BirdLife: The Magazine June 2017 - Page 14

THE SEX ISSUE I n the late 1960s, it was generally assumed that the vast majority of birds were monogamous. Indeed, the conventional wisdom was that the females of most animal species were monogamous, mating with and remaining faithful to a single male partner. Then something extraordinary happened. In 1962, Vero Copner Wynne-Edwards, in his book Ani- mal Dispersion in Relation to Social Behaviour, promoted the idea that animals behaved for the good of the species, or the good of the group in which they lived. He suggested that if, for example, food became scarce in the environ- ment, some individuals would withhold from breeding so that there would be sufficient food for others to reproduce. FEMALES? NOT NATURALLY MONOGAMOUS Wynne-Edwards’s thesis provoked a strong response from a handful of biologists who understood natural selection. Experts, such as David Lack and George Williams, pointed out that his group selection ideas were flawed: nat- ural selection operated on individuals, not on groups or species. Nevertheless, a new area of research was born from this debate that eventu- ally became known as behavioural ecology. FEATHERED FORNICATION Of polygamy, polyandry, rape, and sperm competition. Welcome to the secret reproductive life of birds. Shocked? Blame it on natural selection Tim Birkhead* This new kind of individual selection thinking made sexual selection relevant — and exciting — again. Proposed by Charles Darwin in the late 1800s to explain the difference in the appear- ance and behaviour of males and females, sex- ual selection enjoyed a brief spell in the spot- light. By the 1940s and 1950s that light had faded, thanks largely to Julian Huxley, a great populariser of science who did not understand the way selection worked. In the early part of the twentieth-century, Hux- ley pioneered the study of animal behaviour through his now classic study of Great Crested Grebe Podiceps cristatus courtship. Since the grebes’ elaborate displays occurred after pair formation, Huxley argued that they could have nothing to do with attracting a partner, and hence, nothing to do with sexual selection. Less well known is Huxley’s study of the courtship and mating behaviour of Mallard Anas platy- rhynchos, conducted at around the same time. The contrast between his two study species could hardly have been greater: the elegant grebes seemed obviously monogamous with their magnificent mutual courtship displays; while the dreadfully promiscuous male ducks forced themselves on females, sometimes with such brutality and in such numbers that the females drowned. Huxley’s explanation was that the grebes had evolved to a higher level than the dirty ducks. Moreover, since Huxley believed that selection operated for the good of the species, duck rape could not be anything other than harmful. JUNE 2017 • BIRDLIFE THROUGH THE MID 1970s AND 1980s IT BECAME CLEAR THAT SEXUAL MONOGAMY, ESPECIALLY AMONG FEMALES, WAS THE EXCEPTION RATHER THAN THE RULE Black-winged Stilt Himantopus himantopus. Photo Sysasya/Shutterstock 4 The undergraduate lecture that changed the course of my life featured an insect, rather than a bird: the yellow dungfly Scatophaga stercoraria. Far from being monogamous, female dungflies were promiscuous, routinely copulating with several males. Males, too, were promiscuous, mating with several females. This behaviour dis- pelled the myth, perpetuated by Darwin, that females were monogamous; it also showed that such promiscuity could be adaptive. Thirdly, it demonstrated that sexual selection did not cease once an individual had acquired a partner, as Darwin assumed, but instead could continue after mating through something called sperm competition. To my young and eager self, this was mind-blowing, exciting stuff: sex, behaviour and a new way of thinking about selection! I wondered whether the promiscuity observed in insects might also occur in birds, and I decided that was what I wanted to study. When I told my undergraduate tutor and friends, they laughed: “Birds are monogamous,” they said, “everyone knows that. You’d be wasting your time.” My PhD was on the behaviour and ecology of Common Murre Uria aalge, and it was my good fortune that they turned out to behave pretty much like dungflies, with a lot of promiscuity, despite having long-term pair bonds. As behavioural ecology developed through the mid 1970s and 1980s, it became clear that sexual monogamy, especially among females, was the exception rather than the rule. Males, of course, had long been known to be promiscuous. Instead of writing off promiscuity as an aberra- tion or hormone imbalance, as was usually the case prior to 1970, researchers now focused on individuals ”getting their genes in to subsequent generations”: what better way to achieve this than by being promiscuous? Just before the beginning of behavioural ecol- ogy, David Lack had published what was to become an incredibly influential book Ecolog- ical Adaptations for Breeding in Birds (1968), in which he stated that over 90% of all birds had a monogamous mating system; the rest were either polygynous, like the Red-winged Black- bird Agelaius phoeniceus or the Ruff Calidris pugnax, while a tiny few, like the jacanas were polyandrous. Monogamy, therefore, was the norm; it was the norm that required study rather than the exceptions. With the birth of behavioural ecology, the focus switched to exceptions, and to the ”exceptions” to monogamy: extra-pair cop- ulations. A key development was the ability to establish paternity through techniques such as DNA fingerprinting; this finally provided the incontrovertible evidence that promiscuity, for males at least, paid off. This also allowed us to 15