BirdLife: The Magazine June 2017 - Page 16

THE SEX ISSUE RELATIVELY LARGE TESTES ARE A SURE SIGN OF FEMALE PROMISCUITY 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 wer e once thought inexplicable. Take testicles, for example. An accidental dis- covery in the 1970s, that massive differences in relative testis size among the great apes mapped onto their mating system, started a series of dis- coveries 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 ency- clopaedia 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 con- text 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 polygynan- drously (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 monoga- mous, 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 fac- tory produces more sperm. In the competition for fertilisations (which is what sperm competi- tion 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. MOST PASSERINES COPULATE FOR ONE OR TWO SECONDS; THE BUFFALO-WEAVER, BY CONTRAST, COPULATES FOR 30 MINUTES 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. 16 Common Murres Uria aalge are very promiscuous, despite having long-term pair bonds and being considered to have a monogamous mating system. Photo Menno Schaefer/ Shutterstock 4 BIRDLIFE • JUNE 2017 JUNE 2017 • BIRDLIFE Most birds possess no penis: sperm are sim- ply transferred from the male’s cloaca to the female’s everted cloaca. Quail, which as we have seen are promiscuous, have evolved a conspic- uous 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 Buba- lornis 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 suc- cess. The precise function of this 1-2 cm rigid rod of connective tissue, with no ducts, con- tinues 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 sec- onds; 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 War- blers have huge testes; molecular studies con- firm that mixed paternity in broods is the norm. My favourite example is the Vasa Parrot Cora- copsis 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 Madagas- car 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 copu- lating frequently and lengthily with several part- ners, 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 17