Matings between relatives have negative consequences for the offspring, a phenomenon known as inbreeding depression. But what if you end up with a related partner? Initiated by a scientist at the Max Planck Research Centre for Ornithology, a study by an international team of scientists showed that social mates that are genetically similar use alternative reproductive behaviors to avoid paying the price of inbreeding. Combining field observations on free-living populations of three shorebirds with molecular methods to determine parentage and relatedness between the partners they found that extra-pair parentage occurred when mates were more closely related (Nature, Oct. 10th, 2002).
Over the past decade, the use of molecular techniques to determine parentage has led to the realization that monogamy is rare in nature. Although most bird species are socially monogamous, broods often contain young that are not related to one of the parents tending the nest. This can be the result of two alternative reproductive behaviors. Extra-pair paternity occurs when females copulate with males other than their social partner, and these copulations lead to fertilizations. Extra-pair paternity is common in songbirds, but much less common in other birds. Quasi-parasitism occurs when a male copulates with another female, who then lays one or more eggs that he fathered in his nest. This is a rare and little understood phenomenon. The reasons why birds are unfaithful to their social partner, with whom they raise the offspring, has been the focus of much debate. A scientist at the Max Planck Research Centre for Ornithology initiated a study on parentage in shorebirds, and in collaboration with researchers at the Konrad Lorenz Institute for Comparative Ethology in Vienna, combined data on three species from three continents. An international team of scientists studied populations of marked individuals in the field and closely monitored their breeding behavior. Based on blood samples from parents and offspring, and using DNA-fingerprinting techniques, they found that extra-pair paternity and quasi-parasitism occurred at low frequencies. More importantly, however, in each of the three species, extra-pair parentage occurred when the parents were more related to each other.
In this way, the study links the occurrence of alternative reproductive strategies with the phenomenon of inbreeding depression. It is well established that if close relatives mate, they suffer reduced breeding success, probably because deleterious recessive alleles are expressed. This suggests that natural selection will favour the avoidance of matings between genetically similar individuals. However, in practice this is not always possible, for example because there are no alternative mates available. The study on the three shorebird species now suggests that females seek extra-pair copulations to avoid inbreeding depression or other negative effects of genetic similarity. Moreover, it provides a similar explanation for the evolution of quasi-parasitism, suggesting it is a male-driven strategy.
The study leaves us with an intriguing implication: males and females must be able to assess how genetically similar they are to their social mate and to potential extra-pair partners. There is evidence from a study on peacocks that males can assess the relatedness to other males, even if they could not use social learning or other environmental cues (e.g. if they would have been raised in the same nest). The challenge of future research will be to determine which cues birds use to assess relatedness with a potential mate or copulation partner.
Another intriguing possibility that can explain why extra-pair paternity occurs when mates are more related has to do with the mechanism of sperm competition. If most females copulate occasionally with other males, then sperm of the social mate and the extra-pair males will be mixed in the female reproductive tract and compete for fertilization of the eggs. If the genetic similarity with the female (or the egg) reduces the competitiveness of sperm, then an extra-pair male might have a much higher chance of fertilizing an egg when pair members are closely related.
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.