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Evolutionary genetics of guppy sex chromosomes

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The unexpected origin of guppy sex chromosomes

Rather than conflict between the sexes promoting the evolution of a Y chromosome, GUPPYSEX reveals that a recently evolved new Y chromosome allowed male-beneficial/female-detrimental colouration mutations to accumulate on the Y.

Fundamental Research icon Fundamental Research

Most of an organism’s genetic material is inherited as chromosome pairs, one from each parent. During sperm and egg formation, most chromosomes, called ‘autosomes’, exchange genes (‘recombine’) with their partners. However, the sex chromosomes, which determine whether an organism is male or female, are inherited differently. In many species, including most mammals, females inherit two X chromosomes, one from each parent, just like the autosomes. Males, however, are XY – they inherit an X from their mother, but fathers pass their Y to sons. The Y and X chromosomes do not recombine in males, except in small ‘pseudo-autosomal’ regions (PARs), and the lack of exchanges eventually leads to the Y losing genes (becoming ‘degenerated’). The human Y chromosome has lost about 98 % of the roughly 1 000 genes carried on the X. The GUPPYSEX project at the University of Edinburgh used a small fish, the guppy, to test whether conflicts between the sexes can explain loss of exchanges between sex chromosome pairs. The project was funded by the European Research Council.

Sexual antagonism

In many species, the sexes differ, sometimes markedly. Such differences suggest that some characteristics that are good for males are bad for females, or ‘sexually antagonistic’. For example, Darwin’s theory of sexual selection suggests that large antlers, while benefiting males competing with rivals, could reduce females’ breeding success. “We chose to study guppies because they show such conflicts. Brightly coloured males get the largest numbers of matings, but brightness increases predation on females. Colouration mutations are therefore most likely to spread in a population if they are inherited only by males, disfavouring exchanges between the X and Y chromosomes,” explains Deborah Charlesworth, coordinator of the GUPPYSEX project.

Sex differences in recombination

The GUPPYSEX team obtained genome sequences and used molecular markers to make genetic maps in parents of both sexes. This revealed that genetic recombination during sperm formation occurs only at the tip of each of the 23 guppy chromosomes. For the XY pair, the lack of exchanges across most of the chromosome means that most of the Y is retained as male-only – sons inherit their fathers’ Y, and Y sequences are rarely, if ever, transmitted to female progeny. “So, instead of suppressed recombination evolving in response to sexual antagonism (SA), as was previously thought, male guppies already lack recombination across most of their chromosomes,” Charlesworth adds. “This would have allowed the recent evolution of a new Y chromosome, carrying a new male-determining factor, and SA colouration genes could then accumulate on this chromosome.” GUPPYSEX’s finding of extensive chromosome regions that rarely recombine in males chimes with recent results from other organisms.

Implications and next steps

GUPPYSEX’s findings contribute to a better understanding of genetic differences between the sexes. Such understanding is valuable in medicine, to help explain sex differences in disease liability. It is also useful for agriculture, for the early determination of sex in animals or fruit crops, and for controlling pests, to target one sex for sterilisation or elimination. “As the guppy Y chromosome probably evolved from an ancestral X, its genes should have started adapting to being predominantly in males. It will be interesting to test whether genes on the sex chromosomes are evolving differently from autosomal ones,” concludes Charlesworth.

Keywords

GUPPYSEX, guppy, chromosome, sex, recombination, genetic, autosome, degenerated, male, female, Darwinian, sexual antagonism

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