While it might seem as though our genes are all working together for our own good, some of them are actually rather selfish. Scientists have known about ‘selfish genetic elements’ for nearly a century, but research to understand their behaviour and effects is ongoing. Recent research in GEE reveals how sexually selected traits are signalling selfish genetic elements (or a lack of them) in the same way they are used to signal male quality and health.
Selfish Genes and the Balance of the Sexes
Selfish genetic elements are variants (alleles) of genes which, rather than acting to the benefit of the individual, act in their own interest to ensure maximum replication of themselves. One type of selfishness that genes can exhibit is called meiotic drive, and is associated with alterations to the sex ratio of offspring. Sex ratios for most species tend towards 1:1, for sound evolutionary reasons, but this isn’t in the best interest of all genes. Genes that lie on one of the sex chromosomes (X or Y in mammals, Z or W in birds) are not equally successful in both sexes – if you happen to lie on the X chromosome, for example, there’ll be two copies of you in each female offspring but only a single copy in male offspring. Meiotic drive occurs when selfish genetic elements skew the sex ratio in order to favour their own replication – usually caused by genes on the X chromosome creating a female-biased sex ratio.
Sex ratios tend to be roughly even in nature because offspring sex ratio is a trait that is under strong stabilising selection. In populations with a biased sex ratio, the underrepresented sex immediately becomes extremely valuable, simply by virtue of its rarity. Imagine a village consisting of 20 women and a single man – that man would undoubtedly have the pick of the ladies, and would likely produce more offspring. If you are the mother of that male, you’ll have done very well for yourself. In a population with a skewed sex ratio, offspring of the underrepresented sex are more valuable, and natural selection to produce them is very powerful. Any mechanism by which females could identify a male that will produce these valuable offspring would be strongly favoured by selection.
Stalk-eyed flies are found in Africa and Southeast Asia and show striking sexual dimorphism (physical differences between the sexes). Both males and females have their eyes placed on the end of long stalk-like appendages, but in males these ‘stalks’ can be very long. This is a sexually selected trait – males with longer eyestalks are healthier, carry fewer harmful mutations and are better at attracting females, meaning they tend to have more offspring.
In the laboratory, stalk-eyed flies often produce very female-biased broods; this is thought to be a result of meiotic drive that causes male sperm (carrying a Y chromosome) to degenerate, but female sperm (carrying an X chromosome) to persist. Researchers believe that the length of eyestalks may be linked to meiotic drive, and long-eye stalks may signal to females that a male does not carry the harmful selfish allele. In the laboratory, it has already been shown that males selectively bred for short-eye spans tend to produce female-biased broods, and four loci on the X-chromosome have been identified that are associated with female-bias.
Beyond the Laboratory – Tests in Wild Populations
Expanding on this research, academics in GEE wanted to investigate this phenomenon in the wild. Their work, recently published in Heredity, investigated eyespan and sex ratio biases in 12 populations of wild stalk-eyed flies in Malaysia. Dr Alison Cotton and colleagues at UCL and the University of Debrecen, Hungary, collected nearly 500 wild stalk-eyed flies, measured their eyestalks and other physical characteristics, and collected DNA samples. The researchers used a technique known as microsatellite genotyping to identify regions of the X-chromosome where genes responsible for meiotic drive and for eyestalk length were located. Microsatellites are repeating DNA sequences that tend to vary in their length (the number of repeats) between individuals. Microsatellites can be used as genomic markers for nearby genes of interest – we expect that different microsatellite alleles will be consistently associated with different alleles of interesting genes nearby. Because they vary in physical length, microsatellite alleles can easily be identified by separating DNA sequences out according to size.
The authors found that one microsatellite, ms395, was strongly associated with male eyestalk length. This relationship was not found in females. Longer ms395 alleles tended to be associated with smaller male eyespans.
Males collected from 5 wild populations were taken back to the lab where they were allowed to mate, so that researchers could investigate the sex ratio of their offspring. Around a quarter of wild-caught males produced biased sex ratios, most often producing more females than males. Males producing sex-biased offspring tended to have smaller eyestalks, when their overall body size was controlled for. They also tended to have longer ms395 alleles.
The authors were able to show that microsatellite ms395 is associated both with sex ratio biases and with male eyestalk length, suggesting that the genes controlling eyestalk length and meiotic drive are located on the X-chromosome near ms395, and that eyespan may be a signal of the genetic quality of the male. For females, a male that carries a selfish genetic element that causes meiotic drive (and a lack of male offspring) is of poor genetic quality, but by preferentially mating with males with longer eyestalks, females can avoid these harmful genes. This may indicate that eyestalks are an example of the good genes hypothesis for sexual selection, which suggests that physical characteristics involved in mate choice are associated with alleles that produce high quality males and are therefore used as an honest signal of the quality of potential mates.
This study is the first to demonstrate meiotic drive in wild populations of the stalk-eyed fly (Teleopsis dalmanni) and adds strong support to previous research suggesting that male eyestalk length is a signal of the presence of meiotic drive. As long as these genes remain in close proximity to each other through evolutionary time, the association should be maintained and eyestalks can be used as a reliable way for females to identify good quality males. Or at least males that are likely to give them a nice even sex ratio in their offspring.
This research was made possible by funding from the Natural Environment Research Council (NERC), the Engineering and Physical Sciences Research Council (EPSRC) and Marie Curie Action.