Gouldian Finches - Erythrura gouldiae - occur in two morphs. Red heads or Black heads.
Red-headed females prefer red-headed males – and black prefer blacks.
In the small populations it is not always possible for the finches to
chose their own type. When they cross the results are not good. However,
a “hybrid” female will always have less viability than “hybrid” male.
The stress of mating the “wrong” kind makes the Gouldian Finch able to
regulate the outcome producing more male “hybrid” offspring which has
better viability.
Female Gouldian finches, can adjust the sex ratio of their chicks based on the quality of their mates. This might seem like a strange quirk, but this is not as unusual as you might think. Further, the biological underpinnings
of this phenomenon are poorly understood and they have profound and
far-reaching implications for our understanding of reproduction and
developmental biology as well as conservation of this and similar
endangered species.
Gouldian finches are brilliantly-coloured and intricately-patterned
passerines that live in the deserts of Australia’s “outback”. They are
socially monogamous and have a colour polymorphism - black or red head
plumage colour - that provides a visual cue indicating each individual
bird’s genetic compatibility.
“Gouldian finches wear their genes on their head”, said Sarah Pryke, a behavioral ecologist at Macquarie University in Sydney Australia.
Female Gouldian finches choose their mates based on the plumage
colour of the male’s head: females with black head plumage choose
black-headed males whilst red-headed females choose red-heads.
“Daughters produced from mixed matings — where parents differ in head
color — suffer from genetic incompatibilities between their parents
that cause about 84 per cent to die young”, Dr Pryke explained.
In Gouldian finches, female mate choice stems from the tremendous
fitness cost incurred by having a genetically incompatible mate with the
wrong head colour — sons from these “mixed marriages” experience a
40.2% greater mortality whilst daughters experience a 83.8% greater
mortality than chicks produced by genetically compatible pairs where
both partners have the same head-plumage colour. These unfortunate youngsters die before they have the opportunity to breed.
This characteristic is a critical conservation matter for Gouldian
finches because they are endangered in the wild: no subpopulation has
more than 250 adults, and there are not more than 2,500 adults alive in
the wild today. Even though black-headed birds comprise 70 percent of
the wild population, severe limitations on the number of adult birds
results in incompatible “mixed marriages” for twenty to thirty percent
of all pairings. When a female is stuck between choosing to breed with a
genetically incompatible mate or to not breed at all, she invariably
chooses to breed. But the female compensates for the huge mortality rate
in her daughters by overproducing sons, often by more than 80 percent.
“Females really don’t want to mate with a male with a different head
color”, stated Dr. Pryke. “But there simply aren’t enough compatible
males, so later in the mating season they seem to use this control to
make the best of a bad situation.”
Unlike mammals, where females are XX, female birds are the
heterogametic sex, having one Z and one W chromosome. So the mother can
control the sex ratio of her chicks, either by controlling which sex
chromosomal is placed into an egg or by influencing the survival one sex
over the other during embryonic development.
But how does a female Gouldian finch do this? Maternal body condition
and territory quality are two factors that can influence chick sex
ratio. Previous research has shown that maternal body condition and
physiological state are influenced by the female’s hormonal milieu, and
hormones are, in turn, influenced by social and environmental cues —
such as the quality of a male’s territory and genetic compatibility.
Because hormones act as chemical messengers that orchestrate and time
specific biological events, is plausible that hormones could trigger a
cellular mechanism that skews sex ratios in chicks.
Further, recent research shows that female Gouldian finches paired
with genetically incompatible “low quality” mates have significantly
higher concentrations of the stress hormone, corticosterone, circulating
in their bloodstreams.
To investigate whether corticosterone influences chick sex ratios in
Gouldian finches, Dr Pryke and her colleagues took 50 red-headed and 50
black-headed female finches and randomly paired them with either a
black-headed (homozygous recessive Zr) male or a homozygous dominant red-headed male. (Interestingly, heterozygous ZRZr
red-headed males are genetically incompatible with red-headed females).
After the female’s first brood fledged, she was paired with a male of
the other colour morph.
On the morning when the female finches laid their second egg, they
were quickly captured and a tiny blood sample was collected. Plasma
corticosterone was measured in the blood plasma of each female and
compared to when she was paired with a compatible and incompatible mate.
To summarise, when female Gouldian finches are paired with a
genetically incompatible mate, they experience stress levels that
elevate the concentration of corticosterone in their bloodstream. They
then adjust the sex ratio of their chicks to partially compensate for
increased chick mortality (particularly among their daughters), which
then creates a bias towards sons. Because the red-headed gene is
dominant to black, and because these birds are biasing their
reproductive effort towards producing sons, their offspring will
overwhelmingly be male red-headed heterozygotes. As I mentioned earlier,
heterozygous red-headed males are not genetically compatible with
either red-headed females nor with black-headed females. I am sure, at
this point, that the consequences of this situation are obvious.
This is the clearest and perhaps the most extreme example of sex
biasing that has been described to date. Already, Dr Pryke and her
colleagues have gathered more data from a series of studies designed to
further uncover the developmental mechanisms of this particular system.
(I am eagerly awaiting these results and plan to tell you about them.)
Even though these visually stunning birds have such fascinating
biology, there is an important practical reason to study them: wild
Gouldian finches are seriously endangered. They occur in several very
small and isolated populations where an imbalance in colour morphs or
sexes could easily drive each population, and indeed, the entire
species, into extinction. So understanding the reproductive system of
these birds is critical if we are to preserve the species — indeed, we
wish to conserve these birds anywhere outside of a pet shop.