THE SEX ISSUE
I
n the late 1960s, it was generally
assumed that the vast majority of birds
were monogamous. Indeed, the conventional
wisdom was that the females of most animal
species were monogamous, mating with and
remaining faithful to a single male partner. Then
something extraordinary happened. In 1962,
Vero Copner Wynne-Edwards, in his book Ani-
mal Dispersion in Relation to Social Behaviour,
promoted the idea that animals behaved for the
good of the species, or the good of the group
in which they lived. He suggested that if, for
example, food became scarce in the environ-
ment, some individuals would withhold from
breeding so that there would be sufficient food
for others to reproduce.
FEMALES?
NOT NATURALLY
MONOGAMOUS
Wynne-Edwards’s thesis provoked a strong
response from a handful of biologists who
understood natural selection. Experts, such as
David Lack and George Williams, pointed out
that his group selection ideas were flawed: nat-
ural selection operated on individuals, not on
groups or species. Nevertheless, a new area of
research was born from this debate that eventu-
ally became known as behavioural ecology.
FEATHERED
FORNICATION
Of polygamy, polyandry, rape, and sperm competition.
Welcome to the secret reproductive life of birds. Shocked? Blame it on natural selection
Tim Birkhead*
This new kind of individual selection thinking
made sexual selection relevant — and exciting
— again. Proposed by Charles Darwin in the late
1800s to explain the difference in the appear-
ance and behaviour of males and females, sex-
ual selection enjoyed a brief spell in the spot-
light. By the 1940s and 1950s that light had
faded, thanks largely to Julian Huxley, a great
populariser of science who did not understand
the way selection worked.
In the early part of the twentieth-century, Hux-
ley pioneered the study of animal behaviour
through his now classic study of Great Crested
Grebe Podiceps cristatus courtship. Since the
grebes’ elaborate displays occurred after pair
formation, Huxley argued that they could have
nothing to do with attracting a partner, and
hence, nothing to do with sexual selection. Less
well known is Huxley’s study of the courtship
and mating behaviour of Mallard Anas platy-
rhynchos, conducted at around the same time.
The contrast between his two study species
could hardly have been greater: the elegant
grebes seemed obviously monogamous with
their magnificent mutual courtship displays;
while the dreadfully promiscuous male ducks
forced themselves on females, sometimes with
such brutality and in such numbers that the
females drowned. Huxley’s explanation was
that the grebes had evolved to a higher level
than the dirty ducks. Moreover, since Huxley
believed that selection operated for the good
of the species, duck rape could not be anything
other than harmful.
JUNE 2017 • BIRDLIFE
THROUGH THE MID
1970s AND 1980s
IT BECAME CLEAR
THAT SEXUAL
MONOGAMY,
ESPECIALLY AMONG
FEMALES, WAS THE
EXCEPTION RATHER
THAN THE RULE
Black-winged Stilt
Himantopus himantopus.
Photo Sysasya/Shutterstock
4
The undergraduate lecture that changed the
course of my life featured an insect, rather than a
bird: the yellow dungfly Scatophaga stercoraria.
Far from being monogamous, female dungflies
were promiscuous, routinely copulating with
several males. Males, too, were promiscuous,
mating with several females. This behaviour dis-
pelled the myth, perpetuated by Darwin, that
females were monogamous; it also showed that
such promiscuity could be adaptive. Thirdly,
it demonstrated that sexual selection did not
cease once an individual had acquired a partner,
as Darwin assumed, but instead could continue
after mating through something called sperm
competition. To my young and eager self, this
was mind-blowing, exciting stuff: sex, behaviour
and a new way of thinking about selection!
I wondered whether the promiscuity observed in
insects might also occur in birds, and I decided
that was what I wanted to study. When I told my
undergraduate tutor and friends, they laughed:
“Birds are monogamous,” they said, “everyone
knows that. You’d be wasting your time.”
My PhD was on the behaviour and ecology of
Common Murre Uria aalge, and it was my good
fortune that they turned out to behave pretty
much like dungflies, with a lot of promiscuity,
despite having long-term pair bonds.
As behavioural ecology developed through the
mid 1970s and 1980s, it became clear that sexual
monogamy, especially among females, was the
exception rather than the rule. Males, of course,
had long been known to be promiscuous.
Instead of writing off promiscuity as an aberra-
tion or hormone imbalance, as was usually the
case prior to 1970, researchers now focused on
individuals ”getting their genes in to subsequent
generations”: what better way to achieve this
than by being promiscuous?
Just before the beginning of behavioural ecol-
ogy, David Lack had published what was to
become an incredibly influential book Ecolog-
ical Adaptations for Breeding in Birds (1968), in
which he stated that over 90% of all birds had
a monogamous mating system; the rest were
either polygynous, like the Red-winged Black-
bird Agelaius phoeniceus or the Ruff Calidris
pugnax, while a tiny few, like the jacanas were
polyandrous. Monogamy, therefore, was the
norm; it was the norm that required study rather
than the exceptions.
With the birth of behavioural ecology, the
focus switched to exceptions, and to the
”exceptions” to monogamy: extra-pair cop-
ulations. A key development was the ability to
establish paternity through techniques such
as DNA fingerprinting; this finally provided the
incontrovertible evidence that promiscuity, for
males at least, paid off. This also allowed us to
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