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.genetic parentage | monogamy B ateman's study (1) of within-sex selection in Drosophila melanogaster is a foundational paper in sexual selection, second only to Darwin's pioneering book (2); it empirically anchored within-sex variance in number of mates (V NM ) as a key correlate of variance in reproductive success (V RS ) and as the metric of sexual selection. Bateman said his results showed that male number of mates (NM) was more variable than female NM; male reproductive success (RS) was more variable than female RS; and RS in males, but not in females, was because of NM. His conclusions were: sexual selection acted primarily on males through female choice and through male competition and profligacy in mating, so that some males mated more frequently than others, producing higher V RS among males than among females because of the positive relationship between number of mates and reproductive success for males, but not for females.Bateman's (1) paper was cited relatively infrequently before its rediscovery by Trivers (3), who used Bateman's results to buttress his arguments that the sex-differential cost of reproduction selectively favored coy, discriminating females and competitive, ardent males. After Trivers (3), citation of Bateman soared (4), as it did again after Arnold (5) discussed "Bateman's Principles" as corollaries of sex differences in behavior and fitness variances. Given its paradigmatic status, Bateman's paper has inspired further studies of V NM and V RS (6, 7), many o...

Repetition of Bateman challenges the paradigm

“…Taken together, all the preceding studies, along with the replicate by Gowaty et al (7) in PNAS, suggest that, at best, Bateman's principles should be considered hypotheses and approached with great care. For example, it is fairly common for studies of Bateman gradients to disregard alternative explanations, including the null hypothesis that stochastic and nonheritable factors can produce results similar to Bateman's (5,20).…”

“…Although Bateman's results have been repeatedly questioned since the 1980s (e.g., 3-6), there had been no known attempt to replicate his study. A paper by Gowaty et al (7) in PNAS repeats Bateman's experiments, using the same Drosophila strains and methodology employed in the original study. The authors report that they cannot confirm Bateman's conclusions and find no evidence for sexual selection.…”

Bateman's principle is reversed in a cooperatively breeding bird

“…selection on traits used to increase social status or gain access to resources related to reproduction [17]) could still be occurring in this and other cooperatively breeding species, mutual sexual selection seems to be important. Bateman's classic work on Drosophila has recently been challenged [18], and the significance of positive Bateman gradients in females has been questioned [5]. Instead of reflecting selection on females to mate multiply, positive female Bateman gradients could result from males targeting fecund females, the increased likelihood of extra-pair mate detection with increases in brood size, or iteroparous mate resampling [5].…”

Genetic analysis of human extrapair mating: heritability, between-sex correlation, and receptor genes for vasopressin and oxytocin

“…There have been proposed a number of adaptive explanations for female extrapair mating, along with challenges to the traditional theoretical and empirical basis for the expectation of sex-differentiation in adaptation for extrapair mating (Gowaty et al 2012;Gowaty 2013). The dominant explanation of female extrapair mating has been that it can be adaptive if females are able to obtain extrapair mates of higher genetic quality than their social mates, thereby increasing the genetic quality of their offspring and increasing their number of grandoffspring (Jennions and Petrie 2000;Neff and Pitcher 2005).…”