The Darwin-Bateman Paradigm in Historical Context

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Sperm are the most diverse of all animal cell types, and much of the diversity in sperm design is thought to reflect adaptations to the highly variable conditions under which sperm function and compete to achieve fertilization. Recent work has shown that these conditions often evolve rapidly as a consequence of multiple mating, suggesting a role for sexual selection and sexual conflict in the evolution of sperm design. However, very little of the striking diversity in sperm design is understood functionally, particularly in internally fertilizing organisms. We use phylogenetic comparative analyses covering 16 species of the hermaphroditic flatworm genus Macrostomum to show that a complex sperm design is associated with reciprocal mating and that this complexity is lost secondarily when hypodermic insemination-sperm injection through the epidermis-evolves. Specifically, the complex sperm design, which includes stiff lateral bristles, is likely a male persistence trait associated with sexual conflicts over the fate of received ejaculates and linked to female resistance traits, namely an intriguing postcopulatory sucking behavior and a thickened epithelium of the sperm-receiving organ. Our results suggest that the interactions between sperm donor, sperm, and sperm recipient can change drastically when hypodermic insemination evolves, involving convergent evolution of a needle-like copulatory organ, a simpler sperm design, and a simpler female genital morphology. Our study documents that a shift in the mating behavior may alter fundamentally the conditions under which sperm compete and thereby lead to a drastic change in sperm design.Platyhelminthes | sexually antagonistic coevolution | simultaneous hermaphrodite | sperm morphology | traumatic insemination P arker's (1-3) far-reaching extension of Darwin's (4) narrow focus on precopulatory mating interactions highlighted that sexual selection continues to operate after mating partners have agreed to mate and that considering postcopulatory sexual selection therefore is crucial to understand the evolution of many reproductive traits (5, 6). This insight has led to extensive research in evolutionary biology that focused on understanding the biology of sperm (7), the most diverse of all animal cell types (8,9). From this research emerged an apparent consensus that the diversity in sperm design-the strikingly variable ways of constructing a sperm-reflects the highly variable physiological and morphological environments in which sperm have to survive, function, and compete for fertilization (5,(10)(11)(12)(13)(14). Moreover, recent studies have documented clearly that these environments can evolve rapidly, probably because of coevolutionary interactions linked to multiple mating and the resulting sexual selection and sexual conflicts (15-21). However, the bewildering diversity in sperm design is poorly understood at the functional level, particularly in internally fertilizing organisms (9,12,22). A recent review on the evolution of sperm morphological diversity concluded...

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confidence: 99%

Mating behavior and the evolution of sperm design

Schärer

Littlewood

Waeschenbach

et al. 2011

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312

“…The beta distribution is convenient because a beta random variate takes values from 0 to 1, as fitness does, and a beta distribution can assume a very large diversity of shapes depending on its 2 parameters, nu () and omega (), from flat to strongly unimodal, left or right skewed, and even bimodal. We illustrate several possible fitness distributions in the analyses including beta (1, 1), which gives a uniform probability density from 0 to 1; beta (8,3), which is skewed to high values; beta (3,8), which is skewed to low values; and beta (5,5), which has a strong central tendency. Note that although we use a beta probability density function in the SPT, there is no necessity for the w distribution to be beta for the SPT to be valid.…”

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confidence: 99%

Reproductive decisions under ecological constraints: It's about time

Gowaty

Hubbell

2009

105

119

The switch point theorem (SPT) is the quantitative statement of the hypothesis that stochastic effects on survival, mate encounter, and latency affect individuals' time available for mating, the mean and variance in fitness, and thus, originally favored the evolution of individuals able to make adaptively flexible reproductive decisions. The SPT says that demographic stochasticity acting through variation in (i) individual survival probability, s; (ii) individual encounter probability, e; (iii) latency, l; (iv) the number of potential mates in the population, n; and (v) the distribution of fitness conferred, the w distribution, together affect average lifetime fitness, and induce adaptive switches in individual reproductive decisions. The switch point is the rank of potential mates at which focal individuals switch from accepting to rejecting potential mates, a decision rule that the SPT proves maximizes the average lifetime fitness of a focal individual under given values of ecological constraints on time. The SPT makes many predictions, including that the shape of the distribution of fitness conferred affects individual switch points. All else equal, higher probabilities of individual survival and encounter decrease the fraction of acceptable potential mates, such that focal individuals achieve higher average lifetime fitness by rejecting more potential mates. The primary prediction of the SPT is that each decision a focal individual makes is determined jointly by e, s, l, n, and the w distribution.demographic stochasticity ͉ encounter probability ͉ mate choice ͉ sexual selection ͉ survival probability

“…We conclude from our repetition of Bateman's experiment and from the evidence in his paper reviewed herein and elsewhere (4,(8)(9)(10)16), that he had relatively weak evidence for his conclusions that (i) sexual selection acted primarily on males through female choice and male competition and profligacy in mating, and (ii) some males mated more frequently than others, producing higher V RS among males than among females.…”

Section: Discussionmentioning

confidence: 71%

“…Given its paradigmatic status, Bateman's paper has inspired further studies of V NM and V RS (6,7), many of which are consistent with Bateman's main conclusions. Despite consistency in some studies and the apparent simplicity of Bateman's original design, Bateman's methods, the generality of Bateman's conclusions, and their implications are controversial (3,(8)(9)(10)(11) (SI Text), suggesting that "Bateman's Principles" might be better phrased as "Bateman's Hypotheses." Thus, it is interesting that the present report is unique in being a replication of Bateman's experiment that explicitly used his methodology of inferring who mated with whom by assigning parentage to offspring inheriting dramatic parental mutant phenotypes.…”

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confidence: 99%

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

Gowaty

Kim²,

Anderson³

2012

106

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...