Animals have evolved in a range of reproductive adaptations from oviparity to viviparity. Nevertheless, the traditional typology does not seem relevant enough to clarify the level of parental investment. Thus, lecithotrophy did not provide any information on the retention of zygotes inside the body and matrotrophy only indicate that nutrients are provided by mother with no differences with maternal care. Therefore, a new scientific typology of the different reproductive modes could be proposed discriminating five classes:

-       ovuliparity,

-       oviparity,

-       ovo-viviparity,

-       histotrophic viviparity and

-        hemotrophic viviparity.

Based on the development stage of the zygote and on its interrelation with the parent, this classification details the degree of contrivances by which animals provide alternative investment in their offspring. These different modes of reproduction do represent a sequence with ovuliparity the most primitive and hemotrophic viviparity the most derived. Thus, the comparative analysis of different reproductive modes in vertebrates suggests that cold conditions could be one of the strongest selection pressures for egg retention and viviparity.

Modes of reproduction undoubtedly represent one of the most critical life history traits because they intimately affect fitness and survival. The natural evolution of these different sexual reproductive modes reveals the increase of parental investment during phylogeny [11, 37, 46]. Numerous animals devote considerable energy to protecting their eggs and to raising and feeding their offspring, and can even take care of their own zygotes before birth, enhancing the offspring's chance of surviving. In turn, parental care influences mating strategies, and Trivers' model argues that individuals facing higher levels of parental investment become increasingly selective in their choices of mate.

It may be suspected that parental care promotes the evolution of more complex modes of reproduction. Although in some species with external fertilization, males show the strongest parental care, females generally invest more in offspring than males [2]. Providing offspring with additional nutrition should be favored by natural selection when the consequent increased fitness [37, 40] but retaining zygotes and the first stages of embryogenesis within the female's body is one way by which numerous animals increasingly favor the development of their offspring during their most vulnerable life stage. Parent-offspring conflict over the degree of parental investment has been argued to be one of the main selective factors in the evolution of reproductive strategies [13]. The reproductive modes certainly influence the level at which males reduce or increase their parental care, and alternative forms of embryo nutrition allow parents to redirect their parental investment. 

In general, all birds and prototherian mammals are oviparous, while therian mammals are viviparous, but the modes of reproduction are remarkably diversified, especially in arthropods, fishes, reptiles and amphibians. Some of these groups have even developed certain aspects of viviparous development. For instance, the fire salamander is considered to exhibit an ovo-viviparous reproductive mode, but some subspecies such as Salamandra s. fastuosa or S. s. bernadezi show viviparous development with fully metamorphosed juveniles [16, 24]. Likewise, the black salamander S. atra gives birth to live young [48]. The viviparity of salamanders could be understood as an adaptation to facing the rarity of liquid water, either because of the harsh mountain climate or because of the droughts they experience [9, 48]. Therefore, these reproductive habits are not only the translation of the phylogeny but appear as adaptive replies to environmental constraints. For example, the common lizard Lacerta/Zootoca vivipara lays eggs in mountains but shows an ovo-viviparous development in plains [20, 34, 39, 43].

Such variations in reproductive strategies and the different modes of fertilization and of retention and growth of the fertilized eggs within the maternal body lead to a certain confusion in the use of the terms “oviparity” and “viviparity”. Oviparity is assumed to be the ancestral condition in lineages of animals but the term encompasses a variety of situations. Oviparity is generally defined as any spawning of oocytes (unfertilized) or fertilized eggs, and viviparity is defined as “any mechanism for live-bearing or maintenance of development, by either maternal or paternal parent in or on any part of the body”, while ovo-viviparity includes other intermediate modes [49]. In fact, this classification of different modes of reproduction into three classes is old and is primarily based on empirical observations; so much confusion is still attached to this descriptive classification in front of the known variety of reproductive strategies [7]. Thus, if birds could be qualified as really oviparous, could numerous fishes, such as salmonids, be considered as oviparous since the female does not spawn eggs but produces only unfertilized ova? The use of the term “ovuliparity” appears most informative when fertilization is external [30]. Similarly, many fishes are considered as viviparous but without presenting the characteristics of mammalian reproductive schedules such as the placenta [50]. Finally, what about the species whose embryonic development does not occur inside the genital tract of the female, as expected either in ovo-viviparous or viviparous animals, but in organs as different as the vocal sacs of the male toad Rhinoderma [10] or in the ventral pouch of the male seahorse?

Actually, oviparity and viviparity are traditionally described based on the final development stage of the newborn, but such descriptions, which usually cannot be given adaptive significance remain insufficient to prove any reproductive mode [7, 12]. The variety of reproductive modes also shows that parental investment and parent-offspring conflict could also occur inside the bodies of adults, especially inside the female. By the way, it has been proposed that the classification should retain the source of nutrients for embryonic development, distinguishing nutrients derived from yolk, i.e. lecithotrophy, and nutrients provided by mother i.e. matrotrophy [51]. Nevertheless, matrotrophy is the feeding of the zygote by the mother and this distinction did not provide any evolutionary details on the mode of nutrition (histotrophy or hemotrophy?) whereas two distinct types of nutritional viviparity should be distinguished revealing the level of parental investment. Similarly, lecithotrophy did not provide any information on the retention of zygotes inside the body and remain based only on the discrimination between the old categories oviparity and viviparity [45]. Finally, numerous clades include both oviparous and viviparous species, and should allow a new understanding of the evolutionary process of reproduction [40].

A new typology of reproductive modes, A PROPOSAL

Here, the objective is not to detail all anatomical or physiological features involved in different modes of sexual reproduction, but to build a scientific typology corroborated by some characteristic examples. Based on relationships between parents and offspring, including a typology of embryonic development (external fertilization, internal fertilization, retention of eggs or embryos, stages of embryonic development) and the mode of intake of nutrients (feeding external oophagy, intra-uterine cannibalism, histotrophic or hemotrophic supply), I propose to scientifically define five categories of different reproduction modes: ovuliparity, oviparity, ovo-viviparity, histotrophic viviparity and hemotrophic viviparity. Taking into account the relationships between parental investment and embryonic development, such a classification may be very relevant to evolutionary biology (Table 1).

Table 1. Typology in five classes of reproductive modes detailing the degree of parental investment

1. Ovuliparity: ovuliparity refers to the release of oocyte from female tract. A species is considered as ovuliparous when the female emits ova in the environment which are fertilized externally by the male. Ovuliparity is hence characterized by external fertilization; the male sprays his milt on ova sometimes deposited in a nest. Here, the chorion develops from the surface of the yolk sac. The fertilized eggs continue their development in the environment outside the body of the parents. Ovuliparity can be considered as quite a primitive mode of reproduction. Typically, toads and frogs amplexus [6] are cases of ovuliparity.

2. Oviparity: oviparity is characteristic of species with internal fertilization, where the embryos are set up in the genital tract of the female. Oviparity is typically lecithotrophic reproduction, the egg being provided with an abundant yolk. The egg is generally associated with a chorion and is often protected by a robust, complex and durable eggshell [17, 22]. After spawning, embryonic development will then continue outside the female's body without any direct nutritive interaction. However, parents may develop specific interactions with the brood, for example to promote incubation. Oviparity could be single (each egg laid individually) or multiple (some eggs are briefly retained, and then spawned together with the more recent ones). Typically, birds show external oviparous reproduction, laying an egg provisioned with an abundant yolk. No avian feature is known to be incompatible with viviparous reproduction [8]. The reason why all birds exhibit oviparous reproduction could be that, like warm-blooded animals, birds can externally incubate their eggs, something amphibians and reptiles do not do. In oviparous animals, most poikilotherms use nests to retain heat to incubate eggs, but this requires optimal, warm environmental conditions. This also suggests that cold conditions could be one of the strongest selection pressures for egg retention and viviparity. Viviparity evolves in cold climate reptiles because females are able to maintain stable body temperature Multiple oviparity appears as an intermediate stage in the extended retention of eggs i.e. ovo-viviparity. The primitive prototherian mammals such as the platypus or echidnas are oviparous.

3. Ovo-viviparity: ovo-viviparity is characterized by an internal incubation, based on the extent of retention of fertilized eggs during part of embryonic development but with no direct internal nutritive exchanges between the parent and embryo. Fertilization can be external or internal but the embryonic development will continue inside the parent body so that ovo-viviparity is often lecithotrophic reproduction. Several different “embryo retention” mechanisms have evolved in fishes, amphibians and reptiles. The retention of fertilized eggs occurs most often in the oviduct of females, but internal fertilization is required for oviductal retention of the embryo. When other more or less specialized organs are used to house incubation, externally fertilized zygotes should be ingested or deposited in these organs. Nevertheless, organic retention i.e. skin brooding, or mouth and stomach incubation, probably derives from parental care of juveniles, whereas oviductal incubation could be a first stage in viviparity retention, as suggested by the thinness of the shell. It seems that the retention of developing eggs in the uterus by oviparous squamates enhances maternal fitness due to accelerated developmental rates of eggs in utero compared to in the nest [36]. 

4. Histotrophic viviparity: this mode of reproduction is characterized by the development of embryos inside the female's body with a steady supply of nutrients. Fertilization is hence internal but in addition to yolk, maternal nutrition is provided (“matrotrophy”). The term aplacental viviparity that was formerly used should be abandoned as it refers to the “absence” of a placenta and is uninformative. Similarly, the term “matrotrophy” only refers to maternal feeding, with no information on the characteristics of nutriment. Nutrient input into the oviduct of female embryonic development promotes a small number of juveniles, usually one per oviduct. Glandular contributions, i.e. adenotrophy, may provide for the offspring’s nutrition. As suggested by viviparous amphibians, reptiles and mammals, viviparity may have evolved as an evolutionary response to cold conditions in animals able to keep their body temperatures stable. Many insects show adenotrophic viviparity, i.e. when offspring are supplied by specialized glandular secretion, such as in diptera (glossinidae flies, mosquitoes), or in lepidoptera (moths). Eggs, with a chorion, are retained within the female's body and are nourished through glandular secretion until the developed larvae are ready to pupate. It should be noted that the extended retention of eggs in the oviducts of the female evolves concurrently with a reduction in egg yolk, influenced by progesterone, thus favoring the formation of blood vessel connections between mother and embryo and the future development of placenta-like structures in hemotrophic viviparity. The female can also feed the offspring through the production of ova or eggs that are consumed by the juveniles, i.e. oophagy. In some cases, the first one to hatch inside the female body can feed on other eggs, and even directly from other larvae; this is intra-uterine cannibalism, i.e. adelphophagy. Thus the black salamander Salamandra atra and some terrestrial salamanders Salamandra salamandra fastuosa produce only two juveniles (one per oviduct) fully developed through intra-uterine cannibalism.

5. Hemotrophic viviparity: fertilization and embryogenesis occur in the female genital tract. The growing embryo derives continuous nourishment from the mother –“matrotrophy”- usually through a placenta or a similar structure i.e. hemotrophy. Producing a yolkless egg, hemotrophic viviparity is a mode of reproduction in which embryonic development is stimulated by nutrient inputs through the bloodstream of the parent. The bloodstreams of the mother and the embryo are separated (by a barrier), but special tissues, i.e. a placenta or placenta-like structures, facilitate the exchange of nutrients and waste [see 14]. Viviparity involves the direct contact of tissues of the mother and embryo, with a shared surface facilitating respiratory and metabolic exchange. The embryonic development often occurs in a specialized organ, such as the uterus, and the zygote can be implanted more or less deeply inside the mucosa.

In the frogs Nectophrynoides occidentalis, Gastrotheca marsupiata and G. ovifera, the gills of tadpoles have foliaceous expansions which allow an exchange of nutritive fluid through the maternal, richly vascularized tissues. We can therefore consider that these frogs are probably viviparous, nutrient intake being assured through the bloodstream of the parent. Uterine specializations are also found in elasmobranchs Rhizoprionodon  terraenovae and Carcharhinus plumbeus in which the uterus assumes the additional function of providing nutrients to the developing embryos after the yolk stores have been depleted. Some teleosts are known to develop a pseudo-placenta enabling viviparity, but because there is no attachment between embryonic and maternal tissues, maternal-embryonic exchanges are mediated by the uterine wall. In mammals, the developing fetuses are connected to a special membranous organ with a rich blood supply -the placenta - that lines the uterus in pregnant mammals and provides nourishment to the fetus. In metatherian mammals, an omphaloplacenta reinforces embryo-mother relationships, but in therian mammals, the allantoplacenta, formed both by uterine mucosa and by fetal membranes, greatly favors exchanges of nutriments.

It is possible to reduce the confusion linked to the traditional terms employed in sexual reproduction by using this rigorous scientific typology. Here, each of the five proposed categories is clearly defined without ambiguity for the classification of species whose reproductive habits are known.

Furthermore, such typology of sexual reproductive modes emphasizes the role of parental investment and relationships between the parents and their offspring, illustrating evolutionary transitions from ovuliparity and oviparity to viviparity [30]. Sex evolved as the privileged mode of reproduction in eukaryotes and genetic exchanges appear to be a very archaic process, occurring in primitive steps of proto-cell development [18, 31, 42].

These different modes of reproduction do represent a sequence in a continuum with ovuliparity the most primitive and hemotrophic viviparity the most derived. Retention and then histotrophy appear as logical steps in an evolutionary scenario of the evolution of viviparity, through lessening in ovum size, reduction of eggshells, maternal nutrition and modification of uterine tissues, and further changes in embryo morphology. The evolutionary shift between oviparity and viviparity presumably occurs via increased duration of egg retention and an increase in vascularity of embryonic and maternal tissues [1, 27]. Thus, skin feeding, oophagy, adelphophagy and adenophagy may constitute intermediate and primitive stages for the fetal feeding inside the oviduct of viviparous animals, while the initial growth of oviparous animals chiefly depends on the provision of yolk. In fact, providing an embryo with nutrition inside the adult body should be promoted by natural selection when the consequent increased fitness of the offspring leads to reduced fecundity [49]. Likewise, fitness consequences of the duration of retention of eggs may result in a trade-off in ovo-viviparity modes.

Although any evolutionary change requires a new understanding of trade-offs, life-history traits, such as modes of reproduction, are undoubtedly the most critical evolutionary features because they affect fitness and survival so intimately.

Th. Lodé

from:

Lodé T 2001. Les stratégies de reproduction des animaux. -Reproductive strategies in animal kingdom- Paris, Dunod-Masson Sciences

Lodé T.  2012  Oviparity or viviparity ? That is the question…. Reproductive Biology 12: 259-264