No evidence of sexual selection in a repetition of Bateman's classic study of Drosophila melanogaster

Abstract

We are unique in reporting a repetition of Bateman [Bateman AJ (1948) Heredity (Edinb) 2:349-368] using his methods of parentage assignment, which linked sex differences in variance of reproductive success and variance in number of mates in small populations of Drosophila melanogaster. Using offspring phenotypes, we inferred who mated with whom and assigned offspring to parents. Like Bateman, we cultured adults expressing dramatic phenotypes, so that each adult was heterozygous-dominant at its unique marker locus but had only wild-type alleles at all other subjects' marker loci. Assuming no viability effects of parental markers on offspring, the frequencies of parental phenotypes in offspring follow mendelian expectations: one-quarter will be double-mutants who inherit the dominant gene from each parent, the offspring from which Bateman counted the number of mates per breeder; half of the offspring must be single mutants inheriting the dominant gene of one parent and the wild-type allele of the other parent; and one-quarter would inherit neither of their parent's marker mutations. Here we show that inviability of double-mutant offspring biased inferences of mate number and number of offspring on which rest inferences of sex differences in fitness variances. Bateman's method overestimated subjects with zero mates, underestimated subjects with one or more mates, and produced systematically biased estimates of offspring number by sex. Bateman's methodology mismeasured fitness variances that are the key variables of sexual selection.

Fig. 1.

(A) The distribution of differences in RS of parent (fathers minus mothers) is significantly different from zero. RS for mothers was Σ M^♀M^♂+ w^♀M^♂ and for fathers was Σ M^♀M^♂+ w M^♂. The actual estimate of difference in the repetition is 6.4 ± 15.67 (SD), df = 45, t test = 2.784, P > |t| = 0.0078 and signed-rank test = 226, P > |t| = 0.0091. It is logically impossible in sexual diploid species for more offspring to have fathers than mothers. Bateman’s method of estimating RS produced a systematic bias with males having more offspring than females, a bias that could have inappropriately decreased the estimate of maternal RS, producing inaccurate estimates of sex differences in “Bateman gradients” (4). There were seemingly more fathers’ children than mothers’ children in Bateman’s original experiment as well. (B–D) The frequency distributions of double-mutant (M^♀M^♂ indicated by white bars), single-mutant (M^♀w^♂ indicated by light gray bars and w^♀M^♂ indicated by dark gray bars), and no mutant (w^♀w^♂ indicated by black bars) offspring in 46 trials that replicated Bateman. Frequencies of offspring mutant combinations in each population are in Tables S10–S13. Parent marker sets: (B) ♀♀ = Pm, H, Mé and ♂♂ = B, Cy, Mc; likelihood ratio χ² = 260.5, df = 3, P < 0.0001. (C) ♀♀ = Hw, Pm, Sb, H, Mé and ♂♂ = B, Cy, ap^Xa, Bl, Mc; likelihood ratio χ² = 157.1, df = 3, P < 0.0001. (D) ♀♀ = B, Cy, Mc and ♂♂ = Pm, H, Sb; likelihood ratio χ² = 89.1, df = 3, P < 0.0001. Within each marker set and for almost all populations there were significantly fewer than 25% double-mutant offspring, indicating that offspring inviability confounded estimates of NM and V_NM (see also Table S9), potentially biasing any estimates of Bateman gradients.