Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae.

The causes and consequences of the evolution of placentotrophy (post-fertilization nutrition of developing embryos of viviparous organisms by means of a maternal placenta) in non-mammalian vertebrates are still not fully understood. In particular, in the fish family Poeciliidae there is an evolutionary link between placentotrophy and superfetation (ability of females to simultaneously bear embryos at distinct developmental stages), with no conclusive evidence for which of these two traits facilitates the evolution of more advanced degrees of the other. Using a robust phylogenetic comparative method based on Ornstein-Uhlenbeck models of adaptive evolution and data from 36 poeciliid species, we detected a clear causality pattern. The evolution of extensive placentotrophy has been facilitated by the preceding evolution of more simultaneous broods. Therefore, placentas became increasingly complex as an adaptive response to evolutionary increases in the degree of superfetation. This finding represents a substantial contribution to our knowledge of the factors that have shaped placental evolution in poeciliid fishes.

Superfetation reduces the negative effects of pregnancy on the fast-start escape performance in live-bearing fish.

Superfetation, the ability to simultaneously carry multiple litters of different developmental stages in utero, is a reproductive strategy that evolved repeatedly in viviparous animal lineages. The evolution of superfetation is hypothesized to reduce the reproductive burden and, consequently, improve the locomotor performance of the female during pregnancy. Here, we apply new computer-vision-based techniques to study changes in body shape and three-dimensional fast-start escape performance during pregnancy in three live-bearing fishes (family Poeciliidae) that exhibit different levels of superfetation. We found that superfetation correlates with a reduced abdominal distension and a more slender female body shape just before parturition. We further found that body slenderness positively correlates with maximal speeds, curvature amplitude and curvature rate, implying that superfetation improves the fast-start escape performance. Collectively, our study suggests that superfetation may have evolved in performance-demanding (e.g. high flow or high predation) environments to reduce the locomotor cost of pregnancy.

Superfetation in the viviparous fish Heterandria formosa (Poeciliidae).

Heterandria formosa is a viviparous poeciliid native of the southeastern of United States of America. H. formosa exhibits unique reproductive features as: (a) production of extremely small eggs with scarce quantity of yolk (microlecithal eggs), (b) consequently, a high level of matrotrophy and development of a complex follicular placenta, (c) ovarian sperm storage that allows the continuous fertilization of oocytes and production of offspring and (d) development of high degree of superfetation. The degree of superfetation refers to the number of broods in different simultaneous stages of gestation. Morphological evidence of the degree of superfetation in H. formosa has not been documented. Therefore, and because of the general interest in the complex process of superfetation, the goal of this study is to morphologically define the degree of superfetation of H. formosa through two procedures: (a) histological analysis of entire ovaries in gestation and (b) dissection of visible embryos and the histological analysis of the remaining ovarian tissue. Results indicate that H. formosa can gestate up to seven broods at the same time.

Comparative life histories of fishes in the genus Phallichthys (Pisces: Poeciliidae).

This study presents a description of the life histories of all four species of the genus Phallichthys, found primarily in the Atlantic slope of Central America (ranging from northern Panama to Mexico), based on a combination of data collected from preserved and living specimens. All species produced a single litter of offspring before developing another brood (i.e. no superfoetation). In the laboratory, the mean time interval between successive litters ranged from 24 to 48 days, further suggesting that they lack superfoetation. Embryos lose from 15 to 65% of their dry mass during development, meaning all or the large majority of resources required for development are provided prior to fertilization (lecithotrophy). All mature male size distributions were platykurtotic and appeared either bimodal or multimodal. Multimodal and skewed size distributions have been associated with genetic polymorphisms for size at maturity in other species of Poeciliidae. As the sister clade to Phallichthys includes genera in which all species have superfoetation (Neoheterandria and Poeciliopsis), these results suggest that their common ancestor with Phallichthys also had superfoetation and that the trait has been lost.

Unpredicted ovulations and conceptions during early pregnancy: an explanatory mechanism of human superfetation.

In this bioessay, a literature review on human superfetation was performed in order to find epidemiological variables associated with this phenomenon. Thereafter, an explanatory mechanism of superfetation compatible with the endocrinological, histological and physiological changes undergone by women during early pregnancy is proposed. Superfetation can be defined as the ovulation, fertilisation and implantation of a second or additional embryo(s) during pregnancy. The literature review evidences a small discordance in gestational age between dizygotic twins in humans (range: 2-4 weeks; mean ± s.e.m.: 3.3 ± 0.3 weeks). This difference is compatible with a luteal out-of-phase (LOOP; i.e. atypical increase in E2 levels in the mid-luteal phase)-like event occurring between 1 and 3 weeks after the ovulation that allowed the first pregnancy to take place. The LOOP-like event may allow passive sperm transport from the vaginal fornix to the Fallopian tube ipsilateral to the ovulatory ovary and trigger a LH peak and ovulation. Furthermore, during very early pregnancy, the decidual reaction is not yet completed and at least one proximal Fallopian ostium may be opened, allowing the passage of the spermatozoa ascending to the fertilisation site and the extra embryo(s) descending to the implantation site(s).

[Superfetation: case report and review of the literature]. / Superfoetation: à propos d'un cas et revue de la littérature.

We report the case of a dichorionic-diamniotic pregnancy in which a discordance in the size of the fetuses was observed as early as the first trimester. This discordance in size was maintained over time and the two fetuses continued their respective growths. We suggest the very rare phenomenon of superfetation as a diagnosis because less than 10 cases are described in the literature. Even though a formal proof of the diagnosis is difficult to obtain, the elements described in this article rally in favor of this hypothesis. Superfetation is defined by the fertilization and the implantation of a second oocyte in a uterus already containing the product of a previous conception. After a description of the case, a review of the literature enables us to describe the frequency, the possible risk factors and the existing case reports on the subject. The rarity of this case justifies its publication for the information of clinicians.

[Superfecundation and superfetation--the forgotten entities].

Superfecundation and superfetation are rare and obscure phenomena with no clear clinical significance but with legal and moral-social meanings. These obstetric rarities are known since the times of the ancient Greeks. There are several physiological explanations that account for superfecundation but not for superfetation, yet, both have been described. In this era of assisted reproductive techniques it is reasonable to assume that the prevalence of superfecundation increases, which may also apply to superfetation. Today, there are several reliable diagnostic techniques to verify heteropaternity in multifetal pregnancies, hence superfecundation. Nevertheless, our knowledge regarding these amazing phenomena remains limited due to both ethical and medico-legal barriers that prevent their implementation.

Gonadotrophins and sex steroids during pregnancy and natural superfoetation in captive brown hares (Lepus europaeus).

In brown hares, which are induced ovulators, sexual behaviour occurs episodically at the beginning of pregnancy. From Day 34 (length of pregnancy is 41 days), the frequency of sexual chases followed by mating, ovulation and fertilization increased and 59% of pregnant females presented a natural superfoetation. The pattern of circulating luteinizing hormone (LH), follicle-stimulating hormone (FSH), oestradiol and progesterone was studied in 13 pregnant females left permanently with a male, and in 10 females isolated from males around Day 20 of pregnancy. In the 2 groups FSH concentrations were high at the beginning and end of pregnancy. All females presented a peak value of FSH in the last 4 days of pregnancy, regardless of mating stimuli. This peak value was higher for females left permanently with a male than for isolated ones. Oestradiol concentrations fluctuated between 20 and 100 pg/ml, without any clear correlation with sexual behaviour, stage of pregnancy or profiles of other hormones. Prepartum matings occurred when progesterone values were still greater than 50 ng/ml; they were followed by a transient rise in LH and by a periovulatory progesterone secretion, with values above 100 ng/ml in the morning after mating. Such modifications of LH and progesterone were not detected before Day 34, suggesting that mating stimuli are not able to induce an LH surge at the beginning of pregnancy. After Day 34, mating can induce an LH surge, ovulation and superfoetation.