The Society for Integrative and Comparative Biology
Bateman Gradients in Field and Laboratory Studies: A Cautionary Tale1
1 Department of Biology, University of Missouri–St. Louis, 8001 Natural Bridge Road, St. Louis, Missouri 63121
Since tools of molecular genetics became readily available, our understanding of bird mating systems has undergone a revolution. The majority of passerine species investigated are socially monogamous, but have been shown to be genetically polygamous. Data sets from natural populations of juncos suggest that multiple mating by females results in a sexual selection gradient as steep for females as for males (a result that does not support Bateman's predictions). However, in males, fitness is enhanced directly through fertilization success with multiple matings; in females fitness benefits may be enhanced immediately through direct access to food, protection against predators, or other resources received from males, or they may be delayed through improvement in offspring quality (e.g., through good genes, or greater genetic compatibility between the female and the extra-pair male). But a steep sexual selection gradient for females can be difficult to interpret. If all females copulate with multiple partners that are equally likely to fertilize eggs, then females that produce larger clutch sizes, for any reason, will appear to have copulated with more males. That is, multiple sires have a higher probability of detection in larger clutches than in smaller ones, giving the impression that females that mate with multiple males increase their reproductive success. Yet, in most studies in which there is a correlation between number of offspring produced by females and number of extra-pair males, causation has not been clearly established and other factors may explain the results. Additional complications in understanding male and female reproductive strategies are: (1) Molecular studies cannot detect extra-pair copulations that did not result in fertilizations; yet if a female acquires food or other resources from extra-pair males, such extra-pair matings may have significant effects on female fitness. Thus, molecular studies provide only a conservative estimate of the number of extra-pair copulations or "mates" that a female has. (2) Clutch size affects the probability that any given male will be successful in fertilizing a female's eggs. Specifically, at any given point, a male's chances of fertilizing at least one egg in the female's clutch will be greater as clutch size increases. We predict that in avian species with small clutch sizes, males may be selected to be choosy and avoid extra-pair copulations, while females should be selected to be less discriminating. Moreover, if extra-pair males provide resources that increase female fitness, the females should seek extra-pair copulations, whether or not the males are likely to fertilize any of her eggs.
Laboratory studies with insects have yielded clearer evidence of the causal relationship between multiple mating and increased female fitness. We review studies on a tenebrionid beetle in which female fecundity increases directly with number of mates. In these experiments, the nutritive value of the spermatophores does not fully explain the increase in female reproductive success.
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