Male fitness increases when females are eliminated from gene pool: implications for the Y chromosome

Abstract

Because the two sexes share a common gene pool while performing many different biological functions, mutations benefiting one sex may not accumulate due to counter selection in the other sex. In these experiments 99% of a haploid genome of Drosophila melanogaster was constrained to segregate like a male-limited Y chromosome for 41 generations, thereby eliminating potential counter selection in females. The synthetic Y chromosomes rapidly accumulated genetic variation that increased male fitness and decreased female fitness. The survival and fertility of females declined when they were mated to males expressing the synthetic Y chromosomes. These results suggests that opposing selection between the sexes may substantially interfere with sex-specific adaptation. They also demonstrate how intersexual evolutionary conflict can lead to perpetual degeneration of the Y via genetic hitchhiking of deleterious mutations.

Figure 1

Males expressing synthetic Y chromosomes (line EAB) surpass controls (CAB) in all fitness measures except defense. (a) Mating speed is faster for the experimental males (P = 0.008, directed (24) conditional binomial exact test (25, CBET). (b) Remating rate is higher for the experimental males [▪, histograms from generation 38; □, histograms from the net offense assay in generation 40; P = 0.0002, directed, consensus P value (26) for the three χ² contingency tests]. (c) Defense is the same for experimental and control males (P = 0.40, directed χ² contingency test). The histogram tallies families from individually cultured females that had been first mated to EAB (▪, n = 147) or CAB (□, n = 152) males for 1 hr and then housed with p^P competitor males for 24 hr. Families were divided into four discrete categories grading from low defense (all pink, females remated to the p^P competitor males and no progeny produced from the first male’s sperm) to high defense (all red, no progeny produced from the p^P competitor males). (d) Offense is higher for experimental (EAB) than control (CAB) males (P = 0.016, directed χ² contingency test). The histogram tallies percent of families from individually cultured females, that had been first mated to p^P competitor males for 1 hr and then housed with EAB (▪, n = 145) or CAB (□, n = 149) males for 24 hr. Families were divided into four discrete categories grading from low offense (all pink, progeny exclusively derived from the p^P competitor males’ sperm and none from remating with the experimental or control males) to high defense (all red, females remated to experimental or control males and no progeny produced from the p^P competitor male’s sperm).

Figure 2

Females expressing the experimental, synthetic Y chromosomes have retarded development, but no other reductions in fitness. (a) The fraction of females emerging vs. time since eggs were laid, for females expressing a synthetic Y from experimental EA (N_{G = 29} = 107, N_{G = 30} = 143) and EB (N_{G = 29} = 130, N_{G = 30} = 153), or control CA′ (N_{G = 29} = 114, N_{G = 30} = 141) and CB′ (N_{G = 29} = 126, N_{G = 30} = 148) males. The fraction of females emerging by day 10 is significantly lower in the experimental lines (P_{G = 29} = 0.0163, P_{G = 30} = 0.0161, directed Student’s t tests, df = 2). (b) The total number of adult offspring (measures net female fitness independent of development time) produced by EAB or CAB females (red-eyed offspring) in competition with tester-females (pink-eyed offspring). There is no significant difference between lines (P = 0.625, directed χ² contingency test).

Figure 3

Mortality and sterility are higher for females mated to experimental EAB compared with control CAB males. (a) Cumulative numbers of dead tester-females when mated to, and continuously housed with, experimental or control males. Mortality is significantly different at day 4 and beyond (P ≤ 0.035 in all cases, directed CBET). (b) Number of sterile and dead females, from offense or defense assays (Fig. 2), that had previously been mated to EAB or CAB males. Statistical significance was determined via a multiple modulus test (27). This is a hierarchical-staged test that proceeds, in a priori order and conditioned on the previous test being significant, from global to more specific tests. Net harm (mortality + sterility) to females, pooling across offense and defense tests, was greater from experimental (EAB) than control (CAB) males (P < 10⁻⁶, directed CBET). This same pattern was manifest in both the defense test (P = 0.024, directed CBET) and the offense test (P = 0.05, directed CBET). Focusing next on specific types of harm to females, and first pooling data from both offense and defense tests, both sterility and mortality were higher for females exposed to EAB experimental males (P < 0.037 for both tests, directed CBET). Neither mortality nor sterility were individually significant when testing the offense and defense data individually.

Figure 4

Model for the degeneration of the Y via chase-away antagonistic coevolution between the sexes. Males are assumed to be the heterogametic sex. A parallel chase-away process can ensue that is driven by antagonistic coevolution between male offense and defense phenotypes or other forms of interlocus contest evolution (18).