THE SEX ISSUE
RELATIVELY LARGE
TESTES ARE A SURE
SIGN OF FEMALE
PROMISCUITY
distinguish between ”social monogamy” and
”sexual monogamy” in birds. Understanding
sexual selection processes both before (e.g.
mate choice) and after (e.g. sperm competition)
insemination helps to explain phenomena that
wer e once thought inexplicable.
Take testicles, for example. An accidental dis-
covery in the 1970s, that massive differences in
relative testis size among the great apes mapped
onto their mating system, started a series of dis-
coveries in various animal taxa that eventually
revealed what amounts almost to a general rule:
relatively large testes are a sure sign of female
promiscuity. It was an idea with a long, albeit
incomplete history, for in 1676, when Francis
Willughby and John Ray wrote the first ency-
clopaedia of ornithology, they commented on
the huge testes of the Common Quail Coturnix
coturnix, commenting, ”whence we infer it is a
salacious bird”. The Common Quail is indeed
promiscuous, but without an evolutionary con-
text there was little else that could be said about
the phenomenon. Yet the observation holds
true; birds with large testes for their body size
invariably have extraordinary mating systems.
The Dunnock Prunella modularis is one of our
most promiscuous of birds, breeding variously
as monogamous pairs, in polyandrous trios (two
males and one female) and even polygynan-
drously (two males sharing two females); it has
testes that represent some 3.4% of the male’s
body weight. In contrast, the Eurasian Bullfinch
Pyrrhula pyrrhula appears to be strictly monoga-
mous, having the smallest testes relative to body
size, at just 0.29% of male body mass.
The testis acts as a sperm factory; a larger fac-
tory produces more sperm. In the competition
for fertilisations (which is what sperm competi-
tion is), the more sperm the better the prospects
of success. It is like trying to win a raffle: your
chances are improved the more tickets you buy.
MOST PASSERINES
COPULATE
FOR ONE OR TWO
SECONDS; THE
BUFFALO-WEAVER,
BY CONTRAST,
COPULATES
FOR 30 MINUTES
Such is the competition for the fertilisations
that in many species simply having a bigger
bucket of sperm isn’t enough. After all, the way
selection works, any advantage over another
male increases an individual’s chances of leaving
descendants. Between two males that each have
huge, but equally sized sperm stores, one that
has a penis slightly longer than the other is able
to place its sperm in a more propitious location
within the female oviduct, thus enhancing its
chances of fertilisation. Obviously, this male is
more likely to win the fertilisation competition;
hereafter, selection selects for penis length.
In species in which female promiscuity is rife,
the anatomical and behavioural adaptations
to enhance male reproductive success seem
almost limitless. Across the animal kingdom
examples abound, but let’s focus on birds.
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Common Murres
Uria aalge are very
promiscuous, despite having
long-term pair bonds and
being considered to have a
monogamous mating system.
Photo Menno Schaefer/
Shutterstock
4
BIRDLIFE • JUNE 2017
JUNE 2017 • BIRDLIFE
Most birds possess no penis: sperm are sim-
ply transferred from the male’s cloaca to the
female’s everted cloaca. Quail, which as we have
seen are promiscuous, have evolved a conspic-
uous gland adjacent to the male’s cloaca that
delivers a dollop of shaving-cream-like foam at
insemination; this enhances the vigour of their
sperm. The Red-billed Buffalo-weaver Buba-
lornis niger breeds in a polygynous harem-like
arrangement, but with two males forming a
coalition and sharing a group of up to twelve
females. Competition for fertilisation is stiff, and
males have evolved a false penis directly in front
of their cloaca to facilitate their fertilisation suc-
cess. The precise function of this 1-2 cm rigid
rod of connective tissue, with no ducts, con-
tinues to be a mystery. It isn’t inserted into the
female’s cloaca, but instead is rubbed against it
during their enormously protracted copulations.
Most passerines copulate for one or two sec-
onds; the Buffalo-weaver, by contrast, copulates
for 30 min. This prolonged cloacal massage by
the male apparently ”persuades” the female that
she should use his sperm rather than that of the
other coalition male.
The Aquatic Warbler Acrocephalus paludicola, a
nondescript little brown bird that breeds in the
fen mires of Poland and Belarus, also copulates
for about half an hour. This species appears to
be utterly promiscuous with no bonds between
the sexes. Fertile females seem to copulate
opportunistically; the male clings to the female’s
back so that the pair hop around together in
the vegetation like a couple of mice. The male
inseminates the female every seven minutes or
so during this time, with one main objective: to
flood her system with sperm. Male Aquatic War-
blers have huge testes; molecular studies con-
firm that mixed paternity in broods is the norm.
My favourite example is the Vasa Parrot Cora-
copsis vasa; I had never encountered anything
quite so extreme in birds as this. It was like the
protracted copulatory tie that occurs in dogs:
male and female as one, joined for over half-an-
hour by their genitalia. A colleague in Madagas-
car has also seen wild Vasa Parrots copulating
promiscuously. On dissecting a wet-preserved
male museum specimen and finding that
the testes were very large, I decided that this
extraordinary species would make a fascinating
PhD study; and so it proved. The mating system
was utterly promiscuous, with both sexes copu-
lating frequently and lengthily with several part-
ners, and females essentially trading food from
males (that they would take to feed their chicks)
for sex. Males copulated with as many females
as possible, in the ”hope” of securing a winning
lottery ticket, feeding the chick-rearing females
in return. The copulatory tie is an adaptation to
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