Revisiting the Trivers-Willard theory on birth sex ratio bias: Role of paternal condition in a Malagasy primate

Abstract

Within current theories on potential adaptive manipulation of offspring sex ratio, giving birth to a male or to a female is assumed to depend on the capacity of the mother to invest in offspring to maximize her fitness. The active role of the father in sex ratio bias at birth has been neglected until recently. The human sex ratio at birth is biased towards sons, although in occidental populations, the ratio has decreased regularly for 30 years and could be the consequence of the adverse effects of environmental chemicals on male hormones. In a Malagasy primate, the lesser mouse lemur, the potential effect of paternal testosterone levels on sex ratio bias at birth was tested on 130 litters (278 babies) produced in 52 mixed-sex groups. For each group, social dominance among males was characterized based on aggressive interactions and sexual behaviours. Using a multi correspondence analysis, high testosterone levels in grouped males, particularly those of the dominant male, were significantly correlated with more infants produced in male-biased litters, independent of the female condition. According to these results, predictions for sex ratio bias towards one sex or the other in mouse lemurs were discussed considering the influence of both parents.

Fig 1. Relationship between plasma testosterone levels and dominance index based on aggressive interactions between males within each group.

Fig 2. Principal component analysis.

(A)—Variable factor map on the 52 tested groups with quantitative variables:—body mass (BM) and age of both males and females,—parity,—testosterone levels (T) for the dominant male and the subordinate males in each group, -litter sex ratio and number of babies produced. Variables are represented by their scores on Dim1 (x-axis) and Dim2 (y-axis). The X and Y axis represent principal component loadings on Dim1 and Dim2 respectively, which corresponded to the weights of each original variable graphically visualized by arrows. Dim1 (26.3%) represents the influence of parents ‘ body condition on the litters data among which the parity and age of the grouped females were the primary affecting factor. Dim2 (16.5%) shows the strong relationship between testosterone levels of the dominant male and offspring production biased towards males. (B)—Group factor map on the 52 tested groups with litter types as qualitative variable. PCA clearly separates groups producing male-biased litters (M, black) from groups producing female-biased litters (F, red circles). Well-balanced litters appeared intermediate (E, blue).

Fig 3. –Predictions on the direction of sex ratio (SR) bias et potential production in mouse lemurs.

According to the level of parents’ sexual hormones prior to conception (+++ good or +- low), the future reproductive fitness of offspring ♀ and ♂ might be low (small symbol) or good (large symbol) depending on the sex ratio of the litter.