Why do placentas evolve? An evaluation of the life-history facilitation hypothesis in the fish genus Poeciliopsis

Abstract

1. The Northern Clade of the fish genus Poeciliopsis includes six closely related species, three of which lack placentas and three that have placentas but vary in the extent of post-fertilization provisioning. 2. We used this diversity to evaluate a series of hypotheses proposed in earlier publications concerning why the placenta has evolved. All hypotheses share the attribute of arguing that the placenta evolved to enhance the evolution of some other life-history trait, such as to reduce the age at maturation or to increase offspring size. We refer to these hypotheses collectively as ‘life-history facilitation hypotheses’. 3. A general way to evaluate the plausibility of such proposals is to ask whether the evolution of the placenta is predictably associated with the evolution of other components of the life history. 4. We evaluated such associations in two ways. First, we performed a multivariate analysis of life-history data for fish collected and preserved in nature. This analysis included 16 populations across all six species. Secondly, we performed a more complete quantification of the life histories of the laboratory descendents from five populations representing four species, then performed a similar multivariate analysis. The laboratory study added information about the timing of reproduction (age at maturity, frequency of reproduction). 5. Both analyses yielded similar results, which were that the evolution of increased placentation is correlated with the evolution of a smaller size at first reproduction, the production of fewer and smaller offspring per litter, but an increase in the number of litters that were developing simultaneously in the ovary (superfetation). Increased placentation is associated with progressively earlier ages at maturation and shorter intervals between the birth of successive litters of offspring. Overall, increased placentation was associated with an increase in the rate of production of offspring early in life. A peculiar attribute of placentation is that this increase in the rate of offspring production can be attained despite a simultaneous reduction in the proportional quantity of resources devoted to reproduction. 6. These trends support one of the life history facilitation hypotheses, which is that placentation facilitates earlier maturity and a higher rate of reproduction early in life. They also suggest a possible connection between the evolution of the placenta and the well-established theory of life-history evolution, since these same life history attributes are predicted to evolve in response to exposure to high extrinsic rates of adult mortality.