Jan T. Lifjeld

Females increase offspring heterozygosity and fitness through extra-pair matings

Females in a variety of species commonly mate with multiple males, and there is evidence that they benefit by producing offspring of higher genetic quality; however, the nature of these genetic benefits is debated. Enhanced offspring survival or quality can result from intrinsic effects of paternal genes—‘good genes’—or from interactions between the maternal and paternal genomes—‘compatible genes’. Evidence for the latter process is accumulating: matings between relatives lead to decreased reproductive success, and the individual level of inbreeding—measured as average heterozygosity—is a strong fitness predictor. Females should thus benefit from mating with genetically dissimilar males. In many birds, social monogamy restricts mate choice, but females may circumvent this by pursuing extra-pair copulations. Here we show that female blue tits, Parus caeruleus, increase the heterozygosity of their progeny through extra-pair matings. Females thereby produce offspring of higher reproductive value, because less inbred individuals have increased survival chances, a more elaborate male secondary sexual trait (crown colour) and higher reproductive success. The cost of inbreeding may therefore be an important factor driving the evolution of female extra-pair mating.

Female bluethroats enhance offspring immunocompetence through extra-pair copulations.

Female birds frequently copulate with extra-pair males, but the adaptive value of this behaviour is poorly understood. Some studies have suggested that ‘good genes’ may be involved, where females seek to have their eggs fertilized by high-quality males without receiving any material benefits from them. Nevertheless, it remains to be shown that a genetic benefit is passed on to offspring. Here we report that nestling bluethroats, Luscinia svecica , sired by extra-pair males had a higher T-cell-mediated immune response than their maternal half-siblings raised in the same nest. The difference could not be attributed to nestling body mass, sex or hatching order, but may be an effect of paternal genotype. Extra-pair young were also more immunocompetent than their paternal half-sibs raised in the genetic fathers own nest, which indicates an additional effect of maternal genotype. Our results are consistent with the idea that females engage in extra-pair copulations to obtain compatible viability genes, rather than ‘good genes’ per se.

POLYGYNY IN BIRDS: THE ROLE OF COMPETITION BETWEEN FEMALES FOR MALE PARENTAL CARE

In many polygynous birds the reproductive success of females is strongly dependent on male parental care, and females mated with the same male will compete for a limited amount of male assistance. Mated females may benefit from trying to prevent or delay the settlement of other females. Hence, female aggression may affect male mating success and thus play a role in the evolution of avian mating systems. We present a modified version of the polygyny threshold model that takes female aggression into account. A review on female aggression, male allocation of parental care, and delayed breeding of secondary females supports the model. An alternative model also predicts delayed breeding of secondary females when they benefit from reducing the breeding overlap with the respective primary females. However, recent studies suggest that secondary females may benefit from breeding as early as possible relative to the primary female. Our review also shows that secondary females generally have a reduced reproductive success compared with simultaneous, monogamous females. This difference may arise from a restricted mate search by females and does not necessarily contradict the polygyny threshold model.

Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment

The blue throat feathers of male bluethroats (Luscinia s. svecica) show a reflectance peak in the ultraviolet (UV) waveband (320 to 400 nm). The throat is actively displayed during courtship, suggesting a role for sexual selection on an ultraviolet signal. Indeed, a recent aviary experiment demonstrated that females discriminated against males with artificially reduced UV reflectance (Andersson and Amundsen 1997). Here, we report the results of a similar experimental manipulation applied on free–ranging males. UV–reduced (UVR) males had a lower success in attracting mates, as judged from a significantly later start of egg laying, compared with control (C) males. UVR males also spent significantly less time advertising for additional mates when their own mate was fertile, and they had a lower success in achieving extra–pair fertilizations. Furthermore, UVR males tended to guard their mates more closely and lose more paternity in their own brood than C males did. We conclude that the treatment affected both social and extra–pair mate choice. This is the first experimental evidence that UV signalling influences male mating success in free–ranging birds.

On the cost of searching for a mate in female pied flycatchers Ficedula hypoleuca

Abstract Female pied flycatchers, Ficedula hypoleuca , were trapped in one area and released in another a few kilometres away, where the positions of all available nest sites and males were known beforehand. Many of the females moved only a short distance before mating, settling after about 2 (0–6) days in early spring and about 1 day later on. The length of the premating period was negatively correlated with female body weight and prevailing air temperature, indicating that the females were subject to an energy constraint when searching. The premating period was longer for females that settled with an alreadymated male than for those mating with an unmated male. The significance of the results is discussed in relation to the evolution of avian mating systems, and of male behaviour and plumage colour. Competition for a mate, rather than for food, may explain the spacing of males (territoriality).

Female control of extra-pair fertilization in tree swallows

SummaryIn a Canadian population of tree swallows, Tachycineta bicolor, DNA fingerprinting has previously shown that half of all broods contain many offspring resulting from extra-pair copulations (EPCs), whereas the other half contain only legitimate offspring. This bimodal pattern of extra-pair paternity might be due to variation in the effectiveness of male paternity guards, variation in female ability to resist EPCs, and/or variation in female pursuit of EPCs. Here we report experimental evidence for female control of copulations and fertilizations and the occurrence of two alternative copulation strategies among females in this population. Ten paired male tree swallows were removed on the day their mates laid the first egg. Replacement males took over the nestbox within 0.5–23 h and attempted to copulate with the widowed female. Assuming that eggs were fertilized approximately 24 h prior to laying, the first two eggs were fertilized before the male was removed, while the third and subsequent eggs could potentially be fertilized by the replacement male. Fingerprinting revealed that the first two eggs were sired by the resident males in five nests and by extra-pair males in the remaining five nests. The widows that had been faithful to their initially chosen mate rejected copulation attempts by the replacement male until most of the eggs had been laid. Consequently, nearly all eggs laid by these females were sired by the original male. The widows that had been unfaithful prior to male removal copulated sooner with the replacement male than females that were faithful to their mate. However, these replacement males also had a very low fertilization success; most eggs were sired by males that were not associated with the nest. This is consistent with the situation in non-experimental nests where unfaithful females copulate with their mate at the same rate as faithful females, yet unfaithful females have a majority of offspring sired by extra-pair males. We conclude that fertilization patterns to a large extent are determined by the female through active selection and rejection of copulation partners, though our results also allow some speculation that females have control over sperm competition. Female copulation tactics are probably determined some currently unknown fitness benefits of having the offspring sired by particular males.

Low frequency of extra-pair paternity in pied flycatchers revealed by DNA fingerprinting

SummaryGenetic parentage of 135 nestlings from 27 broods of polygynous and monogamous pied flycatchers Ficedula hypoleuca was analyzed by means of multilocus DNA fingerprinting. The minisatellite probe alpha-globin 3′HVR detected approximately 12 scorable bands per fingerprint, and the proportion of bands shared between presumably unrelated adults averaged 0.22+0.08 SD. The fingerprints of 125 of the 135 nestlings made a complete match to those of their putative parents. In 4 nestlings a single mismatched band occurred, but since band sharing with both putative parents was high, the single mismatches were assumed to be caused by mutation. The 6 remaining nestlings had 5 or more mismatched bands each, low band-sharing proportions with their putative father and high band-sharing proportions with their putative mother. We thus conclude that they were all sired through extra-pair copulations (EPCs). Hence, only 4% of nestlings were sired through EPCs, and none resulted from intraspecific brood parasitism. One of the cuckolding males was identified, explaining all 5 mismatched bands in the nestlings fingerprint. Three of the illegitimate nestlings were from primary nests of polygynous males; 3 were from nests of monogamous males. The fact that many males in this study started to advertise for a second female in a distant territory several days before their first mate began egglaying, and still managed to secure almost exclusive paternity in their first brood, suggests that male polyterritoriality is not costly in terms of lost paternity. Common anti-cuckoddry tactics performed by male birds, like high rate of within-pair copulation and continuous mate-guarding thoughout the females fertilizable period, do not seem to be important in pied flycatchers.

Influence of Male and Female Quality on Clutch Size in Tits (Parus Spp.)

Field experiments were designed to examine the effects of parental ability on clutch size, for the two sexes separately. To handicap parental ability we removed feathers from the wings and the tail of three tit species (Parus spp.) during the initial incubation period. We then removed their first clutches, and examined the effect of the handicap on the subsequent nesting. In Blue Tits (P. caeruleus), and Coal Tits (P. ater), handicapped females reduced the size of the repeat clutch more than control females. In Blue Tits handicapped females fed their young at a lower rate, lost more body mass during the nestling period, and at fledging time their broods were significantly smaller than those of controls. Their fledglings had a body mass, similar to the control fledglings. Handicapped female Great Tits (P. major) only reduced their clutch size a small amount; consequently, at fledging time, their body mass and those of their young were lower than for controls. The males of the three species of tits did not seem to increase parental investment when their mate was handicapped. When male Blue and Coal Tits were handicapped their mates did not reduce clutch size more than did those of the control group, despite a reduction in parental investment by handicapped males. However, breeding success was not significantly affected by handicapping males. We conclude that the clutch size determination of female tits is primarily based on their own ability to feed their young, and not on the quality of their mate. Male tits seem to have a lesser influence on breeding success than females, and males seem less willing or less able to increase their parental investment.

The function of courtship feeding during incubation in the pied flycatcher Ficedula hypoleuca

The male pied flycatcher Ficedula hypoleuca feeds his female frequently while she is incubating. The present paper focuses on the adaptive value of this behaviour. Results of a nest predation experiment, forcing birds to re-nest, did not support the hypothesis that courtship feeding strengthens the bond between the sexes. Furthermore, there was no evidence that the rate of courtship feeding is a reliable indicator of the quality of male parental care. Instead, the food provided by the male seems to be of essential nutritional value to the female. There was a positive correlation between the body weight of the female and the rate of courtship feeding. Females in good condition during incubation showed a reduced incubation period and produced heavy fledglings. Courtship feeding is only one activity that would enhance male fitness, others include polyterritorial and polygamous behaviour and extra-pair copulations. Polyterritorial males fed their mates less often than those with a single territory. The proportion of male effort allocated to courtship feeding may vary according to local circumstances such as the availability of nest sites, the number of potential mates, and the probability of nesting failure.

Mate choice and imprinting in birds studied by cross-fostering in the wild

Sexual–selection theories generally assume that mating preferences are heritable traits. However, there is substantial evidence that the rearing environment may be important for the development of mating preferences, indicating that they may be learnt, or modified by experience. The relative importance of such sexual imprinting across species remains largely unexplored. Here, we report results of a large–scale cross–fostering experiment in the wild in which nestling birds were raised by parents of a different species. We show that resulting sexual imprinting may have a negative effect on pairing success in one species (the great tit, Parus major), but not in two other species (the blue tit, P. caeruleus and the pied flycatcher, Ficedula hypoleuca). A remarkable variation thus seems to exist, even between species that are congeneric and have similar breeding ecologies. The cross–fostering resulted in heterospecific pairings between the two tit species (female blue tit breeding with male great tit), which has never, to our knowledge, been previously documented. However, the chicks fledging from these nests were all blue tit.