In a paper published in Nature in 1982, Malte Andersson showed, experimentally, that female long-tailed widowbirds choose mates based on the lengths of their tails. Andersson’s study was, arguably, the first experimental support for Darwin’s Sexual Selection theory. Thirty-four years after the paper was published, I spoke to Malte Andersson about the making of this study and what we have learnt since about mate choice in widowbirds.
(Questions sent by email on 7 July 2016; responses received on 17 September 2016)
Citation: Andersson, M. (1982). Female choice selects for extreme tail length in a widowbird. Nature 299: 818-820.
Hari Sridhar: What was your motivation for doing this study ? How and when did you first come to know about long-tailed widowbirds?
Malte Andersson: My interest in sexual selection and signaling was seeded around 1970, during my doctoral studies of behaviour and ecology of long-tailed skuas in Lapland, Northern Sweden. The long-tailed skua is a relative of auks and gulls, and turns rodent predator in the far North during the breeding season. Inspired by the comparative ethological studies of gulls by Niko Tinbergen’s group, my aim was to study skua behaviour and its adaptations to an ecological lifestyle very different from that of its phylogenetic relatives. I was aware that both sexes in skuas have a pair of elongated central tail feathers that differ markedly in shape and length among the four Northern hemisphere species. In the field, I found that both sexes raise and expose the tail conspicuously during courtship, and I wondered about its function. Perhaps the elongated feathers are important for species recognition in pair formation? But at their breeding grounds, the species are easy to tell apart for a human observer, based on size, calls, coloration and other aspects. So why should the birds need different tail shapes for that purpose? Species recognition did not seem an entirely plausible hypothesis. On the other hand, catching the same individuals over several years, I found that the central tail feathers became longer and therefore reflected age and perhaps also survivorship. I wondered if that might somehow be relevant.
About a decade earlier, Peter O’Donald, Ronald Fisher’s last doctoral student, had studied sexual selection of color morphs in Arctic skuas. Reading his pioneering papers made me aware of Darwin’s and Fisher’s theory of sexual selection by female choice. I also read widely outside the curriculum, visiting our university library each weak, skimming journals in behavior, ecology and evolution for interesting new studies. I was also influenced by books on evolution, selection and adaptation by George Williams, John Maynard Smith and John Merritt Emlen, which strengthened my interest in evolution. After my dissertation, these research fields, in particular sexual selection, full of interesting theory and unsolved problems, were on my mind. During a visit to East Africa in 1975, I saw long-tailed and Jackson’s widowbirds on their savanna breeding grounds in the Kenyan highlands. Why were male long-tailed widowbirds, with their black plumage, red wing epaulet and, especially, a half meter long unwieldy tail, so different from the females, which resembled dull females of other weaverbirds (Ploceidae)?
HS: This is the first test of Darwin's hypothesis about male sexual ornaments. Why do you think it took so long for it to be experimentally tested?
MA: Most biologists for a long period were skeptical about Darwin’s ideas on mate choice, and many remained skeptical even after the ‘evolutionary synthesis’ in the mid 1900’s (e.g. Huxley, Lack). And, in spite of early pioneering work by Niko Tinbergen, experimental tests of behavior in the wild gained momentum only in the 1970’s and 80’s. Then, new results made it increasingly clear that field experiments in the natural environment could often provide decisive results and distinguish between hypotheses in behavioral and evolutionary ecology, clarifying the function and adaptive significance of a trait. Controlled field experiments thereafter became more common.
HS: During this study, what was a typical day in field like?
MA: Usually going to the field site a while after sunrise, when widowbird males returned to their grassland territories from the night roost. We caught territorial males with a clap-net trap. Before and after catching and manipulating a male, I measured his display activity. After the sun dried out the morning dew from the tall grass, I searched for nests of females breeding in the territory, doing so once a week until the end of the breeding season.
HS: You started the fieldwork for this study in November 1981. In the same month, a conceptual paper on sexual selection you wrote was accepted in the Biological Journal of the Linnean Society. Did this paper, in some way, motivate your study on widowbirds?
MA: Yes, in a general way, as work on theoretical aspects of sexual selection made me read and think about debated issues of female choice and male ornaments. Fisherian runaway selection was one possibility, and it also seemed likely to me that ornaments could indicate phenotypic and genetic fitness, through resource allocation, as portrayed in a figure in the paper you mention. I thought that, in spite of lingering skepsis among many researchers, female choice based on male ornaments was plausible, encouraging me to attempt an experimental test.
HS: Did you do all the fieldwork on your own or did you have help in field?
MA: In catching the birds and during the experimental manipulations, a field assistant, first Uno Unger, then Kuria Mwaniki, helped me. He held the male in a suitable position, while I cut and glued the tail feathers. This way there was no need for anesthetics, and the bird could be released immediately after being manipulated and ringed.
HS: How difficult was it to find the nests?
MA: It was more time-consuming than difficult. Females build their rather large-domed grass nest in the upper third of 0.5 – 0.8 m tall grass in the male’s territory. Females usually flew from the nest when I was several meters away. By systematically searching the grass areas of the territory in parallel walks about 2 m apart, I located the nests, and I repeated the search each week until the end of the breeding season, when no new nests were started.
HS: Walk us through how you came up with the idea of modifying the tail lengths of these birds? Was it tricky to cut and paste the tail feathers back? Did you use a particular brand of glue for this?
MA: Controlled field experiments was an approach I had used in several earlier studies during work with skuas and lemmings in Lapland. And I was aware of the nice experimental tests of the function of red wing epaulets in red-winged blackbirds in USA. So, experimental testing of a conspicuous male ornament, potentially involved in female choice, was not a far-fetched approach. In fact, I had been thinking about this possibility for a long time, but then with the epitome of male ornaments in mind: the train of the peacock. I explored possibilities for doing such a field experiment during a visit to Sri Lanka in 1979, but found that such a study of peacocks in the wild would be difficult for several reasons. The lek sites I found in a national park were in jungle with plenty of elephants and wild buffalo around; not an ideal situation. In addition, manipulating trains of unwilling peacocks in the wild seemed to present some problems of its own. That made me think again about the African widowbirds, which appeared more manageable.
When I planned the experiments, rapidly hardening cyanoacrylate superglue was coming on the market. The brand I used was called “Hot Stuff”, from Satellite City Instant Glues. Testing with feathers from other birds, I found that the glue hardened quickly enough, in just a few seconds, to be suitable for use in the field for tail elongation. I practiced and improved my skill at feather manipulation at the lab before going to Kenya for the study. During manipulations in the field, the assistant sat in front of me holding the bird, while I cut, trimmed and glued the tail feathers.
HS: Fig. 1 in this paper is one of the nicest figures I have seen in a scientific paper. Whose idea was it to include the widowbird illustrations perched on the bars in the graph? How was this figure made at that time?
MA: I thought carefully about how to include, without overloading the figure, as much information as possible. For instance the number of nests for each individual male at the bottom of the bars. The idea of having perched widowbirds with relevant tail lengths on the bars came rather naturally, because this was the way I often saw males in the field. There were many cattle fences in the area, and fence poles were the favorite perch sites for territorial males. I made the first version of the figure, which was then redrawn in ink by a departmental lab assistant, Aino Falk Wahlström, skilled at illustration work.
HS: One of the unique aspects of your study is the elegant “double control” you used for the experiments. Was this the first time such a design was being used?
MA: I am not aware of any previous study with such a design, but it may well have been used before. I first planned to use only the color-ringed birds as control, but became worried that the cut-and-glue operation might have an important effect, so added a control for that.
HS: Your paper presents a lot of natural history information on the widowbird. Was this already known or did it come from your own observations?
MA: Some of it was known from earlier studies of the South and the East African subspecies (e.g. Craig 1980). Other aspects I learned during fieldwork.
HS: Today, do we know more about aspects of this bird's ecology which weren't well-known then, e.g. nest-site choice by females, role of tail length in competition, and territory ownership?
MA: There has apparently not been much more fieldwork on this species, but several other widowbirds have been studied extensively by observations, experiments and comparative phylogenetic analyses, in particular by my former PhD student Staffan Andersson (no relative!) and his research group.
HS: Today, do we know more about why females choose long-tailed males in this species?
MA: Our knowledge about mate choice in other widowbirds, and of course more generally, has increased vastly in the 34 years since the study was published, but there have been no further studies of mate choice in this species. The reason may be that a number of other widowbirds, whydas and other species also have long tails. Researchers have apparently preferred to study some of these other species rather than the one I already studied. Focusing on another species permits both another independent test of tail function, and can show if ornamental long tail plays a role in female choice more generally among birds. A number of studies of different species have found that it does.
HS: Your work was entirely experimental. Have there been studies looking at whether your findings hold true with respect to natural variation in males?
MA: Not in this species, but in many other birds, studies based on natural variation have found that male mating success correlates with ornament size.
HS: Did this paper create a buzz - within academia and outside - when it was published?
MA: Yes, it raised much interest among biologists, demonstrating sexual selection by mate choice of a conspicuous ornament, of the kind that long puzzled Darwin, until he arrived at the essentially correct explanation. It also raised interest in general news media, some of which reported that now it has been proved: the length matters.
HS: How important has this paper been in your career? Has it had a major influence on the course of your future research?
MA: It had a major influence. Sexual selection is a field full of both fascinating natural history and interesting debated theory. Partly as a consequence of the simultaneous publication of the widowbird study and my theoretical paper in Biological Journal of the Linnean Society, I was invited by editors at Princeton University Press to write a monograph about sexual selection. Not anticipating the eruption of coming studies I gladly accepted. That decision kept me busy for a number of years. When the first version of the book manuscript was finished, it was necessary to revise almost every chapter, because so many new important results had been presented in the meantime. And the same procedure had to be repeated again also when the revision was finished, until I could finally deliver a manuscript that was reasonably up to date with the latest findings. Writing the book greatly reduced my available time for widowbird work and other research. Fortunately Staffan Andersson, after presenting his thesis on Jackson’s widowbird, could continue comparative and experimental studies of sexual selection of coloration and other ornamental traits in widowbirds and bishops, which remains a successful ongoing project. After gaining more time for own research when the book was finished, I have worked for instance on various aspects of breeding systems.
HS: Have you ever gone back and read this paper after it was published? What aspects about it strike you now? What memories does it bring back?
MA: Yes, I have read the paper in preparing some talks and lectures. A nice aspect is its brevity. The experimental design, planned after a pilot visit to the study site a year before the experiment, made the outcome rather clear and easy to write about, resulting in a short informative paper. Reading it now recalls exciting fieldwork in a beautiful rural part of the Kenya highlands, with cool nights and hot sunny days, helpful and friendly Kikuyu farmers, and the Nyandarua Mountains as a magnificent backdrop under a clear sky. (There were thunderstorms and torrent rains too, but they seem to have thinned out in my memory.)
HS: If you compare this paper to papers you write today, do you find any striking differences, e.g. in writing style?
MA: Not that I am aware of. I try, but of course fail, to write as simply and briefly as possible, without sacrificing clarity and readability. A researcher that in my opinion wrote lucidly about quantitative evolutionary problems was John Maynard Smith. Authors with such writing style were for instance George Orwell and Kurt Vonnegut.
HS: Have you had the opportunity to go back to your study site after the paper was published? Has the site changed a lot since the time you worked there, in 1981-82?
MA: I have not been back since the mid-1980s, but even then, some of the breeding habitat of long-tailed widowbirds was disappearing, being turned into arable fields or plots for growing vegetables, and the nesting grass (Eleusinae) was being cut for thatching of roofs.
HS: This paper has been cited 793 times (Google scholar) as of today. Did you anticipate that it would generate so much interest? Do you know what your paper has mostly been cited for?
MA: I had no idea it would raise so much interest. It has probably been cited mostly because it experimentally demonstrated female choice based on a conspicuous male ornament in the wild.
HS: What would you tell a student who is about to read this paper today? Any caveats? What should he or she take-away from it?
MA: I spent much time thinking about the experimental design, and exploring the possibility for such a study by a pilot visit to the field site. So the importance of careful planning is probably a useful takeaway. Viewed today, there are many caveats. For instance, there is no paternity determination, as DNA methods were not then available. And the adaptive reasons for female choice of males with long tail could not be studied in this brief experiment. But the successful experimental demonstration of female choice in the wild may have helped encourage subsequent better studies.
HS: Among all the papers you have written, is this your favourite?
MA: Yes, I believe it is my best paper because it is short and informative, reporting a fairly clear outcome of a controlled, interesting experiment. It demonstrated, in the wild, female choice of mate based on a conspicuous ornament, one of Darwin’s most controversial ideas. Another often cited sexual selection paper is a model (Evolution 40:804-816) showing that a genetic indicator process of mate choice can work, taking to higher frequencies a female preference and a preferred male ornament that reflects genetic viability. This, together with similar results from other researchers, may have helped generate more interest and more sophisticated modeling and empirical testing of such processes in sexual selection.