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Dr. Bart Kempenaers

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Publication references

Katharina Foerster, Kaspar Delhey, Arild Johnsen, Jan T. Lifjeld & Bart Kempenaers
Females increase offspring heterozygosity and fitness through extra-pair matings

Behavioural Biology . Ecology

Unfaithful songbirds increase offspring fitness

Max Planck scientists show that female promiscuity can reduce the negative consequences of inbreeding in socially monogamous birds.

October 15, 2003

Bird parents typically raise their young in seemingly peaceful cooperation and were therefore seen as reflecting the ideal of monogamous partnership. This view has changed dramatically over the last decade: since molecular ‘fingerprinting’ techniques became available, behavioural ecologists have routinely used paternity analyses to study mating systems. We now know that unfaithful behaviour - referred to as extra-pair copulations - is more the rule than the exception, in particular in socially monogamous songbirds. A team of scientists from the Max Planck Research Centre for Ornithology in Seewiesen, Germany, and from the Zoological Museum in Oslo, Norway, now show the evolutionary advantages of this behaviour, using data from a long term study on the blue tit, a small hole-nesting songbird (Nature, October 16 2003). Through extra-pair copulations with distantly breeding males, females produce offspring that are more outbred and therefore genetically more diverse, compared to their half-siblings sired by the social father.

Monogamy is rare among animals. Even species that form socially monogamous pairs of one male and one female are often not monogamous in the strict sense. Males and females commonly copulate with more than one partner during a single reproductive event. Therefore, young raised in the same brood are often sired by different males. The evolutionary advantage of unfaithful behaviour is obvious for males: the clutch- or litter size of the partner limits the maximum number of offspring that can be produced. Extra-pair copulations with other females provide the only opportunity for a male to sire additional young. For females, the significance of promiscuity is less obvious. If evolution only favours high numbers of offspring, then females would not benefit from mating with multiple males. However, evolutionary biologists have convincingly shown that the genetic quality of the young has a crucial influence on their subsequent survival and reproductive success. Consequently, not only the quantity, but also the genetic quality of the progeny determines how successfully an individual will spread its genes in future generations.

Female blue tits (Parus caeruleus) choose a single social partner. This male defends a territory with a nestbox, and he provides help with offspring care. Since many females compete for only a few vacant males with territories, some of them will end up with less than the ‘man-of-their-dreams’. Extra-pair copulations may then be an option to improve the genetic quality of the progeny. Zoom Image
Female blue tits (Parus caeruleus) choose a single social partner. This male defends a territory with a nestbox, and he provides help with offspring care. Since many females compete for only a few vacant males with territories, some of them will end up with less than the ‘man-of-their-dreams’. Extra-pair copulations may then be an option to improve the genetic quality of the progeny. [less]

According to evolutionary biologists, females looking for the optimal sire of their young should consider their options. It pays to be on the lookout for males with ‘good genes’, those that are healthier or more attractive than others. These genes will then be passed on to the females’ offspring and provide them with equally successful attributes. ‘Good genes’ may code for high competitiveness, high viability, good resistance against parasites and pathogens, or high attractiveness to females. However, offspring fitness does not only depend on particular paternal genes, but also on the interactions between the paternal and maternal genome. A good example is the adverse effects of inbreeding, that is, matings with related and therefore genetically similar individuals. Such partners are likely to possess similar alleles at many genes. Their young are of low heterozygosity (i.e. at many genes, they inherited the same allele from both mother and father) and suffer from reduced survival and reproductive success. Hence, females should not only seek ‘good genes’, but also compatible (genetically dissimilar) partners.

The Max Planck team from Seewiesen spent four years in the Viennese forest investigating social pairing and genetic paternity in a population of blue tits. Back in the laboratory in Seewiesen, the scientists determined individual genetic diversity of the nestlings using microsatellite markers. The first path-breaking result of this study was that extra-pair young were more heterozygous (i.e. they possessed more different alleles) than their half-siblings sired by the social father. This was because about half of all extra-pair young were sired by males that were not breeding nearby. The Max Planck scientists found that distantly breeding males were always less related to a female than her social partner or her closest neighbours. Due to this genetic structure in the population, females can make sure that extra-pair copulations with distant males will lead to more heterozygous young than those sired by her social mate.

The positive effect of individual heterozygosity on blue tit fitness was the second important result of this study. By closely monitoring the study population over several years, the scientists found that young birds that survived their first winter and subsequently bred in their native area were more heterozygous than their non-surviving nest mates. This is a crucial advantage, considering that from an average brood of eleven, only one or two blue tit youngsters ever make it to the next spring.

These blue tit siblings share the nest, but not the genetic father. Shortly before fledging they all look equally well developed, but the first winter will separate the chaff from the wheat: those, whose parents were genetically less similar, have a much better chance to survive. Zoom Image
These blue tit siblings share the nest, but not the genetic father. Shortly before fledging they all look equally well developed, but the first winter will separate the chaff from the wheat: those, whose parents were genetically less similar, have a much better chance to survive. [less]

Individual genetic diversity also had effects later in life: more heterozygous adult females produced larger clutches and lived longer. Heterozygous males were more successful in raising their young to fledging, and, ultimately, produced more surviving offspring. Finally, males appeared to advertise their genetic diversity through a secondary sexual signal. Each time a blue tit male was caught to take body measures, to mark him with a unique combination of coloured leg bands, and to take a small blood sample for DNA-extraction, the scientists also recorded the reflectance spectrum of the plumage using a spectrometer. In combination with the genetic data, these measurements showed that the crown feathers of more heterozygous blue tit males reflected stronger in the UV-wavelength range than those of their genetically less diverse colleagues.

Only recently, scientists proposed that the blue tit should rather be called the ‘UV tit’: the crown plumage, brightly blue to the human eye, has its peak reflection in the UV part of the spectrum. To a blue tit with UV-vision, the blue crown must appear quite different. Indeed, earlier studies suggested that females use the variation among males in this specific wavelength range as a quality signal during mate choice. The positive correlation between UV-reflection and individual heterozygosity supports this view.

"The study in the Austrian blue tit population showed convincingly that females increase the heterozygosity of their progeny through extra-pair matings with distantly breeding males. They thereby produce offspring of higher reproductive value, because heterozygous blue tits have better survival chances and a higher reproductive success", says Bart Kempenaers, head of the Junior Research Group. This leaves us with one question: What is the adaptive advantage of the second half of extra-pair young, those that were sired by close neighbours? The Max Planck team was able to confirm a previous result from a Belgian study population: females preferred neighbours for extra-pair copulations that were larger and older than the social mate. Larger males are likely to have a competitive advantage, and old age is a good signal of viability; these qualities will probably be inherited by the male’s progeny. This evidence of female choice for ‘good genes’ was only apparent in close neighbours, but not in distantly breeding extra-pair fathers. Thus, this study is the first to show that two mechanisms may lead to the evolution of female promiscuity in socially monogamous species - the advantage of ‘good genes’, as well as the advantage of inbreeding avoidance (or the benefits of heterozygosity).

Research on the evolutionary origin and consequences of male and female promiscuity are the focus of the Junior Research Group at the Max Planck Research Centre for Ornithology.

 
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