Sources of variance in a female fertility signal: exaggerated estrous swellings in a natural population of baboons

Abstract

Signals of fertility in female animals are of increasing interest to evolutionary biologists, a development that coincides with increasing interest in male mate choice and the potential for female traits to evolve under sexual selection. We characterized variation in size of an exaggerated female fertility signal in baboons and investigated the sources of that variance. The number of sexual cycles that a female had experienced after her most recent pregnancy ("cycles since resumption") was the strongest predictor of swelling size. Furthermore, the relationship between cycles since resumption and swelling size was most evident during rainy periods and was not evident during times of drought. Finally, we found significant differences in swelling size between individual females; these differences endured across cycles (i.e., were not explained by variation within individuals) and persisted in spite of ecological effects. This study is the first to provide conclusive evidence of significant variation in swelling size between female primates (controlling for cycles since resumption) and to demonstrate that ecological constraints influence variation in this signal of fertility.

Keywords: Baboon; Estrous swelling; Fertility.

Fig. 1

Examples of digital images used for data collection and scoring, completed from high resolution color versions. a Images were first subjected to four explicit criteria before they were added to the data set (see Methods). Next, they were rotated until the swelling could be bisected vertically (represented by a dashed white line). Finally, width was measured at the largest point across the swelling (represented by a solid white line). b Multiple images for the same individual on the same day were scored individually, and all contributed to one final measurement of swelling width for a given individual on a given day. Using the pixels/mm conversion associated with each lens extension, a width measurement was generated for each image (displayed at immediate right of image). The mean of these measurements constituted the daily swelling width and the standard deviation was considered the measurement error. A similar procedure was followed for swelling length. c Comparison of measurement errors to detected changes in swelling sizes from d-4 to d-3, d-3 to d-2, d-2 to d-1 for swelling width (closed circles) and swelling length (open circles). Average detectable change in swelling length from d-4 to d-3 and from d-3 to d-2 and from d-2 to d-1 was significantly larger than the average measurement error. Likewise, average detectable change in swelling width from d-4 to d-3 and d-3 to d-2 was statistically larger the average measurement error (*p<0.05; **p<0.01). Error bars represent one standard deviation from the mean

Fig. 2

Bivariate relationships between swelling width (closed circles, solid lines) or swelling length (open circles, dashed lines) and a female age, b female dominance rank, c cycles since resumption. Trend lines are least squares regressions and are not a substitute for the full multivariate analysis. Shaded portion in a represents data points for the oldest females in our data set, which were excluded during the calculation of linear regression. Each female is represented only once for a and b, but may appear multiple times in c

Fig. 3

Comparative distributions during drought conditions (solid line) and wet conditions (dashed line) for a maximal swelling widths b maximal swelling lengths. To reduce noise introduced by within-individual variation, females are represented only once. Maximal swelling sizes were smaller during drought conditions. Insets show quantile-quantile plots demonstrating the differentiation between the distributions

Fig. 4

Least-squared regression of a maximal swelling width and b length on cycles since resumption during both drought periods (triangles, solid line—150 days or over since last wet month) and wet periods (circles, dashed lines—30 days or less since last wet month). Each data point represents maximal swelling size for one cycle. During drought times, cycles since resumption has no effect on swelling size. However, during wet times, cycles since resumption predicts swelling size. Because repeated samples of individual females are represented in this visualization and it should not be considered a substitute for the full post hoc analysis

Fig. 5

Maximal swelling width for 33 unique individuals on their conceptive cycle. Each measure represents a mean calculated from multiple images collected on the same day (range=2–10 images) and error bars represent standard deviation from the mean width for that female on that cycle