The concept of superfetation: a critical review on a ‘myth’ in mammalian reproduction

Abstract

Superfetation is understood as another conception during an already ongoing pregnancy. This implies the existence of young of different developmental stages within the female reproductive tract during certain periods of pregnancy. Nevertheless, a clear definition of the term as well as distinct criteria to identify the occurrence of superfetation in a species is missing. The variable anatomy of mammalian reproductive tracts seems to make the occurrence of superfetation more or less likely but impedes the simple evaluation of whether it is present or not. Additionally, adequate determination methods are missing or are difficult to apply at the right time. Superfetation or rather superfetation-like pregnancies are reported for numerous species including humans, livestock and rodents. The usual criteria to assume a case of superfetation include the finding of discordantly developed young within the uterus during post mortem or parturition of young after a birth interval shorter than the assumed pregnancy length. Often the occurrence of superfetation is concluded because other explanations of reproductive artifacts are missing. Even severe reproductive pathologies are often confused with superfetation. True superfetation or superfetation as a reproductive strategy may exist in some mammals. In the American mink (Neovison (Mustela) vison) and the European badger (Meles meles) superfetation occurs in combination with embryonic diapause. In the European brown hare (Lepus europaeus), superfetation has long been assumed to exist but evidence is still controversial. Superfetation definitely occurs in certain species of poeciliid and zenarchopterid fish, some of which also exhibit viviparity and maternal care. In mammals, the evolution of such a reproductive mechanism poses many interesting evolutionary, endocrine, microbial and immunological questions that require further investigation. Here we review the scant and at times ancient literature on this poorly understood topic. The different manifestations of superfetation are defined and reliable criteria to detect superfetation are outlined. Also, the differentiation of superfetation into a reproductive strategy or as a disrupted, abnormal reproductive function is discussed. Due to the different discussed functional aspects of superfetation, it is appropriate to establish a more detailed scheme to classify the true natural superfetation cases into superfertilization, superconception and superfetation proper. To date, there is no mammal species known for which superfetation proper in terms of finding discordantly developed fetuses has been conclusively demonstrated to be not only a rare occurence but an evolved reproductive strategy.

Frederik Ruysch (1638–1731): Historical perspective and contemporary analysis of his teratological legacy

“…Although true superfetation is known to occur in several mammalian species, either frequently or occasionally, it seems extremely rare in humans and its unequivocal existence has yet to be proven [Roellig et al, 2011]. In most cases of alleged superfetation other causes of discordant development between two (or more) fetuses seem much more probable (or at least cannot be ruled out), such as superfecundation (successive fertilizations of two or more oocytes originating from a single ovulation), delayed nidation (timing differences in implantation of two or more zygotes), growth discordance in multiple pregnancies due to placental insufficiency or twin to twin transfusion syndrome, and pre‐ or immature death of a twin sib [Baijal et al, 2007; Roellig et al, 2011]. From Ruysch's description, it seems very likely that the latter was the case.…”

Posible superfetación en una coneja raza NZB (Oryctolagus cuniculus) concomitante a retraso del desarrollo intrauterino (RDIU)

“…A cesariana urgente revelou seis produtos a termo; um de tamanho superior, morto em posição caudal, o que bloqueava o canal de parto perto do cólon uterino, e um mais sub-introducción En medicina veterinaria los trastornos asociados con la reproducción del conejo son observados ocasionalmente e incluyen urgencias distócicas y abortos [1][2][3][4], agalactia, defectos congénitos o de desarrollo [5], embarazo ectópico [5], pseudogestación [6], toxemia de la preñez y superfetación (sf) [7], entre los más documentados, aunque también se ha reportado la gestación gemelar como rareza reproductiva clínica-mente importante [8]. En el caso de la sf, ha sido definida como el desarrollo de una segunda fertilización de óvulos durante un embarazo establecido, contando con la presencia de críos in Utero bajo diferentes escenarios de desarrollo [9][10][11].…”

“…Sin embargo, una tesis bien documentada [16] indica que existen numerosos reportes de sf en mamíferos como bovinos, burros, caballos, ovejas, cerdos, búfalos y monos, que aporta además datos sobre ciertas especies de peces que exhiben viviparidad seguida de un distintivo cuidado materno posterior al nacimiento de sus crías [11].…”

“…Morfológicamente, los fetos a término registraron pesos de 65,8, 70,7, 61,3, 68,4, 53,7 y 65,3 gramos, respectivamente; el crío subdesarrollado pesó 19,5 gramos y presentó meconio abundante ausente en el resto. Las longitudes corporales totales (lct) realizadas análogamente bajo criterio céfalo-caudal (cc), reportaron 10,7,11,2,9,9,10,9,8,6 y 9,2 cm, respectivamente, y sólo 3,9 cm para el crío subdesarrollado, sin evidencia de malformaciones o infección. Basado en observaciones clínico-quirúrgicas el diagnóstico primario fue de distocia obstructiva, asociada a un sobredesarrollo fetal e inercia uterina secundaria.…”

Artificial induction of superfetation in the European hare (Lepus europaeus)

“…Lincoln (1974) observed ovulation immediately following parturition or sometimes a short before it, but no females ovulated during early and middle phase of pregnancy and no case of superfetation was found. As can be seen, the data on superfetation in hares are very different, and this subject has been recently reviewed in detail by Roellig et al (2010b).…”