Mendel's law reveals fatal flaws in Bateman's 1948 study of mating and fitness

Abstract

Bateman's experimental study of Drosophila melanogaster produced conclusions that are now part of the bedrock premises of modern sexual selection. Today it is the most cited experimental study in sexual selection, and famous as the first experimental demonstration of sex differences in the relationship between number of mates and relative reproductive success. We repeated the experimental methodology of the original to evaluate its reliability. The results indicate that Bateman's methodology of visible mutations to assign parentage and reproductive success to subject adults is significantly biased. When combined in offspring, the mutations decrease offspring survival, so that counts of mate number and reproductive success are mismeasured. Bateman's method overestimates the number of subjects with no mates and underestimates the number with one or more mates for both sexes. Here we discuss why Bateman's paper is important and present additional analyses of data from our monogamy trials. Monogamy trials can inform inferences about the force of sexual selection in populations because in monogamy trials male-male competition and female choice are absent. Monogamy trials also would have provided Bateman with an a priori test of the fit of his data to Mendel's laws, an unstated, but vital assumption of his methodology for assigning parentage from which he inferred the number of mates per individual subject and their reproductive success. Even under enforced monogamous mating, offspring frequencies of double mutant, single mutant and no mutant offspring were significantly different from Mendelian expectations proving that Bateman's method was inappropriate for answering the questions he posed. Double mutant offspring (those with a mutation from each parent) suffered significant inviability as did single mutant offspring whenever they inherited their mother's marker but the wild-type allele at their father's marker locus. These inviability effects produced two important inaccuracies in Bateman's results and conclusions. (1) Some matings that actually occurred were invisible and (2) reproductive success of some mothers was under-estimated. Both observations show that Bateman's conclusions about sex differences in number of mates and reproductive success were unwarranted, based on biased observations. We speculate about why Bateman's classic study remained without replication for so long, and we discuss why repetition almost 60 years after the original is still timely, necessary and critical to the scientific enterprise. We highlight overlooked alternative hypotheses to urge that modern tests of Bateman's conclusions go beyond confirmatory studies to test alternative hypotheses to explain the relationship between mate number and reproductive success.

Keywords: A.J. Bateman; Drosophila melanogaster; Mendel’s rules; fitness variances; genetic parentage tests; number of mates; number of offspring; reproductive success.

Figure 1. Bateman’s (1948) Table 4, p. 357 (reprinted by permission from Macmillan Publishers Ltd. License Number: 2960430598991), showed the logic of Bateman’s method for assigning parentage and thus inferring NM and RS per adult in a given population. The table is the only completely displayed data for any population in Bateman’s study. The tabled values are the number of offspring that carried a parental marker. The only offspring that allowed inference of NM were the double mutants—M^♀M^♂. In the table M^♀M^♂ offspring include the 13 that inherited the mother’s CyL dominant gene and the father’s Sb dominant gene, and so on. To estimate the number of offspring that each mother produced, he took the sum of their M^♀M^♂ + M^♀w^♂ offspring and for each father he took the sum of their M^♀M^♂ + w^♀M^♂ offspring. Most important, however, is that from the data in this table one can compute the frequencies of M^♀M^♂, M^♀w^♂, w^♀M^♂ and w^♀w^♂ and compare them to Mendel’s expectations under the assumption that each adult was a dominant heterozygote at a unique locus and homozygous wild type at every other adults marker loci. The values are a significant departure from Mendelian expectations with M^♀M^♂ significantly fewer than 25%.

Figure 2. A cartoon of the even frequencies of offspring phenotypes when parents are unique heterozygote dominants each at a unique locus. Drosophilist Sergio Castrezana, PhD, painted the image styled as Mayan-like hieroglyphs in a Mexican bark painting in black ink and acrylic on amate paper.

Figure 3. A stylized view of offspring genotypes (A) and observable offspring phenotypes (B) when each parent is a heterozygote dominant at a unique marker locus and wild type at the other parent’s marker locus. In both panels capital letters indicate dominant alleles and lower case indicates wild-type alleles for two parents each with a dominant marker allele each at a different locus. The male’s maker locus is indicated by “B” and the female’s by “R.” Wild-type alleles at mother’s marker locus are indicated by lowercase, “r” and at father’s marker locus by lowercase “b.” In (B) the bolded letters indicate visible mutations.

Figure 4. Subjects seemingly without mates had offspring, which is highly unlikely in a sexually reproducing diploid species. Reproductive success counted as the sum of M^♀M^♂ plus M^♀w^♂ for female subjects (A) and as M^♀M^♂ plus w^♀M^♂ for male subjects (B) against the number of mates counted from M^♀M^♂ offspring for females (A) and for males (B) exposes a biological impossibility. Bateman’s method overestimates the number of individuals with zero mates (21 subjects among females and 43 among males), thereby underestimating the number with one or more mates. The magnitude of error among male subjects (43 males out of a total N of 166 males) was greater than among female subjects (21 females out of a total N of 166 females), which would have falsely increased the V_NM estimates of males relative to females. We use these plots to illustrate one of the most egregious errors in Bateman’s method: subjects who seemed to have no mates had offspring.

Figure 5. Frequencies of M^♀M^♂, M^♀w^♂, w^♀M^♂ and w^♀w^♂ offspring from monogamy trials (5 sets for each parental marker combination). The column on the far left identifies the offspring types: White bars = M^♀M^♂, light gray bars = M^♀w^♂, dark gray bars = w^♀M^♂ and black bars = w^♀w^♂.

Figure 6. The difference in the number of offspring assigned to mothers and fathers computed from M^♀w^♂ and w^♀M^♂ offspring that individual adults confined in monogamous pairs produced. There were five trials of monogamous pairs in each parental combination of unique markers. The distribution of difference scores was significantly different from 0 (t-test = −3.7004, DF = 24, p > |t| = 0.0011).