Both matrotrophy, the maternal provisioning of nutrients to developing embryos after fertilization, and superfetation, the simultaneous presence of two or more groups of embryos at different stages of development, occur at varying degrees among species of the fish family Poeciliidae. However, it is still unclear if these two reproductive modes depend on the presence of relatively complex placentas. We describe the ultrastructure of the maternal follicular placenta of 11 poeciliid fishes using electron microscopy. In addition, we quantified six ultrastructure characteristics that reflect the degree of complexity (number of vesicles, area of vesicles, number of microvilli, microvilli length, thickness of the maternal follicle and follicular area). Using phylogenetic comparative methods, we evaluated the relationship between degree of matrotrophy and placental characteristics. We also analysed the potential effect of the presence of superfetation on placental complexity. We found a positive relationship between the degree of matrotrophy and follicular area, number of microvilli and number and area of vesicles. Similarly, follicular area and number of microvilli were larger in species with superfetation than in those without superfetation. We conclude that high degrees of matrotrophy and superfetation are associated with placental characteristics that increase the efficiency of nutrient transfer between mother and embryos. K E Y W O R D Sfollicular placenta, matrotrophy, placentation, Poeciliidae, superfetation
Superfetation is the ability of females to simultaneously carry multiple broods of embryos, with each brood at a different developmental stage. Matrotrophy is the post-fertilization maternal provisioning of nutrients to developing embryos throughout gestation. Several studies have demonstrated that, in viviparous fishes, superfetation and matrotrophy have evolved in a correlated way, such that species capable of bearing several simultaneous broods also exhibit advanced degrees of post-fertilization provisioning. The adaptive value of the concurrent presence of both reproductive modes may be associated with the production of larger newborns, which in turn may result in enhanced offspring fitness. In this study, we tested two hypotheses: (1) species with superfetation and moderate or extensive matrotrophy give birth to larger offspring compared to species without superfetation or matrotrophy; (2) species with higher degrees of superfetation and matrotrophy (i.e. more simultaneous broods and increased amounts of post-fertilization provisioning) give birth to larger offspring compared to species with relatively low degrees of superfetation and matrotrophy (i.e. fewer simultaneous broods and lesser amounts of post-fertilization provisioning). Using different phylogenetic comparative methods and data on 44 species of viviparous fishes of the family Poeciliidae, we found a lack of association between offspring size and the combination of superfetation and matrotrophy. Therefore, the concurrent presence of superfetation and moderate or extensive matrotrophy has not facilitated the evolution of larger offspring. In fact, these traits have evolved differently. Superfetation and matrotrophy have accumulated gradual changes that largely can be explained by Brownian motion, whereas offspring size has evolved fluidly, experiencing changes that likely resulted from selective responses to the local conditions.
Sperm storage within the female reproductive tract has been reported as a reproductive strategy in several species of vertebrates and invertebrates. However, the morphological structures that allow for sperm to be stored and kept viable for long periods are relatively unknown in osteichthyes. We use histological and stereological tools to identify and quantify sperm storage structures (spermathecae) in 12 species of viviparous Poeciliidae. We found spermathecae in nine species, six of which exhibit superfetation (the ability of females to simultaneously carry within the ovary two or more broods of embryos at different stages of development). These spermathecae are folds of ovarian tissue that close around spermatozoa. We compared the number and size (volume) of spermathecae between species with and without superfetation. Species that exhibit superfetation had a significantly higher number of spermathecae than species that do not exhibit this reproductive strategy. In addition, we found that the mean volume of spermathecae and total volume of spermathecae present in the ovary are marginally higher in species with superfetation. Our results contribute to the understanding of the morphological structures that allow for sperm storage in viviparous osteichthyes and suggest a positive relationship between superfetation and the capacity of females to store sperm.
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