Tim R. Birkhead

Sperm competition and sexual selection

General Themes: G.A. Parker, Sperm Competition and the Evolution of Ejaculates: Towards a Theory Base. A.P. Moller, Sperm Competition and Sexual Selection. W.G. Eberhard, Female Roles in Sperm Competition. J. Wright, Paternity and Paternal Care. Taxonomic Treatments: L.F. Delph and K. Havens, Pollen Competition in Flowering Plants. D.R. Levitan, Sperm Limitation, Gamete Competition and Sexual Selection in External Fertilizers. N.K. Michiels, Mating Conflicts and Sperm Competition in Simultaneous Hermaphrodites. B. Baur, Sperm Competition in Molluscs. M.A. Elgar, Sperm Competition and Sexual Selection in Spiders and Other Arachnids. L.W. Simmons and M.T. Siva-Jothy, Sperm Competition in Insects: Mechanisms and the Potential for Selection. C.W. Petersen and R.R. Warner, Sperm Competition in Fishes. T.R. Halliday, Sperm Competition in Amphibians. M. Olsson and T. Madsen, Sexual Selection and Sperm Competition in Reptiles. T.R. Birkhead, Sperm Competition in Birds: Mechanisms and Function. D.A. Taggart, W.G. Breed, P.D. Temple-Smith, A. Purvis, and G. Shimmin, Reproduction, Mating Strategies and Sperm Competition in Marsupials and Monotremes. M. Gomendio, A.H. Harcourt, and E.R.S. Roldan, Sperm Competition in Mammals. T.R. Birkhead and A.P. Moller, Sperm Competition, Sexual Selection and Different Routes to Fitness. Index.

The genome of a songbird.

The zebra finch is an important model organism in several fields with unique relevance to human neuroscience. Like other songbirds, the zebra finch communicates through learned vocalizations, an ability otherwise documented only in humans and a few other animals and lacking in the chicken—the only bird with a sequenced genome until now. Here we present a structural, functional and comparative analysis of the genome sequence of the zebra finch (Taeniopygia guttata), which is a songbird belonging to the large avian order Passeriformes. We find that the overall structures of the genomes are similar in zebra finch and chicken, but they differ in many intrachromosomal rearrangements, lineage-specific gene family expansions, the number of long-terminal-repeat-based retrotransposons, and mechanisms of sex chromosome dosage compensation. We show that song behaviour engages gene regulatory networks in the zebra finch brain, altering the expression of long non-coding RNAs, microRNAs, transcription factors and their targets. We also show evidence for rapid molecular evolution in the songbird lineage of genes that are regulated during song experience. These results indicate an active involvement of the genome in neural processes underlying vocal communication and identify potential genetic substrates for the evolution and regulation of this behaviour.

Sperm competition in birds

Ornithologists have known for a long time that males of monogamous bird species sometimes copulate with females from other pairs, but it is only in the last few years that researchers have shown that these extra-pair copulations can result in offspring and increase male reproductive success. Males time their extra-pair copulations to coincide with the period when females are fertilizable, and they show a range of remarkable behaviours to help them secure these matings, since in most cases females attempt to avoid them. At the same time, males of most species employ one of two strategies (mate guarding or frequent copulation) to avoid being cuckolded themselves.

Postcopulatory sexual selection.

The female reproductive tract is where competition between the sperm of different males takes place, aided and abetted by the female herself. Intense postcopulatory sexual selection fosters inter-sexual conflict and drives rapid evolutionary change to generate a startling diversity of morphological, behavioural and physiological adaptations. We identify three main issues that should be resolved to advance our understanding of postcopulatory sexual selection. We need to determine the genetic basis of different male fertility traits and female traits that mediate sperm selection; identify the genes or genomic regions that control these traits; and establish the coevolutionary trajectory of sexes.

Copulation behaviour of birds

Inter-specific variation in copulation behaviour among birds is described. The following factors explaining variation in copulation rate are examined: (i) the number of eggs which have to be fertilized (the fertilization hypothesis), (ii) the importance of the pair-bond (the social bond hypothesis), (iii) predation risk during copulation (the predation hypothesis), and (iv) cuckoldry risk (the sperm competition hypothesis). These hypotheses were investigated in preliminary analyses at the generic level using data on copulation behaviour in 131 bird species. The sperm competition hypothesis was supported by several lines of evidence: (i) frequent copulations among genera where males are not able to guard their mates (colonial birds, diurnal birds of prey, and owls), (ii) frequent copulations in polyandrous genera, (iii) copulations inside hole-nests of colonial birds but outside the hole-nests of solitarily nesting genera, and (iv) by the occurrence of forced pair copulations following extra-pair copulation in some species. The predation and social bond hypotheses were not totally dismissed, but there was no evidence that fertilization ability was limited by copulation frequency (i.e. the fertilization hypothesis).

Sperm mobility determines the outcome of sperm competition in the domestic fowl

The aim of this study was to establish whether the mobility of sperm of the domestic fowl, as measured by an in vitro assay, predicted the outcome of sperm competition. Thirteen pairs of New Hampshire roosters, comprising one male categorized as having high–mobility sperm and the other as having average–mobility sperm, were used. Each male provided 25 times 106 sperm, which were mixed and artificially inseminated into between four and seven New Hampshire hens, each of which produced 2 to 11 offspring. The experiment was conducted twice, such that the same pair of males inseminated the same females. Paternity was assigned by using microsatellite markers. There was a clear effect of sperm–mobility phenotype on the outcome of sperm competition: in all 13 pairs the high–mobility male fathered the majority of offspring (73.3% overall; p < 0.0001). The proportion of offspring fathered by the high–mobility male within pairs varied significantly between male pairs (p < 0.0005). This effect was associated with the difference in sperm–mobility scores between males within pairs: there was a significant positive relationship between the proportion of offspring fathered by the high–mobility male and the ratio of mobility scores between males (p < 0.05). In addition, compared with their success predicted from the non–competitive situation, in the competitive situation high–mobility males were disproportionately successful in fertilizing eggs compared with average–mobility males. This may occur because female sperm storage is limited in some way and a greater proportion of high–mobility sperm gain access to the females sperm storage tubules. There was no evidence that female effects accounted for any of the variation in paternity.

Female feral fowl eject sperm of subdominant males

Paternity is often determined by competition between the ejaculates of different males. Males can also use particular behaviours or structures to manipulate how females use sperm. However, the ability of females to bias sperm utilization in favour of preferred males independently of male manipulation has not been demonstrated. Females are predicted to respond differentially to the sperm of different males when the reproductive interests of the sexes differ and when females are coerced into copulating. Here we show that in female feral fowl most copulations are coerced, and that females consistently bias sperm retention in favour of the preferred male phenotype. Females prefer to copulate with dominant males, but when sexually coerced by subordinate males, they manipulate the behaviour of dominant males to reduce the likelihood of insemination. If this fails, females differentially eject ejaculates according to male status in the absence of any male manipulation and preferentially retain the sperm of dominant males.

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata, revealed by DNA fingerprinting

SummaryThe frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of ‘quasi-parasitism’ (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species.

Sophisticated sperm allocation in male fowl

When a female is sexually promiscuous, the ejaculates of different males compete for the fertilization of her eggs; the more sperm a male inseminates into a female, the more likely he is to fertilize her eggs. Because sperm production is limited and costly, theory predicts that males will strategically allocate sperm (1) according to female promiscuity, (2) saving some for copulations with new females, and (3) to females producing more and/or better offspring. Whether males allocate sperm in all of these ways is not known, particularly in birds where the collection of natural ejaculates only recently became possible. Here we demonstrate male sperm allocation of unprecedented sophistication in the fowl Gallus gallus. Males show status-dependent sperm investment in females according to the level of female promiscuity; they progressively reduce sperm investment in a particular female but, on encountering a new female, instantaneously increase their sperm investment; and they preferentially allocate sperm to females with large sexual ornaments signalling superior maternal investment. Our results indicate that female promiscuity leads to the evolution of sophisticated male sexual behaviour.

Cryptic female choice: criteria for establishing female sperm choice.

In this paper, I consider the criteria necessary to demonstrate the postcopulatory ability of females to favor the sperm of one conspecific male over another, that is, sperm choice. In practice it is difficult to distinguish between sperm competition and sperm choice, and sperm choice can be demonstrated only if the effects of sperm competition can be controlled. Few studies have used experimental protocols that do this, so evidence for sperm choice is limited. Moreover, in those studies in which sperm choice occurs, it does so to avoid incompatible genetic combinations and is therefore unlikely to result in directional sexual selection.