives for diversity in gender expres-
sion and sexuality.

Gender multiplicity. Many species have
more than one type of male and female,
so that comparing the males to just one
template and the females to another is
impossible. I call each such template a
‘gender.’ In many species of ½sh, lizards,
and birds, Par exemple, one male gender
has a large body size at reproductive age
but must survive several years to attain
that size, thereby suffering a high cumu-
lative risk of mortality. But once large,
such a male can command a territory

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and defend eggs laid in it. Another gen-
der of males reaches reproductive age
sooner, does not defend territories, et
fertilizes eggs that are in the territories
defended by large males. These species
exhibit two male and one female gen-
ders.

A three-male pattern is observed in

some ½sh and birds, where the large
male solicits the help of a medium-sized
male. The pair together maintains the
territory and participates jointly in
courtship with females. The large male
allows the medium male to fertilize
some of the eggs in the territory. A third
type–the small male–meanwhile re-
mains as a competitor to the large- et
medium-sized males, fertilizing some
of their eggs in spite of their attempts
to chase him away.

These species with multiple male and

female genders all defy any attempt to
apply sexual-selection theory directly
because that theory posits only one tem-
plate each for male and for female ap-
pearance and behavior. Par conséquent, sexu-
al selection theory has been augmented
with additional narratives to account for
more than one gender per sex.

The problem with sexual selection,
cependant, is that it takes the large terri-
tory-holding male gender as the refer-
ence male, while considering the other
genders of males as ‘alternative mating
strategies’ and de½ning them as ‘sexu-
al parasites.’ A pejorative language mas-
querades as description throughout
these peripheral narratives of sexual se-
lection. Sexual selection terms the small
non-territory-holding male a ‘sneaker’
who ‘steals’ copulations that rightfully
belong to the territory-holding male. Il
depicts the sneaker as stealthily entering
the large male’s territory through a back
door.

En fait, small males are often more nu-

merous than large males, so the small

male typi½es ‘maleness’ in the species
more than the large male does; et le
small males often band together in the
open to chase away the large male and
fertilize eggs in the territory, plutôt que
entering singly and stealthily.

Social selection, in contrast, extends
economic theory for the elemental one-
male-one-female economic team to larg-
er teams with more ‘social niches.’ A re-
productive social group subsumes the
concept of a ‘family,’ which is a repro-
ductive social group whose members
happen to be genetically related. In a
reproductive social group, some mem-
bers are ‘prezygotic helpers’–animals
that assist in bringing about courtship
and mating–together with ‘postzygotic
helpers’–members who remain at the
nest to help rear the offspring that have
already been born. Those not included
in the reproductive social group’s coali-
tion form other arrangements to oppose
il, either singly or in coalitions of their
propre.

In this conceptualization, coalitions

may form containing medium-sized
males who assist in recruiting females to
the nests of the large males who control
eggs by means of controlling territory. UN
large-male/medium-male coalition may
then be opposed by a small-male coali-
tion that competes to control the eggs.
The complex social dynamics for these
scenarios can be approached with coop-
erative game theory, which deals with
the formation and dissolution of coali-
tions and with the distribution of the
team’s payoff among its members.

Feminine males. In species with multi-
ple male genders, one gender often has
colors or markings somewhat resem-
bling those of females. In popular writ-
ing, I have termed these males ‘feminine
males.’ In sexual selection, feminine
males are called ‘female mimics’–sex-
ual parasites who steal the reproductive

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investment of territory-holding males
through deceit. A female mimic is dis-
guised as a female to fool the territory-
holding male into allowing him to enter
the territory-holding male’s harem and
mate with his females.

This story has not been demonstrated.
The capacity of a feminine male to fool
a territory-holding male into ‘thinking’
it is a female implausibly requires gulli-
bility by the territory-holding male as
well as craftiness by the feminine male.
En fait, the territory-holding male is of-
ten a visual predator with well-honed
skills at sizing up and identifying prey
from a distance; he is not likely to be
fooled by a feminine male who only im-
perfectly resembles a female. Plutôt,
the courtship between the territory-
holding male and the feminine male is
perhaps best thought of as a job inter-
view prior to joining the team, plutôt
than an elaborate deception.

According to social selection, mark-

ings and colors on animals represent
‘body English’–how animals tell one
another what their social role is, what
their intentions are, and what activities
they promise to perform. Feminine
males are simply participating in a con-
versation on topics and with words used
more frequently by females than by mas-
culine males.

Masculine females. In sexual selection,
masculine females are discussed under
the rubric of ‘female ornaments’–hang-
ing skin flaps (wattles), colored patches
of feathers, antlers, and so forth–usual-
ly considered male ornaments. Darwin
dismissed out-of-place ornaments as
male traits accidentally expressed in fe-
males–a developmental error. Accord-
ing to social selection, cependant, mascu-
line females are simply the reverse of
feminine males, namely, a female using
body English to converse on topics and
with words used more frequently by

males than by feminine females. Tel
conversations might involve establish-
ing and defending territories in species
where these tasks are sometimes carried
out by females. Masculine females ap-
pear underreported because feminine
males draw more sensational attention.
Homosexuality. Biologists are just now
starting to appreciate the extent of ho-
mosexuality as a natural part of the so-
cial systems of animals in their native
habitats. Homosexual behavior is now
documented in the primary literature
for over three hundred species of verte-
brates, not to mention invertebrates;
and many cases are reported in news
media, popular magazines, and wildlife,
agricultural, or hobbyist sources. Dans
some species, homosexuality is mostly
between males; in others, mostly be-
tween females; and in still others, les deux.
In some, homosexuality is relatively un-
common, occurring in about 10 pour cent
of matings; and in others it is as com-
mon as heterosexual matings, account-
ing for 50 percent of all matings.

Sexual selection explains homosex-
uality as an inadvertent mistake, as de-
ceit, or as a deleterious trait maintained
through peculiar population-genetic
mechanisms that promote the persist-
ence of bad genes. A typical deceit narra-
tive postulates that a small male sneaks
into the territory of a large male, tires
the large male by acquiescing to homo-
sexual copulation, and then proceeds to
mate with the females in the large male’s
harem. This behavioral narrative credits
homosexual behavior as adaptive to the
small participant, but views it as exploi-
tation–the gay animal exploits the
straight animal.

Entre-temps, population-genetic narra-
tives of homosexuality consistently por-
tray homosexuality as a genetic defect
or a maladaptive disease maintained by
peculiar genetic schemes, such as sexual-

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ly antagonistic selection, in which the
genes that cause homosexuality decrease
½tness in one sex but are maintained in
the population because they increase
½tness in the other sex. These approach-
es attempt to encode a homophobic nar-
rative of homosexuality as deleterious
and pathological into the hypothesis
structure of evolutionary biology, et
uncritically ignore the many alternative
adaptive hypotheses for homosexuality
in the behavioral literature.

According to social selection, not only

is homosexuality natural and adaptive,
but its explanatory narrative focuses on
positive contributions to both parties.
Homosexuality is grouped with many
other social behaviors involving physi-
cal intimacy, such as mutual grooming,
mutual preening, sleeping together, rub-
bing tongues together, and even mak-
ing interlocking calls and other vocali-
zations. These behaviors allow two ani-
mals to work together as a team, to co-
ordinate their actions so they make
moves simultaneously. En outre,
these behaviors allow animals a tactile
sense of each other’s welfare. Since, dans
social selection, the outcomes of cooper-
ative game theory are realized through
team play and perception of team wel-
fare, homosexuality is one of the physi-
cally intimate behaviors between ani-
mals that enable team play.

How might one apply these contrast-

ing theories to the human case?

Human attractiveness. If the theory of

sexual selection applies to humans,
women are supposed to ½nd handsome
men who display traits indicating their
genetic quality. Inversement, men are sup-
posed to be promiscuous. According
to social selection, males and females
choose each other equally, with the cri-
terion for both being compatibility of
circumstance, temperament, and incli-

nation that underlies effectiveness at
raising offspring in the context of a hu-
man social infrastructure.

Human brain. Sexual selection posits
the human brain as a counterpart of the
peacock’s tail, an ornament used by men
to attract women. One imagines a man
using his big brain to compose lovely
sonnets to woo his mate. The problem
then is to explain why women have
brains. Is a woman’s brain a ‘female or-
nament,’ as out of place in a woman as
a gaudy tail on a peahen? Sexual selec-
tion postulates that females use their
brains to appreciate the brains of males
–only big-brained women are turned
on by the sonnets of big-brained men.
Social selection, on the other hand,
views the human brain as a social-inclu-
sionary trait, a trait needed to partici-
pate in the social infrastructure within
which offspring are reared. This trait
is equally necessary in both men and
women because both share the work of
rearing offspring.

One might have anticipated that evo-

lutionary biologists would react with
glee to an alternative theory to sexual
selection. After all, challenges to the the-
ory of relativity, or to the theoretical ba-
sis of gravity, elicit calls on Congress to
fund expensive experimental facilities
lest billiard balls suddenly change trajec-
tories or gravity suddenly evaporate. Si
sexual selection is wrong, then surely we
need to get the matter right lest sex itself
disappear. This threat to our personal
security seems grave enough to usher in
a bonanza of funding so that evolution-
ary biology might champion the noble
mission of making the world safe for
sex.

But no, rather than seizing the

research opportunity that an alterna-
tive to sexual selection provides, evo-
lutionary biologists have, for the most

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part, tried to discredit me personally
as biased. Even before my book Evolu-
tion’s Rainbow was published, the edito-
rial staff of Nature in 2003 encouraged
a young journalist, Virginia Gewin, à
write: “Some scientists privately won-
der if–whether she likes to admit it or
not–Roughgarden’s own experiences
of social exclusion have biased her view
of the natural world.”7 When the book
appeared in 2004, Alison Jolly’s review
in Science identi½ed me as a “transsexu-
al professor” in the second sentence.8
Then Sarah Hrdy’s review in Nature
continued with, “This evolutionary
biologist becomes a woman, and only
then do the problems occur to her.”9
A month later, Robin Dunbar ridiculed
my book in Trends in Ecology and Evolu-
tion (arbre): “Readers of tree will no
doubt be pleased to know that sexual
selection is dead so they can now get
on with research into more useful top-
ics.”10 Dunbar concludes with the ad-
monition, “It is almost impossible to re-
tain a sense of dispassionate objectivity
when you see yourself as an object of
your own research.” Dunbar is happily
unaware that this applies to him as well.
Jerry Coyne followed up in the Times
Literary Supplement. After outing my for-
mer name in the second sentence of his
revoir, he charges that my “laundry list
is biased. She ignores the much larger
number of species that do conform to
sexual selection theory, focusing entire-

7 V. Gewin, “Joan Roughgarden Pro½le: A Plea
for Diversity,” Nature 422 (2003): 368–369.

8 UN. Jolly, “The Wide Spectrum of Sex and
Gender,” Science 304 (2004): 965–966.

9 S. Hrdy, “Sexual Diversity and the Gender
Agenda,” Nature 429 (2004): 19–21.

ly on the exceptions.” In fact, no one
knows how many species conform to
Darwinian sex-role templates, and many
thousands do not, as I have already dis-
têtu. Coyne accuses me of being an-
thropomorphic but then goes on himself
to illustrate sexual-selection theory with
a human example: “The Guinness Book
of Records awards the laurels for repro-
ductive output to a Moroccan emperor
who sired more than 900 progéniture. Le
female record–though in some ways
more remarkable–is a mere sixty-nine.”
Michael Ruse, a philosopher who has
written books advocating Darwinism,
continued in the Toronto Globe and Mail.
He dismisses Evolution’s Rainbow as a
“cryptic autobiography” and “polemic”
against sexual-selection theory directed
to campus audiences in “areas like cul-
tural studies that are big into . . . the he-
gemony of heterosexism and all that
sort of thing.”11 Ruse also plays the
transsexual card, excusing himself by
adage, “Normally, one would not start
discussing a person’s thesis by talking
about the person herself, but in this
case it is both legitimate and necessary.”
He goes on to argue that the concept of
gender cannot be widened to include
animals because a bullfrog could never
say, “I was a man trapped in a woman’s
body.” Ruse objects to theorizing that
homosexuality in animals evolved to
promote bonds because this cannot ex-
plain human “bathhouse culture.”

The gold medal for insult goes to a
Peter Conrad writing in a U.K. Sunday
newspaper, The Observer, Guardian Un-
limited. He declares Evolution’s Rainbow
to be a “practical joke,” refers to San
Francisco as “frisky,” and disparages
my “strange allegorical surname” by

10 R.. Dunbar, “Is Sexual Selection Dead?»
Trends in Ecology and Evolution 19 (2004): 289–
290.

11 M.. Ruse, “Why Not a Third Sex? And a
Fourth, et . . . ” Toronto Globe and Mail, Juillet
10, 2004.

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claiming my life consists of “tending her
mutated physique as if it were a rough
garden that has now been weeded and
manicured into femininity.”12

Another angry defense of sexual selec-
tion was broadcast by Michael Ghiselin
in the magazine California Wild. Ghiselin
claims a previous article of mine in the
same magazine “gives no indication of
the author’s ulterior motivations for
writing it.”13 He proceeds to out me as
someone who “at age 51 . . . had himself
transformed into Joan Roughgarden”
and dismisses Evolution’s Rainbow as “a
work of self-justi½cation.” Meanwhile,
Giselin privileges himself as an “honest
seeker after truth” who does not “want
to see the issues misrepresented.”

De la même manière, together with collaborators,

I recently presented in Science our two-
tier alternative to sexual-selection theo-
ry, introducing cooperative game theory
for the behavioral tier, as well as conven-
tional competitive game theory for the
evolutionary tier.14 It evoked ten indig-
nant letters of reply that were also pub-
lished in Science, representing over forty
authors.15 Nick Atkinson of The Scientist
contacted the sexual-selection defenders
and recorded comments ranging from
“the ‘new’ theory is merely part of the
existing body of Darwinian sexual selec-

12 P.. Conrad, “Frisky in Frisco,” The Observer,
Guardian Unlimited, Août 1, 2004.

13 J.. Roughgarden, “The Myth of Sexual Selec-
tion,” California Wild (Été 2005); M.. Ghis-
elin, “Sexual Selection,” California Wild (Hiver
2005).

14 J.. Roughgarden, M.. Oishi, and E. Akçay,
“Reproductive Social Behavior: Cooperative
Games to Replace Sexual Selection,” Science
311 (2006): 965–969.

15 Etta Kavanagh, éd., “Debating Sexual Selec-
tion and Mating Strategies,” Science 312 (2006):
689–697.

tion theory,” from Kate Lessells of the
Netherlands Institute of Ecology, et
“sexual selection theory . . . happily in-
cludes all of the points Roughgarden et
al. try and make,” from David Shuker at
the University of Edinburgh, to “many
people felt that this was completely
shoddy science and poor scholarship, tous
motivated by a personal agenda,” from
Troy Day at Queens University in Can-
ada.16 Put together, these comments
claim at once that social selection is part
of sexual selection and also bad schol-
arship, a position sexual selectionists
should ½nd discomforting.

Sexual selectionists also attempt to in-
timidate by noting I have been the “tar-
get” of critiques “involving more than
50 distinguished behavioral ecologists,»
according to a recent anonymous grant
reviewer, as though I should now be si-
lent. The panel summary then charges
that “the pi [Roughgarden] does a ma-
jor disservice to the ½eld and to her own
recherche . . . . The panel feels that the pi is
setting up a straw man.” Is sexual selec-
tion a straw man?

In response to this devastating recep-

tion, I sought to change my name and
escape to Tierra del Fuego. But the vil-
lage elders there declined my visa appli-
cation. Having now been declared per-
sona non grata even to the ends of the
earth, I am left no choice but to stand
my ground. Darwin’s theory of sexual
selection is locker-room bravado pro-
jected onto animals and then retrieved
as though a fact of nature.

Heureusement, the relentless dirge of
anger directed against Evolution’s Rain-
bow was punctuated briefly in 2005,
when the book received thoughtful and
extensive reviews by Robert Dorit in The

16 Nick Atkinson, “Sexual Selection Alterna-
tive Slammed: Biologists Write to Science to
Defend the Theory of Sexual Selection,” The
Scientist, May 5, 2006.

Challenging
Darwin’s
theory of
sexual selec-
tion

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Dædalus Spring 2007

Joan
Rough-
garden
sur
sex

American Scientist and Douglas Futuyma
in Evolution.17

The criticisms of Evolution’s Rainbow
and later work do not deal with substan-
tive issues, and instead employ personal
attack to deflect attention from the seri-
ousness of sexual selection’s limitations.
I have evidently stumbled upon a Dar-
wingate. The invective in the criticisms
may signal unease at unraveling a cover-
en haut, a fear that decades of professional
and personal investment in the sexual-
selection narratives will collapse.

The invective may also scratch the

vein of a deep-seated transphobia
among evolutionary biologists. Legit-
imizing diverse expressions of gender
and sexuality is clearly threatening.
Ghiselin issues the threat explicitly:

Had Roughgarden simply argued that
there is more to reproductive strategies
than just male combat and female choice,
and presented some reinterpretations of
the data, there would have been no reason
to respond. But here we have an effort to
discredit perfectly good science.

Ainsi, it would be okay to add a little
fluff to sexual selection to account for
gay and gender-bending animals, so long
as I do not touch the central narrative.
I invite readers to consider the pos-

sibility that sexual selection is com-
pletely wrong because it started out on
the wrong track, and that refusing to
reconsider sexual selection’s ground-
ing assumptions is leading subsequent
research to compound the original er-
rors. Only by devising and testing alter-
native evolutionary theories of repro-
ductive social behavior can we truly
strengthen evolutionary biology.

17 R.. Dorit, “Rethinking Sex,” American Sci-
entist 92 (5) (September–October 2004); D.
Futuyma, “Celebrating Diversity in Sexuality
and Gender,” Evolution 59 (2005): 1156–1159.

Dædalus Spring 2007

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