Differential Allocation and Compensatory Investment of Resources to Offspring

The Scientist (Oct 1999)
Testosterone boost to favored offspring
Ricki Lewis

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."

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

Abstract
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

Abstract
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.

Science. 323(5921): 1605-7 (Mar 20, 2009)
Genetic incompatibility drives sex allocation and maternal investment in a polymorphic finch.
S. R. Pryke, S. C. Griffith

Abstract
Genetic compatibility may drive individual mate choice decisions because of predictable fitness effects associated with breeding with incompatible partners. In Gouldian finches (Erythrura gouldiae), females paired with genetically incompatible males of alternative color morphs overproduce sons, presumably to reduce investment in inviable daughters. We also observed a reduced overall investment in clutch size, egg size, and care to offspring resulting from incompatible matings. Within-female experimental pairings demonstrate that female birds have the ability to adaptively adjust the sex of their eggs and allocate resources on the basis of partner quality. Female Gouldian finches thus make cumulative strategic allocation decisions to minimize the costs of poor-quality pairings when faced with a genetically incompatible partner.

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

Abstract
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.