For years, people assumed most birds were monogamous. This idyllic image was blown apart when research revealed lifestyles of polygamy, polyandry, marathon mating sessions and sperm competition. Welcome to the secret reproductive life of birds. Shocked? Blame it on natural selection.
In 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 Animal 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 environment, some individuals would withhold from breeding so that there would be sufficient food for others to reproduce.
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: natural selection operated on individuals, not on groups or species. Nevertheless, a new area of research was born from this debate that eventually became known as behavioural ecology.
Females are not naturally monogamous
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 appearance and behaviour of males and females, sexual selection enjoyed a brief spell in the spotlight. 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, Huxley 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 platyrhynchos, 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.
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 dispelled 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!
It became clear that sexual monogamy, especially among females, was the exception rather than the rule
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 aberration 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 ecology, David Lack had published what was to become an incredibly influential book Ecological 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 Blackbird 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.
Relatively large testes are a sure sign of female promiscuity
With the birth of behavioural ecology, the focus switched to exceptions, and to the “exceptions” to monogamy: extra-pair copulations. 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 distinguish between ”social monogamy” and ”sexual monogamy” in birds. Understanding sexual selection processes both before (e.g. mate choice) and after (e.g. sperm competition) insemination helps to explain phenomena that were once thought inexplicable.
Take testicles, for example. An accidental discovery in the 1970s, that massive differences in relative testis size among the great apes mapped onto their mating system, started a series of discoveries in various animal taxa that eventually revealed what amounts almost to a general rule: relatively large testes are a sure sign of female promiscuity. It was an idea with a long, albeit incomplete history, for in 1676, when Francis Willughby and John Ray wrote the first encyclopaedia of ornithology, they commented on the huge testes of the Common Quail Coturnix coturnix, commenting, ”whence we infer it is a salacious bird”. The Common Quail is indeed promiscuous, but without an evolutionary context there was little else that could be said about the phenomenon.
Yet the observation holds true; birds with large testes for their body size invariably have extraordinary mating systems. The Dunnock Prunella modularis is one of our most promiscuous of birds, breeding variously as monogamous pairs, in polyandrous trios (two males and one female) and even polygynandrously (two males sharing two females); it has testes that represent some 3.4% of the male’s body weight. In contrast, the Eurasian Bullfinch Pyrrhula pyrrhula appears to be strictly monogamous, having the smallest testes relative to body size, at just 0.29% of male body mass.
The testis acts as a sperm factory; a larger factory produces more sperm. In the competition for fertilisations (which is what sperm competition is), the more sperm the better the prospects of success. It is like trying to win a raffle: your chances are improved the more tickets you buy.
Such is the competition for the fertilisations that in many species simply having a bigger bucket of sperm isn’t enough. After all, the way selection works, any advantage over another male increases an individual’s chances of leaving descendants. Between two males that each have huge, but equally sized sperm stores, one that has a penis slightly longer than the other is able to place its sperm in a more propitious location within the female oviduct, thus enhancing its chances of fertilisation. Obviously, this male is more likely to win the fertilisation competition; hereafter, selection selects for penis length.
In species in which female promiscuity is rife, the anatomical and behavioural adaptations to enhance male reproductive success seem almost limitless. Across the animal kingdom examples abound, but let’s focus on birds.
Most passerines copulate for one or two seconds. The Buffalo-weaver, by contrast, copulates for 30 minutes
Most birds possess no penis: sperm are simply transferred from the male’s cloaca to the female’s everted cloaca. Quail, which as we have seen are promiscuous, have evolved a conspicuous gland adjacent to the male’s cloaca that delivers a dollop of shaving-cream-like foam at insemination; this enhances the vigour of their sperm. The Red-billed Buffalo-weaver Bubalornis niger breeds in a polygynous harem-like arrangement, but with two males forming a coalition and sharing a group of up to twelve females. Competition for fertilisation is stiff, and males have evolved a false penis directly in front of their cloaca to facilitate their fertilisation success.
The precise function of this 1-2 cm rigid rod of connective tissue, with no ducts, continues to be a mystery. It isn’t inserted into the female’s cloaca, but instead is rubbed against it during their enormously protracted copulations. Most passerines copulate for one or two seconds; the Buffalo-weaver, by contrast, copulates for 30 min. This prolonged cloacal massage by the male apparently “persuades” the female that she should use his sperm rather than that of the other coalition male.
The Aquatic Warbler Acrocephalus paludicola, a nondescript little brown bird that breeds in the fen mires of Poland and Belarus, also copulates for about half an hour. This species appears to be utterly promiscuous with no bonds between the sexes. Fertile females seem to copulate opportunistically; the male clings to the female’s back so that the pair hop around together in the vegetation like a couple of mice. The male inseminates the female every seven minutes or so during this time, with one main objective: to flood her system with sperm. Male Aquatic Warblers have huge testes; molecular studies confirm that mixed paternity in broods is the norm.
My favourite example is the Vasa Parrot Coracopsis vasa; I had never encountered anything quite so extreme in birds as this. It was like the protracted copulatory tie that occurs in dogs: male and female as one, joined for over half an hour by their genitalia. A colleague in Madagascar has also seen wild Vasa Parrots copulating promiscuously. On dissecting a wet-preserved male museum specimen and finding that the testes were very large, I decided that this extraordinary species would make a fascinating PhD study; and so it proved. The mating system was utterly promiscuous, with both sexes copulating frequently and lengthily with several partners, and females essentially trading food from males (that they would take to feed their chicks) for sex. Males copulated with as many females as possible, in the “hope” of securing a winning lottery ticket, feeding the chick-rearing females in return. The copulatory tie is an adaptation to monopolise females for an additional half hour or so, to maximise his chances of his sperm being used to fertilise the female’s ova, while keeping other males at bay.
The final (for now) male adaptation is their sperm cells. Early on in the study of sperm competition, it was assumed that sperm were undifferentiated; what counted was numbers. In fact, we now know that both quantity and quality count. Sperm vary both within and between males, both in design and performance. As you might expect from their highly promiscuous mating arrangements, male Dunnocks produce huge numbers of uniformly sleek, Porsche-like sperm. The Bullfinch, on the other hand, produces a limited, motley collection of Trabant-like sperm that are highly variable and not especially well made, although amongst them are sufficient good ones to ensure fertilisation. If the chances of having to compete with another male are low, why bother investing in quality control? The male Bullfinch’s strategy is simply to ensure that it makes enough decent sperm to ensure that his partner’s ova are fertilised. For the Dunnock, every sperm counts and quality control is essential.
When it comes to sperm, we now know that both quantity and quality count: long sperm swim faster
One of our most extraordinary findings in the avian sperm department relates to another species that is fairly monogamous, the Zebra Finch Taeniopygia castanotis. Like the Bullfinch, the Zebra Finch produces rather variable sperm. Some male Zebra Finches produce long sperm with a long midpiece (essentially, the sperm’s energy supply), others have a long sperm with a short midpiece, and yet others produce short sperm with a short midpiece. These different designs are genetically determined; they dictate the speed at which the sperm swim, and hence their competitive ability when pitted against the sperm of another male. Overall, long sperm swim faster, and are most likely to fertilise a female’s ova.
So far, my examples have focused predominantly on males. What about females? For a long time it was assumed that females were merely passive receptacles and conduits for male gametes; sexual selection operated predominantly on males. Certainly, there was nothing as obvious as the variation in relative testes size to offer an anatomical clue to female promiscuity. It had however, suggested that promiscuous females might be able to decide which of several males’ sperm they would use to fertilise their ova. Where might we find such “cryptic female choice” going on? The most obvious opportunity lay in those circumstances in which females do not appear to have any pre-copulatory choice of inseminating partner. The most obvious situation in which cryptic female choice (”cryptic” because the choice, would occur out of sight within the female’s oviduct) might be found was in Huxley’s ducks, where males, armed with a phallus, effectively rape females.
I decided to explore this and, with a post-doctoral researcher, Patricia Brennan, examined the reproductive system of female ducks. To our surprise, they were different from the large numbers of other female birds (all road kill) that I had dissected over the years, in which the vagina was a simple tube. To cut a long story short, female ducks of different species have complex vaginas; that complexity correlates with the length of the male’s penis. In some waterfowl species the penis is tiny, in others like the Lake Duck Oxyura vittata of Argentina, it is longer than the male’s body!
The vaginas of some waterfowl contain a spiral-like structure at the junction with the uterus or shell gland, and a variable number (up to three) side branches. These are devices, we believe, to keep the sperm of raping males at arms’ length. When forcibly inseminated, the female has only to clench the spiral tight to prevent further intromission, sending the male’s snake-like penis down one of the blind-ending alleys where his sperm have little chance of fertilising eggs. When with her partner, whom she “wants” to fertilise her eggs, the female duck relaxes and allows him to deposit his semen in the appropriate location.
There’s a final twist. The beginning of new life differs between birds and mammals, including ourselves. As is well known, it takes only one sperm to fertilise an ovum and start a new life. Not so in birds. A single sperm will certainly fertilise a bird’s ovum, but it will not result in a new life. Since the early 1900s, it has been known that soon after ovulation a bird’s ovum contains several (up to 60) sperm in the germinal disc (the region where the female DNA resides); strictly, these are the nuclei of that number of sperm. Curiously, no one queried this, until very recently.
Why do females bother to copulate with more than one male? What’s in it for them? It’s a puzzle waiting for an answer
What were all those extra sperm for? Using our Zebra Finches, we discovered a way of allowing only a single sperm into the ovum; we thus showed that, while that was sufficient for fertilisation per se, there was no subsequent embryo development. When we allowed more sperm in, we got both fertilisation and embryo development. The extra sperm are “helpers” in some way, clearly essential to triggering embryo development. This is remarkable at a developmental level, but it also raises some questions that relate to promiscuity. If a female is inseminated by, let’s say, two males, and both males’ sperm reach the ovum, could a situation ever arise where the “helper sperm” are not those of the male whose sperm DNA has fused with the female’s DNA? Could there be a situation where one male unwittingly helps to start a new life fathered by another male? Still so much to discover.
From a behavioural ecology perspective there is one outstanding puzzle. Why do females bother to copulate with more than one male? What’s in it for them? For males, promiscuity pays: it results in more offspring. For females this is not the case. There have been lots of explanations for female promiscuity, including the idea that extra-pair offspring are of better quality, but despite numerous studies, that does not seem to be the case. It is a puzzle waiting for an answer.
Tim Birkhead FRS is Professor of Behavioural Ecology at the University of Sheffield. His most recent book is The Most Perfect Thing: the Inside (and Outside) of a Birds’ Egg, Bloomsbury 2016.