Testosterone in egg yolks: An ornithologist's perspective

The past decade has seen a number of exciting discoveries regarding the passage of nutrients (1) and scarce secondary compounds (2) to mates and/or offspring through copulation and oogenesis. Until now, most of these discoveries have been in studies of insects, and biologists studying vertebrates may have been left, for no good a priori reason, with the impression that their organisms are simpler in this regard. Mammals, with their considerable postfertilization transfer of nutrients and hormones from mother to fetus during gestation, represent a fundamentally different pattern than is present in most insects. From this perspective, the reproductive patterns of birds are really much more insect-like: the bulk of the embryo's development takes place after the formation of the shell and its membranes, which effectively seal the chick in a capsule open only to gas exchange to develop with the material resources its mother included during oogenesis. The report by Schwabl (3) in this issue of the Proceedings opens up a new chapter in our understanding of just what those maternal resources can include. Suddenly, the developing chick's inheritance can include not only genes and the long-appreciated fat, protein, water, and minerals that every fertile egg is known to contain but also hormones. The presence of hormones in variable concentration suggests many possibilities for future work. As an ornithologist with a decidedly nonendocrinological background, I will comment here on the fascinating possibilities that may lie ahead for a fusion of research in endocrinology and behavior, but all such comment is predicated on the completion of a good deal of supporting research verifying biological links that some will no doubt feel I too blithely assume. These biological links revolve around our rudimentary knowledge of the actual effects of testosterone (and other steroids) on the behavior of chicks all the way from hatching to adulthood. Much of what I will suggest assumes that variation in embryonic testosterone concentrations can lead to changes in aggressiveness and activity levels of chicks at hatching and that higher levels early on may transfer to higher levels of endogenously produced testosterone later in life. Schwabl cites one study (4) that indicates androgen action on the spinal chord during embryonic development in the chick as well as a study with similar results in mice (5), but there is clearly a great deal to be learned about how testosterone affects the development of chick behavior at all ages. Schwabl's results show that the behavioral dominance of canary fledglings is positively and significantly related to the yolk testosterone concentrations of the eggs from which they hatched. But we need to know considerably more about how these changes develop in the chicks, how laying order might affect dominance independently of testosterone concentrations, how endogenously produced testosterone vs. yolk testosterone affect development, and how changing sensitivity of target tissues translates differences in yolk testosterone concentrations to differences in chick (and adult) behavior. In much of what follows, I will also assume that females can actually control levels of testosterone in the eggs they lay. The differences that Schwabl reports between patterns of hormomes in the eggs of canaries and zebra finches, between different eggs laid by a given female canary, and between different females suggest considerable variation in this trait. But to establish parental control of yolk hormone levels, considerable work on the concentrations of hormones in the female's blood and the solubilities of the various hormones in yolk would have to be conducted to show that hormone concentrations in the eggs are not merely a direct reflection of circulating hormone levels in the female's blood stream at the time of yolk formation. Otherwise, females would not be able to change yolk hormone levels without also altering their own hormonal state, and the behavioral effects on the female are likely to serve as a strong selective deterrent to altering the levels of hormones in yolks. These considerable caveats aside, I will now venture out on some pretty long limbs in the hope that the-sweetness of the fruits that appear at their tips justifies the risk! Interactions between parent birds and their young have been of keen interest for almost 20 years. One aspect of this interaction was focused by Trivers (6) when he articulated the concept of parent-offspring contlict and explored its consequences for behavioral ecology. In brief, since parent and offspring bear on average only half of their genes in common by descent, then the genetic interests of parent and offspring can be expected to diverge, especially in cases where the needs of offspring diminish and/or costs to parents increase. Much of the early work on this subject was dominated by a debate (reviewed in ref. 7) over whether the offspring could ever be expected to prevail in these conflict situations. If, as Schwabl suggests, testosterone in the yolk can increase the vigor and competitive ability of nestlings, his findings would suggest a ta gible mechanism by which maternal control might be achieved. Many chicks will presumably benefit from having the elevated activity levels that result from higher testosterone concentrations, and conflict might then arise between parent and offspring over which chicks receive little or no testosterone. But it is easy to imagine that some embryos may not have sufficient reserves or sufficient inputs from their parents to sustain such elevated activity, and activity may rob resources from growth and maintenance and result in a net detriment to some chicks. In any event, if testosterone shows up in variable concentrations in the eggs of many wild species, and if chicks cannot counter variation in yolk testosterone by adjusting their endogenous production of the hormone or the sensitivity of their target tissues to it, there would be a strong indication that the mother has an effective means of gaining the upper hand in parent-offspring conflict. Other authors in the literature on parent-offspring conflict, most notably O'Connor (8), avoided the debate over who is in control and focused instead on the implications of the complicated web of relatedness and conflicts inherent not only between parent and offspring but al'so among the offspring within a brood as well. He predicted a spectrum of behaviors ranging from fratricide to infanticide and even suicide in response to d creasing food supply. Clearly, maternal manipulation of testosterone concentrations in eggs could either accentuate or ameliorate the conflicts of interest inherent in a brood of nestlings and its parents, and sampling testosterone concentrations of fresh eggs of known laying order in a variety of wild species should now be a high priority. Schwabl's findings also provide the blueprint for a valuable experi-