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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 speciesPoeciliopsis 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.

 

Abstract The placenta is a complex organ that shows high morphological diversity. Among fish, the first vertebrates that have evolved a placenta, the family Poeciliidae exhibits very diverse modes of maternal provisioning even among congeneric species. Here, we investigated the embryonic growth curve across seven recently-described species of the highly diverse genus Phalloceros (Eigenmann, 1907). We also investigated possible intraspecific differences and whether other female characteristics affected embryo mass. We found that embryo mass decreased until around stage 20 and then increased, resulting in a 1.5 to 3-fold mass gain from fertilization to birth. Embryo mass changed non-linearly with stage of development and was affected by species identity (or locality) and female somatic dry mass. This initial loss then gain of embryonic mass during development is unique among other Poeciliidae species and was conserved across populations and species, even though size at birth can vary. Other species instead either lose mass if they lack placentas or gain mass exponentially if they have placentas. The Phalloceros mode of maternal provisioning could thus represent a different form from that seen in other species of Poeciliidae. 

Abstract The evolutionary origin of complex organs challenges empirical study because most organs evolved hundreds of millions of years ago. The placenta of live-bearing fish in the family Poeciliidae represents a unique opportunity to study the evolutionary origin of complex organs, because in this family a placenta evolved at least nine times independently. It is currently unknown whether this repeated evolution is accompanied by similar, repeated, genomic changes in placental species. Here, we compare whole genomes of 26 poeciliid species representing six out of nine independent origins of placentation. Evolutionary rate analysis revealed that the evolution of the placenta coincides with convergent shifts in the evolutionary rate of 78 protein-coding genes, mainly observed in transporter- and vesicle-located genes. Furthermore, differences in sequence conservation showed that placental evolution coincided with similar changes in 76 noncoding regulatory elements, occurring primarily around genes that regulate development. The unexpected high occurrence of GATA simple repeats in the regulatory elements suggests an important function for GATA repeats in developmental gene regulation. The distinction in molecular evolution observed, with protein-coding parallel changes more often found in metabolic and structural pathways, compared with regulatory change more frequently found in developmental pathways, offers a compelling model for complex trait evolution in general: changing the regulation of otherwise highly conserved developmental genes may allow for the evolution of complex traits. 

Abstract Placentation evolved many times independently in vertebrates. While the core functions of all placentas are similar, we know less about how this similarity extends to the molecular level. Here we study Poeciliopsis, a unique genus of live-bearing fish that have independently evolved complex placental structures at least three times. The maternal follicle is a key component of these structures. It envelops yolk rich eggs and is morphologically simple in lecithotrophic species, but has elaborate villous structures in matrotrophic species. Through sequencing the follicle transcriptome of a matrotrophic, P. retropinna, and lecithotrophic, P. turrubarensis, species we found genes known to be critical for placenta function expressed in both species despite their difference in complexity. Additionally, when we compare the transcriptome of different river populations of P. retropinna, known to vary in maternal provisioning, we find differential expression of secretory genes expressed specifically in the top layer of villi cells in the maternal follicle. This provides some of the first evidence that the placental structures of Poeciliopsis function using a secretory mechanism rather than direct contact with maternal circulation. Finally, when we look at the expression of placenta proteins at the maternal-fetal interface of a larger sampling of Poeciliopsis species, we find expression of key maternal and fetal placenta proteins in their cognate tissue types of all species, but follicle expression of Prolactin is restricted to only matrotrophic species. Taken together, we suggest that all Poeciliopsis follicles are poised for placenta function, but require expression of key genes to form secretory villi.