I HAVE ALREADY mentioned one type of selfish genetic element. These are mobile elements that can move about and reproduce within the genome, and include the transposon and retrotransposons. A second similar type of selfish genetic element are the homing endonucleases. These come in two forms, as introns which are spliced out of RNA and then translated into protein instead of being discarded, or as inteins that splice out of the protein once it has been synthesized. In both cases the homing endonuclease then during meiosis attacks the allele that does not contain the homing endonuclease intron or intein and triggers DNA repair that duplicates the homing endonuclease’s sequence. Since mobile elements and homing endonucleases either attack at a wide variety of sites or duplicate onto both of a pair of chromosomes, they are passed on according to Mendelian inheritance patterns. But there are other selfish genetic elements that are passed on preferentially, and a new paper in Genetica focuses on the effects of these selfish elements upon fertility in carrier males.
Some selfish genetic elements are able to manipulate cellular processes using a process called meiotic drive, which produces a ratio of carrier gametes greater than 50%. Sometimes this is done by the production of a toxin that kills gametes not carrying the selfish element. Gametocidal elements tend to be carried by males, since the destruction of sperm or pollen is less costly than the destruction of much larger and fewer eggs. Other selfish genetic elements take this tactic a step further by killing offspring early in development that lack that selfish element. Selfish elements that utilize meiotic drive are often nuclear elements. These are usually either sex chromosomes (which will skew the sex ratio of the offspring) or autosomal chromosomes, but other times may be B chromosomes, parasitic chromosomes that provide no benefit to the host.
There also are cytoplasmic factors that are passed only from a mother to her offspring due to the larger cytoplasmic volume of eggs compared to sperm or pollen. An interesting twist on this is the way that many of these cytoplasmic elements have evolved the ability to kill male offspring, since selection on these selfish elements disfavors maternal investment in male embryos if it occurs at the expense of carrier female embryos. Others instead feminize male offspring, causing them to develop as females. These male-killing and feminizing tactics are often used by one type of selfish genetic element that is actually a separate organism–Wolbachia bacteria, which are arthropod intracellular parasites that are transmitted only via the egg.
According to Price and Wedell’s compilation of studies, males carrying selfish genetic elements that are lucky enough not to be killed or converted into females still suffer a decrease in fertility. This seems to be due to a combination of a variety of factors. In the case of a sex-linked driving selfish element, females not carrying that element are under selection for avoidance of male carriers because this avoidance increases their number of male offspring. Sex-linked meiotic drive produces a skewed sex ratio, with many females and few males. Since males are scarce, females producing a larger proportion of male offspring will enjoy higher fitness as their sons produce more offspring. Even when a male carrying a driving X-chromosome does mate, studies from a variety of species show his sperm seem to succeed in fertilizing an egg less often than expected. This may be due to detrimental side-effects to X-carrying sperm during gametocide of Y-carrying sperm. In other cases this decrease in fertility may be accidental, the result of a male carrying mitochondria with a selfish genetic element that is beneficial to females but detrimental to males. Since mitochondria are passed down only in the egg and not in sperm, they are susceptible to selfish elements favoring daughters, although not necessarily male-killing. However, mitochondrial elements with an anti-male bias are favored in hermaphroditic species, and are often found in plants where they prevent the production of pollen while increasing the production of seeds, which pass these mitochondria on to their offspring. Even selfish genetic elements on autosomal and B chromosomes cause a reduction in male fertility, although the reason for this is not clear. It may again be related to the mechanisms used to distort the inheritance ratio of that chromosome.
It has been proposed that successful sperm competition to weed out sperm from males carrying selfish genetic elements generates positive selection for polyandry across multiple species. There is some evidence from Drosophila (fruit flies) that females that do mate with males carrying selfish genetic elements then breed again more rapidly. Since sperm from males with selfish elements seem to typically have decreased fitness, this could have evolved due to a decrease in the female’s risk in case of accidental mating with a carrier male.
The authors note that selfish genetic elements are often carried by sperm, and that mutations increasing the number of sperm produced should increase the success of selfish genetic elements if not balanced out by the decrease in success of these sperm.
The question is whether this advantage is counterbalanced by the reduction in fertility experienced by sperm affected by SGEs [selfish genetic elements], which, as we have argued, may promote polyandry (and hence increase sperm competition). The key to this paradox is likely to be the relative frequency of SGE-carrying males in the population, which may determine the degree of polyandry, coupled with the cost to these males in terms of paternity reduction in sperm competition. The outcome is likely to be dynamic and may result in either stable polymorphisms or cyclical changes in frequency of SGEs and polyandry between populations (e.g. stable frequencies of SR [sex ratio] and polyandry in D. pseudoobscura populations (Dobzhansky and Epling 1944; Beckenbach 1996)), although this situation clearly needs to be modelled. Nevertheless, despite the diversity of SGEs, it is clear they adversely affect male fertility, thus providing a potential mechanism favouring polyandry.
Polyandry is insufficiently explained in many populations, and exploring selfish genetic elements in these populations may shed light on the selective forces behind this behavioral pattern.
Price, T.A., Wedell, N. (2008). Selfish genetic elements and sexual selection: their impact on male fertility. Genetica, 132(3), 295-307. DOI: 10.1007/s10709-007-9173-2