Surprising Heredity in Birds

Proc. Biol. Sci. 279(1728): 523-528 (Feb 7, 2012)
Male attractiveness regulates daughter fecundity non-genetically via maternal investment
Lucy Gilbert, Kathryn A. Williamson, and Jefferson A. Graves

Mothers can non-genetically influence offspring phenotype in response to environmental conditions, including mate attractiveness. If such 'maternal effects' influence the offspring's reproduction and F2 generation, there is a mechanism for non-genetic trans-generational effects on phenotype, including epigenetic phenomena, with implications for evolution and population dynamics. We demonstrate in the zebra finch Taeniopygia guttata such non-genetic effects on offspring fecundity and the size of early stage F2 (eggs) in response to experimentally manipulated father's attractiveness. Our experimental design allowed us to deduce that the mechanism for this non-genetic paternal effect was via maternal investment in eggs. This affected female offspring size and, consequently, fecundity and F2 (egg) size. This demonstrates that female perception of mate attractiveness can have non-genetic, trans-generational fitness consequences and this may have important implications for the evolution of sexually selected traits and population dynamics.

Hormones and Behavior 59: 306-314 (2011)
Epigenetics and the origins of paternal effects
James P. Curley, Rahia Mashoodh, Frances A. Champagne

For example, when mated with males sporting red leg bands (i.e. artificially made more attractive), female zebra finches laid heavier eggs, had offspring that spent more time begging, and had faster growth rates than offspring of females who were paired randomly with males sporting green leg bands (i.e. artificially made unattractive) (Gilbert et al., 2006). In contrast, another study reported increased egg volumes and elevated yolk carotenoids and testosterone levels when female zebra finches were paired with less attractive males (Bolund et al., 2009). Likewise, young female mallards increased their egg volume when mated with highly attractive males (Cunningham and Russell, 2000), but older females increase their egg volume when mated with less attractive males (Bluhm and Gowaty, 2004). The decision to withhold resources or increase maternal investment may involve an interaction between mate quality and the reproductive life-history of the female, the availability of attractive males within a population, or the degree of reproductive skew (Harris and Uller, 2009). It has also been argued that reproductive compensation is more likely to occur in situations where females are not allowed to make a free choice with whom to mate (Gowaty et al., 2007; Harris and Uller, 2009; Sheldon, 2000).

Proc. Biol. Sci. 276, 707-715. (2009)
Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males
E. Bolund, H. Schielzeth, W. Forstmeier

The classical version of the differential allocation hypothesis states that, when females reproduce over their lifetime with partners that differ in their genetic quality, they should invest more in reproduction with high-quality males. However, in species with lifetime monogamy, such as the zebra finch, partner quality will typically remain the same. In this case, the compensatory investment (CI) hypothesis predicts higher investment for low-quality males, because low genetic quality offspring are more dependent on maternal resources. Here, we show that female zebra finches invested more resources, both in terms of egg volume and yolk carotenoid content, when paired to a low genetic quality male, as judged from his previous ability to obtain extra-pair paternity in aviary colonies. We also found that females deposited slightly larger amounts of testosterone into eggs when paired to a low parental quality male, as judging from his previous success in rearing offspring. This is, to our knowledge, the first experimental support for the CI hypothesis in a species with lifetime monogamy. We stress that in more promiscuous species, the benefits of classical differential allocation may partly be neutralized by the supposed benefits of CI.

Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 1039-1048. (2009)
Reproductive investment when mate quality varies: differential allocation versus reproductive compensation
W. E. Harris, T. Uller

Reproductive investment decisions form an integral part of life-history biology. Selection frequently favours plasticity in investment that can generate maternal effects on offspring development. For example, if females differentially allocate resources based on mate attractiveness or quality, this can create a non-genetic link between mate attractiveness and offspring fitness with potential consequences for ecological and evolutionary dynamics. It is therefore important to understand under what conditions differential investment into offspring in relation to male quality is expected to occur and the direction of the effect. Two opposite predictions, increased investment into offspring produced with high-quality mates (differential allocation (DA)) and increased investment with low-quality males (reproductive compensation (RC)) have been suggested but no formal theoretical treatment justifying the assumptions underlying these two hypotheses has been conducted to date. Here, we used a state-based approach to investigate the circumstances under which the variation in mate quality results in differential female investment into offspring and how this interacts with female energetic resource levels. We found that a pattern of increased investment when mating with high-quality mates (i.e. DA) was the most common optimal investment strategy for females in our model. By contrast, increased investment when mating with low-quality mates (i.e. RC) was predicted only when the relative impact of parental investment on offspring quality was low. Finally, we found that the specific pattern of investment in relation to male quality depends on female energetic state, the likelihood for future mating opportunities and the expected future distribution of mate quality. Thus, the female's age and body condition should be important factors mediating DA and RC, which may help to explain the equivocal results of empirical studies.

The Scientist (Oct 1999)
Testosterone Boost to Favored Offspring

Offspring of highly ornamental males tend to beat their siblings in the survival stakes—in birds at least. Experiments reveal a new twist to the old idea that these offspring either are blessed with better genes or receive a disproportionate share of maternal care—females secrete more testosterone into yolks after mating with the avian version of sexy males (D. Gil et al, "Male attractiveness and differential testosterone investment in zebra finch eggs," Science, 286:126-8, Oct. 1, 1999.). Female zebra finches were mated to males with either red bands or green bands on their legs. Apparently the ladies went for the red. "Each female had two clutches with a different male in each of them, and we compared the difference between clutches for the same females," notes Diego Gil, a University of Paris postdoc. Chicks of red-banded males enjoyed the benefits of high testosterone, but not the chicks of green-banded males. And testosterone level can make a big difference in young birds' lives, providing strength and stamina that enable them to outcompete less manly nestmates. How the female controls testosterone production and secretion remains unknown. "My hunch is that she is responding to a higher degree of stimulation by the male, but options are open," speculates Gil. "It could also be that males are manipulating females by their behavior."—Ricki Lewis

New Scientist p. 20 (16 Apr 1987)
Finches wear their hearts on their legs

IN 1982, Nancy Burley, of the University of Illinois at Urbana-Champaign, upset many students of animal behaviour. She showed that the mating preferences of zebra finches (Poephila guttata) were altered by the coloured bands scientists commonly put on birds' legs to identify them. Females found males wearing orange leg bands much more attractive than those wearing no bands or other colours. The result was greeted with scepticism because it seemed so unnatural, but in a recent paper Burley has confirmed the original finding. Furthermore, she has gone on to show that the discovery may indeed have some relevance to the natural life of the zebra finch (Animal Behaviour, vol 34, p 1732).

Burley noted that the colours the zebra finches liked were those found on other zebra finches, while the ones they avoided were not part of the normal zebra finch colour scheme. Perhaps the attractive colours were so precisely because they enhanced the signals normally given out by prospective mating partners. To test this she repeated the study using the zebra finch's closest relative, the double-bar finch (P. bichenovii).

Both species are members of the Australian finch family the Estrildidae, but there are also important differences between them. For a start, they look quite different and zebra finches are sexually dimorphic, the males being much more colourful and with a redder beak than the females. Their legs are orange. Double-bar finches are not as colourful as male zebra finches, and both sexes look the same, with two chocolate-coloured bands across the chest. The beak and legs are bluish‑grey.

Burley gave males and females of each species a choice between three different target birds. The three birds wore either red bands, or blue bands, or no bands. The results were quite clear. Female double-bar finches preferred males adorned with a blue band over those with no band. They seemed to avoid males wearing a red band. Zebra finches made exactly the opposite choices; they preferred red-banded males over plain males, and plain males over ones with a blue band. Males produced similar results; double-bar males preferred blue-banded females over the others, while zebra finch males preferred females wearing red bands.

The results are consistent with Burley's hypothesis that finches prefer to mate with individuals that display exaggerated identity badges, blue for double-bars and red for zebra finches, but several questions remain. How does the preference originate? Is it learnt, in some sort of imprinting, or is it genetically determined?

Burley thinks that an even more interesting question is "how and why the beak colours and plumage patterns of these closely related species came to differ so". Among the Australian finches behaviour, such as courtship songs and dances, differs far less than plumage. Burley thinks that this may be the result of different plumage preferences being favoured, quite by accident, in isolated populations. These preferences would then be the foundation on which new species could evolve.