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The placenta is a complex life‐history trait that is ubiquitous across the tree of life. Theory proposes that the placenta evolves in response to high performance‐demanding conditions by shifting maternal investment from pre‐ to post‐fertilisation, thereby reducing a female's reproductive burden during pregnancy. We test this hypothesis by studying populations of the fish species Poeciliopsis retropinna in Costa Rica. We found substantial variation in the degree of placentation among natural populations associated with predation risk: females from high predation populations had significantly higher degrees of placentation compared to low predation females, while number, size and quality of offspring at birth remained unaffected. Moreover, a higher degree of placentation correlated with a lower reproductive burden and hence likely an improved swimming performance during pregnancy. Our study advances an adaptive explanation for why the placenta evolves by arguing that an increased degree of placentation offers a selective advantage in high predation environments. [ABSTRACT FROM AUTHOR]

Maternal effects often provide a mechanism for adaptive transgenerational phenotypic plasticity. The maternal phenotype can profoundly influence the potential for such environmentally induced adjustments of the offspring phenotype, causing correlations between offspring and maternal traits. Here, we study potential effects of the maternal phenotype on offspring provisioning prior to and during gestation in the matrotrophic live‐bearing fish species Poeciliopsis retropinna. Specifically, we examine how maternal traits such as body fat, lean mass, and length relate to pre‐ (i.e., allocation to the egg prior to fertilization) and post‐fertilization (i.e., allocation to the embryo during pregnancy) maternal provisioning and how this ultimately affects offspring size and body composition at birth. We show that pre‐ and post‐fertilization maternal provisioning is associated with maternal length and body fat, but not with maternal lean mass. Maternal length is proportionally associated with egg mass at fertilization and offspring mass at birth, notably without changing the ratio of pre‐ to post‐fertilization maternal provisioning. This ratio, referred to as the matrotrophy index (MI), is often used to quantify the level of matrotrophy. By contrast, the proportion of maternal body fat is positively associated with post‐fertilization, but not pre‐fertilization, maternal provisioning and consequently is strongly positively correlated with the MI. We furthermore found that the composition of embryos changes throughout pregnancy. Females invest first in embryo lean mass, and then allocate fat reserves to embryos very late in pregnancy. We argue that this delay in fat allocation may be adaptive, because it delays an unnecessary high reproductive burden to the mother during earlier stages of pregnancy, potentially leading to a more slender body shape and improved locomotor performance. In conclusion, our study suggests that (a) offspring size at birth is a plastic trait that is predicted by both maternal length and body fat, and (b) the MI is a plastic trait that is predicted solely by the proportion of maternal body fat. It herewith provides new insights into the potential maternal causes and consequences of embryo provisioning during pregnancy in matrotrophic live‐bearing species. Maternal effects are particularly important, frequently having widespread consequences for offspring phenotype and fitness. Here, we studied potential effects of the maternal phenotype on offspring provisioning prior to and during gestation in the matrotrophic live‐bearing fish species Poeciliopsis retropinna. We show that maternal traits strongly correlate with embryo size and body composition throughout pregnancy. Though, different maternal traits are differently related to pre‐ and post‐fertilization maternal provisioning. We furthermore found that the composition of embryos changes during pregnancy independently of the maternal phenotype. [ABSTRACT FROM AUTHOR]

Summary 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. [ABSTRACT FROM AUTHOR]

Matrotrophic fish in the genus Poeciliopsis (Poeciliidae) have a placenta-like structure used in postfertilization maternal provisioning of the developing embryo. To understand better the structure and function of the Poeciliopsis placenta, we derived cDNA libraries from the maternal follicular placenta of 2 matrotrophic Poeciliopsis sister species, P. turneri and P. presidionis. These species inherited their placenta from a common ancestor and represent one of 3 independent origins of placentas in Poeciliopsis. Expressed sequence tags (ESTs) were generated and putative function was determined using BLASTX homology searches and Gene Ontology (GO) annotation. Reverse transcription–polymerase chain reaction was used to verify placenta tissue expression of a putative candidate gene, alpha-2 macroglobulin. In total, 1956 (71.5% of the total submitted ESTs) and 924 (71.0% of the total submitted ESTs) unique transcripts were identified for the P. turneri and P. presidionis placenta, respectively. Homology search and GO annotation revealed putative genes whose products may be involved in specific transport functions of the maternal follicle. These putative genes are excellent candidates for future research on the evolution of the placenta. We discuss our results in light of the parent–offspring conflict theory of placental evolution and in terms of the Poeciliid placenta structure and function. [ABSTRACT FROM PUBLISHER]

The Trexler-DeAngelis model shows that placentas are most likely to evolve in environments with consistent, high levels of resource availability. An assumption imperative to the model is that placental species abort embryos in low food conditions. However, a previous experimental test of this assumption using the northern clade of Poeciliopsis showed no evidence for abortion. To distinguish between the alternatives that placental species either sacrifice body condition to maintain reproduction when resources are restricted, or that the previously documented pattern of resource allocation is a function of other life-history correlates of placentation rather than placentation alone, we perform a similar experiment on the southern clade of Poeciliopsis. The southern clade has the opposite relationship between life-history traits and placentation as seen in the northern clade. Our results mirror those from the northern clade, indicating that reproductive mode, rather than life history, dictates the pattern of resource allocation. These results add to the difficulties of explaining placental evolution within the constraints of the Trexler-DeAngelis model by restricting the range of resource conditions in which placental species can outcompete nonplacental species. They also lend support to hypotheses that suggest parent-offspring conflict in utero drives the evolution of the placenta. [ABSTRACT FROM AUTHOR]

1. We investigate how resource level affects reproduction in matrotrophic ( Poeciliopsis prolifica) and lecithotrophic ( P. monacha) fishes. 2. One of our goals was to test an assumption of the Trexler–DeAngelis model for the evolution of matrotrophy, which was that matrotrophic species can adjust litter size by aborting offspring in low food conditions. Our more general goal was to elucidate other differences between the reproductive modes. 3. Both species have superfetation and c. 30-day development time. Females of each species were assigned to high or low food availability for 30 days, or one gestation period. Any young born during that time interval would have initiated development before the initiation of the experiment. If embryos are aborted, then this would be seen as a reduction in brood size in the low food treatment relative to the high food treatment within this period. 4. Our results suggest P. monacha responds to low food by sacrificing reproduction to maintain lipids, while P. prolifica maintains reproduction at the expense of lipids. Neither species showed a significant reduction in offspring number over the course of the experiment, suggesting that these species do not abort offspring in low food conditions. [ABSTRACT FROM AUTHOR]