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T R Birkhead

Publications and source records attributed to T R Birkhead.

8 recordsLinked to original sources

Sperm competition in birds.

Sperm competition in birds occurs when a female is inseminated by more than one male during a single breeding cycle. Despite most birds being socially monogamous, sperm competition is widespread and results in frequent extra-pair paternity. Sperm competition is a fundamental part of sexual selection since it results in differential reproductive success among males. Male adaptations to sperm competition include relatively large testes, large sperm stores and long spermatozoa, mate guarding and frequent pair copulations. Females show no obvious morphological adaptations to sperm competition but, by controlling whether copulations are successful, they probably determine its frequency and extent. Despite this, the evolutionary benefits females acquire from extra-pair fertilizations are poorly understood. Experiments in which females are inseminated with equal numbers of spermatozoa from two males usually show last male sperm precedence. Understanding the mechanism of sperm competition requires understanding of why the last male to inseminate a female fertilizes a disproportionate number of eggs. The data from sperm competition studies on the domestic fowl, turkeys and zebra finches are consistent only with a passive sperm loss model of sperm competition. The mechanism is as follows: after insemination, spermatozoa enter the sperm storage tubules located in the oviduct, from which they are lost at a constant rate over days or weeks. All else being equal, the interval between two inseminations determines the probability of fertilization: the second of two inseminations fertilizes most eggs simply because, by the time fertilization occurs, fewer of these spermatozoa have been lost. Other factors also affect the outcome of sperm competition: the timing of insemination relative to oviposition, the differential fertilizing capacity of males and differences in the numbers of spermatozoa inseminated; as a consequence, last male sperm precedence is not automatic. On the basis of the mechanism of sperm competition, the optimal strategy for both males and females to maximize their likelihood of extra-pair fertilization is to copulate with an extra-pair partner as close as possible to the onset of oviposition.

Adaptation, Physiological

Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata.

We tested the idea that female preference for relatively attractive extra-pair males arises because the morphological and behavioural features that females find attractive covary with ejaculate features: Sheldon's (Proc. R. Soc. Lond. B 257 25-30 (1994) phenotype-linked fertility insurance hypothesis. Two phenotypic traits that female zebra finches find attractive in males are song rate and symmetry of chest band plumage, but we found neither of these to be significantly related to any of the following ejaculate features: number of sperm, percentage of live sperm, absolute number of sperm, sperm length or sperm swimming velocity. Furthermore, and surprisingly, we did not find the predicted negative relationship between male song rate and fluctuating asymmetry of chest band plumage. Because most ejaculate features (except sperm numbers in rested males) show low levels of repeatability, it is unlikely that female zebra finches could reliably obtain a better quality ejaculate by choosing to copulate with a more attractive male. There was thus no evidence for the phenotype-linked fertility insurance hypothesis. Nor did we obtain evidence for the more general fertility insurance hypothesis: we found that female zebra finches paired to a vasectomized male, and hence receiving no sperm, were no more likely to seek an extra-pair copulation than females paired to an intact male.

Animals

Sperm competition: evolutionary causes and consequences.

The interaction between functional and mechanistic approaches to sperm competition and between male and female perspectives are described and illustrated by a study of the zebra finch, Taeniopygia guttata. Sperm competition experiments in the laboratory show that last male sperm precedence occurs (as it does in many other taxa) although the mechanism is unknown (as in most other taxa). Empirically-derived values were used to construct a mathematical model of sperm competition in the zebra finch. The model indicates that precedence occurs as a consequence of: (i) the temporal pattern of pair copulations; (ii) the rate at which sperm are lost from the female tract; and (iii) more sperm being transferred during extra-pair copulations than during pair copulations. The latter effect is a consequence of males seeking extra-pair copulations after their own pair copulation period has ended. The effect of sperm numbers on the pattern of sperm precedence may be further increased by: (i) extra-pair males increasing ejaculate size (sperm numbers) (for which there is no evidence); (ii) extra-pair males being of a better quality and transferring more sperm or better quality sperm (for which there is some evidence); and (iii) cryptic female choice. Females eject over 99% of sperm following insemination; if they eject fewer sperm from males chosen as extra-pair copulation partners, the potential for cryptic female choice is considerable. However, this is still being investigated. The model also predicts the optimal time for an extra-pair copulation to occur (from either a male or female perspective). A comparison between the predicted and observed pattern suggests that the optimal timing of extra-pair copulations is constrained in both sexes.

Animals

A comparative study of sperm-egg interactions in birds.

A comparative study was made of the number of spermatozoa trapped on the outer perivitelline layer and the number of spermatozoa penetrating the inner perivitelline layer of the eggs of 27 species of bird. The total number of spermatozoa (trapped spermatozoa plus holes made by spermatozoa) varied between 29 and 164,000 per egg among species and was significantly and positively correlated with size of the ovum. In most species, holes formed a 'halo' around the germinal disc area and the density of holes was much greater in this region than elsewhere, especially in passerine birds. In some species, a high proportion of holes occurred at some distance from the germinal disc. This seems to be an artefact due to the fact that some spermatozoa trapped in the outer perivitelline layer undergo proteolytic activity between fertilization and oviposition and create additional holes in the inner perivitelline layer both at and away from the germinal disc. Across all species and within most individual species, the number of trapped spermatozoa was positively correlated with the number of holes in the inner perivitelline layer. Decreases in the total number of spermatozoa on successive eggs of a clutch provided an index of the rate at which spermatozoa were used from the sperm storage tubules.

Animals

Selection and utilization of spermatozoa in the reproductive tract of the female zebra finch Taeniopygia guttata.

The numbers and proportion of spermatozoa reaching different parts of the female reproductive tract after a single natural insemination were investigated in zebra finches Taeniopygia guttata. The number of spermatozoa transferred during a single, natural copulation was estimated by comparing the number of spermatozoa in the seminal glomera of males that had performed a single copulation with control males. The mean number of spermatozoa per ejaculate was 5.8 x 10(6) +/- 1.80 x 10(6) SEM. The mean number of spermatozoa stored in the sperm storage tubules in the uterovaginal junction following a single, natural insemination was 6027 +/- 1874, 0.104% of those inseminated. The mean number of spermatozoa reaching the infundibulum and trapped on the perivitelline layer of all eggs of the clutch after a single copulation was 45.6 +/- 9.18 and a further 36 penetrated the perivitelline layer of the ovum, i.e. 82 in total (1.4% of the spermatozoa in the sperm storage tubules and 0.001% of spermatozoa in the ejaculate). Female zebra finches that completed a natural breeding cycle with a mean of 12 copulations had 404 +/- 111 spermatozoa trapped on the perivitelline layer of all eggs of the clutch, and an estimated further 173 spermatozoa penetrated the perivitelline layer. A smaller proportion of spermatozoa was trapped on the perivitelline layer of zebra finch eggs, than in chicken or turkey eggs.

Animals

Extra-pair copulation and sperm competition in the zebra finch.

Most birds are monogamous, but recent studies have shown that extra-pair copulations (EPCs) occur frequently despite a range of paternity guards, including mate-guarding and frequent copulation. Although EPCs are known to result in extra-pair paternity, there are no previous quantitative estimates of the success of EPCs in fertilizing eggs. We present here estimates of the likelihood of success of extra-pair copulations in a monogamous passerine, the zebra finch Poephila guttata. We show that (1) EPCs occurring under semi-natural conditions in captivity result in extra-pair paternity, (2) sperm from the last male to mate has precedence over previous matings: a single EPC occurring last is disproportionately successful in fertilizing eggs, but EPCs followed by further pair copulations have a low probability of success. These results have important implications for sexual selection theory.

Animals