The effects of synthetic estrogen exposure on premating and postmating episodes of selection in sex-role-reversed Gulf pipefish

Abstract

Environmental estrogens have been shown to affect populations of aquatic organisms in devastating ways, including feminization of males, alterations in mating behaviors, and disruption of sexual selection. Studies have shown 17α-ethinylestradiol (EE2) exposure to induce female-like secondary sexual traits in male Gulf pipefish, changing how females perceive affected males. We aimed to understand the effects of EE2 exposure on the sex-role-reversed mating system and the strength of selection in Gulf pipefish. We used artificial Gulf pipefish breeding aggregations and microsatellite-based parentage analysis to determine maternity. We then calculated the opportunity for selection and selection differentials on body size for both sexes during three consecutive episodes of selection. Exposure to EE2 did not affect the strength of selection, likely due to the unusual sex-role-reversed mating system found in this species. With respect to multiply mated females, EE2-exposed females produced more eggs with higher embryo survivorship than nonexposed females. Thus, short-term exposure to low concentrations (2.0 ng/L) of EE2 in Gulf pipefish enhanced female reproductive success. However, higher EE2 concentrations (5.0 ng/L) caused complete reproductive failure in Gulf pipefish males. These results call for more work on the long-term effects of EE2 exposure in Gulf pipefish in artificial and natural populations.

Keywords: EE2; Gulf pipefish; selection; sex-role-reversed mating system; synthetic estrogen.

Figure 1

Histograms displaying mating success for males and females across both treatments with black bars for the control and gray bars for the EE2 treatment. The y-axis represents the frequencies, and the x-axis represents the number of mates.

Figure 2

Number of eggs transferred and proportion of surviving embryos for females in the EE2 and control treatments. The graph on the left (A) shows the number of eggs females transferred to their mates over the entire experiment. Solid bars represent singly mated females, and striped bars represent multiply mated females. The graph on the right (B) shows the proportion of surviving embryos for singly mated (solid bars) and multiply mated (striped bars) males in the control and EE2 treatments. Within each figure, bars with shared letters are not significantly different from one another (Tukey's post hoc test). Error bars represent one standard error from the mean.

Figure 3

Absolute Bateman gradients for females in the EE2 and control treatments. The black line represents the linear regression of total number of offspring on number of mates for the control treatment, whereas the gray line shows the same linear regression for the EE2 treatment. The Bateman gradient for females in the EE2 treatment is significantly steeper than the Bateman gradient for females in the control replicates (ancova, with replicate as a random effect: P = 0.009).