Dancing Cockatoos and the Dead Man Test by Marlene Zuk
Dancing Cockatoos and the Dead Man Test by Marlene Zuk
A scientist's duty is incomplete until she writes about her work, first for the specialists in her field, then for the larger scientific community, and finally for the larger public. And the final step will inevitably include research beyond her own laboratory. Few scientists complete all three tasks; worse, many feel they are unnecessary. In recent times, I am delighted to see some outstanding exceptions. Recently, I had the great pleasure of reading two remarkable books (in the form of pre-publication manuscripts):
The Social Lives of Birds by Joan Strassmann, a wasp and slime mold researcher and
The Origin of Language: How We Learned to Speak and Why by the Honey Bee researcher Madeleine Beekman.
And now I just read Dancing Cockatoos and the Dead Man Test: How Behavior Evolves and Why It Matters by Marlene Zuk, an expert on chirping crickets.
Marlene Zuk is now a Professor of Ecology, Evolution, and Behavior at the University of Minnesota. I first met Marlene in the early 1980s when she shot to fame very early in her career with the publication of a paper in Science co-authored with WD Hamilton. In Heritable True Fitness and Bright Birds: A Role for Parasites?, they proposed a novel idea that has since come to be known as the Hamilton-Zuk Hypothesis (1).
As is now well-known, Charles Darwin proposed the theory of sexual selection, distinct from natural selection, in 1872 (2). Darwin proposed that sexual selection can work by two mechanisms: male-male competition and female choice. The male-male competition idea was easy to accept, and people could see how the winning male would get preferential access to the desired female. Darwin's proposal of female choice as another mechanism of sexual selection, however, ran into much trouble. For one thing, people were probably unwilling to give females sufficient agency to make this critical choice! It was also unclear how the females would choose and what they would look for in potential mates. Of course, females should choose males with good genes, but how would they detect the good genes hidden in them?
Hamilton and Zuk proposed that females should prefer males who are resistant to parasites, and they could make a good enough guess by looking at how brightly coloured the males were. But, "How could animals choose resistant mates?" they wondered. In one memorable passage, they argued that:
"The methods used should have much in common with those of a physician checking eligibility for life insurance. Following this metaphor, the choosing animal should unclothe the subject, weigh, listen, observe vital capacity, and take blood, urine, and fecal samples. General good health and freedom from parasites are often strikingly indicated in plumage and fur, particularly when these are bright rather than dull or cryptic. The incidence of bare patches of skin, which may expose the color of the blood in otherwise furry or feathered animals, and the number of courtship displays involving examination of male urine, are of interest in this regard. Vigor is also conveyed by success in fights and by the frequently exhausting athletic performances of many displaying animals".
What I like most about the Hamilton-Zuk hypothesis is that it makes two diametrically opposite predictions. It predicts that within a species parasite resistant individuals should be more brightly coloured and display healthy plumage compared to their susceptible counterparts. However, it also predicts that between species, those experiencing more parasite loads should be brightly coloured compared to species that have fewer problems with parasites. The logic here is that in species where parasites are a problem, it should be more important for males to display their health and vigor despite the prevalence of parasites in the environment, an argument reminiscent of Zahavi's Handicap Principle (3).
Hamilton and Zuk state clearly that:
"Our hypothesis is contradicted if within a species preferred mates have most parasites; it is supported if among species those with most evident sexual selection are most subject to attack by debilitating parasites".
In their 1982 paper, Hamilton and Zuk report support for the second prediction. They found that:
"Combination of seven surveys of blood parasites in North American passerines reveals weak, highly significant association over species between incidence of chronic blood infections (five genera of protozoa and one nematode) and striking display (three characters: male "brightness," female "brightness," and male song)".
Marlene Zuk has gone on to make fundamental discoveries. Continuing her interest in parasites and sexual selection, she found a remarkable way to dissect the tradeoff between natural and sexual selection. She studies crickets that sing to attract mates (positive sexual selection), but by doing so, they attract a parasite (negative natural selection). Her most vivid demonstration of the tradeoff became possible when she and her group found that in one of the Hawaiian-Islands where they study these crickets, a mutation had appeared that altered the male wings (flatwing mutant) so that it was impossible for them to stridulate (sing). This mutant spread rapidly to make up 90% of the population in a mere 20 generations. The silent crickets attracted no parasites and were favoured by natural selection. And they continue to find mates by becoming more sensitive to the songs of the few remaining singing males and mating with females who approach them (4). More recently, another variant male has evolved, which produces a different 'purring' song to attract females (5), but the parasite appears to be catching up (6). The saga goes on, but what is special is that we are witnessing evolution in real-time. The pioneering studies begun by Marlene Zuk continue to inspire many researchers to track the relative roles of natural and sexual selection in the evolution of hosts and parasites.
Marlene Zuk has contributed more than her share of writing for the larger scientific community and the general public without letting any tradeoff reduce her publications for the specialists. Her books include:
Sexual Selections: What We Can and Can't Learn About Sex from Animals (2002),
Riddled With Life: Friendly Worms, Ladybug Sex, and the Parasite That Makes Us Who We Are (2007),
Sex on Six Legs: Lessons on Life, Love, and Language from the Insect World (2011),
Paleofantasy: What Evolution Really Tells Us about Sex, Diet and How We Live (2013),
Sexual Selection: A Very Short Introduction (2018) [with Leigh W. Sommons]
and
Dancing Cockatoos and the Dead Man Test (2022).
In Dancing Cockatoos and the Dead Man Test, Marlene Zuk takes us on a romp through discoveries in animal behaviour across taxa to explore how behaviour evolves, always emphasizing the complex entanglement of genes and environment. With wit, humour, and sarcasm, and many fascinating anecdotes, she takes a swipe at the many myths, excessive anthropomorphism, and sex stereotyping prevalent the popular and even some academic literature. The book is a pleasure to read for the public and specialists alike. In the opening chapter, she lays bare the inevitable messiness of biology and concludes with much-needed wisdom that:
"In the end, I think we're better off living with the sometimes messy boundaries—between species, between behavior and other characteristics, and certainly between genes and the environment or culture".
And then she goes on to "explore how behavior, with all its blurry lines and uncertain edges, evolves".
I learnt many things, including that:
- one way to define behaviour is that a dead man can't do it,
- invertebrates can have intelligence, anxiety, and mental health problems,
- animals in zoos can be unhappy and may need psychotic drugs to "perform" for visitors,
- innovative bird species are less likely to go extinct,
- Paul Sherman's famed theory of the adaptive significance of spicy food in hot countries has been called into question,
- And much more.
I have only read this one book by Marlene Zuk, but the experience of doing so has promoted her other books to be near the top of my reading list. Stay tuned.
1. W. D. Hamilton, M. Zuk, Heritable True Fitness and Bright Birds: A Role for Parasites? Science 218, 384–387 (1982).
2. C. Darwin, The descent of man and selection in relation to sex. Reprinted with an Introduction by J.T.Bonner and R.M.May. (Princeton University Press, 1981).
3. A. Zahavi, A. Zahavi, The Handicap Principle - A Missing Piece of Darwin's Puzzle (Oxford University Press, 1997).
4. M. Zuk, J. T. Rotenberry, R. M. Tinghitella, Silent night: adaptive disappearance of a sexual signal in a parasitized population of field crickets. Biology Letters 2, 521–524 (2006).
5. S. L. Fitzgerald, S. C. Anner, R. M. Tinghitella, Varied female and male courtship behavior facilitated the evolution of a novel sexual signal. Behavioral Ecology 33, 859–867 (2022).
6. E. D. Broder, et al., Behavioral responses of a parasitoid fly to rapidly evolving host signals. Ecology and Evolution 12, e9193 (2022).
https://www.goodreads.com/book/show/58999206-dancing-cockatoos-and-the-dead-man-test
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