Not long ago red kites were facing extinction in the UK. Thanks to hard work and dedicated conservation efforts, the red kite population is now doing quite well. So well in fact, that a visit to Gigrin farm (a red kite feeding site) is nothing short of a wildlife bonanza! The skies of this valley in mid-Wales are filled by hundreds of these majestic birds every afternoon.
Although it is an absolute privilege to witness the aerobatic displays performed by the red kites, for me the real treat is observing the interactions between the birds. And it's not just the red kites that turn up for the free lunch. Rooks, crows and buzzards were all keen for an easy meal!
You can almost feel the tension in the air as the birds circle above Gigrin valley. After the food is delivered, there is a hesitation before the feeding begins - no one wants to be the first to take the dive and swoop down to take a snack. It seemed to be the role of the buzzards to set the pace - as soon as a bold buzzard touches down, an air raid of red kites rains down to snatch tasty morsels and devour them on the wing.
Much of our current understanding of testosterone comes from studies of species that inhabit the northern temperate region of the globe, perhaps unsurprisingly, because northern temperate species are readily accessible to universities in the developed world. From these studies there is a reasonable amount of evidence that testosterone plays an important role in the production of song by male songbirds. But there are very few studies of birds in other regions and this is important because the role of testosterone is not necessarily conserved across species in these different environments. So we need to study tropical and subtropical species too.
And so I set out to ask:
does circulating testosterone regulate male song production in white-browed sparrow weavers in the kalahari?
Throughout the breeding season, I got up at 3am to monitor male song production (they sing their solo songs almost exclusively at dawn) and I caught the birds late at night to collect a blood sample (when individual males can be readily caught from their sleeping chambers). It was hard and tiring work that meant I had to sleep in short (3-4hr) shifts at night and in the middle of the day (when temperatures were over 30 degrees C!). I then spent weeks analysing the samples in a collaborator's laboratory in order to measure testosterone concentration, and more weeks analysing song files.
And when all the data was in, the answer came back: NO.
There was no evidence that circulating testosterone concentrations were directly related to dominant male song production. or that males who sang more had higher testosterone than males that sang less.
Digging into the literature it quickly became clear that correlative evidence for a direct relationship between song production and circulating testosterone was not all that common. On the other hand, experimental manipulation of circulating testosterone did affect song production in many cases. So did our result mean that there is a latitudinal difference in the role of circulating testosterone for male song production? Or was there more to it? If the relationship between circulating testosterone concentration and song production is not strong and consistent across studies, then perhaps there is something more complicated going on under the hood?
And indeed, recent work indicates that this is very much the case. There are at least 3 important reasons why a direct relationship between circulating testosterone concentration and song production might not be necessary or could be obscured:
1. variation in receptor expression - the androgen receptors that circulating testosterone bind to can vary in number or density, which could account for the effectiveness of circulating testosterone concentration without variation in circulating testosterone levels
2. local conversion - aromatase coverts circulating testosterone into estradiol, which may then bind to estradiol receptors at target sites, therefore the concentration of estradiol may be more directly related to behaviour than that of circulating testosterone
3. local synthesis - testosterone and other steroids can also be synthesised locally at target tissue sites, which means that peripheral measurements don't necessarily tell us an awful lot about what is going on in the brain or at other specific sites.
So what does this all mean? Well it means that there is still a lot more work to be done! We need to better incorporate an understanding of the complexity of neuroendocrine mechanisms into evolutionary hypotheses about the role that testosterone may play in life-history trade-offs and animal communication systems. Often, working hypotheses are based on the assumption that there is a simple concentration-dependent effect of testosterone, which need not be the case.
More generally, we need to take the approach that hormones are more than mechanistic links in the translation of genotype to phenotype. Due to their pleiotropic effects on gene expression, hormones can structure genetic variances and covariances that determine how a population responds to selection. But hormonal mechanisms are more than simply the circulating hormone acting alone, so we need to characterise the other components too.
Further studies of songbirds outside the northern temperate zone are now essential in order that we can begin to understand whether endocrine systems are conserved or divergent across species, and why this is the case.
You can read more about this work and the associated literature here in the open access article.
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