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.

Bateman's Data: Inconsistent with “Bateman's Principles”

“…Our analysis tactics were inspired by the multiple challenges to AJB's methods noted in Sutherland (1985), Snyder and Gowaty (2007), and Gowaty et al. (2012, 2013).…”

“…To determine whether the data in each population reliably informed questions about the NM and RS of each subject, we used likelihood ratio chi‐square tests in each population to evaluate consistency with the expectations from a Punnett square (Table 3) of the frequencies of offspring phenotypes given possible parental genotype/phenotypes (Table 1) (see discussion in Gowaty et al. (2012, 2013)). In addition, for each population, we also tested whether the number of assigned mothers and fathers was statistically similar (Table 3) as they must be in diploid species.…”

“…(2012), Gowaty, Kim, and Anderson (2013) replicated AJB's original study using the same fly lines AJB had used. The replication (Gowaty et al., 2012, 2013) had 46 populations with 5 males and 5 females or with 3 males and 3 females similar to AJB's original set up, and it produced 8,093 offspring (Bateman's 65 populations produced 9,951 offspring). In the repetition, fathers' nametags appeared in offspring significantly more frequently than mothers' nametags, contrary to the expectation in diploid species that parental nametags should occur at similar frequencies for both sexes of parent.…”

“…To find out, Gowaty et al. (2012), Gowaty, Kim, and Anderson (2013) replicated AJB's original study using the same fly lines AJB had used. The replication (Gowaty et al., 2012, 2013) had 46 populations with 5 males and 5 females or with 3 males and 3 females similar to AJB's original set up, and it produced 8,093 offspring (Bateman's 65 populations produced 9,951 offspring).…”

“…AJB carefully alerted readers to a potential problem in his method of assigning NM when he said “ assuming the complete viability of all the markers, half the progeny of each fly would be identified” (p. 353, Bateman, 1948), yet there is no evidence in his paper or in the laboratory note data that he tested the viability of the markers, either by calculation of expected distributions of types of offspring (see Table 2 above) or by monogamous control experiments (see Gowaty et al., 2012; Gowaty et al., 2013 for a description of control experiments) that had he done them, would have eliminated any possibility of intrasexual selection, but would have revealed that double‐mutant offspring were often absent, as was obvious in Bateman's original Table 4 (shown herein as Figure 2a,b). The inference from the large repetition and the monogamous control experiments (Gowaty et al., 2012, 2013) is that offspring inheriting both parental nametags often died before eclosion when parental nametags would express, thereby biasing estimates of NM and critically V NM : The repetition proved that AJB's assumption of “complete viability of all the markers” was false. Consideration of the missing offspring in the critical category of double‐mutant offspring in the repetition also proved that estimates of sex differences in V NM overestimated the NM of individuals with zero mates while underestimating the number of individuals with one or more mates.…”