Why do placentas evolve? Evidence for a morphological advantage during pregnancy in live-bearing fish

Abstract

A live-bearing reproductive strategy can induce large morphological changes in the mother during pregnancy. The evolution of the placenta in swimming animals involves a shift in the timing of maternal provisioning from pre-fertilization (females supply their eggs with sufficient yolk reserves prior to fertilization) to post-fertilization (females provide all nutrients via a placenta during the pregnancy). It has been hypothesised that this shift, associated with the evolution of the placenta, should confer a morphological advantage to the females leading to a more slender body shape during the early stages of pregnancy. We tested this hypothesis by quantifying three-dimensional shape and volume changes during pregnancy and in full-grown virgin controls of two species within the live-bearing fish family Poeciliidae: Poeciliopsis gracilis (non-placental) and Poeciliopsis turneri (placental). We show that P. turneri is more slender than P. gracilis at the beginning of the interbrood interval and in virgins, and that these differences diminish towards the end of pregnancy. This study provides the first evidence for an adaptive morphological advantage of the placenta in live-bearing fish. A similar morphological benefit could drive the evolution of placentas in other live-bearing (swimming) animal lineages.

Fig 1. Predicted change in female body volume during pregnancy in two hypothetical lecithotrophic (non-placental) and placentotrophic (placental) live-bearing fish species, assuming an equal female length, offspring number and offspring size at birth (IB = 1): (1) the placental species (dash-dot line) will have a smaller volume during its entire pregnancy than the lecithotrophic species (dashed line) and (2) the relationship for the placental species will show a steeper slope than for the lecithotrophic species, indicating that the difference in body volume will be greatest at the beginning of the pregnancy and gradually diminish towards zero at end of the interbrood interval (redrawn after [9]).

Similar plots could be constructed for frontal or wetted surface area. For heuristic purposes the temporal patterns are assumed linear, because the exact shape of the relationship between female volume and time is currently unknown [20].

Fig 2. Morphological measurement and 3D model construction.

(A) Lateral and ventral photographs in which the trunk (green), abdomen (orange) and eyes (red) are outlined by manually indicated polygons. The longitudinal axis is depicted by white lines. (B) At 251 equidistant points along the longitudinal axis, the width and height of the polygons are converted into ellipse-like cross-sections; in the abdominal area, the vertical position of the horizontal axis is shifted. (C) Stitching the cross-sections of trunk and eyes results in a 3D model from which volume, wetted surface area and frontal surface area (projection at the right) can be calculated. For illustrative purposes these examples only consist of one-fourth of the number of cross-sections.

Fig 3. Shape parameters of pregnant P. turneri (with placenta) and P. gracilis (without placenta) from N = 122 three-dimensional models.

The multi-level longitudinal growth models (MLM) indicate changes in normalized (A) maximum width, (B) maximum height, (C) frontal surface area, (D) wetted surface area and (E) volume during one interbrood interval for pregnant P. turneri (red, N = 14) and P. gracilis (blue, N = 10). To account for individual variation in body size, one-dimensional parameters (A and B) were normalized by dividing the values by standard length (L_SL), the surface areas (C and D) by dividing by L_SL² and volume (E) by dividing by L_SL³. Connected circles represent individual female growth trajectories, solid lines are plotted from the MLM estimates for intercept and slope with equal litter wet mass (NS = P > 0.05, * = 0.01 < P < 0.05, ** = 0.001 < P < 0.01, *** = P < 0.001). Projections show examples of the respective model projections (A–C) or the complete model (D,E).