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The stresses of Mr Wrong

Having a genetically incompatible mate can increase a female bird's stress hormone levels which then can affect the sex ratio of her offspring

A black-headed female Gouldian finch, Erythrura gouldiae, chooses her mate.

Image: Sarah Pryke (with permission) [velociraptorise]

As any finch breeder can tell you, female Gouldian finches, Erythrura gouldiae, can adjust the sex ratio of their chicks based on the quality of their mates (as I have written about before). This might seem like a strange quirk, but this is not as unusual as you might think. Further, even though the biological underpinnings of this phenomenon are poorly understood, 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 [doi:10.1111/j.1558-5646.2008.00584.x]. Most of these unfortunate youngsters die before they have the opportunity to breed.


"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."


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 (as I have written about before).



DOI: 10.1093/beheco/arr040


When Dr Pryke and her team compared to the number of sons that each female produced to the concentrations of corticosterone in the mother's bloodstream, they found a strong relationship:

DOI: 10.1093/beheco/arr040

These data clearly show that when female finches were paired with a compatible male, they produced chicks with an unbiased sex ratio, but when paired with an incompatible male, they overproduced male chicks, ending up with four times more fledgling sons than daughters. This overproduction of sons was not correlated with the chicks' "birth order", nor with the female's circulating testosterone levels, nor with maternal body weight. Additionally, Dr Pryke and her colleagues found that nests with incompatible parents produced more infertile eggs, more eggs with early embryonic mortality and higher nestling mortality.

Newly-hatched Gouldian finch chicks in nest.

Image: Sarah Pryke (with permission) [velociraptorise]





Genetics+%2C+Reproduction%2C+Zoology%2C+Ornithology%2C+corticosterone%2C+Gouldian+finch%2C+Erythrura+gouldiae%2C+mate+choice%2C+maternal+effects%2C+sex+ratios">Pryke, S., Rollins, L., Buttemer, W., & Griffith, S. (2011). Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment. Behavioral Ecology, 22 (4), 717-722 DOI: 10.1093/beheco/arr040

Sarah Pryke [email; 24 June 2011]

Evolution&rft_id=info%3Adoi%2F10.1111%2Fj.1558-5646.2008.00584.x&;bpr3.tags=Biology%2CEvolutionary+Biology%2C+Ornithology%2C+Assortative+mating%2C+color+polymorphism%2C+Gouldian+finch%2C+Erythrura+gouldiae%2C+postzygotic+incompatibility%2C+reproductive+isolation%2C+Genetics%2C+Reproduction%2C+Zoology">Pryke, S., & Griffith, S. (2009). Postzygotic genetic incompatibility between sympatric color morphs. Evolution, 63 (3), 793-798 DOI: 10.1111/j.1558-5646.2008.00584.x




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