Yolk androgen deposition as a female tactic to manipulate paternal contribution

The differential allocation hypothesis (DAH) predicts that females should invest more in reproduction when mated with an attractive male (Burley 1988; Sheldon 2000); and, according to this hypothesis, females mated with attractive males frequently invest more resources in eggs (Cunningham and Russell 2000; Saino et al. 2002; Rutstein et al. 2004). In zebra finches (Taeniopygia guttata) and barn swallows (Hirundo rustica), females deposit more androgens (testosterone, 5adihydrotestosterone, androstenedione) in eggs when mated with attractive males (Gil et al. 1999; Gil, Ninni, et al. 2006). Similarly, canary (Serinus canaria) females deposit more androgens when exposed to attractive male songs (Gil et al. 2004). Because some studies have shown that yolk androgens improve nestling growth and survival (Schwabl 1993; Eising et al. 2001; Pilz et al. 2004), it has been suggested that this pattern is consistent with the DAH. However, other studies have shown that yolk androgens may have detrimental effects on nestling growth and survival, especially reducing the immune capacity (Sockman and Schwabl 2000; Gil 2003; Groothuis, Eising, et al. 2005; Müller, Groothuis, Kasprzik, et al. 2005). Therefore, it is unclear whether this pattern is consistent with the DAH. On the other hand, recent studies (Michl et al. 2005; Navara et al. 2006a) have shown that females of other species (collared flycatcher, Ficedula albicollis, and house finches, Carpodacus mexicanus) deposit more androgens when mated with unattractive males, thereby contradicting the DAH. These studies suggested that yolk androgen deposition may act as a compensatory strategy (the compensatory strategy hypothesis, CSH) employed by females mated with males of low parental quality. The CSH might also explain results found in the barn swallow (Gil, Ninni, et al. 2006) and the zebra finch (von Engelhardt et al. 2006), as in these species attractive males invest less in parental care. However, yolk androgens may be detrimental for nestlings in some situations (Sockman and Schwabl 2000; Groothuis, Eising, et al. 2005; Müller, Groothuis, Kasprzik, et al. 2005), and thus, this hypothesis hardly explains such behavior, as yolk androgens do not always compensate for low parental care. It has also been proposed that yolk androgen deposition may act as a female mechanism to manipulate paternal contribution (here, the manipulating androgens hypothesis, MAH) (Michl et al. 2005; also Gil, Ninni, et al. 2006; von Engehardt et al. 2006). Yolk androgens increase nestling begging behavior in some species (Schwabl 1996; Eising and Groothuis 2003; von Engelhardt et al. 2006), and begging may increase male contribution to the feeding rate more than the female contribution (Ottosson et al. 1997). Therefore, it may be feasible that, by increasing androgen deposition, females manipulate male contribution throughout nestling begging. The premises for this hypothesis are as follows: 1. Female birds may strategically vary the quantity of androgens that they deposit in egg yolk. Empirical evidence suggests that this is probable. In an experiment with the lesser black-backed gull (Larus fuscus), food-supplemented females had more androgens in plasma, but deposited less androgens in eggs, than control females (Verboven et al. 2003). Similarly, plasma androgens in the mothers were unrelated with yolk androgens in the house sparrow (Passer domesticus) and the eastern bluebird (Sialia sialis) (Mazuc, Bonneaud, et al. 2003; Navara et al. 2006). These findings strongly suggest that androgen deposition is not simply the result of a passive transmission from female plasma. 2. Yolk androgens increase the begging behavior of nestlings. Empirical studies suggest that yolk androgens favor begging in canaries, black-headedgulls (Larus ridibundus), and female zebra finches (Schwabl 1996; Eising and Groothuis 2003; von Engelhardt et al. 2006). However, starling (Sturnus vulgaris), yellow-legged gull (Larus michahellis), and male zebra finch chicks from eggs supplemented with testosterone do not beg more fiercely (Pilz et al. 2004; Boncoraglio et al. 2006; von Engelhardt et al. 2006). Therefore, the effect of yolk androgens on nestling begging cannot be generalized, but the MAH is possible only in species where yolk androgens affect begging. 3. Females cannot maximize the androgen deposition because their production is costly for female or yolk androgens are costly for nestlings. Although evidence for production costs are unclear (Gilbert et al. 2005; Gil, Marzal, et al. 2006), there is clear support for the contention that androgens imply a trade-off between growth and immune capacity in nestlings and excessive yolk androgens may be detrimental for nestlings (Sockman and Schwabl 2000; Groothuis, Eising, et al. 2005; Müller, Groothuis, Kasprzik, et al. 2005; Navara et al. 2005). Some studies have shown negative effects of yolk androgens on male chicks only (Müller, Groothuis, Eising, and Dijkstra. 2005; Saino et al. 2006). Other costs are also possible (Gil 2003). 4. Male parents aremore responsive to the begging behavior of nestlings than are female parents. The parental feeding rate is determined, in part, by the begging behavior of the brood (Kilner and Johnstone 1997). Inmany bird species, males contribute less than females to the feeding rate (e.g., Moreno-Rueda 2004); therefore, males have a broader scope to respond to the brood begging by increasing their feeding rate than females have. For the hypothesis be feasible, males should respond more strongly than females to the chick begging. This result has been shown, for example, in the superb fairy-wren (Malurus cyaneus) and the pied flycatcher (Ficedula hypoleuca), where males, but not females, increased feeding rate when exposed to playbacks of begging (Ottosson et al. 1997; MacGregor and Cockburn 2002). Similarly, in the great tit (Parus major), males, but not females, increased the feeding rate in response to an elevated nestling begging provoked by ectoparasites (Christe et al. 1996). Yolk androgens appear to modulate the relative allocation of resources delivered to the immune system and to the growth of nestlings (Navara et al. 2006b). On these premises, Behavioral Ecology doi:10.1093/beheco/arl106 Advance Access publication 17 January 2007