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Sexual Selection’s Mystique Lingers
ARTHUR ALLEN
Choosing a mate: Flies do it, fish do it, but understanding it is no simple matter.
D
eep inside On the Origin of Species,
Charles Darwin deposited a second theory of evolution. The process
occurred not only as a result of natural
selection of the fittest individuals, he
wrote, but through “a struggle between
males for possession of the females”
and the opportunity to mate. Twelve
years later, in 1871’s The Descent of
Man, Darwin elaborated on the evolution of sex differences: “Many female
peacock progenitors… by the continued preference of the most beautiful
males, [must have] rendered the peacock the most splendid of living birds.”
The same was true of traits such as big
antlers, which gave some males a fighting advantage that enabled females
to pick the most vigorous and wellarmed mates.
Darwin’s peers were not crazy about
his second big idea. They thought
females too intellectually feeble to
assert choice and animals quite incapable of aesthetic appreciation. The
idea of sexual selection received relatively little attention until 1972, when
biologist Robert Trivers hypothesized
that females were choosier about mates
and more inclined to care for their
young, because they had fewer—and,
therefore, more precious—gametes to
pass on. Males, with plenty of sperm
to spare, maximized their evolutionary
fitness by gadding about as much as
possible.
Trivers’s essay turned sexual selection into a research hotspot, with
hundreds of scientists examining
the range of sexual behavior and
sexual ornamentation in nature. But
a decade ago, Stanford University
The male peacock’s tail may not be a magnet for the opposite sex after all, according
to new research. Shown here are a pair of common peafowls (Pavo cristatus).
Photograph: Dick Daniels, http://carolinabirds.org.
biologist Joan Roughgarden launched
a frontal attack on the theory. In her
books Evolution’s Rainbow: Diversity,
Gender, and Sexuality in Nature and
People (2004) and The Genial Gene:
Deconstructing Darwinian Selfishness
(2009) and in a controversial 2006
Science article (http://io.aibs.org/
cooperative), Roughgarden stated
that sexual selection was flat-out
wrong and an artifact of paternalistic
Victorian thinking. Using game theory
models from John Nash, she urged
that theories of sexual selection be
replaced by a system stressing the evolution of communication, signaling,
and cooperation among the sexes and
individuals. Scientists should focus
on the social infrastructure around
raising offspring, rather than the sex
acts that mechanically produce them,
she argued. Her approach allowed for
cooperative dynamics, in contrast to
the view that all behavior be seen as
competitive.
“The sexual-selection system proposes a worldview of nature that
emphasizes conflict, deceit, and dirty
gene pools,” Roughgarden wrote
(http://io.aibs.org/teamwork), whereas
social selection favors “cooperation
as much or more than competition.”
BioScience 64: 375–380. © 2014 Allen. All rights reserved.
doi:10.1093/biosci/biu047
http://bioscience.oxfordjournals.org
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Social pleasure and coordination could
be evolved traits, she wrote. “The act of
cooperation itself is hypothesized to be
pleasurable.”
Roughgarden’s assault on sexual
selection failed, at least for now, but
it may have given researchers a fresh
opportunity to reflect on the status of
their work on sexual behavior, which
grows more complex each year as
fieldwork and genetic examinations
reveal phenomena that would have
been unimaginable in Darwin’s time or
even in the early 1970s.
As the field moves well beyond
sexual selection between promiscuous males and coy females, however,
a few specialists worry that it has
entered an unwieldy phase. “Our current understanding of mating systems
is based predominantly on post hoc
explanations of individual patterns,”
Suzanne Alonzo, associate professor
of ecology and evolutionary biology
at Yale University, wrote recently. This
is frustrating. “We don’t want to make
up stories after the fact,” she said in an
interview. “We need nuanced a priori
theories.”
But although sexual selection grows
more complex all the time, few are
inclined to discard the theory. “I don’t
know any scientist with an evolution
background,” says Alonzo, “who thinks
there’s anything wrong with sexual
selection.”
An unappreciated maverick
Roughgarden’s papers have received
few citations in the scientific literature,
and peers have generally not been kind.
“She started from left field, climbed the
fence, and dove right into the deep
end,” says Janet L. Leonard, a biologist
at the University of California, Santa
Cruz, who studies sexual selection in
hermaphrodites, such as sea slugs.
Many scientists, such as the
University of Chicago’s Jerry Coyne,
attacked Roughgarden’s ideas on the
grounds that they were biased by a personal agenda. In Evolution’s Rainbow,
in particular, Roughgarden protested
the social constraints of gender roles
and laid some of the blame for it on
biologists and their theories.
376 BioScience • May 2014 / Vol. 64 No. 5
Joan Roughgarden in the canopy of a rainforest tree near Manaus, Brazil,
overlooking a tributary of the Amazon River. Roughgarden has challenged
sexual selection theory. Photograph: Joan Roughgarden.
Other scientists maintained that
Roughgarden had misinterpreted
empirical research, whereas a few
found some of her ideas intriguing—
but difficult to test. The most common
complaint about Roughgarden’s thesis
was that she had made assumptions
about a field that had long ago accommodated the ideas that she introduced
as new. “I have sympathy for her, but I
think she made much ado about nothing in terms of her claim that Darwin
got sexual selection wrong, because
the field has moved on,” says Patricia
Adair Gowaty, distinguished professor
of ecology and evolutionary biology
at the University of California, Los
Angeles.
And although there are endless
forms of reproductive diversity and
miles to go before we disentangle them,
Darwin’s sexual selection system can
still do this, says David Shuker, of the
University of St. Andrews, Scotland.
“Joan’s thing is, ‘It’s all about cooperation.’ But if there’s a benefit to being
cooperative, there will be competition
among individuals to be a good cooperator, genetically speaking,” Shuker
adds. “Natural selection, in general,
is competitive. It’s all about genetic
representation in the next generation.”
Roughgarden’s argument has found
its most receptive audience among
historians and philosophers of science.
Feminist scholars were interested
“in part because sexual selection is
a point of tension between humanities and science,” says Erika Milam,
a Princeton University historian of
science. Roughgarden’s critique was
especially harsh on the discipline of
evolutionary psychology, which many
liberal academics feel has colonized
popular thinking about sex differences
with conservative ideas.
The philosopher of science Thomas
Kuhn wrote that it was not the amassing of anomalies that resulted in a paradigm shift, but, rather, the development
of an explanatory model that wins
over the field. So far, Roughgarden’s
model has had few takers. “The gambit
she played is fascinating. She tried to
elevate her hypothesis to a paradigm
shift,” says biologist Joel Brown of the
University of Illinois at Chicago. “But
at the end of the day, the opportunity
to come up with a groundbreaking
model hasn’t happened.” The paradigm didn’t shift; the gambit failed.
Roughgarden, however, asserts that
she was never challenging the neoDarwinian paradigm and insists that
it’s too early to determine whether her
alternative hypothesis to sexual selection will win the day.
Adds Shuker, “Where we’ve gone
since the Science paper is, people have
asked, ‘What do you think sexual
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selection is?’ And that’s a legitimate
question. The only shame is that she
initially presented her ideas as iconoclastic, and I don’t think they really
are.”
Animals defy stereotypes
Few of the scientists interviewed for
this article felt that Roughgarden had
much to do with it, but the field of sexual selection has incorporated increasingly complex and diverse thinking.
Contemporary definitions of sexual
selection look at competition for mates
more generally and frequently involve
the effects of chance and the environment. Molecular techniques, such as
genetic paternity testing, have allowed
scientists to find promiscuity in unexpected places. The nests under birds
once thought to be monogamous turn
out to have eggs with many sires. Male
fish are often the ones taking care of
the eggs laid by mates—even if many
of the eggs were fertilized by other
fish. Even the peacock’s tail—which
inspired Darwin to create the theory
of sexual selection—may not play
such a crucial role in mating. In 2008,
Japanese scientists published a study
describing 7 years of observing Indian
peacocks. Far from being drawn to
males with the most spectacular arrays,
they said, the peahen’s mating choices
were seemingly random.
In addition to new findings of female
promiscuity, the field includes an area
called female cryptic choice, which
refers to the fact that, in many species, females have reproductive tracts
that selectively reject male sperm after
multiple matings. Studies have incorporated social cooperation into sexual
selection models and have shown that
the genetic expression of male and
female traits can vary within sexes
depending on environmental cues.
Recent neurobiological research has
revealed that animal perceptions that
evolved for survival (say, by improving
awareness of predators) may bias mate
selection preferences.
Areas of ardent controversy remain.
One debate revolves around the ­socalled sexy-sons and good-genes hypo­­
theses, two explanations for why females
http://bioscience.oxfordjournals.org
The flashiness of markings on the male collared flycatcher (Ficedula albicollis)
does not translate into fitness with respect to fatherhood, researchers found.
Photograph: Frank Vassen.
choose mates. The sexy-sons concept,
suggested in the 1930s by British
researcher Ronald Fisher, postulates
that, by mating with males whom they
find attractive, females are more likely
to give birth to attractive sons, who
will, in turn, successfully attract mates,
and therefore, the attractive trait will
continue through future generations.
The good-genes hypothesis goes like
this: Females choose mates with, say,
enormous, impractical tails because
they send a signal that says, “I’m so
robust I can drag this around the
jungle without getting eaten by predators,” as Janet Leonard puts it. In
other words, the tail (or song, or walk,
or color, or other seemingly useless
trait) tells the female that the peacock has good genes that her children
will inherit. The late British biologist William Hamilton and Marlene
Zuk, who is currently at the University
of Minnesota, theorized in 1982 that
outstanding traits like longer tails
or brighter plumage showed that an
animal was more resistant to parasites and, therefore, of sturdier stock.
The female did not have to think this
through—but her choice evolved to
keep her genes in the pool by linking
them to healthy male inheritance.
However, in many instances, the
good-genes hypothesis has failed in the
field. The most popular traits often do
not translate into offspring with better
genes. For example, a 24-year study of
collared flycatchers by Swedish scientists showed that, although male
offspring of male birds that had flashy
white head badges often inherited the
badges, the badge boys—although
they were attractive—were no fitter in
terms of survival or fathering offspring
than were other birds. In a 2012 metaanalysis (http://io.aibs.org/choosy) in
which studies of 55 different animals
were examined, Zofia Prokop and her
colleagues at Jagiellonian University, in
Poland, found similar results. Sexiness
was inherited, fitness not so much.
In 2010, similar findings inspired
Yale biologist Richard Prum, the
William Robertson Coe Professor
of Ornithology, Ecology, and Evolu­
tionary Biology at the Yale Peabody
Museum of Natural History, to propose
that, in general, mate choice should be
considered a genetically random event,
linked not to hopes for good genetic
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offspring but to the mate’s hope for
direct benefits. Females choose mates
because they think that the mates will
help them—in defense, say, or foraging, or guarding the nest—or, perhaps,
just because they think they are hot.
Not all the preference comes from
the female side. In a study published
last fall (http://io.aibs.org/competition),
Tracy Langkilde, associate professor
of biology, and her graduate student
Lindsey Swierk, at Pennsylvania State
University found that male fence lizards in the southeastern United States,
which bear blue bands along their
sides, preferred to mate with females
that lacked the coloring. Their research
showed that the bands are an indicator of testosterone levels and that
blue-banded females bore eggs later,
which might make them more vulnerable as winter approached. Despite this
finding, more than two-thirds of the
female lizards do have the blue bands,
which does not fit the theory. Says
Langkilde, “It could be that what we’re
seeing is the gradual disappearance
of this trait in females. Alternately,
perhaps the blue-banded females get
some other benefit from having additional testosterone; maybe they are
more aggressive at finding mates or
guarding the nest. We’re not even close
to knowing.”
Although it is still a cornerstone
of the field, Trivers’s parental investment theory has taken some hits. In
many species, males take care of litters or clutches, and male sexiness
is not always turning out to be an
unmitigated plus in terms of the next
generation’s fitness: Male traits that
are seemingly good for sons may be
bad for daughters. For example, highly
sexed male voles are more likely to
father less-fertile daughters, according
to research by Mikal Mokkonen, of the
University of Jyväskylä, in Finland.
Trivers’s theory would predict that,
because males have more chances to
spread their genes, hermaphrodites
would prefer reproducing as males.
That is not the case in the sea slugs that
Leonard studies in California. When
two slugs meet, both indicate that
they would prefer to mate as females.
378 BioScience • May 2014 / Vol. 64 No. 5
The male blue-throated fence lizard (Sceloporus occidentalis) seems
to prefer females without the band of blue, which is associated with higher
levels of testosterone. However two-thirds of females have a blue band.
Photograph: Langkilde Lab, Pennsylvania State University.
Perhaps this is because females can
either eat the sperm or use it to fertilize eggs. The sea slug’s penis is right
next to its head, which makes it difficult to forage while it mates. Mating
as a female, however, it can keep right
on feeding.
Assigning sex roles is complicated
by the fact that, in some species, a
single sex may have multiple, clearly
delineated gender roles. In the ocellated wrasse, a fish that Alonzo has
studied on rocky reefs near Corsica
for the past two decades, males can be
sneakers, satellites, or nesters. Sneakers,
the smallest males, and satellites, the
midsize model, are adept at stealth
fertilization. The large nesters are the
homebodies. Male wrasse often occupy
two of the three roles in a single 2-year
life span. The female prefers the larger,
more brightly colored nesters—not the
agile sneakers and satellites—because,
as the name suggests, the nesters guard
the cup-shaped reef niches where the
female lays her hundreds of thousands
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of eggs. To care for them, the nester
fights off predatory fish and carries
away parasitic snails, all the while aerating the eggs with a fanning motion
of his fins, and he does this even
though many of the eggs he guards
were probably fertilized by sneakers
or satellites. (Because he is guarding
thousands to tens of thousands of eggs,
Alonzo explains, he does not have to
worry about his genetic legacy. Even if,
say, only half of the eggs are his, he still
has thousands of offspring.)
The bird world has also provided
many surprises. House finch females
prefer more-intensely colored males—
which happen to be the older ones.
Perhaps this behavioral trait is linked
to the fact that, by virtue of being
older, the males have demonstrated
higher fitness. However, in the zebra
finch, which has been bred for pet
stores because of the male’s lovely
coloring, this trait seems to play no
role in attracting females, according to
Wolfgang Forstmeier, who studies the
birds at the Max Planck Institute for
Ornithology, near Munich. “Why the
beautiful feathers and beaks? That’s the
million-dollar question,” he says.
Forstmeier and other finch students
are also trying to wrap their minds
around the variable fidelity of their
birds. In the wild, the zebra finch pairs
for life and is almost always faithful. In
captivity, however, about a third of the
eggs in a given clutch will have been
fathered by finches from outside the
pair. Wild zebra finches brought into
captivity, however, are about midway—
in terms of their fidelity—between
finches born in captivity and those
that continue to live in the wild. Do
they cheat more in captivity because
the nesting areas are more crowded,
making it easier to find a casual sex
partner? Or do the more limited populations of finches in captive nesting
areas make it less likely that the female
finch will find a soul mate with whom
to bond and mate for life?
Meanwhile, new experimental work
has shown that females often have
perfectly good evolutionary reasons
to play the field. Nina Weddell, of
the University of Exeter, in England,
http://bioscience.oxfordjournals.org
The female ocellated wrasse (Symphodus ocellatus; far left) prefers the domestic
traits of a large nesting male (center) over the flighty sneaker (top) or satellite
(far right) males. Photograph: Kelly Stiver
Zebra finches (Taeniopygia guttata) appear to be faithful life partners in the
wild. But in captivity—not so much. Researchers are trying to figure out why.
Photograph: Peripitus.
for example, showed that female fruit
flies and other species gain fitness
from multiple mating, or poly­andry.
In the fruit fly Drosophila pseudo­
obscura, a so-called selfish genetic
element that destroys sperm that
carry a Y-chromosome means that
females that mate only with any one
male are at risk of producing only
female offspring, which might lead to
May 2014 / Vol. 64 No. 5 • BioScience 379
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daughters’ having no males with whom
to mate in the population. Polyandrous
females have been found so frequently
now—among birds, insects, reptiles,
and mammals—that Weddell and her
Oxford colleague Tommaso Pizzari
last year edited a special issue of the
Philosophical Transactions of the Royal
Society B entitled “The polyandry
revolution.”
It is also becoming clear that the
environment affects sexual selection
in unpredictable ways. Chance occurrences in individual lives may or may
not influence decisions to mate, which
makes it hard to predict how males and
females in a given species operate. The
frequency of mating among different
animals in a given area varies tremendously and is hard to predict, says
Gowaty. “We can’t separate out what’s
due to selection and what’s due to random chance,” she says. Individuals that
are sick or in the presence of predators
are more likely to mate with whoever
is around. “It may be that if you have
an immense amount of time, you’re
discriminating in your mate, and if
not, you do it like bunnies—quick,” she
says. “Our models show that the best
predictor of fitness is to be sometimes
indiscriminate, sometimes choosy.”
Meanwhile, after the disappointing
reaction to her work, Roughgarden
regrouped. After a discussion at a
London conference in 2011, she and
Shuker, who is very much part of
the mainstream of sexual selection
theory, agreed to see whether they
380 BioScience • May 2014 / Vol. 64 No. 5
Researchers in the Gowaty Lab study Drosophila mettleri, a nonmodel
species of fly. Some D. mettleri males skip courtship when mating.
Photograph: Sergio J. Castrezana.
could further a fruitful discussion.
Roughgarden invited Shuker and 32
other specialists to a workshop at
the National Evolutionary Synthesis
Center (NESCent) in Durham,
North Carolina, last July. Afterward,
Roughgarden, who retired from
Stanford in 2011 and now teaches at
the Hawai’i Institute of Marine Biology,
said that she had been pleased to see
some subtle shifts in the field. “At the
NESCent meeting, no one spoke up
on behalf of promiscuous males and
coy females,” she says. “I’m not sure
many people would say they’ve made
modifications because of me. But it’s
not a coincidence that modifications
are taking place.”
The title of the gathering was perhaps a bit ironic: “Sexual selection studies: Progress, challenges, and future
directions.” As it turned out, those in
attendance could not even agree on a
definition of sexual selection, but that
will not keep them from studying it.
Arthur Allen ([email protected]) is the
author of Vaccine: the Controversial Story of
Medicine’s Greatest Lifesaver (2007, Norton)
and the forthcoming The Fantastic Laboratory
of Dr. Weigl: How Two Brave Scientists Battled
Typhus and Sabotaged the Nazis (2014, Norton).
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