Inheritance asymmetry

The inheritance symmetry is known to be broken in two contexts. First, some nuclear genes, such as those on the sex chromosomes, are transmitted more effectively through one sex (Hamilton 1967).Y chromosomes that are able to bias the sex ratio towards the heterogametic sex (XY males in mammals) should be favoured over those that do not, because the homogametic sex (XX females in mammals) never transmits them. Similarly, the X chromosome will be favoured by a bias towards the homogametic sex, but not as strongly since it is also transmitted through the heterogametic sex (only half as efficiently).

These so-called driving sex chromosomes, or meiotic drivers, are now known from a number of organisms. Most, like 'segregation distorter' in Drosophila fruit flies, are X chromosomes that cause female bias. One possible reason is that Y chromosome drive is likely to be very strong and may cause extinction of a population (through elimination of one sex) before counter-measures can evolve. Driving Y chromosomes will therefore usually not persist long enough to be observed. Countermeasures may come from modifier genes on other chromosomes that suppress the action of the driver gene. In the fly Drosophila simulans, X-linked drive is suppressed by modifier genes on the Y chromosome and all the major autosomes (see Capillon and Atlan 1999).

Other, non-nuclear genetic elements can also select for sex ratio bias. Mitochondria are cytoplasmic organelles originating from symbiotic bacteria (see Chapter 2). They are inherited only through eggs which carry the cytoplasm for the zygote. In plants, mitochondrial mutants are responsible for the phenomenon known as cytoplasmic male sterility (CMS), whereby otherwise cosexual plants become entirely female (see Saumitou-Laprade et al. 1994). CMS is common in agricultural plants, such as maize, rice, sunflowers, and beans. Many insects similarly possess a symbiotic bacterium called Wolbachia, which is cytoplasmically inherited (Figure 5.3). Wolbachia can have several effects on insects, including the production of all-female lines (parthenogenesis). Incredible evidence for this first came when males were discovered for the first time in some parasitic wasp species after adding antibiotics to their diet, which killed the Wolbachia (Stouthamer et al. 1990). Another class of maternally inherited microbes are known as male-killers because of the way they achieve female biased sex ratios. They have been found in species in a number of insect orders, including wasps, beetles, butterflies, and flies. Wolbachia can act as a male killer in some insects and is responsible for producing the most extreme sex ratio biases known: in the butterfly Hypolimnas bolina, on Upolu island in Samoa (Figure 5.3). Ninety-nine per cent of individuals are female in this population (Dyson and Hurst 2004).

Fig. 5.3 (a) The butterfly H. bolina (wingspan 7 cm), whose sex ratios are extremely female biased due to male-killing. (b) Wolbachia (length 2 pm), shown here in an H. bolina egg. Photos courtesy of Greg Hurst.

Therefore, breaking the one-father one-mother symmetry frequently leads to sex ratio bias, as well as conflict between different genetic elements over the sex ratio. This is important as will be seen later in this chapter and later in the book, because conflict of interest may be a powerful driver of evolutionary change.

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