Sex chromosome linkage of mate preferences and color signal maintains assortative mating between interbreeding finch morphs

Sarah R. Pryke

Published in: Evolution (2010) 64: 1301-1310

Assortative mating is a widespread mechanism for avoiding out-breeding in which individuals use a variety of phenotypic cues (e.g., appearance and vocal cues) to recognize and choose potential mates that largely resemble themselves. Assortative mating is a key aspect in the speciation process because it is important for both initial divergence and maintenance of distinct species. However, it is unknown how assortative mating evolves when diverging populations are undergoing gene flow (interbreeding). Contrary to the predominant view on the development of sexual preferences in birds, cross-fostered offspring did not imprint on the phenotype of their conspecific (red or black morphs) or heterospecific (Bengalese finch) foster parents. Instead, the mating preferences of offspring were consistent with inheritance on the sex chromosomes, which are also the location for genes controlling color expression and the genes causing low fitness of intermorph-hybrids. Preferences for mates of the same head-colour morph are thus genetically inherited and not learned through sexual imprinting on their parents.

Maternal adjustment of parental effort in relation to mate compatibility affects offspring development

Sarah R. Pryke & Simon C. Griffith

Published in: Behavioral Ecology (2010) 21: 226-232

Parents should adjust reproductive investment in a current breeding attempt by considering the relative fitness benefits of current and future reproductive attempts. Using a within-individual experimental design, in which both males and females were forced to breed with mates of the same and different colour morph, females, but not males, increased their provisioning effort when breeding with compatible mates. By crossfostering offspring within and between matched and mixed pairs, foster offspring reared by matched pairs, with increased female provisioning, were also healthier, grew and developed faster, and fledged earlier than offspring reared by mixed pairs. This shows that females, but not males, differentially provision their offspring in response to mate quality.

Is red an innate or learned signal of aggression and intimidation?

Sarah R. Pryke

Published in: Animal Behaviour (2009) 78: 393-398

Red colouration has been associated with dominance and aggression in a number of animals. However, it is unclear whether the increased aggression of red individuals or the avoidance of red opponents is an intrinsic (inherent) or learnt response. By experimentally controlling for genetic and environmental effects, the competitive differences in sexually immature (uncoloured) red and black head colour morphs was tested. Despite juveniles being reared by foster parents of the same and different colour morphs, there were no differences in competitive abilities between uncoloured red and black males. However, when a red head mask was painted onto uncoloured males, red (but not black and novel blue coloration) was associated with winning contests. In addition, uncoloured opponents expressed higher stress responses (corticosterone) and avoided conflicts with red-painted competitors. Thus, the association between red coloration and aggression may be an innate response to aid facultative fight or submissive decisions, and adds to growing evidence in other animals suggesting that red coloration may be a general signal of intimidation.

Some of the articles by the Media on this paper: Nature News, New Scientist, NeuroDojo

Socially mediated trade-offs between aggression and parental effort in competing color morphs

Sarah R. Pryke & Simon C. Griffith

Published in: American Naturalist (2009) 174: 155-164

Individuals often face trade-offs between investment in parental care and alternative investments of time, energy, and resources into other life-history components, such as dominance, attractiveness, and health. Selection is thought to promote the optimal balance between the costs and the benefits of these conflicting activities by favoring individuals that adopt different tactics to gain the best fitness benefits in different environments. To test this, we experimentally manipulated both aggression (i.e., competitive environment) and parental effort (i.e., brood size) in red and black morphs of the Gouldian finch. Although aggressive red males provide parental effort comparable to that of black males in environments where competition is low, they severely reduce or provide no parental care in highly competitive environments. In contrast, the non-aggressive black males are largely unaffected by the competitive environment and instead adaptively adjust their parental care to the demands of their brood. Consequently, in highly competitive environments, although dominant red males defend higher quality nest sites, they produce fewer and lower-quality offspring than black males do.

The historical frequency of head-colour morphs in the Gouldian Finch (Erythrura gouldiae)

Amanda J. Gilby, Sarah R. Pryke & Simon C. Griffith

Published in: Emu (2009) 109: 222-229

The Gouldian Finch possesses a genetic colour polymorphism in the form of three genetically determined head-colours (yellow, black and red) that coexist in the same population. To investigate how these head-colour morphs have changed temporally and spatially over time, museum collections around the world were surveyed, identifying 614 wild-caught skins and obtaining accurate data on the morphs of 552 of these. The yellow morph was found at very low numbers (only 15 skins), consistent with its rarity in contemporary populations. Red- and black-morph individuals were found at relatively constant ratios across the geographical range over which they were sampled, and across the 140-year period during which these skins were collected, although this differed slightly for males and females (males: 62.6% black, 37.4% red; females: 79.1% black, 20.9% red). Spatial and temporal stability in the frequency of alternative morphs is extremely rare. These results suggest that the genetic architecture underlying the trait and selective pressures acting on the separate morphs of the Gouldian Finch differ between the sexes, but are fairly constant across highly variable environmental conditions.

Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch

Sarah R. Pryke & Simon C. Griffith

Published in: Science (2009) 323: 1605-1607

The idea that female birds can bias the gender of their offspring (broods) has been a highly controversial issue in recent biology. Using a very controlled experimental design, we found that when females were forced to mate with an incompatible male, or were tricked into thinking they were, they overproduced sons. This is adaptive because sons resulting from genetically incompatible pairings have a much better chance of survival than daughters. Females in incompatible pairs will also reduce overall investment in clutch size, egg size, and care to offspring. These results demonstrate that birds have the ability to adjust the sex of their eggs and allocate resources depending on the quality of their partner, and therefore may have much more influence over the outcome of reproduction than has previously been recognised.

Some of the articles by the Media on this paper: BBC News (UK), ABC News, Sydney Morning Herald, Canberra Times, Science News (USA), Cosmos Magazine (Australia), Discover Magazine (USA), The Science Show (ABC with Robyn Williams)

Postzygotic genetic incompatibilities between sympatric color morphs

Sarah R. Pryke & Simon C. Griffith

Published in: Evolution (2009) 63: 793-798

Genetically determined colour morphs, such as the different head-colour forms of the Gouldian finch, are believed to successfully interbreed. However, we have recently discovered that there are genetic incompatibilities between red and black colour morphs. Using a balanced within-female experimental design, where females were forced to breed with a male of both the same and different head-colour, we found that offspring produced from mixed-morphs (e.g. black-red) produced fewer surviving offspring than birds breeding with mates of their own head colour. In particular, daughters (the heterogametic sex) suffered much higher mortality than sons, which is actually what is predicted when two species, subspecies or races interbreed. These results suggest that the red and black morphs were probably geographically separated in the past, during which time they diverged, before coming back into contact again (i.e. now coexist together in wild populations).

The relative role of male vs. female mate choice in maintaining assortative pairing among discrete colour morphs

Sarah R. Pryke & Simon C. Griffith

Published in: Journal of Evolutionary Biology (2007) 20: 1512-1521

Mate choice is an important process because it influences the number and quality of offspring that an individual can produce (i.e. with a good or bad mate), and in polymorphic species, such as the Gouldian finch, it will also affect the genetics and head color of the resulting offspring. Using a specialized apparatus where birds have to choose among different mates, we found that both females and males are very choosy about who they prefer to mate with - and both prefer partners of the same head colour as themselves (e.g. reds prefer reds). Females also prefer to breed with males who have longer tails and more intensely UV-coloured blue head bands, which the males display to females during their courtship display by erecting the feathers to form a 'halo' around the head mask.

Frequency-dependent physiological trade-offs between competing colour morph

Sarah R. Pryke, Lee B. Astheimer, William A. Buttemer & Simon C. Griffith

Published in: Biology Letters (2007) 3: 494-497

Why are red-heads so aggressive? By placing birds into a range of different environments (some aggressive, some not), we found that red birds are not 'genetically dominant' but rather that they have a sensitive genetic disposition to different social environments. When birds were kept in complete isolation (i.e. single bird per cage), there were no physiological differences between red and black males. However, in socially competitive environments (i.e. when the number of aggressive reds increases), red birds responded aggressively, dramatically elevating their testosterone levels, while the non-aggressive black birds responded passively (reduced their testosterone levels). Although red birds get a huge dominance advantage, this higher aggression also carries large costs. In highly competitive situations, red birds suffer high stress and large health risks as they cannot maintain normal levels of immune function. Thus, red and black birds respond very differently to competitive environments. 

Some of the articles by the Media on this paper (see also Media Coverage): The Age, Macquarie News, 2SER Radio, A Question of Balance

Fiery red heads: female dominance among head color morphs in the Gouldian finch

Sarah R. Pryke

Published in: Behavioral Ecology (2007) 18: 621-627

Although dominance is typically considered the domain of males, dominance can also be very important for resolving conflicts between females, such as over access to limited food, mates and nest sites. By examining differences in dominance behaviours, red females were found to dominate both black and yellow females in competition for food. This effect of red dominance also persisted when the head colours of the different morphs were experimentally altered (by dying them different colors) - like males, females with red heads (whether natural or dyed) dominated the other birds. Thus, ultimately, red-heads rule.

Red dominates black: agonistic signaling among head morphs in the colour polymorphic Gouldian finch

Sarah R. Pryke & Simon C. Griffith

The Gouldian finch: a bird's eye view

Sarah R. Pryke

Published in: The Gouldian Finch (2005). Indruss Productions, Australia (editors: Stewart Evans & Mike Fidler)

The Gouldian finch is arguably one of the most brightly coloured birds. To most of us, it is an amazing and even gaudy kaleidoscope of different colours - violet, blue, green, yellow, orange, red, black and white. However, what we see and what another Gouldian finch sees is likely to be quite different. This is because birds have a far superior colour vision to humans - one the differences between us is the ability of birds to see in a fourth dimension, that of ultraviolet to which humans are completely blind. Although we can never fully 'see' what birds do, the large ultraviolet component of colours, such as the blue head band, is likely to appear much brighter and more vibrant to other finches. Therefore, although Gouldian finches look pretty bright to us, they no doubt look a whole lot brighter to each other.

Further details on this article can be found in The Gouldian Finch