Michael Brooke reappraises Julian Huxley's pioneering classic of animal behaviour on its centenary.
As a scion of the family that produced 'Darwin's Bulldog' Thomas Henry Huxley, novelist Aldous Huxley and Nobel-prizewinning biologist Andrew Huxley, Julian Huxley (1887–1975) seemed destined to shine. He did, notably as an architect of the mid-twentieth-century evolutionary synthesis that merged Darwin's ideas on natural selection with population genetics. Decades before that, however, he helped to pioneer the field of animal behaviour with his groundbreaking work on avian ethology, the 1914 Courtship Habits of the Great Crested Grebe. In it, he demonstrated how detailed observations of individual birds can prompt profound biological questions, and sometimes reveal the outline of the answers.
Huxley was keenly interested in ornithology from his youth. In 1911, while away from lecturing duties at the University of Oxford, UK, he began observing the courtship of the redshank Tringa totanus in Cardigan Bay, Wales. He found that although female redshanks did not actively select a mate from among competing males, they had the power to accept or reject each suitor — supporting part of Darwin's theory of sexual selection. The following April, Huxley and his brother Trevenen spent two weeks watching the courtship of great crested grebes (Podiceps cristatus). They did so at a reservoir near the Hertfordshire town of Tring, now renowned as home to the matchless bird collections of the Natural History Museum. The result was a paper published in the Proceedings of the Zoological Society of London in 1914 and later, in slightly abbreviated form, as a pocket-sized book.
By the month of the brothers' observations, the grebes had already paired. Nevertheless, male and female, whose plumages are virtually identical, engaged in striking behaviours such as the “cat attitude” and the “penguin dance”, as Huxley colourfully labelled them. These he interpreted as necessary to bring the two birds into what he perceived as the emotional synchrony needed for coition, nest-building and egg-laying. To achieve this, some behaviours have undergone a gradual change from useful action to symbol to ritual.
It was Huxley's landmark paper that identified this process of ritualization in animal behaviour (he organized a Royal Society symposium to discuss it in 1965). Huxley also realized that ritualization extended to mammals, including people. With a sprinkling of references to Dante, Plato and Shakespeare's Romeo and Juliet, he digresses to muse on how human courtship so often and so predictably proceeds from hand-holding to kissing to more. More formally, he realized that behaviours may be shaped by evolution.
Darwin conceived sexual selection as having two principal components. The first, which still prevails, was that males would compete among themselves for access to females — leading, for example, to the huge size of belligerent bull elephant seals striving to monopolize a stretch of breeding beach. Second, he thought that ornamentation in one sex, most often the male, might be favoured by a mating preference of the other sex.
Huxley found this concept more difficult because of the similar breeding plumage in both sexes of great crested grebe, and because courtship continues well after the birds have paired off. Huxley's difficulties barely surface in the book, although he does presage the idea of runaway sexual selection, in which female preference for a male trait leads to ever more extravagant male traits. This latter idea was subsequently developed by Ronald Fisher in The Genetical Theory of Natural Selection (1930). But in 1938, Huxley published a paper in The American Naturalist that effectively poured cold water on any enthusiasm for female choice, and even more for mutual choice.
There matters largely rested until the early 1980s, when Malte Andersson showed that female choice did select for extreme male tail length in the African widowbird (Euplectes progne). Ten years later, Ian Jones and Fiona Hunter studied the crested auklet (Aethia cristatella), a monogamous seabird in which both sexes are ornamented. The parallels with the great crested grebe are obvious. Jones and Hunter showed that both males and females responded to accentuated models of the opposite sex with more frequent displays — confirming that ornaments in both sexes could be favoured by mutual mating preferences. Although beyond the scope of that study, it also seemed possible that ornament size influenced the likelihood of re-pairing the following year. That would have further undermined Huxley's reluctance to concede a role for sexual selection in any display after birds have paired for the season.
In 1946, Huxley became the first director of the fledgling United Nations Educational, Scientific and Cultural Organization (UNESCO), and he was instrumental in the 1961 founding of the World Wildlife Fund, now known as WWF. In the field of evolution, his overwhelming influence may have put a brake on the study of sexual selection, and his grebe-courtship observations have largely been superseded by those of zoologist Ken Simmons. But nobody has put two weeks' birdwatching in the spring sunshine beside an English reservoir to greater heuristic effect.
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Brooke, M. In retrospect: The Courtship Habits of the Great Crested Grebe. Nature 513, 484–485 (2014). https://doi.org/10.1038/513484a
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