Maternal effects on male weaponry: female dung beetles produce major sons with longer horns when they perceive higher population density

Abstract

Background: Maternal effects are environmental influences on the phenotype of one individual that are due to the expression of genes in its mother, and are expected to evolve whenever females are better capable of assessing the environmental conditions that their offspring will experience than the offspring themselves. In the dung beetle Onthophagus taurus, conditional male dimorphism is associated with alternative reproductive tactics: majors fight and guard females whereas minors sneak copulations. Furthermore, variation in dung beetle population density has different fitness consequences for each male morph, and theory predicts that higher population density might select for a higher frequency of minors and/or greater expenditure on weaponry in majors. Because adult dung beetles provide offspring with all the nutritional resources for their development, maternal effects strongly influence male phenotype.

Results: Here we tested whether female O. taurus are capable of perceiving population density, and responding by changing the phenotype of their offspring. We found that mothers who were reared with other conspecifics in their pre-mating period produced major offspring that had longer horns across a wider range of body sizes than the major offspring of females that were reared in isolation in their pre-mating period. Moreover, our results indicate that this maternal effect on male weaponry does not operate through the amount of dung provided by females to their offspring, but is rather transmitted through egg or brood mass composition. Finally, although theory predicts that females experiencing higher density might produce more minor males, we found no support for this, rather the best fitting models were equivocal as to whether fewer or the same proportions of minors were produced.

Conclusions: Our study describes a new type of maternal effect in dung beetles, which probably allows females to respond to population density adaptively, preparing at least their major offspring for the sexual competition they will face in the future. This new type of maternal effect in dung beetles represents a novel transgenerational response of alternative reproductive tactics to population density.

Figure 1

The relationships between female weight, brood mass weight, and pronotum width of their male offspring. A. The body weight of female Onthophagus taurus positively affected the weight of the brood masses they produced (the shaded area represent predicted values based on the 95% confidence intervals of the parameters of the model used). B. The weight of these brood masses positively affected the pronotum width of the male offspring that emerged from them (the shaded area represent predicted values based on the 95% confidence intervals of the parameters of the model used).

Figure 2

The allometry of horn length on pronotum width of males in Onthophagus taurus. Males in the sample were the pooled offspring produced by females from all our experimental groups (see Methods). Both axes were transformed using natural logarithms, the curve was fitted with a Richards’ growth function (parameters in Table 3), and the shaded area represents predicted values based on the 95% confidence intervals of the parameters of the model used.

Figure 3

The horn length allometry of the male offspring produced by females from different experimental groups. These groups differed in the population density experienced by females during their pre-mating (PM) period. Offspring produced by females from the low-density experimental group are indicated by open circles and a continuous curve, whereas offspring produced by females from the high-density experimental group are indicated by crosses, and a broken curve. Again, both axes were transformed using natural logarithms, and the curves were fitted with a Richards’ growth function, but this time (A) only parameter μ (Model 4), (B) or parameter λ (Model 5) were allowed to vary between the experimental groups, whereas parameters A and v were always common across experimental groups (see Table 4). A. According to the model that allows only parameter μ to vary between experimental groups (Model 4, Table 4), the vertical dotted line depicts a value of body size for which the model predicts a horn length 8.4% greater for offspring of females that experienced high population density in their pre-mating period (upper dotted horizontal line) than for offspring of females that experienced low population density during their pre-mating period (lower dotted horizontal line). This line was chosen to depict the biggest possible difference in the horns of offspring produced by females of the two experimental groups described above.